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THE ANCESTOR'S TALE

By the same author:

The Selfish Gene

A Devil's Chaplain

THE ANCESTOR'S TALE
A PILGRIMAGE TO
THE DAWN OF LIFE

RICHARD DAWKINS

with additional research by YAN WONG

WEIDENFELD & NICOLSON

John Maynard Smith (1920-2004)

He saw a draft and graciously accepted the dedication, which now, sadly, must become

In Memoriam

‘Never mind the lectures or the "workshops"; be Mowed to the motor coach excursions to local beauty spots; forget your fancy visual aids and radio microphones; the only thing that really matters at a conference is that John Maynard Smith must be in residence and there must be a spacious, convivial bar. If he can't manage the dates you have in mind, you must just reschedule the conference... He will charm and amuse the young research workers, listen to their stories, inspire them, rekindle enthusiasms that might be flagging, and send them back to their laboratories or their muddy fields, enlivened and invigorated, eager to try out the new ideas he has generously shared with them..’

It isn't only conferences that will never be the same again.

ACKNOWLEDGEMENTS

I was persuaded to write this book by Anthony Cheetham, founder of Orion Books. The fact that he had moved on before the book was published reflects my unconscionable delay in finishing it. Michael Dover tolerated that delay with humour and fortitude, and always encouraged me by his swift and intelligent understanding of what I was trying to do. The best of his many good decisions was to engage Latha Menon as a freelance editor. As with A Devil's Chaplain, Latha's support has been beyond all estimation. Her grasp of the big picture simultaneously with the details, her encyclopaedic knowledge, her love of science and her selfless devotion to promoting it have benefited me, and this book, in more ways than I can count. Others at the publishers helped greatly, but Jennie Condell and the designer, Ken Wilson, went beyond the call of duty.

My research assistant Yan Wong has been intimately involved at every stage of the planning, researching and writing of the book. His resourcefulness and detailed familiarity with modern biology have been matched only by his green fingers with computers. If, here, I have gratefully assumed the role of apprentice, it could be said that he was my apprentice before I was his, for I was his tutor at New College. He then did his doctorate under the supervision of Alan Grafen, once my own graduate student, so I suppose Yan could be called my grandstudent as well as my student. Apprentice or master, Yan's contribution has been so great that, for certain tales, I have insisted on adding his name as joint author. When Yan left to cycle across Patagonia, the book in its final stages benefited greatly from Sam Turvey's extraordinary knowledge of zoology and his conscientious care in deploying it.

Advice and help of various kinds were willingly given by Michael Yudkin, Mark Griffith, Steve Simpson, Angela Douglas, George McGavin, Jack Pettigrew, George Barlow, Colin Blakemore, John Mollon, Henry Bennet-Clark, Robin Elisabeth Cornwell, Lindell Bromham, Mark Sutton, Bethia Thomas, Eliza Howlett, Tom Kemp, Malgosia Nowak-Kemp, Richard Fortey, Derek Siveter, Alex Freeman, Nicky Warren, A. V. Grimstone, Alan Cooper, and especially Christine DeBlase-Ballstadt. Others are acknowledged in the Notes at the end.

I am deeply grateful to Mark Ridley and Peter Holland, who were engaged by the publishers as critical readers and gave me exactly the right kind of advice. The routine authorial claim of responsibility for the remaining shortcomings is more than usually necessary in my case.

As always, I gratefully acknowledge the imaginative generosity of Charles Simonyi. And my wife, Lalla Ward, has once again been my help and strength.

RICHARD DAWKINS

CONTENTS

• THE CONCEIT OF HINDSIGHT 8
• THE GENERAL PROLOGUE 16
• THE PILGRIMAGE BEGINS 27
• The Farmer's Tale 28
• The Cro-Magnon's Tale 34
• RENDEZVOUS 0 ALL HUMANKIND 36
• The Tasmanian's Tale 39
• Eve's Tale 44
• ARCHAIC HOMO SAPIENS 56
• The Neanderthal's Tale 58
• ERGASTS 59
• The Ergast's Tale 63
• HABILINES 68
• The Handyman's Tale 69
• APE-MEN 77
• Little Foot's Tale 80
• Epilogue to Little Foot's Tale 84
• RENDEZVOUS 1 CHIMPANZEES 88
• The Bonobo's Tale 92
• RENDEZVOUS 2 GORILLAS 94
• The Gorilla's Tale 95
• RENDEZVOUS 3 ORANG UTANS 98
• The Orang Utan's Tale 99
• RENDEZVOUS 4 GIBBONS 104
• The Gibbon's Tale 107
• RENDEZVOUS 5 OLD WORLD MONKEYS 118
• RENDEZVOUS 6 NEW WORLD MONKEYS 122
• The Howler Monkey's Tale 125
• RENDEZVOUS 7 TARSIERS 134
• RENDEZVOUS 8 LEMURS, BUSHBABIES AND THEIR KIN 134
• The Aye-Aye's Tale 140
• THE GREAT CRETACEOUS CATASTROPHE 144
• RENDEZVOUS 9 COLUGOS AND TREE SHREWS 148
• The Colugo's Tale 150
• RENDEZVOUS 10 RODENTS AND RABBITKIND 152
• The Mouse's Tale 155
• The Beaver's Tale 157
• RENDEZVOUS 11 LAURASIATHERES 162
• The Hippo's Tale 165
• Epilogue to the Hippo's Tale 170
• The Seal's Tale 171
• RENDEZVOUS 12 XENARTHRANS 178
• The Armadillo's Tale 178
• RENDEZVOUS 13 AFROTHERES 182
• RENDEZVOUS 14 MARSUPIALS 188
• The Marsupial Mole's Tale 191
• RENDEZVOUS 15 MONOTREMES 194
• The Duckbill's Tale 196
• What the Star-Nosed Mole said to the Duckbilled Platypus 204
• MAMMAL-LIKE REPTILES 207
• RENDEZVOUS 16 SAUROPSIDS 214
• Prologue to the Galapagos Finch's Tale 217
• The Galapagos Finch's Tale 220
• The Peacock's Tale 222
• The Dodo's Tale 231
• The Elephant Bird's Tale 235
• Epilogue to the Elephant Bird's Tale 242
• RENDEZVOUS 17 AMPHIBIANS 246
• The Salamander's Tale 252
• The Narrowmouth's Tale 261
• The Axolotl's Tale 263
• RENDEZVOUS 18 LUNGFISH 268
• The Lungfish's Tale 269
• RENDEZVOUS 19 COELACANTHS 272
• RENDEZVOUS 20 RAY-FINNED FISH 274
• The Leafy Sea Dragon's Tale 274
• The Pike's Tale 278
• The Mudskipper's Tale 279
• The Cichlid's Tale 281
• The Blind Cave Fish's Tale 288
• The Flounder's Tale 290
• RENDEZVOUS 21 SHARKS AND THEIR KIN 292
• RENDEZVOUS 22 LAMPREYS AND HAGFISH 296
• The Lamprey's Tale 299
• RENDEZVOUS 23 LANCELETS 302
• The Lancelet's Tale 303
• RENDEZVOUS 24 SEA SQUIRTS 306
• RENDEZVOUS 25 AMBULACRARIANS 310
• RENDEZVOUS 26 PROTOSTOMES 314
• The Ragworm's Tale 322
• The Brine Shrimp's Tale 325
• The Leaf Cutter's Tale 329
• The Grasshopper's Tale 331
• The Fruit Fly's Tale 343
• The Rotifer's Tale 352
• The Barnacle's Tale 359
• The Velvet Worm's Tale 362
• Epilogue to the Velvet Worm's Tale 373
• RENDEZVOUS 27 ACOELOMORPH FLATWORMS 380
• RENDEZVOUS 28 CNIDARIANS 384
• The Jellyfish's Tale 388
• The Polypifer's Tale 390
• RENDEZVOUS 29 CTENOPHORES 396
• RENDEZVOUS 30 PLACOZOANS 398
• RENDEZVOUS 31 SPONGES 400
• The Sponge's Tale 404
• RENDEZVOUS 32 CHOANOFLAGELLATES 406
• The Choanoflagellate's Tale 407
• RENDEZVOUS 33 DRIPs 410
• RENDEZVOUS 34 FUNGI 412
• RENDEZVOUS 35 AMOEBOZOANS 416
• RENDEZVOUS 36 PLANTS 418
• The Cauliflower's Tale 422
• The Redwood's Tale 425
• RENDEZVOUS 37 UNCERTAIN 434
• The Mixotrich's Tale 439
• THE GREAT HISTORIC RENDEZVOUS 445
• RENDEZVOUS 38 ARCHAEA 448
• RENDEZVOUS 39 EUBACTERIA 450
• The Rhizobium's Tale 450
• Taq's Tale 459
• CANTERBURY 464
• THE HOST'S RETURN 482


• FURTHER READING 507
• NOTES 507
• BIBLIOGRAPHY 510
• INDEX 516

THE CONCEIT OF HINDSIGHT

‘History doesn't repeat itself, but it rhymes.’

MARK TWAIN

‘History repeats itself; that's one of the things that's wrong with history.’

CLARENCE DARROW

History has been described as one damn thing after another. The remark can be seen as a warning against a pair of temptations but, duly warned, I shall cautiously flirt with both. First, the historian is tempted to scour the past for patterns that repeat themselves; or at least, following Mark Twain, to seek reason and rhyme for everything. This appetite for pattern affronts those who insist that, as Mark Twain will also be found to have said, ‘History is usually a random, messy affair’, going nowhere and following no rules. The second connected temptation is the vanity of the present: of seeing the past as aimed at our own time, as though the characters in history's play had nothing better to do with their lives than foreshadow us.

Under names that need not trouble us, these are live issues in human history and they arise with greater force, and no greater agreement, on the longer time-scale of evolution. Evolutionary history can be represented as one damn species after another. But many biologists will join me in finding this an impoverished view. Look at evolution that way and you miss most of what matters. Evolution rhymes, patterns recur. And this doesn't just happen to be so. It is so for well understood reasons: Darwinian reasons mostly, for biology, unlike human history or even physics, already has its grand unifying theory, accepted by all informed practitioners, though in varying versions and interpretations. In writing evolutionary history I do not shrink from seeking patterns and principles, but I try to be careful about it.

What of the second temptation, the conceit of hindsight, the idea that the past works to deliver our particular present? The late Stephen Jay Gould rightly pointed out that a dominant icon of evolution in popular mythology, a caricature almost as ubiquitous as lemmings jumping over cliffs (and that myth is false too), is a shambling file of simian ancestors, rising progressively in the wake of the erect, striding, majestic figure of Homo sapiens sapiens: man as evolution's last word (and in this context it always is man rather than woman); man as what the whole enterprise is pointing towards; man as a magnet, drawing evolution from the past towards his eminence.

There is a physicist's version which is less obviously vainglorious and which I should mention in passing. This is the ‘anthropic’ notion that the very laws of physics themselves, or the fundamental constants of the universe, are a carefully tuned put-up job, calculated to bring humanity eventually into existence. It is not necessarily founded on vanity. It doesn't have to mean that the universe was deliberately made in order that we should exist. It need mean only that we  {8}  are here, and we could not be in a universe that lacked the capability of producing us. As physicists have pointed out, it is no accident that we see stars in our sky, for stars are a necessary part of any universe capable of generating us. Again, this does not imply that stars exist in order to make us. It is just that without stars there would be no atoms heavier than lithium in the periodic table, and a chemistry of only three elements is too impoverished to support life. Seeing is the kind of activity that can go on only in the kind of universe where what you see are stars.

But there is a little more that needs to be said. Granted the trivial fact that our presence requires physical laws and constants capable of producing us, the existence of such potent ground rules may still seem tantalisingly improbable. Depending upon their assumptions, physicists may reckon that the set of possible universes vastly outnumbers that subset whose laws and constants allowed physics to mature, via stars into chemistry and via planets into biology. To some, this means that the laws and constants must have been deliberately premeditated from the start (although it baffles me why anybody regards this as an explanation for anything, given that the problem so swiftly regresses to the larger one of explaining the existence of the equally fine-tuned and improbable Premeditator).

Other physicists are less confident that the laws and constants were free to vary in the first place. When I was little it was not obvious to me why five times eight had to give the same result as eight times five. I accepted it as one of those facts that grownups assert. Only later did I understand, perhaps through visualising rectangles, why such pairs of multiplications are not free to vary independently of one another. We understand that the circumference and the diameter of a circle are not independent, otherwise we might feel tempted to postulate a plethora of possible universes, each with a different value of p. Perhaps, argue some physicists such as the Nobel Prize-winning theorist Steven Weinberg, the fundamental constants of the universe, which at present we treat as independent of one another, will in some Grand Unified fullness of time be understood to have fewer degrees of freedom than we now imagine. Maybe there is only one way for a universe to be. That would undermine the appearance of anthropic coincidence.

Other physicists, including Sir Martin Rees, the present Astronomer Royal, accept that there is a real coincidence in need of explanation, and explain it by postulating many actual universes existing in parallel, mutually incommunicado, each with its own set of laws and constants^*. Obviously we, who find ourselves reflecting upon such things, must be in one of those universes, however rare, whose laws and constants are capable of evolving us.

The theoretical physicist Lee Smolin added an ingenious Darwinian spin which reduces the apparent statistical improbability of our existence. In Smolin's model, universes give birth to daughter universes, which vary in their laws and constants. Daughter universes are born in black holes produced by a parent universe, and they inherit its laws and constants but with some possibility of small random change — ‘mutation’. Those daughter universes that have what it takes to reproduce (last long enough to make black holes, for  {9}  instance) are, of course, the universes that pass on their laws and constants to their daughters. Stars are precursors to black holes which, in the Smolin model, are the birth events. So universes that have what it takes to make stars are favoured in this cosmic Darwinism. The properties of a universe that furnish this gift to the future are the self-same properties that incidentally lead to the manufacture of large atoms, including vital carbon atoms. Not only do we live in a universe that is capable of producing life. Successive generations of universes progressively evolve to become increasingly the sort of universe that, as a by-product, is capable of producing life.

The logic of the Smolin theory is bound to appeal to a Darwinian, indeed to anyone of imagination, but as for the physics I am not qualified to judge. I cannot find a physicist to condemn the theory as definitely wrong — the most negative thing they will say is that it is superfluous. Some, as we saw, dream of a final theory in whose light the alleged fine-tuning of the universe will turn out to be a delusion anyway. Nothing we know rules out Smolin's theory, and he claims for it the merit — which scientists rate more highly than many laymen appreciate — of testability. His book is The Life of the Cosmos and I recommend it.

But that was a digression about the physicist's version of the conceit of hindsight. The biologist's version is easier to dismiss since Darwin, though harder before him, and it is our concern here. Biological evolution has no privileged line of descent and no designated end. Evolution has reached many millions of interim ends (the number of surviving species at the time of observation), and there is no reason other than vanity — human vanity as it happens, since we are doing the talking — to designate any one as more privileged or climactic than any other.

This doesn't mean, as I shall continue to argue, that there is a total dearth of reasons or rhymes in evolutionary history. I believe there are recurring patterns. I also believe, though this is more controversial today than it once was, that there are senses in which evolution may be said to be directional, progressive and even predictable. But progress is emphatically not the same thing as progress towards humanity, and we must live with a weak and unflattering sense of the predictable. The historian must beware of stringing together a narrative that seems, even to the smallest degree, to be homing in on a human climax.

A book in my possession (in the main a good book, so I shall not name and shame it) provides an example. It is comparing Homo habilis (a human species, probably ancestral to us) with its predecessors the australopithecines^*. What the book says is that Homo habilis was ‘considerably more evolved than the Australopithecines’. More evolved? What can this mean but that evolution is moving in some pre-specified direction? The book leaves us in no doubt of what the presumed direction is. "The first signs of a chin are apparent." ‘First’ encourages us to expect second and third signs, towards a ‘complete’ human chin. ‘The teeth start to resemble ours ...’ As if those teeth were the way they were, not because it suited the habiline diet but because they were embarking upon the road towards becoming our teeth. The passage ends with a telltale remark about a later species of extinct human, Homo erectus:  {10} 

Although their faces are still different from ours, they have a much more human look in their eyes. They are like sculptures in the making, ‘unfinished’ works.

In the making? Unfinished? Only with the unwisdom of hindsight. In excuse of that book it is probably true that, were we to meet a Homo erectus face to face, it might well look to our eyes like an unfinished sculpture in the making. But that is only because we are looking with human hindsight. A living creature is always in the business of surviving in its own environment. It is never unfinished — or, in another sense, it is always unfinished. So, presumably, are we.

The conceit of hindsight tempts us at other stages in our history. From our human point of view, the emergence of our remote fish ancestors from water to land was a momentous step, an evolutionary rite of passage. It was undertaken in the Devonian Period by lobe-finned fish a bit like modern lungfish. We look at fossils of the period with a pardonable yearning to gaze upon our forebears, and are seduced by a knowledge of what came later: drawn into seeing these Devonian fish as ‘halfway’ towards becoming land animals; everything about them earnestly transitional, bound into an epic quest to invade the land and initiate the next big phase of evolution. That is not the way it was at the time. Those Devonian fish had a living to earn. They were not on a mission to evolve, not on a quest towards the distant future. An otherwise excellent book about vertebrate evolution contains the following sentence about fish which

ventured out of the water on to the land at the end of the Devonian Period and jumped the gap, so to speak, from one vertebrate class to another to become the first amphibians...

The ‘gap’ comes from hindsight. There was nothing resembling a gap at the time, and the ‘classes’ that we now recognise were no more separate, in those days, than two species. As we shall see again, jumping gaps is not what evolution does.

It makes no more sense (and no less) to aim our historical narrative towards Homo sapiens than towards any other modern species — Octopus vulgaris, say, or Panthera leo or Sequoia sempervirens. A historically minded swift, understandably proud of flight as self-evidently the premier accomplishment of life, will regard swiftkind — those spectacular flying machines with their swept-back wings, who stay aloft for a year at a time and even copulate in free flight — as the acme of evolutionary progress. To build on a fancy of Steven Pinker, if elephants could write history they might portray tapirs, elephant shrews, elephant seals and proboscis monkeys as tentative beginners along the main trunk road of evolution, taking the first fumbling steps but each — for some reason — never quite making it: so near yet so far. Elephant astronomers might wonder whether, on some other world, there exist alien life forms that have crossed the nasal rubicon and taken the final leap to full proboscitude.

We are not swifts nor elephants, we are people. As we wander in imagination through some long-dead epoch, it is humanly natural to reserve a special warmth and curiosity for whichever otherwise ordinary species in that ancient  {11}  landscape is our ancestor (it is an intriguingly unfamiliar thought that there is always one such species). It is hard to deny our human temptation to see this one species as ‘on the main line’ of evolution, the others as supporting cast, walk-on parts, sidelined cameos. Without succumbing to that error, there is one way to indulge a legitimate human-centrism while respecting historical propriety. That way is to do our history backwards, and it is the way of this book.

Backward chronology in search of ancestors really can sensibly aim towards a single distant target. The distant target is the grand ancestor of all life, and we can't help converging upon it no matter where we start — elephant or eagle, swift or salmonella, wellingtonia or woman. Backward chronology and forward chronology are each good for different purposes. Go backwards and, no matter where you start, you end up celebrating the unity of life. Go forwards and you extol diversity. It works on small timescales as well as large. The forward chronology of the mammals, within their large but still limited timescale, is a story of branching diversification, uncovering the richness of that group of hairy warmbloods. Backward chronology, taking any modern mammal as our starting point, will always converge upon the same unique ur-mammal: shadowy, insectivorous, nocturnal contemporary of the dinosaurs. This is a local convergence. A yet more local one converges on the most recent ancestor of all rodents, who lived somewhere around the time the dinosaurs went extinct. More local still is the backward convergence of all apes (including humans) on their shared ancestor, who lived about 18 million years ago. On a larger scale, there is a comparable convergence to be found if we work backwards from any vertebrate, an even larger convergence working backwards from any animal to the ancestor of all animals. The largest convergence of all takes us from any modern creature — animal, plant, fungus or bacterium — back to the universal progenitor of all surviving organisms, probably resembling some kind of bacterium.

I used ‘convergence’ in the last paragraph, but I really want to reserve that word for a completely different meaning in forward chronology. So for the present purpose I shall substitute ‘confluence’ or, for reasons that will make sense in a moment, ‘rendezvous’. I could have used ‘coalescence’, except that, as we shall see, geneticists have already adopted it in a more precise sense, similar to my ‘confluence’ but concentrating on genes rather than species. In a backward chronology, the ancestors of any set of species must eventually meet at a particular geological moment. Their point of rendezvous is the last common ancestor that they all share, what I shall call their ‘Concestor’^*: the focal rodent or the focal mammal or the focal vertebrate, say. The oldest concestor is the grand ancestor of all surviving life.

We can be very sure there really is a single concestor of all surviving life forms on this planet. The evidence is that all that have ever been examined share (exactly in most cases, almost exactly in the rest) the same genetic code; and the genetic code is too detailed, in arbitrary aspects of its complexity, to have been invented twice. Although not every species has been examined, we already have enough coverage to be pretty certain that no surprises — alas — await us. If we now were to discover a life form sufficiently alien to have a  {12}  completely different genetic code, it would be the most exciting biological discovery in my adult lifetime, whether it lives on this planet or another. As things stand, it appears that all known life forms can be traced to a single ancestor which lived more than 3 billion years ago. If there were other, independent origins of life, they have left no descendants that we have discovered. And if new ones arose now they would swiftly be eaten, probably by bacteria.

The grand confluence of all surviving life is not the same thing as the origin of life itself. This is because all surviving species presumably share a concestor who lived after the origin of life: anything else would be an unlikely coincidence, for it would suggest that the original life form immediately branched and more than one of its branches survive to this day. Current textbook orthodoxy dates the oldest bacterial fossils at about 3.5 billion years ago, so the origin of life must at least be earlier than that. If we accept a recent disputation^* of these apparently ancient fossils, our dating of the origin of life might be a bit more recent. The grand confluence — the last common ancestor of all surviving creatures — could pre-date the oldest fossils (it didn't fossilise) or it could have lived a billion years later (all but one of the other lineages went extinct).

Given that all backward chronologies, no matter where they start, culminate in the one grand confluence, we can legitimately indulge our human preoccupation and concentrate upon the single line of our own ancestors. Instead of treating evolution as aimed towards us, we choose modern Homo sapiens as our arbitrary, but forgivably preferred, starting point for a reverse chronology. We choose this route, out of all possible routes to the past, because we are curious about our own great grancestors. At the same time, although we need not follow them in detail, we shall not forget that there are other historians, animals and plants belonging to other species, who are independently walking backwards from their separate starting points, on separate pilgrimages to visit their own ancestors, including eventually the ones they share with us. If we retrace our own ancestral steps, we shall inevitably meet these other pilgrims and join forces with them in a definite order, the order in which their lineages rendezvous with ours, the order of ever more inclusive cousinship.

Pilgrimages? Join forces with pilgrims? Yes, why not? Pilgrimage is an apt way to think about our journey to the past. This book will be cast in the form of an epic pilgrimage from the present to the past. All roads lead to the origin of life. But because we are human, the path we shall follow will be that of our own ancestors. It will be a human pilgrimage to discover human ancestors. As we go, we shall greet other pilgrims who will join us in strict order, as we reach the common ancestors we share with them.

The first fellow pilgrims we shall greet, some 5 million years ago, deep in Africa where Stanley memorably shook hands with Livingstone, are the chimpanzees. The chimpanzee and bonobo pilgrims will already have joined forces with each other ‘before’ we greet them. And here we have a little linguistic trickiness which I must face at the outset, before it dogs us any further. I placed ‘before’ in inverted commas because it could confuse. I used it to mean before in the backwards sense — ‘before, in the course of the pilgrimage to the past’. But that of course means after in the chronological sense, the exact opposite meaning!  {13}  My guess is that no reader was confused in this particular case, but there will be other instances where the reader's patience may be tested. While writing this book I tried the experiment of coining a new preposition, tailored to the peculiar needs of a backward historian. But it didn't fly. Instead, I shall adopt the convention of ‘before’ in inverted commas. When you see ‘before’, remember that it really means after! When you see before, it really means before. And the same for ‘after’ and after, mutatis mutandis.

The next pilgrims with whom we shall rendezvous as we push back along our journey are gorillas, then orang utans (quite a lot deeper into the past, and probably no longer in Africa). Next we shall greet gibbons, then Old World monkeys, then New World monkeys, then various other groups of mammals... and so on until eventually all the pilgrims of life are marching together in one single backward quest for the origin of life itself. As we push on back, there will come a time when it is no longer meaningful to name the continent in which a rendezvous takes place: the map of the world was so different, because of the remarkable phenomenon of plate tectonics. And further back still, all rendezvous take place in the sea.

It is a rather surprising fact that we human pilgrims pass only about 40 rendezvous points in all, before we hit the origin of life itself. At each of the 40 steps we shall find one particular shared ancestor, the Concestor, which will bear the same labelling number as the Rendezvous. For example, Concestor 2, whom we meet at Rendezvous 2, is the most recent common ancestor of gorillas on the one hand and {humans + {chimpanzees + bonobos}} on the other. Concestor 3 is the most recent common ancestor of orang utans and {{humans + {chimpanzees + bonobos}} + gorillas}. Concestor 39 is the grand ancestor of all surviving life forms. Concestor 0 is a special case, the most recent ancestor of all surviving humans.

We shall be pilgrims, then, sharing fellowship ever more inclusively with other pilgrim bands, which also have been swelling on their own way to their rendezvous with us. After each meeting, we continue together on the high road back to our shared Archaean goal, our ‘Canterbury’. There are other literary allusions, of course, and I almost made Bunyan my model and Pilgrim's Regress my title. But it was to Chaucer's Canterbury Tales that I and my research assistant Yan Wong kept returning in our discussions, and it seemed increasingly natural to think of Chaucer throughout this book.

Unlike (most of) Chaucer's pilgrims, mine do not all set out together, although they do set off at the same time, the present. These other pilgrims aim towards their ancient Canterbury from different starting points, joining our human pilgrimage at various rendezvous along the road. In this respect, my pilgrims are unlike those who gathered in London's Tabard Inn. Mine are more like the sinister canon and his understandably disloyal yeoman, who joined Chaucer's pilgrims at Boughton-under-Blee, five miles short of Canterbury. Following Chaucer's lead, my pilgrims, which are all the different species of living creature, will have the opportunity to tell tales along the way to their Canterbury which is the origin of life. It is these tales that form the main substance of this book.  {14} 

Dead men tell no tales, and extinct creatures such as trilobites are deemed not to be pilgrims capable of telling them, but I shall make exceptions of two special classes. Animals such as the dodo, which survived into historical times and whose DNA is still available to us, are treated as honorary members of the modern fauna setting off on pilgrimage at the same time as us, and joining us at some particular rendezvous. Since we are responsible for their so recent extinction, it seems the least we can do. The other honorary pilgrims, exceptions to the rule that dead men tell no tales, really are men (or women). Since we human pilgrims are directly seeking our own ancestors, fossils that might plausibly be considered candidates for being our ancestors are deemed members of our human pilgrimage and we shall hear tales from some of these ‘shadow pilgrims’, for example the Handyman, Homo habilis.

I decided it would be twee to let my animal and plant tale-tellers speak in the first person singular, and I shall not do so. Save for occasional asides and prefatory remarks, Chaucer's pilgrims don't either. Many of Chaucer's Tales have their own Prologue, and some have an Epilogue too, all written in Chaucer's own voice as narrator of the pilgrimage. I shall occasionally follow his example. As with Chaucer, an epilogue may serve as a bridge from one tale to the next.

Before his Tales begin, Chaucer has a long General Prologue in which he sets out his cast list: the professions and in some cases the names of the pilgrims who are about to set off from the tavern. Instead, I shall introduce new pilgrims as they join us. Chaucer's jovial host offers to guide the pilgrims, and encourages them to tell their tales to while away the journey. In my role as host I shall use the General Prologue for some preparatory remarks about methods and problems of reconstructing evolutionary history, which must be faced and solved whether we do our history backwards or forwards.

Then we shall embark on our backwards history itself. Although we shall concentrate on our own ancestors, noting other creatures usually only when they join us, we shall from time to time look up from our road and remind ourselves that there are other pilgrims on their own more or less independent routes to our ultimate destination. The numbered rendezvous milestones, plus a few intermediate markers necessary to consolidate the chronology, will provide the scaffolding for our journey. Each will mark a new chapter, where we halt to take stock of our pilgrimage, and maybe listen to a tale or two. On rare occasions, something important happens in the world around us, and then our pilgrims may pause briefly to reflect on it. But, for the most part, we shall mark our progress to the dawn of life by the measure of those 40 natural milestones, the trysts that enrich our pilgrimage.

THE GENERAL PROLOGUE

How shall we know the past, and how date it? What aids to our vision will help us peer into theatres of ancient life and reconstruct the scenes and the players, their exits and their entrances, of long ago? Conventional human history has three main methods, and we shall find their counterparts on the larger time-scale of evolution. First there is archaeology, the study of bones, arrowheads, fragments of pots, oystershell middens, figurines and other relics that survive as hard evidence from the past. In evolutionary history, the most obvious hard relics are bones and teeth, and the fossils that they eventually become. Second, there are renewed relics, records that are not themselves old but which contain or embody a copy or representation of what is old. In human history these are written or spoken accounts, handed down, repeated, reprinted or otherwise duplicated from the past to the present. In evolution, I shall propose DNA as the main renewed relic, equivalent to a written and recopied record. Third, there is triangulation. This name comes from a method of judging distances by measuring angles. Take a bearing on a target. Now walk a measured distance sideways and take another. From the intercept of the two angles, calculate the distance of the target. Some camera rangefinders use the principle, and map surveyors traditionally relied upon it. Evolutionists can be said to ‘triangulate’ an ancestor by comparing two (or more) of its surviving descendants. I shall take the three kinds of evidence in order, beginning with hard relics and, in particular, fossils.

FOSSILS

Bodies or bones may survive for our attention, having somehow escaped that of hyenas, burying beetles and bacteria. The ‘Ice Man’ of the Italian Tyrol was preserved in his glacier for 5,000 years. Insects have become embalmed in amber (petrified gum from trees) for 100 million years. Without benefit of ice or amber, hard parts like teeth, bones and shells stand the best chance of being preserved. Teeth last longest of all because, to do their job in life, they had to be harder than anything their owner was likely to eat. Bones and shells need to be hard for different reasons, and they too can last a long time. Such hard parts and, under exceptionally lucky circumstances, soft parts too, occasionally become petrified as stone fossils that last for hundreds of millions of years. In spite of the fascination of fossils, it is surprising how much we would still  {16}  know about our evolutionary past without them. If every fossil were magicked away, the comparative study of modern organisms, of how their patterns of resemblances, especially of their genetic sequences, are distributed among species, and of how species are distributed among continents and islands, would still demonstrate, beyond all sane doubt, that our history is evolutionary, and that all living creatures are cousins. Fossils are a bonus. A welcome bonus, to be sure, but not an essential one. It is worth remembering this when creationists go on (as they tediously do) about ‘gaps’ in the fossil record. The fossil record could be one big gap, and the evidence for evolution would still be overwhelmingly strong. At the same time, if we had only fossils and no other evidence, the fact of evolution would again be overwhelmingly supported. As things stand, we are blessed with both.

The word fossil is conventionally used to mean any relic dating back more than 10,000 years: not a helpful convention, for there is nothing special about a round number like 10,000. If we had fewer or more than ten fingers, we'd recognise a different set of numbers as round.^* When we speak of a fossil, we normally mean that the original material has been substituted or infiltrated by a mineral of a different chemical composition and therefore given, as one might say, a new lease of death. An imprint of the original form may be preserved in stone for a very long time indeed, perhaps mixed with some of the original material. There are various ways in which this can happen. I leave the details — what is technically called taphonomy — for the Ergast's Tale.

When fossils were first discovered and mapped, their ages were unknown. The most we could hope for was a rank ordering of oldness. Age ranking depends upon the assumption known as the Law of Superposition. For obvious reasons, younger strata lie atop older ones, unless the circumstances are exceptional. Such exceptions, though they sometimes cause temporary puzzlement, are usually pretty obvious. A lump of old rock, complete with fossils, may be thrown on top of a younger stratum, say by a glacier. Or a series of strata may be turned over wholesale, and its vertical ordering exactly reversed. These anomalies can be taken care of by comparing equivalent rocks in other parts of the world. Once this is done, the palaeontologist can piece together the true sequence of the whole fossil record, in a jigsaw of overlapping sequences from different parts of the world. The logic is complicated in practice, though not in principle, by the fact (see the Elephant Bird's Tale) that the map of the world itself changes as the ages go by.

Why is the jigsaw necessary? Why can't we just dig down as far as we like, and treat this as equivalent to digging steadily backwards through time? Well, time itself may flow smoothly, but this doesn't mean that anywhere in the world there is a single sequence of sediment deposited smoothly and continuously from start to finish through geological time. Fossil beds are laid down in fits and starts, when the conditions are right.

In any one location, at any one time, it is rather likely that no sedimentary rocks, and no fossils, are being laid down. But it is quite likely that, in some part of the world, fossils are being deposited at any given time. By hopping around the world, from site to site where different strata happen to be accessibly near

Simplified version of the timescale published by the International Commission on Stratigraphy (www.stratigraphy.org). It follows the colour coding system of the Commission de la Carte Géologique du Monde, Paris. The timescale is divided into eons, eras, periods, and epochs. Time is measured in ‘millions of years ago’ (Mya) with the shade of grey used being proportional to this age. Note that the Pleistocene and Holocene Epochs are often informally referred to as the ‘Quaternary’, though this, together with ‘Tertiary’, is part of a now obsolete dating system. The lower limit of the timescale is formally undefined, though it is generally assumed to stretch back to about 4.6 billion years ago, when the Earth and the rest of the solar system were formed.

the surface, the palaeontologist can aspire to piece together something approaching a continuous record. Of course individual palaeontologists don't hop from site to site. They hop from museum to museum looking at specimens in drawers, or from journal to journal in university libraries looking at written descriptions of fossils whose site of discovery has been carefully labelled, and they use these descriptions to piece together the fragments of the puzzle from different parts of the world.

The task is eased by the fact that particular strata, with recognisably characteristic rock properties, and consistently housing the same kinds of fossils, keep turning up in different regions. Devonian rock, so-called because it was first recognised as the ‘Old Red Sandstone’ of the beautiful county of Devon, crops up in various other parts of the British Isles, in Germany, Greenland, North America and elsewhere. Devonian rocks are recognisable as Devonian wherever they may be found, partly because of the quality of the rock but also because of the internal evidence of the fossils that they contain. This sounds like a circular argument but it really isn't: no more so than when a scholar recognises a Dead Sea Scroll, from internal evidence, as a fragment of the First Book of Samuel. Devonian rocks are reliably labelled by the presence of certain characteristic fossils.

The same goes for rocks from other geological periods, right back to the time of the earliest hard-bodied fossils. From the ancient Cambrian through to the present Holocene, the geological periods listed in the chart opposite were mostly separated on the basis of changes in the fossil record. And as a result, the end of one period and the start of another is often delimited by extinctions that conspicuously interrupt the continuity of the fossils. As Stephen Jay Gould has put it, no palaeontologist has any trouble identifying whether a lump of rock lies before or after the great end-Permian mass extinction. There is almost no overlap in animal types. Indeed, fossils (especially microfossils) are so useful in labelling and dating rocks that the oil and mining industries are among their principal users.

Such ‘relative dating’, then, has long been possible by vertical piecing together of the jigsaw of rocks. The geological periods were named for purposes of relative dating, before absolute dating became possible. And they are still useful. But relative dating is more difficult for rocks with scarce fossils — and that includes all rocks older than the Cambrian: the first eight-ninths of Earth's history.

Absolute dating had to wait for recent developments in physics, especially the physics of radioactivity. This needs some explaining, and the details must wait for the Redwood's Tale. For now, it is enough to know that we have a range of reliable methods for putting an absolute age on fossils, or the rocks that contain or surround them. Moreover, different methods in this range provide sensitivity across the whole spectrum of ages from hundreds of years (tree rings), through thousands of years (carbon 14), millions, hundreds of millions (uranium-thorium-lead) to billions of years (potassium-argon).  {19} 

RENEWED RELICS

Fossils, like archaeological specimens, are more-or-less direct relics of the past. We turn now to our second category of historical evidence, renewed relics, copied successively down the generations. For historians of human affairs this might mean eyewitness accounts, handed down by oral tradition or in written documents. We cannot ask any living witnesses what it was like to live in fourteenth-century England, but we know about it thanks to written documents, including Chaucer's. They contain information that has been copied, printed, stored in libraries, reprinted and distributed for us to read today. Once a story gets into print or, nowadays, a computer medium of some kind, copies of it have a fair chance of being perpetuated into the distant future.

Written records are more reliable than oral tradition, by a disconcerting margin. You might think that each generation of children, knowing their parents as well as most children do, would listen to their detailed reminiscences and relay them to the next generation. Five generations on, a voluminous oral tradition should, one might think, have survived. I remember my four grandparents clearly, but of my eight great-grandparents I know a handful of fragmentary anecdotes. One great-grandfather habitually sang a certain nonsense rhyme (which I can sing), but only while lacing his boots. Another was greedy for cream, and would knock the chess board over when losing. A third was a country doctor. That is about my limit. How have eight entire lives been so reduced? How, when the chain of informants connecting us back to the eyewitness seems so short, and human conversation so rich, could all those thousands of personal details that made up the lifetimes of eight human individuals be so fast forgotten?

Frustratingly, oral tradition peters out almost immediately, unless hallowed in bardic recitations like those that were eventually written down by Homer, and even then the history is far from accurate. It decays into nonsense and falsehood after amazingly few generations. Historical facts about real heroes, villains, animals and volcanoes rapidly degenerate (or blossom, depending upon your taste) into myths about demigods, devils, centaurs and fire-breathing dragons.^* But oral traditions and their imperfections needn't detain us because, in any case, they have no equivalent in evolutionary history.

Writing is a huge improvement. Paper, papyrus and even stone tablets may wear out or decay, but written records have the potential to be copied accurately for an indefinite number of generations, although in practice the accuracy is not total. I should explain the special sense in which I mean accuracy and, indeed, the special sense in which I mean generations. If you handwrite me a message and I copy it and pass it on to a third person (the next copying ‘generation’), it will not be an exact replica, for my handwriting is different from yours. But if you write with care, and if I painstakingly match each of your squiggles with exactly one from our shared alphabet, your message has a good chance of being copied by me with total accuracy. In theory this accuracy could be preserved through an indefinite number of ‘generations’ of scribes. Given that there is a discrete alphabet agreed by writer and reader, copying lets a  {20}  message survive the destruction of the original. This property of writing can be called ‘self-normalising’. It works because letters of a true alphabet are discontinuous. The point, reminiscent of the distinction between analogue and digital codes, needs a little more explanation.

There exists a consonant sound which is intermediate between the English hard c and g (it is the French hard c in comme). But nobody would think of trying to represent this sound by writing a character which looked intermediate between c and g. We all understand that a written character in English must be one, and only one, member of our 26-letter alphabet. We understand that French uses the same 26 letters for sounds that are not exactly the same as ours and which may be intermediate between ours. Each language, indeed each local accent or dialect, separately uses the alphabet for self-normalising on different sounds.

Self-normalisation fights against the ‘Chinese Whispers’^* degrading of messages over generations. The same protection is not available to a drawing, copied and recopied along a line of imitative artists, unless the drawing style incorporates ritual conventions as its own version of ‘self-normalisation’. An eyewitness record of some event, which is written down, as opposed to drawn as a picture, has a good chance of still being accurately reproduced in history books centuries later. We have what is probably an accurate account of the destruction of Pompeii in 79 AD because a witness, Pliny the Younger, wrote down what he saw, in two epistles to the historian Tacitus, and some of Tacitus's writings survived, by successive copying and eventually printing, for us to read them today. Even in pre-Gutenberg days when documents were duplicated by scribes, writing represented a great advance in accuracy compared with memory and oral tradition.

It is only a theoretical ideal that repetitive copying retains perfect accuracy. In practice scribes are fallible, and not above massaging their copy to make it say things that they think (no doubt sincerely) the original document ought to have said. The most famous example of this, painstakingly documented by nineteenth century German theologians, is the doctoring of New Testament history to make it conform to Old Testament prophecies.^*

Quite apart from positive massaging, all repeated copying is subject to straightforward errors like skipping a line, or a word in a list. But in any case writing cannot take us back beyond its invention, which was only about 5,000 years ago. Identification symbols, counting-marks and pictures go back a bit further, perhaps some tens of thousands of years, but all such periods are chickenfeed compared with evolutionary time.

Fortunately, when we turn to evolution there is another kind of duplicated information which goes back an almost unimaginably large number of copying generations and which, with a little poetic licence, we can regard as the equivalent of a written text: a historical record that renews itself with astounding accuracy for hundreds of millions of generations precisely because, like our writing system, it has a self-normalising alphabet. The DNA information in all living creatures has been handed down from remote ancestors with prodigious fidelity. The individual atoms in DNA are turning over continually, but the  {21}  information that they encode in the pattern of their arrangement is copied for millions, sometimes hundreds of millions, of years. We can read this record directly, using the arts of modern molecular biology to spell out the actual DNA letter sequences or, slightly more indirectly, the amino acid sequences of protein into which they are translated. Or, much more indirectly as through a glass darkly, we can read it by studying the embryological products of the DNA: the shapes of bodies and their organs and chemistries. We don't need fossils to peer back into history. Because DNA changes very slowly through the generations, history is woven into the fabric of modern animals and plants, and inscribed in its coded characters.

DNA messages are written in a true alphabet. Like the Roman, Greek and Cyrillic writing systems, the DNA alphabet is a strictly limited repertoire of symbols with no self-evident meaning. Arbitrary symbols are chosen and combined to make meaningful messages of unlimited complexity and size. Where the English alphabet has 26 letters and the Greek one 24, the DNA alphabet is a four-letter alphabet. Most useful DNA spells out three-letter words from a dictionary limited to 64 words, each word called a ‘codon’. Some of the codons in the dictionary are synonymous with others, which is to say that the genetic code is technically ‘degenerate’.^*

The dictionary maps 64 code words onto 21 meanings — the 20 biological amino acids, plus one all-purpose punctuation mark. Human languages are numerous and changing, and their dictionaries contain tens of thousands of distinct words, but the 64-word DNA dictionary is universal and unchanging (with very minor variations in a few rare cases). The 20 amino acids are strung into sequences of typically a few hundred, each sequence a particular protein molecule. Whereas the number of letters is limited to four and the number of codons to 64, there is no theoretical limit to the number of proteins that can be spelled out by different sequences of codons. It is beyond all counting. A ‘sentence’ of codons specifying one protein molecule is an identifiable unit often called a gene. The genes are not separated from their neighbours (whether other genes or repetitive nonsense) by any delimiters apart from what can be read from their sequence. In this respect they resemble TELEGRAMS THAT LACK PUNCTUATION MARKS COMMA AND HAVE TO SPELL THEM OUT AS WORDS COMMA ALTHOUGH EVEN TELEGRAMS HAVE THE ADVANTAGE OF SPACES BETWEEN WORDS COMMA WHICH DNA LACKS STOP

DNA differs from written language in that islands of sense are separated by a sea of nonsense, never transcribed. ‘Whole’ genes are assembled, during transcription, from meaningful ‘exons’ separated by meaningless ‘introns’ whose texts are simply skipped by the reading apparatus. And even meaningful stretches of DNA are in many cases never read — presumably they are superseded copies of once useful genes that hang around like early drafts of a chapter on a cluttered hard disk. Indeed, the image of the genome as an old hard disk, badly in need of a spring clean, is one that will serve us from time to time during the book.

It bears repeating that the DNA molecules of long dead animals are not themselves preserved. The information in DNA can be preserved for ever, but  {22}  only by dint of frequent re-copying. The plot of Jurassic Park, though not silly, falls foul of practical facts. Conceivably, for a short while after becoming embalmed in amber, a bloodsucking insect could have contained the instructions needed to reconstruct a dinosaur. But unfortunately, after an organism is dead, the DNA in its body, and in blood that it has sucked, doesn't survive intact longer than a few years — only days in the case of some soft tissues. Fossilisation doesn't preserve DNA either.

Even deep freezing doesn't preserve it for very long. As I write this, scientists are excavating a frozen mammoth from the Siberian permafrost in the hope of extracting enough DNA to grow a new mammoth, cloned in the womb of a modern elephant. I fear this is a vain hope, though the mammoth is only a few thousand years dead. Among the oldest corpses from which readable DNA has been extracted is a Neanderthal man. Imagine the kerfuffle if somebody managed to clone him. But alas, only disjointed fragments of his 30,000-year-old DNA can be recovered. For plants in permafrost, the record is about 400,000 years.

The important point about DNA is that, as long as the chain of reproducing life is not broken, its coded information is copied to a new molecule before the old molecule is destroyed. In this form, DNA information far outlives its molecules. It is renewable — copied — and since the copies are literally perfect for most of its letters on any one occasion, it can potentially last an indefinitely long time. Large quantities of our ancestors’ DNA information survives completely unchanged, some even from hundreds of millions of years ago, preserved in successive generations of living bodies.

Understood in this way, the DNA record is an almost unbelievably rich gift to the historian. What historian could have dared hope for a world in which every single individual of every species carries, within its body, a long and detailed text: a written document handed down through time? Moreover, it has minor random changes, which occur seldom enough not to mess up the record yet often enough to furnish distinct labels. It is even better than that. The text is not just arbitrary. In Unweaving the Rainbow, I made a Darwinian case for regarding an animal's DNA as a ‘Genetic Book of the Dead’: a descriptive record of ancestral worlds. It follows from the fact of Darwinian evolution that everything about an animal or plant, including its bodily form, its inherited behaviour and the chemistry of its cells, is a coded message about the worlds in which its ancestors survived: the food they sought; the predators they escaped; the climates they endured; the mates they beguiled. The message is ultimately scripted in the DNA that fell through the succession of sieves that is natural selection. When we learn to read it properly, the DNA of a dolphin may one day confirm what we already know from the telltale giveaways in its anatomy and physiology: that its ancestors once lived on dry land. Three hundred million years earlier, the ancestors of all land-dwelling vertebrates, including the land-dwelling ancestors of dolphins, came out of the sea where they had lived since the origin of life. Doubtless our DNA records this fact if we could read it. Everything about a modern animal, especially its DNA, but its limbs and its heart, its brain and its breeding cycle too, can be regarded as an archive, a chronicle of its past, even if that chronicle is a palimpsest, many times overwritten.  {23} 

The DNA chronicle may be a gift to the historian, but it is a hard one to read, demanding deeply informed interpretation. It is made more powerful if combined with our third method of historical reconstruction, triangulation. It is to this that we now turn, and again we start with the analogous case of human history, specifically the history of languages.

TRIANGULATION

Linguists often wish to trace languages back through history. Where written records survive it is rather easy. The historical linguist can use the second of our two methods of reconstruction, tracing back renewed relics, in this case words. Modern English goes back via Middle English to Anglo-Saxon using the continuous literary tradition, through Shakespeare, Chaucer and Beowulf. But speech obviously goes back long before the invention of writing, and many languages have no written form anyway. For the earlier history of dead languages, linguists resort to a version of what I am calling triangulation. They compare modern languages and group them hierarchically into families within families. Romance, Germanic, Slavic, Celtic and other European language families are in turn grouped with some Indian language families into Indo-European. Linguists believe that ‘Proto-Indo-European’ was an actual language, spoken by a particular tribe around 6,000 years ago. They even aspire to reconstruct many of its details by extrapolating back from the shared features of its descendants. Other language families in other parts of the world, of equivalent rank to Indo-European, have been traced back in the same way, for instance Altaic, Dravidian and Uralic-Yukaghir. Some optimistic (and controversial) linguists believe they can go back even further, uniting such major families in an even more all-embracing family of families. In this way they have persuaded themselves that they can reconstruct elements of a hypothetical ur-language which they call Nostratic, and which they believe was spoken between 12,000 and 15,000 years ago.

Many linguists, while happy about Proto-Indo-European and other ancestral languages of equivalent rank, doubt the possibility of reconstructing a language as ancient as Nostratic. Their professional scepticism reinforces my own amateur incredulity. But there is no doubt at all that equivalent triangulation methods — various techniques for comparing modern organisms — work for evolutionary history, and can be used for penetrating back hundreds of millions of years. Even if we had no fossils, a sophisticated comparison of modern animals would permit a fair and plausible reconstruction of their ancestors. Just as a linguist penetrates the past to Proto-Indo-European, triangulating from modern languages and from already reconstructed dead languages, we can do the same with modern organisms, comparing either their external characteristics or their protein or DNA sequences. As the libraries of the world accumulate long and exact DNA listings from more and more modern species, the reliability of our triangulations will increase, particularly because DNA texts have such a large range of overlaps.  {24} 

Let me explain what I mean by ‘range of overlaps’. Even when taken from extremely distant relations, for example humans and bacteria, large sections of DNA still unequivocally resemble each other. And very close relations, such as humans and chimpanzees, have much more DNA in common. If you choose your molecules judiciously, there is a complete spectrum of steadily increasing proportions of shared DNA, all the way in between. Molecules can be chosen which, between them, span the gamut of comparison, from remote cousins like humans and bacteria, to close cousins like two species of frogs. Resemblances between languages are harder to discern, all except close pairs of languages like German and Dutch. The chain of reasoning that leads some hopeful linguists to Nostratic is tenuous enough to make the links the subject of scepticism on the part of other linguists. Would the DNA equivalent of triangulating to Nostratic be triangulation between, say, humans and bacteria? But humans and bacteria have some genes that have hardly changed at all since the common ancestor, their equivalent of Nostratic. And the genetic code itself is virtually identical in all species and must have been the same in the shared ancestors. One could say that the resemblance between German and Dutch is comparable to that between any pair of mammals. Human and chimpanzee DNA are so similar, they are like English spoken in two slightly different accents. The resemblance between English and Japanese, or between Spanish and Basque, is so slight that no pair of living organisms can be chosen for analogy, not even humans and bacteria. Humans and bacteria have DNA sequences which are so similar that whole paragraphs are word-for-word identical.

I have been talking about using DNA sequences for triangulation. In principle it works for gross morphological characters as well but, in the absence of molecular information, distant ancestors are about as elusive as Nostratic. With morphological characters, as with DNA, we assume that features shared by many descendants of an ancestor are likely (or at least slightly more likely than not) to have been inherited from that ancestor. All vertebrates have a backbone and we assume that they inherited it (strictly inherited the genes for growing it) from a remote ancestor which lived, the fossils suggest, more than half a billion years ago and also had a backbone. It is this sort of morphological triangulation that has been used to help imagine the bodily forms of concestors in this book. I would have preferred to rely more heavily upon triangulation using DNA directly, but our ability to predict how a change in a gene will change the morphology of an organism is inadequate to the task.

Triangulation is even more effective if we include many species. But for this we need sophisticated methods which rely on having an accurately constructed family tree. These methods will be explained in the Gibbon's Tale. Triangulation also lends itself to a technique for calculating the date of any evolutionary branch point you like. This is the ‘Molecular Clock’. Briefly, the method is to count discrepancies in molecular sequences between surviving species. Close cousins with recent common ancestors have fewer discrepancies than distant cousins, the age of the common ancestor being — or so it is hoped — proportional to the number of molecular discrepancies between their two descendants. Then we calibrate the arbitrary timescale of the molecular clock, translating it  {25}  into real years, by using fossils of known date for a few key branch-points where fossils happen to be available. In practice it isn't as simple as that, and the complications, difficulties and associated controversies will occupy the Epilogue to the Velvet Worm's Tale.

Chaucer's General Prologue introduced the complete cast of his pilgrimage, one by one. My cast list is much too large for that. In any case, the narrative itself is a long sequence of introductions — at the 40 rendezvous points. But one preliminary introduction is necessary, in a way that it wasn't for Chaucer. His cast list was a set of individuals. Mine is a set of groupings. The way we group animals and plants needs introducing. At Rendezvous 10, our pilgrimage is joined by some 2,000 species of rodents, plus 87 species of rabbits, hares and pikas, collectively called Glires. Species are grouped in hierarchically inclusive ways, and each grouping has a name of its own (the family of mouse-like rodents is called Muridae, and of squirrel-like rodents Sciuridae). And each category of grouping has a name. Muridae is a family, so is Sciuridae. Rodentia is the name of the order to which both belong. Glires is the superorder that unites rodents with rabbits and their kind. There is a hierarchy of such category names, family and order being somewhere in the middle of the hierarchy. Species lies near the bottom of the hierarchy. We work up through genus (plural genera), family, order, class, and phylum (plural phyla), with prefixes like sub- and super- offering scope for interpolation.

Species has a particular status, as we shall learn in the course of various tales. Every species has a unique scientific binomial, consisting of its genus name with an initial capital letter, followed by its species name with no initial capital, both printed in italics. The leopard (‘panther’), lion and tiger are all members of the genus Panthera: respectively Panthera pardus, Panthera leo and Panthera tigris, within the cat family, Felidae, which in turn is a member of the order Carnivora, the class Mammalia, the subphylum Vertebrata and the phylum Chordata. I shan't expatiate on the principles of taxonomy any further here, but will mention them, as necessary, during the book.

THE PILGRIMAGE BEGINS

It is time to set off on our pilgrimage to the past, which we can think of as a journey in a time machine in quest of our ancestors. Or more accurately, for reasons to be explained in the Neanderthal's Tale, in quest of our ancestral genes. For the first few tens of thousands of years of our backwards quest, our ancestral genes reside in individuals who look the same as us. Well, that is obviously not literally true, because we don't look exactly the same as each other. Let me rephrase it. For the first tens of thousands of years of our pilgrimage, the people we meet as we step outside our time machine will be no more different from us than we today are different from each other. Bear in mind that ‘we today’ includes Germans and Zulus, Pygmies and Chinese, Berbers and Melanesians. Our genetic ancestors of 50,000 years ago would have fallen within the same envelope of variability as we see around the world today.

If not biological evolution, then, what changes shall we see, as we go back through tens of millennia, as opposed to hundreds or thousands of millennia? There is an evolution-like process, orders of magnitude faster than biological evolution, which, in the early stages of our time machine's journey, will dominate the view from the porthole. This is variously called cultural evolution, exosomatic evolution or technological evolution. We notice it in the ‘evolution’ of the motor car, or of the necktie or of the English language. We mustn't overestimate its resemblance to biological evolution, and it will in any case not detain us long. We have a 4-billion-year road to run, and we shall soon have to set the time-machine into a gear too high to allow us more than a fleeting glimpse of events on the scale of human history.

But first, while our time machine is still in bottom gear, travelling on the timescale of human history rather than evolutionary history, a pair of tales about two major cultural advances. The Farmer's Tale is the story of the Agricultural Revolution, arguably the human innovation that has had the greatest repercussions for the rest of the world's organisms. And the Cro-Magnon's Tale is about the ‘Great Leap Forward’, that flowering of the human mind which, in a special sense, provided a new medium for the evolutionary process itself.  {27} 

The Farmer's Tale

The Agricultural Revolution began at the wane of the last Ice Age, about 10,000 years ago, in the so-called Fertile Crescent between the Tigris and the Euphrates. This is the cradle of human civilisation whose irreplaceable relics in the Baghdad Museum were vandalised in 2003, under the indifferent eyes of American invaders whose priorities led them to protect the Ministry of Oil instead. Agriculture also arose, probably independently, in China and along the banks of the Nile, and completely independently in the New World. An interesting case can be made for yet another independent cradle of agricultural civilisation in the astonishingly isolated highland interior of New Guinea. The Agricultural Revolution dates the start of the new stone age, the Neolithic.

The transition from wandering hunter-gatherers to a settled agricultural lifestyle may represent the first time people had a concept of a home. Contemporaries of the first farmers, in other parts of the world, were unreconstructed hunter-gatherers who wandered more or less continuously. Indeed, the hunter-gather lifestyle (‘hunter’ can include fisher) has not died out. It is still practised in pockets around the world: by Australian Aborigines, by San and related tribes in Southern Africa (wrongly called ‘bushmen’), by various Native American tribes (called ‘Indians’ after a navigational error), and by the Inuit of the Arctic (who prefer not to be called Eskimos). Hunter-gatherers typically do not cultivate plants and do not keep livestock. In practice all intermediates between pure hunter-gatherers and pure agriculturalists or pastoralists are found. But, earlier than about 10,000 years ago, all human populations were hunter-gatherers. Soon, probably none will be. Those not extinct will be ‘civilised’ — or corrupted, depending on your point of view.

Colin Tudge, in his little book Neanderthals, Bandits and Farmers: How Agriculture Really Began, agrees with Jared Diamond (The Third Chimpanzee) that the switch to agriculture from hunting and gathering was by no means the improvement we, in our complacent hindsight, might think. The Agricultural Revolution did not, in their view, increase human happiness. Agriculture supported larger populations than the hunter-gather lifestyle that it superseded, but not in obviously improved health or happiness. In fact, larger populations generally harbour more vicious diseases, for sound evolutionary reasons (a parasite is less concerned to prolong the life of its present host if it can easily find new victims to infect).

Nevertheless, our situation as hunter-gatherers cannot have been a Utopia either. It has lately become fashionable to regard hunter-gatherers and primitive^* agricultural societies as more ‘in balance’ with nature than us. This is probably a mistake. They may well have had greater knowledge of the wild, simply because they lived and survived in it. But, like us, they seem to have used their knowledge to exploit (and often overexploit) the environment to the best of their abilities at the time. Jared Diamond emphasises overexploitation by early agriculturalists leading to ecological collapse, and the demise of their society. Far from being in balance with nature, pre-agricultural hunter-gatherers were probably responsible for widespread extinctions of many large  {28}  animals around the globe. Just prior to the Agricultural Revolution, the colonisation of remote areas by hunter-gatherer peoples is suspiciously often followed in the archaeological record by the wiping out of many large (and presumably palatable) birds and mammals.

We tend to regard ‘urban’ as the antithesis of ‘agricultural’ but, in the longer perspective that this book must adopt, city dwellers should be lumped in with farmers as opposed to hunter-gatherers. Almost all the food of a town comes from owned and cultivated land — in ancient times from fields round about the town, in modern times from anywhere in the world, transported and sold on through middlemen before being consumed. The Agricultural Revolution soon led to specialisation. Potters, weavers and smiths traded their skills for food which others grew. Before the Agricultural Revolution, food was not cultivated on owned land but captured or gathered on unowned commons. Pastoralism, the herding of animals on common land, may have been an intermediate stage.

Whether it was a change for better or worse, the Agricultural Revolution was presumably not a sudden event. Husbandry was not the overnight brainwave of a genius, the neolithic equivalent of Turnip Townsend. To begin with, hunters of wild animals in open and unowned country might have guarded hunting territories against rival hunters, or guarded the herds themselves while following them about. From there it was a natural progression to herding them; then feeding them, and finally corralling and housing them. I dare say none of these changes would have seemed revolutionary when they happened.

Meanwhile the animals themselves were evolving — becoming ‘domesticated’ by rudimentary forms of artificial selection. The Darwinian consequences on the animals would have been gradual. Without any deliberate intention to breed ‘for’ domestic tractability, our ancestors inadvertently changed the selection pressures on the animals. Within the gene pools of the herds, there would no longer be a premium on fleetness or other survival skills of the wild. Successive generations of domestic animals became tamer, less able to fend for themselves, more apt to flourish and grow fat under feather-bedded domestic conditions. There are alluring parallels in the domestication, by social ants and termites, of aphid ‘cattle’ and fungus ‘crops’. We shall hear about these in the Leaf Cutter's Tale, when the ant pilgrims join us at Rendezvous 26.

Unlike modern plant and animal breeders, our forebears of the Agricultural Revolution would not knowingly have practised artificial selection for desirable characteristics. I doubt if they realised that, in order to increase milk yield, you have to mate high-yielding cows with bulls born to other high-yielding cows, and discard the calves of low-yielders. Some idea of the accidental genetic consequences of domestication is given by some interesting Russian work on silver foxes.

D. K. Belyaev and his colleagues took captive silver foxes, Vulpes vulpes, and set out systematically to breed for tameness. They succeeded, dramatically. By mating together the tamest individuals of each generation, Belyaev had, within 20 years, produced foxes that behaved like border collies, actively seeking human company and wagging their tails when approached. That is not very surprising, although the speed with which it happened may be. Less expected  {29}  were the by-products of selection for tameness. These genetically tamed foxes not only behaved like collies, they looked like collies. They grew black-and-white coats, with white face patches and muzzles. Instead of the characteristic pricked ears of a wild fox, they developed ‘lovable’ floppy ears. Their reproductive hormone balance changed, and they assumed the habit of breeding all the year round instead of in a breeding season. Probably associated with their lowered aggression, they were found to contain higher levels of the neurally active chemical serotonin. It took only 20 years to turn foxes into ‘dogs’ by artificial selection.^*

I put ‘dogs’ in inverted commas, because our domestic dogs are not descended from foxes, they are descended from wolves. Incidentally, Konrad Lorenz's well-known speculation that only some breeds of dog (his favourites such as chow chows) are derived from wolves, the rest from jackals is now known to be wrong. He supported his theory with insightful anecdotes on temperament and behaviour. But molecular taxonomy trumps human insight, and molecular evidence clearly shows that all modern breeds of dog are descended from the grey wolf, Canis lupus. The next closest relatives to dogs (and wolves) are coyotes, and Simien ‘jackals’ (which it now seems should be called Simien wolves). True jackals (golden, side-striped and black-backed jackals) are more distantly related, although they are still placed in the genus Canis.

No doubt the original story of the evolution of dogs from wolves was similar to the new one simulated by Belyaev with foxes, with the difference that Belyaev was breeding for tameness deliberately. Our ancestors did it inadvertently, and it probably happened several times, independently in different parts of the world. Perhaps initially, wolves took to scavenging around human encampments. Humans may have found such scavengers a convenient means of refuse disposal, and they may also have valued them as watchdogs, and even as warm sleep comforters. If this amicable scenario sounds surprising, reflect that the medieval legend of wolves as mythic symbols of terror coming out of the forest was born of ignorance. Our wild ancestors, living in more open country, would have known better. Indeed, they evidently did know better, because they ended up domesticating the wolf, thereby making the loyal, trusted dog.

From the wolfs point of view human camps provided rich pickings for a scavenger, and the individuals most likely to benefit were those whose serotonin levels and other brain characteristics (‘propensity to tameness’) happened to make them feel at home with humans. Several writers have speculated, plausibly enough, about orphaned cubs being adopted as pets by children. Experiments have shown that domestic dogs are better than wolves at ‘reading’ the expressions on human faces. This is presumably an inadvertent consequence of our mutualistic evolution over many generations. At the same time we read their faces, and dog facial expressions have become more human-like than those of wolves, because of inadvertent selection by humans. This is presumably why we think wolves look sinister while dogs look loving, guilty, soppy and so on.

A distant parallel is the case of the Japanese ‘samurai crabs’. These wild crabs have a pattern on their back which resembles the face of a Samurai warrior. The Darwinian theory to account for this is that superstitious fishermen tossed back  {30}  into the sea individual crabs that slightly resembled a Samurai warrior. Over the generations, as genes for resembling a human face were more likely to survive in the bodies of ‘their’ crabs, the frequency of such genes increased in the population until today it is the norm. Whether that story of wild crabs is true or not, something like it surely went on in the evolution of truly domesticated animals.

Back to the Russian fox experiment, which demonstrates the speed with which domestication can happen, and the likelihood that a train of incidental effects would follow in the wake of selection for tameness. It is entirely probable that cattle, pigs, horses, sheep, goats, chickens, geese, ducks and camels followed a course which was just as fast, and just as rich in unexpected side-effects. It also seems plausible that we ourselves evolved down a parallel road of domestication after the Agricultural Revolution, towards our own version of tameness and associated by-product traits.

In some cases, the story of our own domestication is clearly written in our genes. The classic example, meticulously documented by William Durham in his book Coevolution, is lactose tolerance. Milk is baby food, not ‘intended’ for adults and, originally, not good for them. Lactose, the sugar in milk, requires a particular enzyme, lactase, to digest it. (This terminological convention is worth remembering, by the way. An enzyme's name will often be constructed by adding ‘-ase’ to the first part of the name of the substance on which it works.) Young mammals switch off the gene that produces lactase after they pass the age of normal weaning. It isn't that they lack the gene, of course. Genes needed only in childhood are not removed from the genome, not even in butterflies, which must carry large numbers of genes needed only for making caterpillars. But lactase production is switched off in human infants at the age of about four, under the influence of other, controlling genes. Fresh milk makes adults feel ill, with symptoms ranging from flatulence and intestinal cramps to diarrhoea and vomiting.

All adults? No, of course not. There are exceptions. I am one of them, and there is a good chance that you are too. My generalisation concerned the human species as a whole and, by implication, the wild Homo sapiens from which we are all descended. It is as if I had said ‘Wolves are big, fierce carnivores that hunt in packs and bay at the moon’, knowing full well that Pekineses and Yorkshire terriers belie it. The difference is that we have a separate word, dog, for domestic wolf, but not for domestic human. The genes of domestic animals have changed as a result of generations of contact with humanity, inadvertently following the same sort of course as the genes of the silver fox. The genes of (some) humans have changed as a result of generations of contact with domestic animals. Lactose tolerance seems to have evolved in a minority of tribes including the Tutsi of Rwanda (and, to a lesser extent, their traditional enemies the Hutu), the pastoral Fulani of West Africa (though, interestingly, not the sedentary branch of the Fulani), the Sindhi of North India, the Tuareg of West Africa, the Beja of Eastern North Africa, and some European tribes from which I, and possibly you, are descended. Significantly, what these tribes have in common is a history of pastoralism.

At the other end of the spectrum, peoples who have retained the normal  {31}  human intolerance of lactose as adults include Chinese, Japanese, Inuit, most Native Americans, Javanese, Fijians, Australian Aborigines, Iranians, Lebanese, Turks, Tamils, Singhalese, Tunisians, and many African tribes including the San, and the Tswanas, Zulus, Xhosas and Swazis of southern Africa, the Dinkas and Nuers of North Africa, and the Yorubas and Igbos of West Africa. In general, these lactose-intolerant peoples do not have a history of pastoralism. There are instructive exceptions. The traditional diet of the Masai of East Africa consists of little else besides milk and blood, and you might think they'd be particularly tolerant of lactose. This is not the case, however, probably because they curdle their milk before consuming it. As with cheese, the lactose is largely removed by bacteria. That's one way of getting rid of its bad effects — get rid of the stuff itself. The other way is to change your genes. This happened in the other pastoral tribes listed above.

Of course nobody deliberately changes their genes. Science is only now beginning to work out how to do that. As usual, the job was done for us by natural selection, and it happened millennia ago. I don't know exactly by what route natural selection produced adult lactose tolerance. Perhaps adults resorted to baby food in times of desperation, and the individuals that were most tolerant of it survived better. Perhaps some cultures postponed weaning, and selection for survival of children under these conditions spilled over gradually into adult tolerance. Whatever the details, the change, though genetic, was culture-driven. The evolution of tameness and increasing milk yields in cattle, sheep and goats paralleled that of lactose tolerance in the tribes that herded them. Both were true evolutionary trends in that they were changes in gene frequencies in populations. But both were driven by non-genetic cultural changes.

Is lactose-tolerance just the tip of the iceberg? Are our genomes riddled with evidences of domestication, affecting not just our biochemistry but our minds? Like Belyaev's domesticated foxes, and like the domesticated wolves that we call dogs, have we become tamer, more lovable, with the human equivalents of floppy ears, soppy faces and wagging tails? I leave you with the thought, and move hastily on.

While hunting was sliding into herding, gathering presumably followed a similar slide into cultivation of plants. Again, it was probably mostly inadvertent. No doubt there were moments of creative discovery, as when people first noticed that if you put seeds in the ground they make plants like those from which they came. Or when somebody first observed that it helps to water them, weed them and manure them. It was probably more difficult to work out that it might be a good idea to keep back the best seed for planting, rather than follow the obvious course of eating the best and planting the dross (my father, as a young man fresh out of college, taught agriculture to peasant farmers in central Africa in the 1940s, and he tells me that this was one of the hardest lessons to get across). But mostly the transition from gatherer to cultivator passed unnoticed by those concerned, like the transition from hunter to herder.

Many of our staple food crops, including wheat, oats, barley, rye and maize, are members of the grass family which have become greatly modified since the dawn of agriculture by inadvertent and later deliberate human selection. It is  {32}  possible that we too have become genetically modified over the millennia to increase our tolerance of cereals, in a way parallel to our evolution of tolerance to milk. Starchy cereals such as wheat and oats cannot have featured prominently in our diets before the Agricultural Revolution. Unlike oranges and strawberries, cereal seeds do not ‘want’ to be eaten. Passing through an animal's digestive tract is no part of their dispersal strategy, as it is of plum and tomato seeds. On our side of the relationship, the human digestive tract is not able, unaided, to absorb much nutriment from seeds of the grass family, with their meagre starch reserves and hard, unsympathetic husks. Some aid comes from milling and cooking, but it also seems conceivable that, in parallel with the evolution of tolerance to milk, we might have evolved an increased physiological tolerance to wheat, compared to our wild ancestors. Wheat intolerance is a known problem for a substantial number of unfortunate individuals who discover, by painful experience, that they are happier if they avoid it. A comparison of the incidence of wheat intolerance in hunter-gatherers such as the San, and other peoples whose agricultural ancestors have long eaten wheat, might be revealing. If there has been a large comparative study of wheat tolerance, like the one that has been made of lactose tolerance across different tribes, I am unaware of it. A systematic comparative study of alcohol intolerance, too, would be interesting. It is known that certain genetic alleles make our livers less capable of breaking down alcohol than we might wish.

In any case, co-evolution between animals and their food plants was nothing new. Grazing animals had been exerting a kind of benevolent Darwinian selection on grasses, guiding their evolution towards mutualistic co-operation, for millions of years before we started domesticating wheat, barley, oats, rye and maize. Grasses flourish in the presence of grazers, and they probably have been doing so for most of the 20 million years since their pollens first announce them in the fossil record. It is not, of course, that individual plants actually benefit by being eaten, but that grasses can withstand being cropped better than rival plants can. My enemy's enemy is my friend, and grasses, even when grazed, thrive when herbivores eat (along with the grasses themselves) other plants that would compete for soil, sun and water. Grasses became ever more able to thrive in the presence of wild cattle, antelopes, horses and other grazers (and eventually lawnmowers), as the millions of years went by. And the herbivores became better equipped, for example with specialised teeth, and complicated digestive tracts including fermentation vats with cultures of micro-organisms, to flourish on a diet of grass.

This isn't what we ordinarily mean by domestication, but in effect it is not far from it. When, starting about 10,000 years ago, wild grasses of the genus Triticum were domesticated by our ancestors into what we now call wheat, it was, in a way, a continuation of what herbivores of many kinds had been doing to the ancestors of Triticum for 20 million years. Our ancestors accelerated the process, especially when we later switched from inadvertent, accidental domestication to deliberate, planned selective breeding (and very recently scientific hybridisation and genetically engineered mutations).

That is all I want to say about the origins of agriculture. Now, as our time  {33}  machine leaves the 10,000-year mark and heads for Rendezvous 0, we briefly pause, one more time, around 40,000 years ago. Here human society, entirely consisting of hunter-gatherers, underwent what may have been an even larger revolution than the agricultural one, the ‘cultural Great Leap Forward’. The tale of the Great Leap Forward will be told by Cro-Magnon Man, named after the cave in the Dordogne where fossils of this race of Homo sapiens were first discovered.

The Cro-Magnon's Tale

Archaeology suggests that something very special began to happen to our species around 40,000 years ago. Anatomically, our ancestors who lived before this watershed date were the same as those who came later. Humans sampled earlier than the watershed would be no more different from us than they were from their own contemporaries in other parts of the world, or indeed than we are from our contemporaries. That's if you look at their anatomy. If you look at their culture, there is a huge difference. Of course there are also huge differences between the cultures of different peoples across the world today, and probably then too. But this wasn't true if we go back much more than 40,000 years. Something happened then — many archaeologists regard it as sudden enough to be called an ‘event’. I like Jared Diamond's name for it, the Great Leap Forward.

Earlier than the Great Leap Forward, man-made artefacts had hardly changed for a million years. The ones that survive for us are almost entirely stone tools and weapons, quite crudely shaped. Doubtless wood (or, in Asia, bamboo) was a more frequently worked material, but wooden relics don't easily survive. As far as we can tell, there were no paintings, no carvings, no figurines, no grave goods, no ornamentation. After the Leap, all these things suddenly appear in the archaeological record, together with musical instruments such as bone flutes, and it wasn't long before stunning creations like the Lascaux Cave murals were created by Cro-Magnon people. A disinterested observer taking the long view from another planet might see our modern culture, with its computers, supersonic planes and space exploration, as an afterthought to the Great Leap Forward. On the very long geological timescale, all our modern achievements, from the Sistine Chapel to Special Relativity, from the Goldberg Variations to the Goldbach Conjecture, could be seen as almost contemporaneous with the Venus of Willendorf and the Lascaux Caves, all part of the same cultural revolution, all part of the blooming cultural upsurge that succeeded the long Lower Palaeolithic stagnation. Actually I'm not sure that our extraplanetary observer's uniformitarian view would stand up to much searching analysis, but it could be at least briefly defended.

David Lewis-Williams's The Mind in the Cave considers the whole question of Upper Paleolithic cave art, and what it can tell us about the flowering of consciousness in Homo sapiens.

Some authorities are so impressed by the Great Leap Forward that they think

Something very special began to happen... This painting of a bull is one of the most striking images from the Lascaux Caves in the Dordogne, France. Discovered in 1940, the paintings, which include a variety of animals, are over 16,000 years old. They show a deep understanding of animal forms and movement, and a fine artistic sense. The purpose of the paintings is unknown.

it coincided with the origin of language. What else, they ask, could account for such a sudden change? It is not as silly as it sounds to suggest that language arose suddenly. Nobody thinks writing goes back more than a few thousand years, and everyone agrees that brain anatomy didn't change to coincide with anything so recent as the invention of writing. In theory, speech could be another example of the same thing. Nevertheless, my hunch, supported by the authority of linguists such as Steven Pinker, is that language is older than the Leap. We'll come back to the point a million years further into the past, when our pilgrimage reaches Homo ergaster (erectus).

If not language itself, perhaps the Great Leap Forward coincided with the sudden discovery of what we might call a new software technique: maybe a new trick of grammar, such as the conditional clause, which, at a stroke, would have enabled ‘what if’ imagination to flower. Or maybe early language, before the leap, could be used to talk only about things that were there, on the scene. Perhaps some forgotten genius realised the possibility of using words referentially as tokens of things that were not immediately present. It is the difference between ‘That waterhole which we can both see’ and ‘Suppose there was a water-hole the other side of the hill’. Or perhaps representational art, which is all but unknown in the archaeological record before the Leap, was the bridge to referential language. Perhaps people learned to draw bison, before they learned to talk about bison that were not immediately visible.

Much as I would like to linger around the heady time of the Great Leap Forward, we have a long pilgrimage to accomplish and we must press on backwards. We are approaching the point where we can start looking for Concestor 0, the most recent ancestor of all surviving humans.

Rotate 90 degrees

HUMANKIND A stylised impression of the human family tree. It is not intended as an accurate depiction — the real tree would be unmanageably dense. Moving down the page means going back in time, with the geological timescale (see page 18) given by the coloured bar on the right. White lines illustrate patterns of interbreeding, with lots of it within continents and occasional migration between them. The numbered circle marks Concestor 0, the most recent common ancestor of all living humans. Verify this by following routes upwards from Concestor 0: you can reach any of the modern-day-human end points.

RENDEZVOUS 0 ALL HUMANKIND

The Human Genome Project has reached completion, hailed by a justly proud humanity. We might pardonably wonder whose genome has been sequenced. Has an illustrious dignitary been singled out for the honour, or is it a random nobody pulled off the street, or even an anonymous clone of cells from a tissue culture lab? It makes a difference because we vary. I have brown eyes while you, perhaps, have blue. I can't curl my tongue into a tube, whereas it's 50/50 that you can. Which version of the tongue-curling gene makes it into the published human genome? What is the canonical eye colour?

I raise the question only to draw a parallel. This book traces ‘our’ ancestors back through time, but whose ancestors are we talking about: yours or mine, a Bambuti Pygmy's or a Torres Strait Islander's? I shall come to the question presently. But first, having raised the analogous question about the Human Genome Project, I can't just leave it dangling. Whose genome is chosen for analysis? In the case of the ‘official’ Human Genome Project the answer is that, for the low percentage of DNA letters that vary, the canonical genome is the majority ‘vote’ among a couple of hundred people chosen to give a good spread of racial diversity. In the case of the rival project initiated by Dr Craig Venter, the genome analysed was mostly that of... Dr Craig Venter. This was announced by the man himself,^* to the mild consternation of the ethics committee which had recommended, for all sorts of warm and worthy reasons, that the donors should be anonymous and drawn from a spread of different races. There are other projects for the study of human genetic diversity itself, which, bizarrely, come under recurrent political attack as though it were somehow improper to admit that humans vary. Thank goodness we do, if not very much.

But now, to our backwards pilgrimage. Whose ancestors are we going to trace? If we go sufficiently far back, everybody's ancestors are shared. All your ancestors are mine, whoever you are, and all mine are yours. Not just approximately but literally. This is one of those truths that turns out, on reflection, to need no new evidence. We prove it by pure reason, using the mathematician's trick of reductio ad absurdum. Take our imaginary time machine absurdly far back, say 100 million years, to an age when our ancestors resembled shrews or opossums. Somewhere in the world at that ancient date, at least one of my personal ancestors must have been living, or I wouldn't be here. Let us call this particular little mammal Henry (it happens to be a family name). We seek to prove that if Henry is my ancestor he must be yours too. Imagine, for a moment, the contrary: I am descended from Henry and you are not. For this to be so, your  {36}  lineage and mine would have to have marched, side by side yet never touching, through 100 million years of evolution to the present, never interbreeding yet ending up at the same evolutionary destination — so alike that your relatives are still capable of interbreeding with mine. This reductio is clearly absurd. If Henry is my ancestor he has to be yours too. If not mine, he cannot be yours.

Without specifying how ancient is ‘sufficiently’, we have just proved that a sufficiently ancient individual with any human descendants at all must be an ancestor of the entire human race. Long-distance ancestry, of a particular group of descendants such as the human species, is an all-or-nothing affair. Moreover, it is perfectly possible that Henry is my ancestor (and necessarily yours, given that you are human enough to be reading this book) while his brother Eric is the ancestor of, say, all the surviving aardvarks. Not only is it possible. It is a remarkable fact that there must be a moment in history when there were two animals in the same species, one of whom became the ancestor of all humans and no aardvarks, while the other became the ancestor of all aardvarks and no humans. They may well have met, and may even have been brothers. You can cross out aardvark and substitute any other modern species you like, and the statement must still be true. Think it through, and you will find that it follows from the fact that all species are cousins of one another. Bear in mind when you do so that the ‘ancestor of all aardvarks’ will also be the ancestor of lots of very different things besides aardvarks (in this case, the entire major group called Afrotheria which we shall meet at Rendezvous 13, and which includes elephants and dugongs, hyraxes and Madagascan tenrecs).

My reasoning was constructed as a reductio ad absurdum. It assumed that ‘Henry’ lived long enough ago for it to be obvious that he begat either all living humans, or none. How long is long enough? That's a harder question. A hundred million years is more than enough to assure the conclusion we seek. If we go back only a hundred years, no individual can claim the entire human race as direct descendants. Between the obvious cases of 100 years and 100 million, what can we say about unobvious intermediates such as 10,000, 100,000 or 1 million years? The precise calculations were beyond me when I explained this reductio in River Out of Eden but, happily, a Yale University statistician called Joseph T. Chang has now made a start on them. His conclusions and their implications form the Tasmanian's Tale, a tale of particular relevance to this rendezvous because Concestor 0 is the most recent common ancestor of all living humans. It is more elaborate versions of calculations like Chang's that we need to do in order to date Rendezvous 0.

Rendezvous 0 is the time when, on our backwards pilgrimage, we first meet a common human ancestor. But according to our reductio there is a point further in the past when every individual that we encounter with our time machine is either a common ancestor or no ancestor at all. And although no one ancestor can be singled out for attention at this more distant milestone, it is worth a nod as we go by, because it marks the point where we can stop worrying about whether it is your ancestors we trace or mine: from that milestone on, all my readers march, shoulder to shoulder, in a phalanx of pilgrims towards the past.  {38} 

The Tasmanian's Tale (written with Yan Wong)

Tracing ancestors is a beguiling pastime. As with history itself, there are two methods. You can go backwards, listing your two parents, four grandparents, eight great-grandparents, and so on. Or you can pick a distant ancestor and go forwards, listing his children, grandchildren, great-grandchildren, until you end up with yourself. Amateur genealogists do both, going back and forth between generations until they have filled in the tree as far as parish registers and family Bibles allow. This tale, like the book as a whole, uses the backwards method.

Pick any two people and go backwards and, sooner or later, we hit a most recent common ancestor — MRCA. You and me, the plumber and the queen, any set of us must converge on a single concestor (or couple). But unless we pick close relatives, finding the concestor requires a vast family tree, and most of it will be unknown. This applies a fortiori to the concestor of all humans alive today. Dating Concestor 0, the most recent common ancestor of all living humans, is not a task that can be undertaken by a practising genealogist. It is a task in estimation: a task for a mathematician.

An applied mathematician tries to understand the real world by setting up a simplified version of it — a ‘model’. The model eases thought, while not losing all power to illuminate reality. Sometimes a model gives us a baseline, departures from which elucidate the real world.

In framing a mathematical model to date the common ancestors of all surviving humans, a good simplifying assumption — a sort of toy world — is a breeding population of fixed and constant size, living on an island with no immigration or emigration. Let it be an idealised population of Tasmanian aboriginals, in happier times before they were exterminated as agricultural vermin by nineteenth-century settlers. The last pure-bred Tasmanian, Truganinni, died in 1876, soon after her friend ‘King Billy’ whose scrotum was made into a tobacco pouch (shades of Nazi lamps). The Tasmanian aboriginals were isolated some 13,000 years ago when land bridges to Australia were flooded by rising sea levels, and they then saw no outsiders until they saw them with a vengeance in their nineteenth-century holocaust. For our modelling purposes, we consider Tasmania to be perfectly isolated from the rest of the world for 13,000 years until 1800. Our notional ‘present’, for modelling purposes, will be defined as l800 AD.

The next step is to model the mating pattern. In the real world people fall in love, or into arranged marriages, but here we are modellers, ruthlessly replacing human detail by tractable mathematics. There's more than one mating model we could imagine. The random diffusion model has men and women behaving as particles diffusing outwards from their birthplace, more likely to bump into near than distant neighbours. An even simpler and less realistic model is the random mating model. Here, we forget about distance altogether and simply assume that, strictly within the island, mating between any male and any female is equally likely.

Of course neither model is remotely plausible. Random diffusion assumes  {39}  that people walk in any direction from their starting point. In reality there are paths or roads which guide their feet: narrow gene conduits through the island's forests and grasslands. The random mating model is even more unrealistic. Never mind. We set up models to see what happens under ideally simplified conditions. It can be surprising. Then we have to consider whether the real world is more surprising or less, and in which directions.

Joseph Chang, following a long tradition of mathematical geneticists, opted for random mating. His model ignored population size by assuming it constant. He did not deal with Tasmania in particular but we shall assume, again as a calculated oversimplification, that our toy population remained constant at 5,000, which is one estimate for Tasmania's aboriginal population in 1800 before the massacres began. I must repeat that such simplifications are of the essence in mathematical modelling: not a weakness of the method but, for certain purposes, a strength. Chang of course doesn't believe people mate at random, any more than Euclid believed lines have no breadth. We follow abstract assumptions to see where they lead, and then decide whether the detailed differences from the real world matter.

So, how many generations would you have to go back, in order to be reasonably sure of finding an individual who was ancestor to everybody alive in the present? The calculated answer from the abstract model is the logarithm (base 2) of the population size. The base 2 logarithm of a number is the number of times you have to multiply 2 by itself to get that number. To get 5,000, you need to multiply 2 by itself about 12.3 times so, for our Tasmanian example, theory tells us to go back 12.3 generations to find the concestor. Assuming four generations per century, this is less than four centuries. It's even less if people reproduce younger than 25.

I give the name ‘Chang One’ to the date of the most recent common ancestor of some specified population. Continuing backwards from Chang One, it doesn't take long before we hit the point — I shall call it ‘Chang Two’ — at which everybody is either a common ancestor or has no surviving descendants. Only during the brief interregnum between Chang One and Chang Two does there exist an intermediate category of people who have some surviving descendants but are not common ancestors of everybody. A surprising deduction is that at Chang Two a large number of people are universal ancestors: about 80 per cent of individuals in any generation will in theory be ancestors of everybody alive in the distant future.

As for the timing, well, the mathematics yield the result that Chang Two is approximately 1.77 times older than Chang One. 1.77 times 12.3 gives just under 22 generations, between five and six centuries. As we ride our time machine backwards in Tasmania, therefore, around the time of Geoffrey Chaucer in England we enter ‘all or nothing’ territory. From there on backwards, to the time when Tasmania was joined to Australia and all bets are off, everyone our time machine encounters will have either the entire population as descendants or no descendants at all.

I don't know about you, but I find these calculated dates astonishingly recent. What's more, the conclusions don't change much if you assume a larger  {40}  population. Taking a model population the size of Britain's today, 60 million, we still need to go back only 23 generations to reach Chang One and our youngest universal ancestor. If the model applied to Britain, Chang Two, when everybody is either the ancestor of all modern British people or of none, is only about 40 generations ago, or about 1000 AD. If the assumptions of the model are true (of course they aren't) King Alfred the Great is the ancestor of either all today's British or none.

I must repeat the cautions with which I began. There are all sorts of differences between ‘model’ and ‘real’ populations, in Britain or Tasmania or anywhere else. Britain's population has climbed steeply in historical time to reach its present size, and that completely changes the calculations. In any real population, people don't mate at random. They favour their own tribe, language group or local area, and of course they all have individual preferences. Britain's history adds the complication that, although a geographical island, its population is far from isolated. Waves of external immigrants have swept in from Europe over the centuries: Romans, Saxons, Danes, and Normans among them.

If Tasmania and Britain are islands, the world is a larger ‘island’ since it has no immigration or emigration (give or take alien abductions in flying saucers). But it is imperfectly subdivided into continents and smaller islands, with not just seas but mountain ranges, rivers and deserts impeding the movement of people to varying degrees. Complicated departures from random mating confound our calculations, not just slightly but grossly. The present population of the world is 6 billion, but it would be absurd to look up the logarithm of 6 billion, multiply it by 1.77 and swallow the resulting 500 AD as the date of Rendezvous o! The real date is older, if only because pockets of humanity have been separated far longer than the orders of magnitude we are now calculating. If an island has been isolated for 13,000 years, as Tasmania was, it is impossible for the human race as a whole to have a universal ancestor younger than 13,000 years. Even partial isolation of sub-populations plays havoc with our all-too-tidy calculations, as does any kind of non-random mating.

The date when the most isolated island population in the world became isolated sets a lower bound on the date of Rendezvous 0. But to take this lower bound seriously, isolation must be absolute. This follows from the calculated figure of 80 per cent that we met earlier. A single migrant to Tasmania, once he has been sufficiently accepted into society to reproduce normally, has an 80 per cent chance of eventually becoming a common ancestor to all Tasmanians. So even tiny amounts of migration are enough to graft the family tree of an otherwise isolated population to that of the mainland. The timing of Rendezvous 0 is likely to depend on the date at which the most isolated pocket of humanity became completely isolated from its neighbour, plus the date at which its neighbour then became completely isolated from its neighbour, and so on. A few island hops may be needed before we can join all the family trees together, but it is then an insignificant number of centuries back until we tumble upon Concestor 0. That would put Rendezvous 0 some tens of thousands of years ago, conceivably somewhere in the low hundreds of thousands, no more.

As to where Rendezvous 0 took place, this is almost as surprising. You might  {41}  be inclined to think of Africa, as was my initial reaction. Africa houses the deepest genetic divides within humankind, so it seems a logical place to look for a common ancestor of all living humans. It has been well said that if you wiped out sub-Saharan Africa you would lose the great majority of human genetic diversity, whereas you could wipe out everywhere except Africa and nothing much would change. Nevertheless Concestor 0 may well have lived outside Africa. Concestor 0 is the most recent common ancestor that unites the most geographically isolated population — Tasmania for the sake of argument — with the rest of the world. If we assume that populations throughout the rest of the world, including Africa, indulged in at least some interbreeding during a long period when Tasmania was totally isolated, the logic of Chang's calculations could lead us to suspect that Concestor 0 lived outside Africa, near the take-off point for the migrants whose offspring became Tasmanian immigrants. Yet African groups still retain most of humanity's genetic diversity. This seeming paradox is resolved in the next tale, when we explore family trees of genes rather than of people.

Our surprising conclusion is that Concestor 0 probably lived tens of thousands of years ago, and very possibly not even in Africa. Other species too may generally have quite recent common ancestors. But this is not the only part of the Tasmanian's Tale that forces us to examine biological ideas in a new light. To professional Darwinian specialists, it seems a paradox that 80 per cent of a population will become universal ancestors. Let me explain. We are used to thinking of individual organisms as striving to maximise a quantity called fitness’. Exactly what fitness means is disputed. One favoured approximation is ‘total number of children’. Another is ‘total number of grandchildren’, but there is no obvious reason to stop at grandchildren, and many authorities prefer to say something like ‘total number of descendants alive at some distant date in the future’. But we seem to have a problem if, in our theoretically idealised population in the absence of natural selection, 80 per cent of the population can expect to have the maximum possible ‘fitness’: that is, they can expect to claim the entire population as their descendants! This matters for Darwinians because they widely presume that ‘fitness’ is what all animals constantly struggle to maximise.

I have long argued that the only reason an organism behaves as a quasi-purposeful entity at all — an entity capable of maximising anything — is that it is built by genes that have survived through past generations. There is a temptation to personify and impute intention: to turn ‘gene survival in the past’ into something like ‘intention to reproduce in the future’. Or ‘individual intention to have lots of descendants in the future’. Such personification can also apply to genes: we are tempted to see genes as influencing individual bodies to behave in such a way as to increase the number of future copies of those same genes.

Scientists who use such language, whether at the level of the individual or the gene, know very well that it is only a figure of speech. Genes are just DNA molecules. You'd have to be barking mad to think that ‘selfish’ genes really have deliberate intentions to survive! We can always translate back into respectable language: the world becomes full of those genes that have survived in the past.  {42}  Because the world has a certain stability and doesn't change capriciously, the genes that have survived in the past tend to be the ones that are going to be good at surviving in the future. That means good at programming bodies to survive and make children, grandchildren and long-distance descendants. So, we have arrived back at our individual-based definition of fitness looking into the future. But we now recognise that individuals matter only as vehicles of gene survival. Individuals having grandchildren and distant descendants is only a means to the end of gene survival. And this brings us again to our paradox. 80 per cent of reproducing individuals seem to be crammed up against the ceiling — saturated out at maximum fitness!

To resolve the paradox, we return to the theoretical bedrock: the genes. We neutralise one paradox by erecting another, almost as if two wrongs could make a right. Think on this: an individual organism can be a universal ancestor of the entire population at some distant time in the future, and yet not a single one of his genes survives into that future! How can this be?

Every time an individual has a child, exactly half his genes go into that child. Every time he has a grandchild, a quarter of his genes on average go into that child. Unlike the first generation offspring where the percentage contribution is exact, the figure for each grandchild is statistical. It could be more than a quarter, it could be less. Half your genes come from your father, half from your mother. When you make a child, you put half of your genes into her. But which half of your genes do you give to the child? On average they will be drawn equally from the ones you originally got from the child's grandfather and the ones you originally got from the child's grandmother. But, by chance, you could happen to give all your mother's genes to your child, and none of your father's. In this case, your father would have given no genes to his grandchild. Of course such a scenario is highly unlikely, but as we go down to more distant descendants, total non-contribution of genes becomes more possible. On average you can expect one-eighth of your genes to end up in each great grandchild, one-sixteenth in each great-great-grandchild, but it could be more or it could be less. And so on until the likelihood of a literally zero contribution to a given descendant becomes significant.

In our hypothetical Tasmanian population, the Chang Two date is 22 generations back. So when we say that 80 per cent of the population can expect to be ancestors of all surviving individuals, we are talking about their 22-greats-grandchildren. The fraction of an ancestor's genome which, on average, we can expect to find in a particular one of his 22-greats-grandchildren is one four-millionth part. Since the human genome has only tens of thousands of genes, it would appear that one four-millionth part is going to be fairly thinly spread! It won't be quite like that, of course, because the population of our hypothetical Tasmania is only 5,000. Any individual may be descended from a particular ancestor through many different routes. But still, it could easily happen by chance that some universal ancestors happen to end up contributing none of their genes to distant posterity.

Perhaps I am biased, but I see this as yet another reason to return to the gene as the focus of natural selection: to think backwards about the genes that have  {43}  survived up to the present, rather than forwards about individuals, or indeed genes, trying to survive into the future. The ‘forward intentional’ style of thought can be helpful if used carefully and not misunderstood, but it is not really necessary. ‘Backwards gene’ language is just as vivid when you get used to it, is closer to the truth, and is less likely to yield the wrong answer.

In the Tasmanian's Tale we have talked about genealogical ancestors: historical individuals who are ancestors of modern ones in the conventional genealogist's sense: ‘people ancestors’. But what you can do for people you can do for genes. Genes too have parent genes, grandparent genes, grandchild genes. Genes too have pedigrees, family trees, ‘Most Recent Common Ancestors’ (MRCA). Genes too have their own Rendezvous 0 and here we really can say that, for the majority of genes, their own Rendezvous 0 was in Africa. This apparent contradiction will take some explaining, and this is the purpose of Eve's Tale.

Before proceeding, I must clear up a possible confusion over the meaning of the word gene. It can mean lots of things to different people, but the particular confusion that threatens here is the following. Some biologists, especially molecular geneticists, strictly reserve the word gene for a location on a chromosome (‘locus’), and they use the word ‘allele’ for each of the alternative versions of the gene that might sit at that locus. To take an oversimplified example, the gene for eye colour comes in different versions or alleles, including a blue allele and a brown allele. Other biologists, especially the kind to which I belong, who are sometimes called sociobiologists, behavioural ecologists or ethologists, tend to use the word gene to mean the same as allele. When we want a word for the slot in the chromosome which could be filled by any of a set of alleles, we tend to say ‘locus’. People like me are apt to say ‘Imagine a gene for blue eyes, and a rival gene for brown eyes’. Not all molecular geneticists like that, but it is a well-established habit with my kind of biologist and I shall occasionally follow them.

Eve's Tale (written with Yan Wong)

There's a telling difference between ‘gene trees’ and ‘people trees’. Unlike a person who is descended from two parents, a gene has one parent only. Each one of your genes must have come from either your mother or your father, from one and only one of your four grandparents, from one and only one of your eight great-grandparents, and so on. But when whole people trace their ancestors in the conventional way, they descend equally from two parents, four grandparents, eight great-grandparents and so on. This means that a ‘people genealogy’ is much more mixed up than a ‘gene genealogy’. In a sense, a gene takes a single path chosen from the maze of criss-crossing routes mapped by the (people) family tree. Surnames behave like genes, not like people. Your surname picks out a thin line through your full family tree. It highlights your male to male to male ancestry. DNA, with two notable exceptions which I shall come to later, is not so sexist as a surname: genes trace their ancestry through males and females with equal likelihood.  {44} 

Some of the best-recorded human pedigrees are of European royal families. In the following family tree of the house of Saxe-Coburg, look particularly at the princes Alexis, Waldemar, Heinrich, and Rupert. The ‘gene tree’ of one of their genes is particularly easy to trace because, unfortunately for them but fortunately for us, the gene concerned was defective. It gave the four princes, and many others of their ill-favoured family, the easily recognised blood disease haemophilia: their blood wouldn't clot properly. Haemophilia is inherited in a special manner: it is carried on the X chromosome. Males have only one X chromosome which they inherit from their mother. Females have two X chromosomes, one inherited from each parent. They suffer from the disease only if they have inherited the defective version of the gene from both their mother and their father (i.e. haemophilia is ‘recessive’). Males suffer from the disease if their single ‘unguarded’ X chromosome bears the defective gene. Extremely few females suffer from haemophilia, therefore, but lots of females are ‘carriers’. They have one copy of the faulty gene, and a 50 per cent chance of passing it on to each child. Carrier females who are pregnant always hope for a daughter, but they still have a substantial risk of haemophiliac grandsons. If a haemophiliac male lives long enough to have children, he cannot pass the gene on to a son (males never receive their X chromosome from their father), but he must pass it on to a daughter (females always receive their father's only X chromosome). Knowing these rules, and knowing which royal males had haemophilia, we can trace the faulty gene. Here is the backwards family tree, with the path the haemophilia gene must have taken highlighted.

It seems that Queen Victoria herself was the mutant. It wasn't Albert, because

Bloodlines in the ill-fated House of Saxe-Coburg

his son, Prince Leopold, was haemophiliac, and sons don't get their X chromosome from their father. None of Victoria's collateral relatives suffered from haemophilia. She was the first royal individual to carry the gene. The mis-copying must have occurred either in an egg of her mother, Victoria of Saxe-Coburg, or, which is more likely for reasons explained by my colleague Steve Jones in The Language of the Genes, ‘in the august testicles of her father, Edward Duke of Kent’.

Although neither of Victoria's parents carried or suffered from haemophilia, one of them did have a gene (strictly an allele) which was the pre-mutated ‘parent’ of the royal haemophilia gene. We can think about (though we cannot detect) the ancestry of Victoria's haemophilia gene, back before it mutated to become a haemophilia gene. For our purposes it is irrelevant, except as a matter of diagnostic convenience, that Victoria's copy of the gene was diseased while its predecessors were not. As we trace back the family tree of the gene we ignore its effects, except insofar as they render it visible. The gene's lineage must go back before Victoria, but the visible trail goes cold when it wasn't a haemophilia gene. The lesson is that every gene has one parent gene even if, through mutation, it is not identical to that parent gene. Similarly it has only one grandparent gene, only one great-grandparent gene, and so on. This may seem an odd way to think, but remember that we are on an ancestor-hunting pilgrimage. The present exercise is to see what an ancestor-hunting pilgrimage would look like from a gene's point of view, instead of an individual's.

In the Tasmanian's Tale we encountered the acronym MRCA (Most Recent Common Ancestor) as an alternative to ‘concestor’. I want to reserve ‘concestor’ for the most recent common ancestor in an entire (people or organism) genealogy. So when talking about genes I shall use ‘MRCA’. Two or more alleles in different individuals (or even, as we shall see, in the same individual) certainly do have an MRCA. It is the ancestral gene of which they are each a (possibly mutated) copy. The MRCA of the haemophilia genes of Princes Waldemar and Heinrich of Prussia sat on one of the two X chromosomes of their mother, Irene von Hesse und bei Rhein. When she was still a foetus, two copies of the one haemophilia gene she carried were peeled off and passed successively into two of her egg cells, the progenitors of her luckless sons. These genes in turn share an MRCA with the haemophilia gene of Tsarévitch Alexis of Russia (1904-1918), in the form of a gene carried by their grandmother, Princess Alice of Hesse. Finally, the MRCA of the haemophilia gene in all four of our chosen princes is the very one that flagged itself up for attention in the first place, the mutant gene of Victoria herself.

Geneticists have a word for this sort of backwards tracing of a gene: it is called the coalescent. Looking backwards in time, two gene lineages can be said to coalesce into one at the point where, looking forwards again, a parent runs off two copies of the gene for two successive children. The point of coalescence is the MRCA. Any gene tree has many coalescence points. The haemophilia genes of Waldemar and Heinrich coalesce into the MRCA gene carried by their mother, Irene. That then coalesces with the lineage heading backwards from Tsarévitch Alexis. And, as we've seen, the grand coalescence of all the royal  {46}  haemophilia genes occurs in Queen Victoria. Her genome holds the MRCA haemophilia gene for the whole dynasty.

In my example, the coalescence of the haemophilia genes of all four princes occurs in the very individual (Victoria) who happens also to be their most recent common genealogical (‘people'}  ancestor, their concestor. But that is just coincidence. If we were to choose another gene (say for eye colour), then the path it took through the family tree would be quite different, and the genes would coalesce in a more distant ancestor than Victoria. If we picked a gene for brown eyes in Prince Rupert and one for blue eyes in Prince Heinrich, then the coalescence must be at least as far off as the separation of an ancestral eye-colour gene into two forms, brown and blue, an event buried in prehistory. Each piece of DNA has a genealogy which may be traced in a way that is separate but parallel to the sort of genealogy where we follow surnames through records of Births, Marriages and Deaths.

We can even do this for two identical genes in the same person. Prince Charles has blue eyes, which means, since blue is recessive, that he has two blue-eyed alleles. Those two alleles must coalesce somewhere in the past, but we can't tell when or where. It could be centuries or millennia ago, but in the special case of Prince Charles it is possible that the two blue-eyed alleles coalesce in as recent an individual as Queen Victoria. This is because, as it happens, Prince Charles is descended from Victoria twice: once via King Edward VII and once via Princess Alice of Hesse. On this hypothesis, a single blue-eyed gene of Victoria made two copies of itself at different times. These two copies of the same gene came down to the present Queen (Edward VII's great-granddaughter) and to her husband, Prince Philip (Princess Alice's great-grandson) respectively. Two copies of one Victorian gene could therefore have met again, on two different chromosomes, in Prince Charles. In fact, that almost certainly has happened for some of his genes, whether for blue eyes or not. And regardless of whether his two blue-eyed genes coalesce in Queen Victoria or in somebody farther back, those two genes must have had an MRCA at some specific point in the past. It doesn't matter whether we are talking about two genes in one person (Charles) or in two people (Rupert and Heinrich): the logic is the same. Any two alleles, in different people or in the same person, are fair game for the question: When, and in whom, do these genes coalesce as we look back? And, by extension, we can ask the same question of any three genes, or any number of genes in the population, at the same genetic location (‘locus’).

Looking much further back still, we can ask the same question for pairs of genes at different loci, because genes give rise to genes at different loci by the process of ‘gene duplication’. We shall meet this phenomenon again in the Howler Monkey's Tale, and in the Lamprey's Tale.

Individual people who are closely related share a large number of gene trees. We share the majority of our gene trees with our close kin. But some gene trees deliver a ‘minority vote’, placing us closer to our otherwise more distant relatives. We can think of closeness of kinship among people as a kind of majority vote among genes. Some of your genes vote for, say, the Queen, as a close cousin. Others argue that you are closer to seemingly much more distant  {47}  individuals (as we shall see, even members of other species). When quizzed, each piece of DNA has a different view of what history is all about, because each has blazed a different path through the generations. We can hope to gain a comprehensive view only by questioning a large number of genes. But at this point we must be suspicious of genes situated close to each other on a chromosome. To see why this is, we need to know something about the phenomenon of recombination, which happens every time a sperm or an egg is made.

In recombination, randomly chosen sections of matching DNA are swapped between chromosomes. On average, only one or two swaps are seen per human chromosome (fewer when making sperm, more when making eggs: it is not known why). But over numerous generations, many different parts of the chromosome will eventually be swapped around. So, generally speaking, the nearer two pieces of DNA are on a chromosome, the lower is the chance of a swap occurring between them, and the more likely they are to be inherited together.

When taking ‘votes’ from genes, therefore, we have to remember that the nearer a pair of genes are to each other on a chromosome, the more likely they are to experience the same history. And this motivates genes which are close colleagues to back up each other's vote. At the extreme are sections of DNA so tightly bound together that the entire chunk has travelled through history as a single unit. Such fellow-travelling chunks are known as ‘haplotypes’ a word that we shall meet again. Among such caucuses within the genetic parliament, two stand out, not because their view of history is more valid, but because they have been extensively used to settle biological debates. Both hold sexist views, because one has come down entirely through female bodies, and the other has never been outside a male body. These are the two major exceptions to unbiased gene inheritance that I previously mentioned.

Like a surname, the (non-recombining portion of the) Y chromosome always passes through the male line only. Together with a few other genes, the Y chromosome contains the genetic material that actually switches an embryo into the male pattern of development rather than the female one. Mitochondrial DNA, on the other hand, passes exclusively down the female line (although in this case it is not responsible for making the embryo develop as a female: males have mitochondria, it is just that they don't pass them on). As we shall see in the Great Historic Rendezvous, mitochondria are tiny bodies inside cells, relicts of once-free bacteria who, probably about 2 billion years ago, took up exclusive residence inside cells where they have been reproducing, non-sexually by simple division, ever since. They have lost many of their bacterial qualities and most of their DNA, but they retain enough to be useful to geneticists. Mitochondria constitute an independent line of genetic reproduction inside our bodies, unconnected with the main nuclear line which we think of as our ‘own’ genes.

Because of their mutation rate, Y chromosomes are most useful for studies of recent populations. One neat study took samples of Y-chromosome DNA in a straight line across modern Britain. The results showed that Anglo-Saxon Y chromosomes moved west across England from Europe, stopping rather abruptly at the Welsh border. It is not hard to imagine reasons why this male-carried  {48}  DNA is unrepresentative of the rest of the genome. To take a more obvious example, Viking ships carried cargoes of Y chromosomes (and other genes) and spread them among widely scattered populations. The distribution of Viking Y-chromosome genes today presumably shows them to be slightly more ‘travelled’ than other Viking genes, which were statistically more likely to favour home-acre over Widow-maker:

Mitochondrial DNA too can be revealing, particularly for very ancient patterns. If we compare your mitochondrial DNA with mine, we can tell how long ago they shared an ancestral mitochondrion. And, since we all get our mitochondria from our mothers, and hence maternal grandmothers, maternal great-grandmothers, etc., mitochondrial comparison can tell us when our most recent female-line ancestor lived. The same can be done for Y chromosomes, to tell us when our most recent male-line ancestor lived but, for technical reasons, it is not so easy. The beauty of Y-chromosomal and mitochondrial DNA is that neither of them is contaminated by sexual mixing. This makes tracing these particular classes of ancestor easy.

The mitochondrial MRCA of all humanity, which pinpoints the ‘people’ common ancestor in the all-female line, is sometimes called Mitochondrial Eve — she whose tale this is. And of course the equivalent in the all-male line might as well be called Y-chromosome Adam. All human males have Adam's Y chromosome (creationists please refrain from deliberate misquotation). If surnames had always been strictly inherited by modern rules we'd all have Adam's surname too, which would rather lose the point of having a surname.

Eve is a great temptress to error and it is good to be forearmed. The errors are quite instructive. First, it is important to understand that Adam and Eve are only two out of a multitude of MRCAs that we could reach if we traced our way back through different lines. They are the special-case common ancestors that we reach if we travel up the family tree from mother to mother to mother, or father to father to father respectively. But there are many, many other ways of going up the family tree: mother to father to father to mother, mother to mother to father to father, and so forth. Each of these possible pathways will have a different MRCA.

Second, Eve and Adam were not a couple. It would be a major coincidence if they ever met, and they could well have been separated by tens of thousands of years. As a subsidiary point, there are independent reasons to believe that Eve preceded Adam. Males are more variable in reproductive success than females: where some females have five times as many children as other females, the most successful males could have hundreds of times as many children as unsuccessful males. A male with a large harem finds it easy to become a universal ancestor. A female, since she is less likely to have a large family, needs a larger number of generations to achieve the same feat. And indeed, today's best  {49}  ‘molecular clock’ estimates for their respective dates are about 140,000 years ago for Eve and only about 60,000 for Adam.

Third, Adam and Eve are shifting honorific titles, not names of particular individuals. If, tomorrow, the last member of some outlying tribe were to die, the baton of Adam, or of Eve, could abruptly be thrown forward several thousand years. The same is true of all the other MRCAs defined by different gene trees. To see why this is so, suppose Eve had two daughters, one of whom eventually gave rise to the Tasmanian aborigines and the other of whom spawned the rest of humanity. And suppose, entirely plausibly, that the female-line MRCA uniting ‘the rest of humanity’ lived 10,000 years later, all other collateral lines descending from Eve having gone extinct apart from the Tasmanians. When Truganinni, the last Tasmanian, died, the title of Eve would instantly have jumped forward 10,000 years.

Fourth, there was nothing to single out either Adam or Eve for particular notice in their own times. Despite their legendary namesakes, Mitochondrial Eve and Y-chromosome Adam were not particularly lonely. Both would have had plenty of companions, and each may well have had many sexual partners, with whom they may also have surviving descendants. The only thing that singles them out is that Adam eventually turned out to be hugely endowed with descendants down the male line, and Eve with descendants down the female line. Others among their contemporaries may have left as many descendants all told.

While I was writing this, somebody sent me a videotape of a BBC television documentary called Motherland, hyped as ‘an incredibly poignant film’, and as ‘truly beautiful, a really memorable piece’. The heroes of the film were three ‘black’^* people whose families had immigrated to Britain from Jamaica. Their DNA was matched up against worldwide databases, in an attempt to trace the part of Africa from which their ancestors were taken as slaves. The production company then staged lachrymose ‘reunions’ between our heroes and their long-lost African families. They used Y-chromosomal and mitochondrial DNA because, for the reasons we have seen, they are more traceable than genes in general. But unfortunately, the producers never really came clean about the limitations this imposed. In particular, no doubt for sound televisual reasons, they came close to actively deceiving these individuals, and also their long-lost African ‘relatives’, into becoming far more emotional about the reunions than they had any right to be.

Let me explain. When Mark, later given the tribal name Kaigama, visited the Kanuri tribe in Niger, he believed he was ‘returning’ to the land of ‘his people’. Beaula was welcomed as a long-lost daughter by eight women of the Bubi tribe on an island off the coast of Guinea, whose mitochondria matched hers. Beaula said,

It was like blood touching blood... It was like family... I was just crying, my eyes were just filled with tears, my heart was pounding. All I just kept thinking was: ‘I'm going to my motherland.’

Sentimental rubbish, and she should never have been deceived into thinking this. All that she, or Mark, were really visiting — at least as far as there was any evidence to suppose — were individuals who shared their mitochondria. As a  {50}  matter of fact, Mark had already been told that his Y-chromosome came from Europe (which upset him and he was later palpably relieved to discover respectable African roots for his mitochondria!). Beaula, of course, has no Y-chromosome, and apparently they didn't bother to look at her father's although that would have been interesting, for she was quite light-skinned. But it was explained to neither Beaula nor Mark, nor the television audience, that genes outside their mitochondria almost certainly came from a huge variety of ‘home-lands’, nowhere near those identified for purposes of the documentary. If their other genes had been traced, they could have had equally emotional ‘reunions’ in hundreds of different sites, all over Africa, Europe and very probably Asia too. That would have spoiled the dramatic impact, of course.

As I have been continually reiterating, reliance on a single gene can be misleading. But the combined evidence from many genes gives us a powerful tool for reaching back into history. The gene trees of a population, and the coalescence points which define them, reflect the events of the past. Not only can we identify these coalescence points, we can also guess at their dates because of the molecular clock. And herein lies the key, because the pattern of branchings through time tells a story. Random mating, the assumption made in the Tasmanian's Tale, generates a very different pattern of coalescence from various kinds of non-random mating — each of which, in turn, imprints its own shape on the coalescence tree. Fluctuations in population size, too, leave their own characteristic signature. So we can work backwards from today's patterns of gene distribution and make inferences about population sizes, and about the timings of migrations. For example, when a population is small, coalescence events will occur more frequently. An expanding population is signified by trees with long end branches, so coalescence points will be concentrated near the base of the tree, back when the population was small. With the aid of the molecular clock, this effect can be used to work out when the population expanded, and when it contracted in ‘bottlenecks’. (Although unfortunately, by wiping out genetic lineages, severe bottlenecks tend to erase the traces of what happened before them.)

Coalescent gene trees have helped resolve a long-standing debate over human origins. The ‘Out of Africa’ theory holds that all surviving peoples outside Africa are descended from a single exodus around a hundred thousand years ago, more or less. At the other extreme are the ‘Separate Origins’ theorists or ‘Multiregionalists’, who believe that the races still living in, say, Asia, Australia and Europe are anciently divided, separately descended from regional populations of the earlier species, Homo erectus. Both names are misleading. ‘Out of Africa’ is unfortunate because everybody agrees that our ancestors are from Africa if you go back far enough. ‘Separate Origins’ is also not an ideal name because, again if you go back far enough, the separation must disappear on any theory. The disagreement concerns the date when we came out of Africa. It might be better to call the two theories ‘Young Out of Africa’ (YOOA) and ‘Old Out of Africa’ (OOOA). This has the added advantage of emphasising the continuum between them.

If today's non-Africans all stem from a single recent emigration from that  {51}  continent, we would expect modern gene distributions to demonstrate a recent, Africa-centred, small-population ‘bottleneck’. Coalescence points would be concentrated around the time of the exodus. If we are separately descended from regional H. erectus, however, then genes should instead show evidence of anciently separated genetic lineages in each region. At the time when YOOA supporters claim an exodus, we would instead see a dearth of coalescence points. Which is it?

By expecting a single answer to this question we have fallen into the same trap as the Motherland television documentary. Different genes tell different stories. It is perfectly possible for some of our genes to have recently come out of Africa, while others have been passed to us from separate H. erectus populations. Or to put it another way, we can be both descendants of a recent African exodus, and simultaneously descendants of regional H. erectus, because at any given time in the past we have a huge number of genealogical ancestors. Some could have recently left Africa. Some could have been resident in, say, Java for thousands of years. And we could have inherited African genes from some and Javan genes from others. A single chunk of DNA, such as from a mitochondrion or Y-chromosome, gives as impoverished a view of the past as a single sentence from a history book. Yet the YOOA position is often supported on the basis of the placement of Mitochondrial Eve. What happens if we quiz the other members of the parliament of genes?

This is, in effect, what the evolutionary biologist Alan Templeton did, and he came up with his engagingly titled theory ‘Out of Africa Again and Again’. Templeton used a type of coalescence theory, similar to that in our haemophilia discussion, but he did it for lots of separate genes instead of just one. This enabled him to reconstruct the history and geography of genes over the whole world and over hundreds of thousands of years. At the moment, I favour Templeton's ‘Out of Africa Again and Again’ theory, because he seems to me to use all the available information in a way that maximises its power to generate inferences; and because he bent over backwards, at every step of his work, to guard against overreaching the evidence.

Here is what Templeton did. He looked through the genetic literature, using strict criteria to skim the cream: he wanted only large studies of human genetics, where samples had been taken from different parts of the world, including Europe, Asia and Africa. The genes examined belonged to long-lived ‘haplotypes’. A haplotype, as we have seen, is a chunk of genome which is either impervious to being broken up by sexual recombination (as with Y-chromosome and mitochondrial DNA), or (as with certain smaller parts of the genome) can be recognised intact through enough generations to cover the timescale of interest. A haplotype is a long-lived, recognisable chunk of genome. You don't go too far wrong if you think of it as a large ‘gene’.

Templeton zeroed in on 13 haplotypes. For each of them, he calculated their ‘gene tree’, and dated the various coalescence points using the molecular clock which is ultimately calibrated with fossils. From these dates, and from the geographical distribution of the samples, he was able to pull out inferences about the genetic history of our species over the past couple of million years.  {52}  He summarised his conclusions in a helpful diagram, reproduced here.

Templeton's main conclusion is that there were not two major migrations out of Africa but three. In addition to the OOOA (Homo erectus) exodus around 1.7 million years ago (which everyone accepts and for which the evidence is mostly from fossils) and the recent migration as promoted by the YOOA theory, there was another Great Trek from Africa to Asia between 840,000 and 420,000 years ago. This middle emigration — shall we call it MOOA? — is supported by extant ‘signals’ from three of the thirteen haplotypes. The YOOA emigration is supported by mitochondrial and Y-chromosomal evidence. Other genetic ‘signals’ betray a major back-migration from Asia to Africa about 50,000 years ago. A little later, mitochondrial DNA and various smaller genes disclose other migrations: from Southern to Northern Europe, from Southern Asia to Northern Asia, across the Pacific and to Australia. Finally, as shown by mitochondrial DNA and archaeological evidence, North America was colonised across what was then the Bering land bridge from north-east Asia, around 14,000 years ago.  {53} 

Colonisation of South America through the Isthmus of Panama rapidly followed. The suggestion, by the way, that either Christopher Columbus or Leif Erickson ‘discovered’ America is nothing short of racist. Equally distasteful, in my view, is relativist ‘respect’ for Native American oral histories which ignorantly deny that their ancestors ever lived outside America.

Between Templeton's three major migrations out of Africa, other genetic signals reveal continual eddies of gene flow back and forth between Africa, southern Europe and southern Asia. His evidence suggests that major and minor immigrations have usually been followed by some interbreeding with indigenous populations, rather than — as might just as well have happened complete extermination of one side or the other. Clearly this has large implications for our evolutionary ancestry.

This tale, and Templeton's study, focused on humans and their genes. But of course all species have family trees. All species inherit genetic material. All species with two sexes have an Adam and an Eve. Genes and gene trees are a ubiquitous feature of life on Earth. The techniques that we apply to recent human history can also be applied to the rest of life. Cheetah DNA reveals a 12,000-year-old population bottleneck important to feline conservationists. Maize DNA has stamped upon it the unmistakable signature of its 9,000 year Mexican domestication. The coalescence patterns of HIV strains can be used by epidemiologists and medical doctors to understand and contain the virus. Genes and gene trees reveal the history of the flora and fauna of Europe: the vast migrations driven by ice ages whose waxing pushed temperate species into southern-European refuges, and whose waning stranded Arctic species on isolated mountain ranges. All these events and more can be traced in the distribution of DNA around the globe, a historical reference book which we are only just learning to read.

We have seen how different genes have different stories to tell, which can be pieced together to reveal something of our history, both modern and ancient. How ancient? Amazingly, our oldest MRCA genes can even date back before we were human at all. This is especially so when natural selection favours variety in the population for its own sake. Here's how it works.

Suppose there are two blood types called A and B, which confer immunity to different diseases. Each blood type is susceptible to the disease against which the other type has immunity. Diseases flourish when the blood type that they can attack is abundant, because an epidemic can get going. So if B people, say, happen to be common in the population, the disease that hurts them will enjoy an epidemic. Consequently, B people will die until they cease to be common, and the A people increase — and vice versa. Whenever we have two types, the rarer of which is favoured because it is rare, it is a recipe for polymorphism: the positive maintenance of variety for variety's sake. The ABO blood group system is a famous polymorphism which has probably been maintained for this kind of reason.

Some polymorphisms can be quite stable — so stable that they span the change from an ancestral to a descendant species. Astonishingly, our ABO polymorphism is present in chimpanzees. It could be that we and chimps have  {54}  independently ‘invented’ the polymorphism, and for the same reason. But it is more plausible that we have both inherited it from our shared ancestor, and independently kept it going during our six million years of separate descent, because the relevant diseases have been continuously at large throughout that time. This is called trans-specific polymorphism, and it may apply to far more distant cousins than chimpanzees are to us.

A stunning conclusion is that, for particular genes, you are more closely related to some chimpanzees than to some humans. And I am closer to some chimpanzees than to you (or to ‘your’ chimpanzees). Humans as a species, as well as humans as individuals, are temporary vessels containing a mix of genes from different sources. Individuals are temporary meeting points on the crisscrossing routes that genes take through history. This is a tree-based way to express the central message of The Selfish Gene, my first book. As I put it there, ‘When we have served our purpose we are cast aside. But genes are denizens of geological time: genes are forever.’ At the concluding banquet to a conference in America, I recited the same message in verse:

And, as the body's immediate reply to the gene, I parodied the very same Harp Song of the Dane Women quoted previously:

We estimated the date of Rendezvous o as probably tens of thousands of years ago, and at most hundreds of thousands. We have not travelled far on our backward pilgrimage. The next rendezvous, our meeting with the chimpanzee pilgrims at Rendezvous 1, is millions of years away, and most of our rendezvous are hundreds of millions beyond that. To stand a chance of completing our pilgrimage, we shall need to speed up, and begin the move into ‘deep time’. We must accelerate past the rest of the 30 or so ice ages that typify the last three million years, past such drastic events as the drying and refilling of the Mediterranean that occurred between 4.5 and 6 million years ago. To ease this initial acceleration, I shall take the otherwise unusual liberty of stopping at a few intermediate milestones en route, and allowing dead fossils to tell tales. The fossilised ‘shadow’ pilgrims we shall meet, and the tales they tell, will help satisfy our natural preoccupation with our direct ancestors.

ARCHAIC HOMO SAPIENS

Our first milestone on the way back to Rendezvous 1 is in the depths of the ice age before last, about 160,000 years ago. I have chosen this way station to look at fossil finds from Herto in the Afar depression of Ethiopia.^* The Herto humans are intriguing because, in the words of their discoverers, Tim White and his colleagues, they are from a ‘population that is on the verge of anatomical modernity but not yet fully modern’. The distinguished palaeoanthropologist Christopher Stringer regards ‘the Herto material as the oldest definite record of what we currently think of as modern H. sapiens’, a record previously held by younger Middle Eastern fossils dating from about 100,000 years ago. Regardless of hair-splitting distinctions between ‘modern’ and ‘nearly modern’, it is clear that the Herto people are on the cusp between modern humans and those predecessors that we know by the catch-all name of ‘Archaic Homo sapiens’. Certain authorities use this name back to about 900,000 years ago where it grades into an earlier species, Homo erectus. As we shall see, others prefer to give various Latin names to the bridging archaic forms. I shall sidestep the disputes by using anglicisms in the style of my colleague Jonathan Kingdon: ‘Moderns’, ‘Archaics’, ‘Erects’, and others that I'll mention as we come to them. We should not expect to draw a neat line between early Archaics and the Erects from whom they evolved, or between Archaics and the earliest Moderns who evolved from them. Don't be confused, incidentally, by the fact that the Erects were even more archaic (with a small a) than the Archaics (with a large A), and that all three types were erect with a small e!

Archaic forms persisted alongside Modern forms until at least 100,000 years ago (longer still if we include the Neanderthals, of whom more in a moment). Archaic fossils are found all around the world, dating from various times during the last few hundred thousand years: examples are the German ‘Heidelberg man’, ‘Rhodesian man’ from Zambia (which used to be called Northern Rhodesia), and the Chinese ‘Dali man’. Archaics had big brains like us, averaging 1,200 to 1,300 cubic centimetres. This is a little smaller than our average of 1,400 cubic centimetres but the range comfortably overlaps with ours. Their bodies were more robust than ours, their skulls were thicker, and they had more pronounced brow ridges and less pronounced chins. They looked more like Erects than we do, and hindsight justly sees them as intermediate. Some taxonomists recognise them as a subspecies of Homo sapiens called Homo sapiens heidelbergensis (where we would be Homo sapiens sapiens). Others do not recognise the Archaics as Homo sapiens at all, but call them Homo heidelbergensis.  {56}  Yet others divide the Archaics into more than one species, for instance Homo heidelbergensis, Homo rhodesiensis, and Homo antecessor. If you think about it, we should be worried if there was not disagreement over the divisions. On the evolutionary view of life, a continuous range of intermediates is to be expected.

Modern Homo sapiens sapiens are not the only offshoot of the Archaics. Another species of advanced humans, the so-called Neanderthals, were our contemporaries for much of our prehistory. They resembled the Archaics more than we do in some respects, and they seem to have emerged from an Archaic root between about one and two hundred thousand years ago — in this case not in Africa but in Europe and the Middle East. Fossils from these regions show a gradual transition from Archaics to Neanderthals with the first unequivocal Neanderthal fossils found just before the beginning of the last Ice Age, about 130,000 years ago. They then persisted in Europe for most of this cold period, vanishing about 28,000 years ago. In other words, for their entire existence Neanderthals were contemporaries of European Modern émigrés from Africa. Some people believe that Moderns were responsible for their extinction, either by killing them directly or by competing with them.

Neanderthal^* anatomy was sufficiently different from ours that some people prefer to give them a separate species name, Homo neanderthalensis. They retained some features of Archaics such as large brow ridges which Moderns did not (which is why some authorities classify them as just another type of Archaic). Adaptations to their cold environment include stockiness, short limbs and enormous noses, and they surely must have been warmly clothed, presumably in animal furs. Their brains were as big as ours or even bigger. Much is made of slight indications that they ceremonially buried their dead. Nobody knows whether they could speak, and opinions differ on this important question. Archaeology hints that technological ideas may have passed both ways between Neanderthals and Moderns, but this could have been by imitation rather than by language.

The rules for the pilgrimage stated that only modern animals setting off from the present were entitled to tell tales. We are making an exception for the dodo and the elephant bird, because they lived in recent historical times. And the fossils Homo erectus and Homo habilis qualify as ‘shadow pilgrims’ because a plausible case could be made that they are our direct ancestors. Do the Neanderthals, too, qualify under this rubric? Are we descended from them? Well, as it happens, that very question is the topic of the tale that the Neanderthals want to tell. Think of the Neanderthal's Tale as a plea to be allowed to tell it.

The Neanderthal's Tale (written with Yan Wong)

Are we descended from Neanderthals? If so, they would have to have interbred with Homo sapiens sapiens. But did they? They overlapped for a long time in Europe, and there was surely contact between them. But did it go beyond contact? Do modern Europeans inherit any Neanderthal genes? This is a hotly debated  {57}  issue, recently reignited by a remarkable extraction of DNA from late Neanderthal bones. So far, we have extracted only the maternally inherited mitochondrial DNA, but this is enough for a tentative verdict. Neanderthal mitochondria are quite distinct from those of all surviving humans, suggesting that Neanderthals are no closer to Europeans than to any other modern peoples. In other words, the female-line common ancestor of Neanderthals and all surviving humans long pre-dates Mitochondrial Eve: about 500,000 years as opposed to 140,000. This genetic evidence suggests that successful interbreeding between Neanderthals and Moderns was rare. And so it is often said that they died out without leaving any descendants.

But don't let's forget that ‘80 per cent’ argument which so surprised us in the Tasmanian's Tale. A single immigrant who managed to break into the Tasmanian breeding population had an 80 per cent chance of joining the set of universal ancestors: the set of individuals who could call themselves ancestors of all surviving Tasmanians in the distant future. By the same token, if only one Neanderthal male, say, bred into a sapiens population, that gave him a reasonable chance of being a common ancestor to all Europeans alive today. This can be true even if Europeans contain no Neanderthal genes at all. A striking thought.

So although few, if any, of our genes come from Neanderthals, it is possible that some people have many Neanderthal ancestors. This was the distinction we met in Eve's Tale between gene trees and people trees. Evolution is governed by the flow of genes, and the moral of the Neanderthal's Tale, if we allow him to tell it, is that we cannot, should not, look at evolution in terms of pedigrees of individuals. Of course individuals are important in all sorts of other ways, but if we are talking pedigrees it is gene trees that count. The words ‘evolutionary descent’ refer to gene ancestors, not genealogical ancestors.

Fossil changes too are a reflection of gene pedigrees, not (or only incidentally) genealogical pedigrees. Fossils indicate that Modern anatomy passed to the rest of the world via young out-of-Africa migrations. But Alan Templeton's work (described in Eve's Tale) suggests that we are also partly ‘descended from’ non-African Archaics, possibly even non-African Homo erectus. The description is both simpler and more powerful if we switch from people talk to gene talk. The genes that determine our Modern anatomy were carried out of Africa by the YOOA migrants, leaving fossils in their wake. At the same time, Templeton's evidence suggests that other genes we now possess were flowing around the world by different routes, but left little anatomical evidence to show for it. Most of our genes probably took the young out-of-Africa route, while just a few came to us through other routes. What could be a more powerful way to express it?

So, have the Neanderthals established their right to tell a tale? Maybe a tale of genealogy if not a tale of genes.

ERGASTS

Moving deeper in time, we touch down again at one million years in search of ancestors. The only likely candidates of this age are of the type usually called Homo erertus, although some would call the African ones Homo ergaster and I shall follow them. In seeking an anglicised form for these creatures, I shall call them Ergasts rather than Erects, partly because I believe the majority of our genes trace back to the African form, and partly because, as I've already remarked, they were no more erect than their predecessors (Homo habilis) or their successors (us). Whatever name we prefer, the Ergast type persisted from about 1.8 million until about a quarter of a million years ago. They are widely accepted as the immediate predecessors, and partial contemporaries, of the Archaics who are in turn the predecessors of us Moderns.

The Ergasts were noticeably different from modern Homo sapiens, and, unlike the Archaic sapiens people, they differed from us in some respects that show no overlap. Fossil finds show they lived in the Middle East and Far East including Java, and represent an ancient migration out of Africa. You may have heard them referred to by their old names of Java Man and Peking Man. In Latin, before they were admitted into the Homo fold, they had the generic names Pithecanthropus and Sinanthropus. They walked on two legs like us, but had smaller brains (900 cc in early specimens to 1,100 cc in late ones), housed in lower, less domed, more ‘swept-back’ skulls than ours, and they had receding chins. Their jutting brow ridges made a pronounced horizontal ledge above the eyes, set in wide faces, with a pinching in of the skull behind the eyes.

Hair doesn't fossilise, so there is no natural place in our history to discuss the obvious fact that at some point in our evolution we lost most of our body hair, with the luxuriant exception of the tops of our heads. Very likely the Ergasts were hairier than us, but we can't rule out the possibility that Ergasts had already lost their body hair by a million years ago. They could have been as hairless as we are. Equally, nobody should complain of an imaginative reconstruction as hairy as a chimpanzee, or any intermediate level of shagginess. Modern people, males at least, remain quite variable in how hairy they are. Hairiness is one of those characteristics that can increase or decrease in evolution again and again. Vestigial hairs, with their associated cellular support structures, lurk in even the barest-seeming skin, ready to evolve into a full coat of thick hair at short notice, or shrink again, should natural selection at any time call them out of retirement. Look at the woolly mammoths and woolly rhinoceroses that rapidly evolved in response to the recent ice ages in Eurasia.  {59}  We shall return to the evolutionary loss of human hair in — strangely enough the Peacock's Tale.

Subtle evidence of repeatedly used hearths suggests that at least some groups of Ergasts discovered the use of fire — with hindsight a momentous event in our history. The evidence is less conclusive than we might hope. Blackening from soot and charcoal does not survive immense timespans, but fires leave other traces that last longer. Modern experimenters have systematically constructed fires of various kinds and then examined them afterwards for their trace effects. It emerges that deliberately built campfires magnetise the soil in a way that distinguishes them from bushfires and from burnt-out tree stumps — I don't know why. But such signs provide evidence that Ergasts, both in Africa and Asia, had camp fires nearly one and a half million years ago. This doesn't have to mean that they knew how to light fires. They could have begun by capturing and tending naturally occurring fire, feeding it and keeping it alive as one might look after a Tamagochi pet. Maybe, before they began to cook food, they used fires to scare away dangerous animals and provide light, heat, and a social focus.

The Ergasts also shaped and used stone tools, and presumably wooden and bone ones too. Nobody knows whether they could speak, and evidence is hard to come by. You might think that ‘hard to come by’ is an understatement, but we have now reached a point in our backward journey when fossil evidence starts to tell. Just as campfires leave traces in the soil, so the needs of speech call forth tiny changes in the skeleton: nothing so dramatic as the hollow bony box in the throat with which the howler monkeys of the South American forests amplify their stentorian voices, but still telltale signs such as one might hope to detect in a few fossils. Unfortunately, the signs that have been unearthed are not telltale enough to settle the matter, and it remains controversial.

There are two parts of the modern human brain which seem to go with speech. When in our history did these parts — Broca's Area and Wernicke's Area — enlarge? The nearest approach we have to fossil brains is endocasts, to be described in the Ergast's Tale. Unfortunately the lines dividing different regions of the brain do not fossilise very clearly, but some experts think they can say that the speech areas of the brain were already enlarged before two million years ago. Those who want to believe that Ergasts possessed the power of speech are encouraged by this evidence.

They are discouraged, however, when they move down the skeleton. The most complete Homo ergaster we know is the Turkana Boy, who died near Lake Turkana, in Kenya, about 1.5 million years ago. His ribs, and the small size of the portholes in the vertebrae through which the nerves pass, suggest that he lacked the fine control over breathing that seems to be associated with speech. Other scientists, studying the base of the skull, have concluded that even Neanderthals, as recently as 60,000 years ago, were speechless. The evidence is that their throat shape would not have allowed the full range of vowels that we deploy. On the other hand, as the linguist and evolutionary psychologist Steven Pinker has remarked, ‘e lengeege weth e smell nember ef vewels cen remeen quete expresseve’. If written Hebrew can be intelligible without vowels, I don't see why spoken Neander or even Ergaster couldn't too. The veteran South African  {60}  anthropologist Philip Tobias suspects that language may pre-date even Homo ergaster, and he may just possibly be right. As we have seen, there are a few who go to the opposite extreme and date the origin of language to the Great Leap Forward, just a few tens of thousands of years ago.

This may be one of those disagreements that can never be resolved. All considerations of the origin of language begin by citing the Linguistic Society of Paris which, in t866, banned discussion of the question because it was deemed unanswerable and futile. It may be difficult to answer, but it is not in principle unanswerable like some philosophical questions. Where scientific ingenuity is concerned, I am an optimist. Just as continental drift is now sewn up beyond all doubt, with multiple threads of convincing evidence, and just as DNA fingerprinting can establish the exact source of a bloodstain with a confidence that forensic experts could once only dream of, I guardedly expect that scientists will one day discover some ingenious new method of establishing when our ancestors started to speak.

Even I, however, have no hope that we shall ever know what they said to each other, or the language in which they said it. Did it begin with pure words and no grammar: the equivalent of an infant babbling nounspeak? Or did grammar come early and — which is not impossible and not even silly — suddenly? Perhaps the capacity for grammar was already deep in the brain, being used for something else like mental planning. Is it even possible that grammar, as applied to communication at least, was the sudden invention of a genius? I doubt it, but in this field I wouldn't rule anything out with confidence.

As a small step towards finding out the date at which language arose, some promising genetic evidence has appeared. A family code-named KE suffers from a strange hereditary defect. Out of approximately 30 family members spread over three generations, about half are normal, but fifteen show a curious linguistic disorder, which seems to affect both speech and understanding. It has been called verbal dyspraxia, and it first shows itself as an inability to articulate clearly in childhood. Other authorities think the trouble stems from ‘feature blindness’, meaning an inability to grasp certain grammatical features such as gender, tense and number. What is clear is that the abnormality is genetic. Individuals either have it or they don't, and it is associated with a mutation of an important gene called FOXP2, which the rest of us have in unmutated form. Like most of our genes, a version of F0XP2 is present in mice and other species, and it probably does various things in the brain and elsewhere.^* The evidence of the KE family suggests that in humans F0XP2 is important for the development of some part of the brain that is involved in language.

So, we naturally want to compare human F0XP2 with the same gene in animals that lack language. You can compare genes either by looking at the DNA sequences themselves, or by looking at the amino acid sequences in the proteins that they encode. There are times when it makes a difference, and this is one of them. F0XP2 codes for a protein chain 715 amino acids long. The mouse and chimpanzee versions of the gene differ in only one amino acid. The human version differs from both these animals in an additional two amino acids. You see what this might mean? Although humans and chimpanzees share the great  {61}  majority of their evolution and their genes, the F0XP2 gene is one place where humans seem to have evolved rapidly in the short time since we split from them. And one of the most important respects in which we differ from chimpanzees is that we have language and they don't. A gene that changed somewhere along the line towards us, but after the separation from chimpanzees, is exactly the sort of gene we should be looking for if we are trying to understand the evolution of language. And it is the very same gene that has mutated in the unfortunate KE family.^* Perhaps it was changes in F0XP2 that made humans, as opposed to chimpanzees, capable of language. Did the Ergasts have the mutated F0XP2 gene?

Wouldn't it be wonderful if we could use this genetic hypothesis to date the origin of language in our ancestors? While we can't do it with certainty, we can do something quite suggestive, along these lines. The obvious approach would be to triangulate backwards from variants among modern humans, and try to calculate the antiquity of the F0XP2 gene. But with the exception of rare unfortunates like the members of the KE family, there is no variation among humans in any of the F0XP2 amino acids. So there isn't enough variation there to triangulate from. Luckily, however, there are other parts of the gene which are never translated into protein and which are therefore free to mutate without natural selection ‘noticing’: they are ‘silent’ code letters, in those parts of the gene that are never transcribed and are called introns (as opposed to ‘exons’ which are ‘expressed’ and therefore ‘seen’ by natural selection). The silent letters, unlike the expressed ones, are quite variable among individual humans, and between humans and chimpanzees. We can get some understanding of the evolution of the gene if we look at the patterns of variation in the silent areas. Even though the silent letters are not subject to natural selection themselves, they can be swept along by selection of neighbouring exons. Even better, the mathematically analysed pattern of variation in the silent introns gives a good indication of when the sweeps of natural selection occurred. And the answer for F0XP2 is less than 200,000 years ago. A naturally selected change to the human form of F0XP2 seems roughly to coincide with the change from archaic Homo sapiens to anatomically modern Homo sapiens. Could this be when language was born? The margin of error in this sort of calculation is wide, but this ingenious genetic evidence counts as a vote against the theory that Homo ergaster could talk. More importantly for me, the unexpected new method boosts my optimism that one day science will find a way to confound the pessimists of the Linguistic Society of Paris.

Homo ergaster is the first fossil ancestor we have met on our pilgrimage who is unequivocally of a different species from ourselves. We are about to embark on a portion of the pilgrimage in which fossils provide the most important evidence, and they will continue to bulk large — though they will never overwhelm molecular evidence — until we reach extremely ancient times and relevant fossils start to peter out. It is a good moment to look in more detail at fossils, and how they are formed. The Ergast will tell the tale.  {62} 

The Ergast's Tale

Richard Leakey movingly describes the discovery, by his colleague Kimoya Kimeu on 22 August 1984, of the Turkana Boy^* (Homo ergaster), at 1.5 million years the oldest near-complete hominid skeleton ever found. Equally moving is Donald Johanson's description of the older, and unsurprisingly less complete, australopithecine familiarly known as Lucy. The discovery of ‘Little Foot’, yet to be fully described, is just as remarkable (see page 79). Whatever freak conditions blessed Lucy, ‘Little Foot’, and the Turkana Boy with their version of immortality, would we not wish it for ourselves when our time comes? What hurdles must we cross to achieve this ambition? How does any fossil come to be formed? This is the subject of the Ergast's Tale. To begin, we need a small digression into geology.

Rocks are built of crystals, though these are often too small for the unaided eye to see. A crystal is a single giant molecule, its atoms arranged in an orderly lattice with a regular spacing pattern repeated billions of times until, eventually, the edge of the crystal is reached. Crystals grow when atoms come out of the liquid state and build up on the expanding edge of an existing crystal. The liquid is usually water. On other occasions, it is not a solvent at all but the molten mineral itself. The shape of the crystal, and the angles at which its plane facets meet, is a direct rendition, in the large, of the atomic lattice. The lattice shape is sometimes projected very large indeed, as in a diamond or amethyst whose facets betray to the naked eye the three-dimensional geometry of the self-assembled atomic arrays. Usually, however, the crystalline units of which rocks are made are too small for the eye to detect them, which is one reason why most rocks are not transparent. Among important and common rock crystals are quartz (silicon dioxide), feldspars (mostly silicon dioxide again, but some of the silicon atoms are replaced by aluminium atoms), and calcite (calcium carbonate). Granite is a densely packed mixture of quartz, feldspar and mica, crystallised out of molten magma. Limestone is mostly calcite, sandstone mostly quartz, in both cases ground small and then compacted from sediments of sand or mud.

Igneous rocks begin as cooled lava (which in turn is molten rock). Often, as with granite, they are crystalline. Sometimes their shape may be visibly that of  {63}  a glass-like solidified liquid and, with great good fortune, molten lava may sometimes be cast in a natural mould, such as a dinosaur's footprint or an empty skull. But the main usefulness of igneous rock to historians of life is in dating. As we shall see in the Redwood's Tale, the best dating methods are available for igneous rocks alone. Fossils usually cannot be precisely dated themselves, but we can look for igneous rocks in the vicinity. We then either assume that the fossil is contemporaneous, or we seek two datable igneous samples that sandwich our fossil and fix upper and lower bounds to its date. This sandwich dating is open to the slight risk that a corpse has been carried by floodwater, or by hyenas or their dinosaur equivalents, to an anachronistic site. With luck this will usually be obvious; otherwise we have to fall back on consistency with a general statistical pattern.

Sedimentary rocks such as sandstone and limestone are formed from tiny fragments, ground by wind or water from earlier rocks or other hard materials such as shells. They are carried in suspension, as sand, silt or dust, and deposited somewhere else, where they settle and compact themselves over time into new layers of rock. Most fossils lie in sedimentary beds.

It is in the nature of sedimentary rock that its materials are continually being recycled. Old mountains such as the Scottish Highlands have been slowly ground down by wind and water, yielding materials which later settle into sediments and may ultimately push up again somewhere else as new mountains like the Alps, and the cycle resumes. In a world of such recycling, we have to curb our importunate demands for a continuous fossil record to bridge every gap in evolution. It isn't just bad luck that fossils are often missing, but an inherent consequence of the way sedimentary rocks are made. It would be positively worrying if there were no gaps in the fossil record. Old rocks, with their fossils, are actively being destroyed by the very process that goes to make new ones.

Often fossils are formed when mineral-charged water penetrates the fabric of a buried creature. In life, bone is porous and spongy, for good engineering and economic reasons. When water seeps through the interstices of a dead bone, minerals are slowly deposited as the ages pass. I say slowly almost as a ritual, but it isn't always slow. Think how fast a kettle furs up. On an Australian beach I once found a bottletop embedded in stone. But the process usually is slow. Whatever the speed, the stone of a fossil eventually takes on the shape of the original bone, and that shape is revealed to us millions of years later, even if — which doesn't always happen — every atom of the original bone has disappeared. The petrified forest in the Painted Desert of Arizona consists of trees whose tissues were slowly replaced by silica and other minerals leached out of ground water. Two hundred million years dead, the trees are now stone through and through, but many of their microscopic cellular details can still be clearly seen in petrified form.

I've already mentioned that sometimes the original organism, or a part of it, forms a natural mould or imprint from which it is subsequently removed, or dissolved. I fondly recall two happy days in Texas in 1987 spent wading through the Paluxy River examining, and even putting my feet in, the dinosaur footprints preserved in its smooth limestone bed. A bizarre local legend grew up that some  {64}  of these are giant manprints contemporary with undoubted dinosaur prints, and in consequence the nearby town of Glen Rose became home to a thriving cottage industry, artlessly faking giant manprints in blocks of cement (for sale to gullible creationists who know, all too well, that ‘There were giants in the earth in those days’: Genesis 6:4). The story of the real footprints has been carefully worked out, and is fascinating. The obviously dinosaurian ones are three-toed. The ones that look faintly like a human foot have no toes, and were made by dinosaurs walking on the back of the foot rather than running on their toes. Also, the viscous mud would have tended to ooze back in at the sides of the footprint, obscuring the side toes of the dinosaurs. More poignant for us, at Laetoli in Tanzania are the companionable footprints of three real hominids, probably Australopithecus afarensis, walking together 3.6 million years ago in what was then fresh volcanic ash. Who does not wonder what these individuals were to each other, whether they held hands or even talked, and what forgotten errand they shared in a Pliocene dawn?

Sometimes, as I mentioned when discussing lava, the mould may become filled with a different material, which subsequently hardens to form a cast of the original animal or organ. I am writing this on a table in the garden whose top is a six-inch thick, seven-foot square slab of Purbeck sedimentary limestone, of Jurassic age, perhaps 150 million years old.^* Along with lots of fossil mollusc shells, there is an alleged (by the distinguished and eccentric sculptor who procured it for me) dinosaur footprint on the underside of the table, but it is a footprint in relief, standing out from the surface. The original footprint (if indeed it is genuine, for it looks pretty nondescript to me) must have served as a mould, into which the sediment later settled. The mould then disappeared. Much of what we know about ancient brains comes to us in the form of such casts: ‘endocasts’ of the insides of skulls, often imprinted with surprisingly full details of the brain surface itself.

Less frequently than shells, bones or teeth, soft parts of animals sometimes fossilise. The most famous sites are the Burgess Shale of the Canadian Rockies, and the slightly older Chengjiang in South China which we shall meet again in the Velvet Worm's Tale. At both these sites, fossils of worms and other soft,

boneless and toothless creatures (as well as the usual hard ones) wonderfully record the Cambrian Period, more than half a billion years ago. We are outstandingly lucky to have Chengjiang and the Burgess Shale. Indeed, as I have already remarked, we are pretty lucky to have fossils at all, anywhere. It has been estimated that 90 per cent of all species will never be known to us as fossils. If that is the figure for whole species, just think how few individuals can ever hope to achieve the ambition with which the tale began, and end up as fossils. One estimate puts the odds at one in a million among vertebrates. That sounds high to me, and the true figure must be far less among animals with no hard parts.

HABILINES

Back another million years from Homo ergaster, 1 million years ago there is no longer any doubt in which continent our genetic roots lie. Everyone agrees, ‘multiregionalists’ included, that Africa is the place. The most compelling fossil bones at this age are normally classified as Homo habilis. Some authorities recognise a second, very similar contemporary type, which they call Homo rudolfensis. Others equate it with Kenyapithecus, described by the Leakey team in 2001. Yet others cautiously refrain from giving these fossils a species name at all, and just call them all ‘Early Homo’. As usual I shan't take a stand on names. What matters is the real flesh and bone creatures themselves, and I shall use ‘Habilines’ as an anglicism for all of them. Habiline fossils, being older, are understandably less plentiful than Ergasts. The best-preserved skull bears the reference number KNM-ER 1470 and is widely known as Fourteen Seventy. It lived about 1.9 million years ago.

The Habilines were about as different from Ergasts as Ergasts from us, and, as we should expect, there were intermediates which are hard to classify. Habiline skulls are less robust than Ergast skulls, and lack the pronounced brow ridges. In this respect, Habilines were more like us. This should cause no surprise. Robustness and brow ridges are peculiarities that, possibly like hair, hominids seem able to acquire and lose again at the drop of an evolutionary hat. Habilines mark the place in our history where the brain, that most dramatic of human peculiarities, starts to expand. Or more accurately, starts to expand beyond the normal size of the already large brains of other apes. This distinction, indeed, is the rationale for placing the Habilines in the genus Homo at all. For many palaeontologists, the large brain is the distinguishing feature of our genus. Habilines, with their brains pushing the 750 cc barrier, have crossed the rubicon and are human. As readers may soon become tired of hearing, I am not a lover of rubicons, barriers and gaps. In particular, there is no reason to expect an early Habiline to be separated from its predecessor by a bigger gap than from its successor. It might seem tempting because the predecessor has a different generic name  {68}  (Australopithecus) whereas the successor (Homo ergaster) is ‘merely’ another Homo. It is true that when we look at living species, we expect members of different genera to be less alike than members of different species within the same genus. But it can't work like that for fossils, if we have a continuous historical lineage in evolution. At the borderline between any fossil species and its immediate predecessor, there must be some individuals about whom it is absurd to argue, since the reductio of such an argument must be that parents of one species gave birth to a child of the other. It is even more absurd to suggest that a baby of the genus Homo was born to parents of a completely different genus, Australopithecus. These are evolutionary regions into which our zoological naming conventions were never designed to go.^*

Setting names to one side frees us for a more constructive discussion about why the brain suddenly started to enlarge. How would we measure the enlargement of the hominid brain and plot a graph of average brain size against geological time? There is no problem about the units in which we measure time: millions of years. Brain size is harder. Fossil skulls and endocasts allow us to estimate brain size in cubic centimetres, and it is easy enough to convert this to grams. But absolute brain size is not necessarily the measure you want. An elephant has a bigger brain than a person, and it isn't just vanity that makes us think we are brainier than elephants. Tyrannosaurus's brain was not much smaller than ours, but all dinosaurs are regarded as small-brained, slow-witted creatures. What makes us cleverer is that we have bigger brains for our size than dinosaurs. But what, more precisely, does ‘for our size’ mean?

There are mathematical methods of correcting for absolute size, and expressing an animal's brain size as a function of how big it ‘ought to be’ given its body size. This is a topic worthy of a tale in its own right, and Homo habilis, handyman, from his uneasy vantage point straddling the brain-size ‘rubicon’, will tell it.

The Handyman's Tale

We want to know whether the brain of a particular creature such as Homo habilis is larger or smaller than it ‘ought’ to be, given that animal's body size. We accept (slightly unwillingly in my case but I'll let it pass) that large animals just have to have large brains and small animals small brains. Making allowance for this, we still want to know whether some species are ‘brainier’ than others. So, how do we make allowance for body size? We need a reasonable basis for calculating the expected brain size of an animal from its body size, so that we can decide whether the actual brain of a particular animal is larger or smaller than expected.

In our pilgrimage to the past, we happen to have met the problem in connection with brains, but similar questions can arise with respect to any part of the body. Do some animals have larger (or smaller) hearts, or kidneys, or shoulder-blades than they ‘ought’ to have for their size? If so, this might suggest that their way of life makes special demands on the heart (kidney or shoulderblade).  {69}  How do we know what size any bit of an animal ‘ought’ to be, given that we know its total body size? Note that ‘ought to be’ doesn't mean ‘needs to have for functional reasons’. It means ‘would be expected to have, knowing what comparable animals have’. Since this is the Handyman's Tale, and since the Handy-man's most surprising feature is his brain, we'll go on using brains for the sake of discussion. The lessons we learn will be more general.

We begin by making a scatter plot of brain mass against body mass for a large number of species. Each symbol on the graph below (from my colleague the distinguished anthropologist Robert Martin) represents one species of living mammal — 309 of them, ranging from the smallest to the largest. In case you are interested, Homo sapiens is the point with the arrow, and the one immediately next to us is a dolphin. The heavy black line drawn through the middle of the points is the straight line that, according to statistical calculation, gives the best fit to all the points.^*

Log-log plot of brain mass against body mass for different species of placental mammal. Flled triangles represent primates. Adapted from Martin [185].

A slight complication, which will make sense in a moment, is that things work better if we make the scales of both axes logarithmic, and that is how this graph was made. We plot the logarithm of an animal's brain mass against the logarithm of its body mass. Logarithmic means that equal steps along the bottom of the graph (or equal steps up the side) represent multiplications by some fixed number, say ten, rather than additions of a number, as in an ordinary graph. The reason ten is convenient is that we can then think of a logarithm as a count of the number of noughts. If you have to multiply a mouse's mass by a million to get an elephant's, this means you have to add six noughts to the mouse's mass: you have to add six to the logarithm of the one, to  {70}  get the logarithm of the other. Halfway between them on the logarithmic scale — three noughts — lies an animal that weighs a thousand times as much as a mouse, or a thousandth of an elephant: a person, perhaps. Using round numbers like a thousand and a million is just to make the explanation easy. ‘Three and a half noughts’ means somewhere between a thousand and ten thousand. Note that ‘halfway between’ when we are counting noughts is a very different matter from halfway between when we are counting grams. This is all taken care of automatically by looking up the logarithms of the numbers. Logarithmic scales call on a different kind of intuition from simple arithmetic scales, which is useful for different purposes.

There are at least three good reasons for using a logarithmic scale. First, it makes it possible to get a pygmy shrew, a horse and a blue whale on the same graph without needing a hundred yards of paper. Second, it makes it easy to read off multiplicative factors, which is sometimes what we want to do. We don't just want to know that we have a bigger brain than we should have for our body size. We want to know that our brain is, say, six times as big as it ‘should’ be. Such multiplicative judgements can be read directly off a logarithmic graph: that is what logarithmic means. The third reason for preferring logarithmic scales takes a little longer to explain. One way of putting it is that it makes our scatterpoints fall along straight lines instead of curves, but there is more to it than that. Let me try to explain to my fellow dysnumerics.

Suppose you take an object like a sphere or a cube, or indeed a brain, and you inflate it evenly so it is still the same shape but ten times the size. In the case of the sphere, this means ten times the diameter. In the case of the cube, or the brain, it means ten times the width (and height and depth). In all these cases of proportionate scaling up, what will happen to the volume? It will not be ten times as great — it will be a thousand times as great! You can prove it for cubes if you imagine stacking sugar lumps. The same applies to uniformly inflating any shape you like. Multiply length by ten and, provided the shape doesn't change, you automatically multiply volume by a thousand. In the special case of a tenfold inflation, this is equivalent to adding three noughts. More generally, volume is proportional to the third power of length, and the logarithm is multiplied by three.

We can do the same sort of calculation for area. But area increases in proportion to the second power of length rather than the third power. Not for nothing is raising to the second power called squaring while raising to the third power is called cubing. The volume of a sugar lump determines how much sugar there is, and what it costs. But how fast it dissolves will be determined by its surface area (not a simple calculation because, as it dissolves, the remaining surface area will shrink more slowly than the volume of sugar remaining). When you uniformly inflate an object by doubling its length (width, etc.), you multiply the surface area by 2 × 2 = 4. Multiply its length by ten, and you multiply the surface area by 10 × 10 = 100 or add two noughts to the number. The logarithm of area increases as double the logarithm of length, while the logarithm of volume increases as treble the logarithm of length. A two-centimetre sugar lump will contain eight times as much sugar as a one-centimetre lump, but it  {71}  will release that sugar into the tea only four times as fast (at least initially), because it is the surface of the lump that is exposed to the tea.

Now imagine that we make a scatter plot of sugar lumps of a wide range of sizes, with mass of lump (proportional to volume) along the bottom axis, and (initial) rate of dissolving up the side of the graph (assumed proportional to area). In a non-logarithmic graph, the points will fall along a curved line, which will be quite hard to interpret and not very helpful. But if we plot the logarithm of mass against the logarithm of initial dissolving rate, we shall see something much more informative. For every threefold increment of log mass, we shall see a doubling of log surface. On the log-log scale, the points will not fall along a curve, they will fall along a straight line. What is more, the slope of the straight line will mean something very precise. It will be a slope of two-thirds: for every two steps along the area axis, the line takes three steps along the volume axis. For every doubling of the logarithm of area, the logarithm of volume is tripled. Two-thirds is not the only informative slope of line we might see in a log-log plot. Plots of this kind are informative because the slope of the line gives us an intuitive feel for what is going on vis-a-vis such things as volumes and areas. And volumes and areas and the complicated relationships between them are extremely important in understanding living bodies and their parts.

I am not particularly mathematical — that's putting it mildly — but even I can see the fascination of this. And it gets better, because the same principle works for all shapes, not just tidy ones like cubes and spheres, but complicated shapes like animals and bits of animals such as kidneys and brains. All that is required is that size change should come about by simple inflation or deflation without a change of shape. This gives us a sort of null-expectation, against which to compare real measurements. If one species of animal is 10 times the length of another, its mass will be 1,000 times as great, but only if the shapes are the same. In fact, shape is very likely to have evolved to be systematically different as you go from small animals to large, and we can now see why.

Big animals need to be a different shape from small animals, if only because of the area/volume scaling rules we have just seen. If you turned a shrew into an elephant just by inflating it, retaining the same shape, it wouldn't survive. Because it is now about a million times heavier, a whole lot of new problems arise. Some of the problems an animal faces depend upon volume (mass). Others depend on area. Still others depend on some complicated function of the two, or on some different consideration altogether. Like a sugar lump's rate of dissolving, an animal's rate of losing heat, or of losing water through the skin, will be proportional to the area that it presents to the outside world. But its rate of generating heat is probably more related to the number of cells in the body, which is a function of volume.

A shrew scaled up to elephant size would have spindly legs that would break under the strain, and its slender muscles would be too weak to work. The strength of a muscle is proportional not to its volume but to its cross-sectional area. This is because muscular movement is the summed movement of millions of molecular fibres, sliding past each other in parallel. The number of fibres you can pack into a muscle depends upon the area of its cross-section (second power  {72}  of linear size). But the task that the muscle has to perform — supporting an elephant, say — is proportional to the mass of the elephant (third power of linear size). So, the elephant needs proportionately more muscle fibres than a shrew, in order to support its mass. Therefore the cross sectional area of elephant muscles needs to be larger than you'd expect from simple scaling up, and the volume of muscle in an elephant must be more than you'd expect from simple scaling up. For different particular reasons, the conclusion is similar for bones. This is why large animals like elephants have massive tree-trunk shaped legs. Galileo was one of the first to realise this, although his diagram exaggerates the true effect.

Galileo was one of the first to realise this Galileo's drawings of relative bone sizes, from Discourses and Mathematical Demonstrations Relating to Two New Sciences, published 1638.

Suppose an elephant-sized animal is 100 times as long as a shrew-sized animal. With no change of shape, the area of its outer skin would be 10,000 times as great as the shrew's and its volume and mass a million times as great. If touch-sensitive cells are equally spaced through the skin, the elephant will need 10,000 times as many of them, and the part of the brain that services them will perhaps need to be scaled in proportion. The total number of cells in the elephant's body will be a million times as great as in the shrew, and they'll all have to be serviced by capillary blood vessels. What does this do to the number of miles of blood vessel that we expect in a large animal, as distinct from a small one? That's a complicated calculation, and one that we'll return to in a later tale. For the moment, it is enough for us to understand that when we calculate it we cannot ignore these scaling rules for volumes and areas. And the logarithmic plot is a good method for getting intuitive clues to such things. The main conclusion is that, as animals get larger or smaller in evolution, we positively expect their shape to change in predictable directions.

We got into this through thinking about brain size. We can't just compare our brains with those of Homo habilis, Australopithecus or any other species without making allowance for body size. We need some index of brain size which makes allowance for body size. We can't divide brain size by body size, though that would be better than just comparing absolute brain sizes. A better way is to make use of the logarithmic plots we have just been discussing. Plot the logarithm of brain mass against the logarithm of body mass for lots of species of different sizes. The points will probably fall around a straight line, as indeed they do in the graph on page 70. If the slope of the line is 1/1 (brain size exactly proportional to body size) it will suggest that each brain cell is capable of servicing some fixed number of body cells. A slope of 2/3 would suggest that brains are like bones and muscles: a given volume of body (or number of body cells) demands a certain surface area of brain. Some other slope would need yet a different interpretation. So, what is the actual slope of the line?

It is neither 1/1 nor 2/3 but something in between. To be exact, it is a remarkably good fit to 3/4. Why 3/4? Well, that is a tale in itself, which will be told, as you will no doubt have guessed, by the cauliflower (well, a brain does look a bit  {73}  like a cauliflower). Without pre-empting the Cauliflower's Tale, I will just say that the 3/4 slope is not special to brains, but crops up all over the place in all sorts of living creatures, including plants like cauliflowers. Applied to brain size, and with the intuitive rationale that must wait for the Cauliflower's Tale, this observed line, with its 3/4 slope, is the meaning we are going to attach to the word ‘expect’ as it was used in the opening paragraphs of this tale.

Although the points cluster about the ‘expected’ straight line of slope 3/4, not all the points fall exactly on the line. A ‘brainy’ species is one whose point on the graph falls above the line. Its brain is larger than ‘expected’ for its body size. A species whose brain is smaller than ‘expected’ falls below the line. The distance above, or below, the line, is our measure of how much bigger than ‘expected’, or smaller, it is. A point that falls exactly on the line represents a species whose brain is exactly the size expected for its body size.

Expected on what assumption? On the assumption that it is typical of the set of species whose data contributed to calculating the line. So, if the line was calculated from a representative range of land vertebrates, from geckos to elephants, the fact that all mammals fall above the line (and all reptiles below) means that mammals have bigger brains than you would ‘expect’ of a typical vertebrate. If we calculate a separate line from a representative range of mammals, it will be parallel to the vertebrate line, still with a slope of 3/4, but its absolute height will be higher. A separate line calculated from a representative range of primates (monkeys and apes) will be higher again, but still parallel with a slope of 3/4. And Homo sapiens is higher than any of them.

The human brain is ‘too’ big, even by the standards of primates, and the average primate brain is too big by the standards of mammals generally. For that matter, the average mammal brain is too big by the standards of vertebrates. Another way to say all this is that the scatter of points in the vertebrate graph is wider than the scatter of points on the mammal graph, which is in turn wider than the primate scatter which it includes. The xenarthran scatter of points on the graph (xenarthrans are an order of South American mammals, including sloths, anteaters and armadillos) sits below the average of mammals, of which the xenarthran scatter forms a part.^*

Harry Jerison, the father of fossil brain size studies, proposed an index, the Encephalisation Quotient or EQ, as a measure of how much bigger, or smaller, the brain of a particular species is than it ‘should’ be for its size, given that it is a member of some larger grouping, such as the vertebrates or the mammals. Notice that the EQ. requires us to specify the larger group which is being used as the baseline for comparison. The EQ of a species is its distance above, or below, the average line for the specified larger grouping. Jerison thought the slope of the line was 2/3, whereas modern studies agree that it is 3/4, so Jerison's own estimates of EQhave to be amended accordingly, as was pointed out by Robert Martin. When this is done, it turns out that the modern human brain is about six times as big as it should be, for a mammal of equivalent size (the EQ would be larger, if calculated against the standard of the vertebrates as a whole, rather than the mammals as a whole. And it would be smaller if calculated against the standard of primates as a whole).^* A modern chimpanzee's brain is about twice

	Plot of Harry Jerison's EQ or ‘braininess index’ against time, in millions of years on a log scale. The results have been corrected for a slope of 3/4 for the reference baseline (see text).

the size it should be for a typical mammal, and so are the brains of australopithecines. Homo habilis and Homo erectus, the species that are probably intermediate in evolution between Australopithecus and ourselves, are also intermediate in brain size. Both have an EQ of about 4, meaning that their brains were about four times as big as they should have been for a mammal of equivalent size.

The graph shows an estimate of EQ, the ‘braininess index’, for various fossil primates and ape-men, as a function of the time at which they lived. With considerable pinches of salt you could read it as a rough graph of decreasing braininess as we go backwards in evolutionary time. At the top of the graph is modern Homo sapiens with an EQ of 6, meaning our brain is six times as heavy as it ‘should’ be for a typical mammal of our size. At the bottom of the graph are fossils who might possibly represent something like Concestor 5, our common ancestor with the Old World monkeys. Their estimated EQ was about 1, meaning they had a brain which would be ‘about right’ for a typical mammal of their size today. Intermediate on the graph are various species of Australopithecus and Homo who might be close to our ancestral line at the time they lived. The drawn line is, once again, the straight line which best fits the points on the graph.

I advised pinches of salt, and let me raise that to ladles of salt. The EQ

Comparison of four hominid skulls, showing clear growth in brain size beginning with Homo habilis. The skulls have been scaled to the same height, and are average profiles based on several fossil examples.
	H. sapiens	H. erectus	H. habilis	A. afarensis

‘braininess’ index is calculated from two measured quantities, the brain mass and the body mass. In the case of fossils, both these quantities have to be estimated from the fragments that have come down to us, and there is a huge margin of error, especially in the estimation of body mass. The point on the graph for Homo habilis shows it as ‘brainier’ than Homo erectus. I don't believe this. The absolute brain size of H. erectus is undeniably larger. The inflation of the H. habilis EQ comes from the much lower estimated body mass. But to get an idea of the margin of error, think of the enormous range of body mass in modern humans. EQas a measure is extremely sensitive to error in measuring body mass, which is raised, remember, to a power in the EQ formula. So, the scatter of points about the line largely reflects erratic estimation of body mass. On the other hand, the trend over time, as represented by the line, is probably real. The methods explained in this tale, in particular the estimates of EQ in the graph at the end, bear out our subjective impression that one of the most important things that has happened during the last 3 million years of our evolution was the ballooning of our already large primate brain. The next obvious question is why. What Darwinian selection pressure drove the enlargement of the brain during the past three million years?

Because it happened after we rose up on our hind legs, some people have suggested that brain inflation was driven by the freeing of the hands and the opportunity this offered for precision-controlled manual dexterity. In a general way I find this a plausible idea, though no more than several others that have been offered. But the enlargement of the human brain looks, as evolutionary trends go, explosive. I think inflationary evolution demands a special kind of inflationary explanation. In Unweaving the Rainbow, in the chapter called ‘The Balloon of the Mind’, I developed this inflationary theme in a general theory of what I called ‘software-hardware co-evolution’. The computer analogy is with software innovations and hardware innovations triggering each other in an escalating spiral. Software innovations demand an escalation in hardware, which in turn provokes an escalation in software, and so the inflation gathers pace. In the brain, my candidates for the kind of thing I meant by a software innovation were language, spoor-tracking, throwing, and mêmes. One theory of brain inflation that I didn't do justice to in my earlier book was sexual selection, and it is for this reason alone that I shall give it special prominence later in this book.

Could the enlarged human brain, or rather its products such as body painting, epic poetry and ritual dances, have evolved as a kind of mental peacock's tail? I have long had a soft spot for the idea, but nobody developed it into a proper theory until Geoffrey Miller, a young American evolutionary psychologist worldng in England, wrote his book, The Mating Mind. We shall hear this idea in the Peacock's Tale, after the bird pilgrims join us at Rendezvous 16.

APE-MEN

The popular literature on human fossils is hyped up with alleged ambition to discover the ‘earliest’ human ancestor. This is silly. You can ask a specific question like ‘Which was the earliest human ancestor to walk habitually on two legs?’ Or ‘Which was the first creature to be our ancestor and not the ancestor of a chimpanzee?’ Or ‘Which was the earliest human ancestor to have a brain volume larger than 600 cc?’ Those questions at least mean something in principle, although they are hard to answer in practice and some of them suffer from the vice of erecting artificial gaps in a seamless continuum. But ‘Who was the earliest human ancestor?’ means nothing at all.

More insidiously, the competition to find human ancestors means that new fossil discoveries are touted as on the ‘main’ human line whenever remotely possible. But as the ground yields up more and more fossils, it becomes increasingly clear that, during most of hominid history, Africa housed several species of hominid simultaneously. This has to mean that many fossil species now thought of as ancestral will turn out to be our cousins.

At various times since Homo first appeared in Africa, it shared the continent with more robust hominids, perhaps several different species of them. As usual their affinities, and the exact number of species, are hotly disputed. Names that have been attached to various of these creatures (we met them in the graph at the end of the Handyman's Tale) are Australopithecus (or Paranthropus) robustus, Australopithecus (or Paranthropus or Zinjanthropus) boisei, and Australopithecus (or Paranthropus) aethiopicus. They seem to have evolved from more ‘gracile’ apes (gracile being the opposite of robust). The gracile apes are also placed in the genus Australopithecus, and we too almost certainly emerged from among gracile australopithecine ranks. Indeed, it is often difficult to distinguish early Homo from gracile australopithecines — which prompted my diatribe on the naming conventions that place them in separate genera.

The immediate ancestors of Homo would be classified as some kind of gracile australopithecine. Let's look at some of the gracile fossils. Mrs Pies is one for whom I have had special affection ever since the Transvaal Museum in Pretoria presented me with a beautiful cast of her skull, on the fiftieth anniversary of her discovery at Sterkfontein nearby, when I gave the Robert Broom Memorial Lecture in honour of her discoverer. She lived about 2.5 million years ago. Her nickname comes from the genus, Plesianthropus, to which she was originally assigned before people decided to incorporate her into Australopithecus; and from the fact that she was thought (perhaps erroneously as is now suspected) to be female.  {77}  Individual fossil hominids often pick up pet names like this. ‘Mr Pies’, naturally, is a more recently discovered fossil from Sterkfontein who is in the same species as Mrs Pies, Australopithecus africanus. Fossils with other nicknames include ‘Dear Boy’, a robust australopithecine also known as ‘Zinj’ because he was originally named Zinjanthropus boisei, ‘Little Foot’ (see below) and the famous Lucy, to whom we now turn.

We meet Lucy as our time machine's odometer touches 3.2 million years. Another gracile australopithecine, she is often mentioned because her species, Australopithecus afarensis, is a hot contender for a human ancestor. Her discoverers, Donald Johanson and his colleagues, also found fossils of 13 similar individuals in the same area, known as the ‘First Family’. Other ‘Lucys’ have since been found between about 3 and 4 million years ago in other parts of East Africa. The 3.6-million-year-old footprints discovered by Mary Leakey at Laetoli (page 66) are attributed to A. afarensis. Whatever the Latin name, evidently somebody was walking bipedally at that time. Lucy is not greatly different from Mrs Pies, and some people think of Lucys as an earlier version of Mrs Pies. They are anyway more like each other than either is like the robust australopithecines. Early East African Lucys are said to have a slightly smaller brain than later South African Mrs Pleses, but there isn't much in it. Their brains were no more different from each other than some modern human brains are from other modern human brains.

As we have come to expect, the more recent afarensis individuals such as Lucy are slightly different from the earliest 3.9 million year old afarensis forms. Differences collect over time and, as we emerge from our time machine 4 million years ago, we find more creatures who might well be ancestral to Lucy and her kin, but who are sufficiently different, in the direction of being more chimpanzee-like, to merit a different species name. Discovered by Meave Leakey and her team, these Australopithecus anamensis consist of more than 80 fossils from two different sites near Lake Turkana. No intact skull has been found, but there is a splendid lower jaw which plausibly could belong to an ancestor of ours.

But the most exciting discovery from this time period, and a good reason for calling a temporary halt here, is a fossil yet to be fully described in print. Affectionately  {78}  known as Little Foot, this skeleton from the Sterkfontein caves of South Africa was originally dated to about three million years ago, but has recently been redated to just over four million. Its discovery is a piece of detective work worthy of a Conan Doyle story. Bits of Little Foot's left foot were dug up from Sterkfontein in 1978, but the bones were stored away, unremarked and unlabelled, until 1994 when the palaeontologist Ronald Clarke, working under the direction of Phillip Tobias, accidentally rediscovered them in a box in the shed used by workers at the Sterkfontein cave. Three years later, Clarke chanced upon another box of bones from Sterkfontein, in a store room at Witwatersrand University. This box was labelled ‘Cercopithecoids’. Clarke had an interest in this kind of monkey, so he looked in the box and was delighted to notice a hominid foot bone in amongst the monkey bones. Several foot and leg bones in the box seemed to match the bones previously found in the Sterkfontein shed. One was half a right shinbone, broken across. Clarke gave a cast of the shinbone to two African assistants, Nkwane Molefe and Stephen Motsumi, and asked them to return to Sterkfontein and look for the other half.

The task I had set them was like looking for a needle in a haystack as the grotto is an enormous, deep, dark cavern with breccia exposed on the walls, floor and ceiling. After two days of searching with the aid of hand-held lamps, they found it on 3 July 1997.

Molefe and Motsumi's jigsaw feat was the more astonishing because the bone that fitted their cast was

at the opposite end to where we had previously excavated. The fit was perfect, despite the bone having been blasted apart by lime workers 65 or more years previously. To the left of the exposed end of the right tibia could be seen the section of the broken-off shaft of the left tibia, to which the lower end of the left tibia with foot bones could be joined. To the left of that could be seen the broken-off shaft of the left fibula. From their positions with the lower limbs in correct anatomical relationship, it seemed that the whole skeleton had to be there, lying face downwards.

Actually, it wasn't quite there but, after pondering the geological collapses in the area, Clarke deduced where it must be and, sure enough, Motsumi's chisel found it there. Clarke and his team were indeed lucky, but here we have a first-class example of that maxim of scientists since Louis Pasteur: ‘Fortune favours the prepared mind.’

Little Foot is still to be fully excavated, described and formally named, but preliminary reports suggest a spectacular find, rivalling Lucy in completeness but older. Although more human-like than chimpanzee-like, the big toe is more divergent than our toes. This might suggest that Little Foot grasped tree boughs with its feet in a way that we cannot. Although it almost certainly walked biped-ally, it probably climbed too and walked with a different gait from us. Like other australopithecines, it may have spent time in trees, perhaps bivouacking in them at night like modern chimpanzees.

Having paused at the 4-million-year milestone, let's take a quick peek at the  {79}  journey yet to unfold. There are some fragmentary remains of a possibly bipedal Australopithecus-like creature even further back in time, about 4.4 million years ago. Tim White and his colleagues discovered it in Ethiopia, quite close to Lucy's last resting place. They named it Ardipithecus ramidus^* although some prefer to keep it in the genus Australopithecus. No skull of Ardipithecus has so far been found, but its teeth suggest that it was more chimpanzee-like than any later humans. Its tooth enamel was thicker than that of chimpanzees, but not as thick as ours. A few isolated cranial bones have been found, and these indicate that the skull rested on top of the vertebral column, as in us, rather than in front of it, as in chimpanzees. This suggests a vertical stance, and such foot bones as have been found support the idea that Ardipithecus was bipedal. Bipedality separates humans from the rest of the mammals so dramatically that

I feel it deserves a tale to itself. And who better fitted to tell it than Little Foot?

Little Foot's Tale

It isn't particularly helpful to dream up reasons why walking on two legs might be generally a good thing. If it were, the chimps would do it too, to say nothing of other mammals. There is no obvious reason for saying that either bipedal or quadrupedal running is faster or more efficient than the other. Galloping mammals can be astonishingly fleet, using the up-and-down flexibility of the backbone to achieve — among other benefits — a lengthened effective stride. But ostriches show that a man-like bipedal gait can be a match for a quadrupedal horse. Indeed a top human sprinter, though noticeably slower than a horse or dog (or ostrich or kangaroo, for that matter), is not disgracefully slow. Quadrupedal monkeys and apes are generally undistinguished runners, perhaps because their bodily designs have to compromise with the needs of a climber. Even baboons, which normally forage and run on the ground, resort to the trees to sleep and as a defence against predators, but baboons can run fast when they need to.

So, when we ask why our ancestors rose up on their hind legs, and when we imagine the quadrupedal alternative that we forsook, it is unfair to ‘think cheetah’, or anything like it. When our ancestors first stood up, there was no overwhelmingly strong advantage in efficiency or speed. We should look elsewhere for the natural selection pressure which drove us to this revolutionary change in gait.

Like some other quadrupeds, chimpanzees can be trained to walk bipedally, and they often do it anyway over short distances. So it probably wouldn't be insuperably difficult for them to make the switch if there were strong benefits to doing so. Orang utans are even better at it. Wild gibbons, whose fastest method of locomotion is brachiation — swinging under the boughs by their arms — also run across clearings on their hind legs. Some monkeys rise upright, to peer over long grass or to wade through water. A lemur, Verreaux's sifaka, although it lives mainly in trees where it is a spectacular acrobat, ‘dances’ across  {80}  the ground between trees on its hind legs, the arms held up with balletic grace. Doctors sometimes ask us to run on the spot in a mask, so they can measure our oxygen consumption and other metabolic indices when we are exerting ourselves. In 1973 some American biologists, C. R. Taylor and V. J. Rowntree, did this with trained chimpanzees and capuchin monkeys, running on a treadmill. By making the animals run the treadmill either on four legs or on two (they were given something to hold on to), the researchers could compare the oxygen consumption and efficiency of the two gaits. They expected that quadrupedal running would be more efficient. This, after all, is what both species naturally do, and it is what their anatomy fits them for. Maybe bipedalism was helped by the fact that they had something to hold on to. In any case, the result was otherwise. There was no significant difference between the oxygen consumption of the two gaits. Taylor and Rowntree concluded that:

The relative energy cost of bipedal versus quadrupedal running should not be used in arguments about the evolution of bipedal locomotion in man.

Even if this is an exaggeration, it should at least encourage us to look elsewhere for possible benefits of our unusual gait. It arouses the suspicion that, whatever non-locomotor benefits of bipedality we might propose as drivers of its evolution, they probably did not have to fight against strong locomotor costs.

What might a non-locomotor benefit look like? A stimulating suggestion is the sexual selection theory of Maxine Sheets-Johnstone, of the University of Oregon. She thinks we rose on our hind legs as a means of showing off our penises. Those of us that have penises, that is. Females, in her view, were doing it for the opposite reason: concealing their genitals which, in primates, are more prominently displayed on all fours. This is an appealing idea but I don't carry a torch for it. I mention it only as an example of the kind of thing I mean by a non-locomotor theory. As with so many of these theories, we are left wondering why it would apply to our lineage and not to other apes or monkeys.

A different set of theories stresses the freeing of the hands as the really important advantage of bipedality. Perhaps we rose on our hind legs, not because that is a good way of getting about, but because of what we were then able to do with our hands — carry food, for instance. Many apes and monkeys feed on plant matter that is widely available but not particularly rich or concentrated, so you must eat as you go, more or less continuously like a cow. Other kinds of food such as meat or large underground tubers are harder to acquire but, when you do find them, they are valuable — worth carrying home in greater quantity than you can eat. When a leopard makes a kill, the first thing it normally does is drag it up a tree and hang it over a branch, where it will be relatively safe from marauding scavengers and can be revisited for meals. The leopard uses its powerful jaws to hold the carcass, needing all four legs to climb the tree. Having much smaller and weaker jaws than a leopard, did our ancestors benefit from the skill of walking on two legs because it freed their hands for carrying food — perhaps back to a mate or children, or to trade favours with other companions, or to keep in a larder for future needs?  {81} 

Incidentally the latter two possibilities may be closer to each other than they appear. The idea (I attribute this inspired way of expressing it to Steven Pinker) is that before the invention of the freezer the best larder for meat was a companion's belly. How so? The meat itself is no longer available, of course, but the goodwill it buys is safe in long-term storage in a companion's brain. Your companion will remember the favour and repay it when fortunes are reversed.^* Chimpanzees are known to share meat for favours. In historic times, this kind of i.o.u. became tokenised as money.

A particular version of the ‘carrying food home’ theory is that of the American anthropologist Owen Lovejoy. He suggests that females would often have been hampered in their foraging by nursing infants, therefore unable to travel far and wide looking for food. The consequent poor nutrition and poor milk production would have delayed weaning. Suckling females are infertile. Any male who feeds a nursing female accelerates the weaning of her current child and brings her into receptiveness earlier. When this happens, she might make her receptiveness especially available to the male whose provisioning accelerated it. So, a male who can bring lots of food home might gain a direct reproductive advantage over a rival male who just eats where he finds. Hence the evolution of bipedalism to free the hands for carrying.

Other hypotheses of bipedal evolution invoke the benefits of height, perhaps standing upright to look over the long grass; or to keep the head above water while wading. This last is the imaginative ‘aquatic ape’ theory of Alister Hardy, ably championed by Elaine Morgan. Another theory, favoured by John Reader in his fascinating biography of Africa, suggests that upright posture minimises exposure to the sun, limiting it to the top of the head which is consequently furnished with protective hair. Moreover, when the body is not hunched close to the ground, it can lose heat more rapidly.

My colleague the distinguished artist and zoologist Jonathan Kingdon has centred a whole book, Lowly Origin, around the question of the evolution of human bipedality. After a lively review of 13 more-or-less distinct hypotheses, including the ones I have mentioned, Kingdon advances his own sophisticated and multifaceted theory. Rather than seek an immediate benefit of walking upright, Kingdon expounds a complex of quantitative anatomical shifts which arose for some other reason, but which then made it easier to become bipedal (the technical term for this kind of thing is pre-adaptation). The pre-adaptation that Kingdon proposes is what he calls squat feeding. Squat feeding is familiar from baboons in open country, and Kingdon visualises something similar in our ape ancestors in the forest, turning over stones or leaf litter for insects, worms, snails and other nutritious morsels. To do this effectively they would have had to undo some of their adaptations to living up trees. Their feet, previously hand-like for gripping branches, would have become flatter, forming a stable platform for squatting on the haunches. You will already be getting a glimmering of where the argument is going. Flatter, less hand-like feet for squatting are later going to serve as pre-adaptations for upright walking. And you will, as usual, understand that this apparently purposeful way of talking — they had to ‘undo’ their tree-swinging adaptations, etc. — is a shorthand which is easily translated  {82}  into Darwinian terms. Those individuals whose genes happened to make their feet more suitable for squat feeding survived to pass on those genes because squat feeding was efficient and aided their survival. I shall continue to employ the shorthand because it chimes with the way humans naturally think.

A tree-swinging, ‘brachiating’ ape could fancifully be said to walk upside down under the branches — run and leap in the case of an athletic gibbon — using the arms as its ‘legs’ and the shoulder girdle as its ‘pelvis’. Our ancestors probably passed through a brachiating phase, and the true pelvis consequently became rather inflexibly bound to the trunk by long blades of bone, which form a substantial part of a rigid trunk that can be swung as a single unit. Much of this, according to Kingdon, would have needed to change, to make an efficient squat feeder out of an ancestral brachiator. Not all, however. The arms could have remained long. Indeed, long brachiating arms would have been a positively beneficial ‘pre-adaptation’, increasing the reach of the squat feeder and decreasing the frequency with which it had to shuffle to a new squatting position. But the massive, inflexible, top-heavy ape trunk would have been a disadvantage in a squat feeder. The pelvis would have needed to free itself and become less rigidly tied to the trunk, and its blades would have shrunk — to more human proportions. This, to anticipate the later stages of the argument again (you might say that anticipation is what a pre-adaptation argument is all about) just happens to make a better pelvis for bipedal walking. The waist became more flexible, and the spine was held more vertically, to allow the squat-feeding animal to search all around with its arms, turning on the platform of the flat feet and the squatting haunches. The shoulders became lighter and the body less top-heavy. And the point is that these subtle quantitative changes, and the balancing and compensating shifts that went with them, incidentally had the effect of ‘preparing’ the body for bipedal walking.

Not for a moment is Kingdon proposing any kind of anticipation of the future. It is just that an ape whose ancestors were tree-swingers, but which has switched to squat feeding on the forest floor, now has a body which feels relatively comfortable walking on its hind feet. And it would have begun to do this while squat feeding, shuffling to a new squatting position as the old one became depleted. Without realising what was happening, squat feeders were, over the generations, preparing their bodies to feel more comfortable when upright and on two legs; to feel more awkward on four. I use the word comfortable deliberately. It is not a trivial consideration. We are capable of walking on all fours like a typical mammal, but it is uncomfortable: hard work, because of our altered body proportions. Those proportional changes which now make us feel comfortable on two legs originally came about, Kingdon suggests, in the service of a minor shift in food habits — to squat feeding.

There is much more in Jonathan Kingdon's subtle and complex theory, but I will now recommend his book, Lowly Origin, and move on. My own slightly way-out theory of bipedality is very different but not incompatible with his. Indeed, most of the theories of human bipedality are mutually compatible, with the potential to assist rather than oppose one another. As in the case of the enlargement of the human brain, my tentative suggestion is that bipedality may have  {83}  evolved through sexual selection, so again I postpone the matter to the Peacock's Tale.

Whatever theory we believe about the evolutionary origins of human bipedality, it subsequently turned out to be an extremely important event. In former times it was possible to believe, as respected anthropologists did up to the 1960s, that the decisive evolutionary event that first separated us from the other apes was the enlargement of the brain. Rising up on the hind legs was secondary, driven by the benefits of freeing the hands to do the kind of skilled work which the enlarged brain was now capable of controlling and exploiting. Recent fossil finds point decisively towards the reverse sequence. Bipedality came first. Lucy, who lived long after Rendezvous 1, was bipedal, nearly or completely as bipedal as we are, yet her brain was approximately the same size as a chimpanzee's. The enlargement of the brain could still have been associated with the freeing of the hands, but the sequence of events was reversed. If anything it would be the freeing of the hands by bipedal walking that drove the enlargement of the brain. The manual hardware came first, then the controlling brainware evolved to take advantage of it, rather than the other way around.

Epilogue to Little Foot's Tale

Whatever the reason for the evolution of bipedality, recent fossil discoveries seem to indicate that hominids were already bipedal at a date which is pushing disconcertingly close to Rendezvous 1, the fork between ourselves and chimpanzees (disconcerting because it seems to leave little time for bipedality to evolve). In the year 2000, a French team led by Brigitte Senut and Martin Pickford announced a new fossil from the Tugen Hills, east of Lake Victoria in Kenya. Dubbed ‘Millennium Man’, dated at 6 million years and given yet another new generic name, Orrorin tugenensis was also, according to its discoverers, bipedal. Indeed, they claim that the top of its femur, near the hip joint, was more human-like than that of Australopithecus. This evidence, supplemented by fragments of skull bones, suggested to Senut and Pickford that orrorins are ancestral to later hominids and that Lucys are not. These French workers go further and suggest that Ardipithecus might be ancestral to modern chimpanzees rather than to us. Clearly we need more fossils to settle these arguments. Other scientists are sceptical of these French claims, and some doubt that there is enough evidence to show whether Orrorin was or was not bipedal. If it was, since 6 million years is approximately the time of the split from chimpanzees according to molecular evidence, this raises difficult questions about the speed with which bipedality must have arisen.

If a bipedal Orrorin pushes back alarmingly close to Rendezvous 1, a newly discovered skull from Chad in southern Sahara, found by another French team led by Michel Brunet, is even more disturbing to accepted ideas. This is partly because it is so old, and partly because the site is far to the west of the Rift Valley (as we shall see, many authorities had thought early hominid evolution confined to the east of the Rift). Nicknamed Tournai (Hope of Life in the local Goran  {84}  language) its official name is Sahelanthropus tchadensis, after the Sahel region of the Sahara in Chad where it was found. It is an intriguing skull, looking rather human from in front (lacking the protruding face of a chimpanzee or gorilla) but chimpanzee-like from behind, with a chimpanzee-sized braincase. It has an extremely well-developed brow-ridge, even thicker than a gorilla's, which is the main reason for thinking Tournai was male.

Hope of Life. Skull of Sahelanthropus tchadensis, or ‘Tournai’, discovered in trie Sahel region of Chad by Michel Brunet and colleagues in 2001.

The teeth are rather human-like, especially the thickness of the enamel which is intermediate between a chimpanzee's and our own. The foramen magnum (the big hole through which the spinal cord passes) is placed further forward than in a chimpanzee or gorilla, suggesting to Brunet himself, though not to some others, that Tournai was bipedal. Ideally, this should be confirmed by pelvis and leg bones but, unfortunately, nothing but a skull has so far been found.

There are no volcanic remains in the area to provide radio metric dates, and Brunet's team had to use other fossils in the area as an indirect clock. These are compared with already known faunas from other parts of Africa which can be dated absolutely. The comparison yields a date for Tournai of between 6 and 7 million years. Brunet and his colleagues claim it as older than Orrorin, which has predictably elicited indignant ripostes from Orrorin's discoverers. One of them, Brigitte Senut, of the Natural History Museum in Paris, has said that Tournai is ‘a female gorilla’, while her colleague Martin Pickford described Tournai's canine teeth as typical ‘of a large female monkey’. These were the two, remember, who (perhaps rightly) wrote off the human credentials of Ardipithecus, another threat to the priority of their own baby, Orrorin. Other authorities have hailed Tournai more generously: ‘Astonishing.’ ‘Amazing.’ ‘This will have the impact of a small nuclear bomb.’

If their discoverers are right that Orrorin and Tournai were bipedal, this poses problems to any tidy view of human origins. The naive expectation is that evolutionary change spreads itself uniformly to fill the time available for it. If 6 million years elapsed between Rendezvous 1 and modern Homo sapiens, the quantity of change ought to be spun out, pro rata one might naively think, through the 6 million years. But Orrorin and Tournai both lived very close to the date identified from molecular evidence as that of Concestor 1, the split between our line and that of chimpanzees. These fossils even pre-date Concestor 1 according to some datings.

Assuming that the molecular and fossil dates are correct, there seem to be four ways (or some combination from among the four) in which we might respond to Orrorin and Tournai.  {85} 

The last three hypotheses all have difficulties, and many authorities are driven to doubt either the dating, or the supposed bipedality, of Tournai and Orrorin. But if we accept these for the moment and look at the three hypotheses that assume ancient bipedality, there is no strong theoretical reason to favour or disfavour any particular one of them. We shall learn from the Galapagos Finch's Tale and the Lungflsh's Tale that evolution can be extremely rapid or can be extremely slow. So Theory 2 is not implausible. The Marsupial Mole's Tale will teach us that evolution can follow the same path, or strikingly parallel paths, on more than one occasion. There's nothing particularly implausible, then, about Theory 3. Theory 4, at first sight, seems the most surprising. We are so used to the idea that we have risen ‘up’ from the apes that Theory 4 seems to put the cart before the horse, and may even insult human dignity into the bargain (often good for a laugh in my experience). Also there is a so-called law, Dollo's Law, which states that evolution never reverses itself, and it might seem that Theory 4 violates it.

The Blind Cave Fish's Tale, which is about Dollo's Law, will reassure us that this last is not the case. There is nothing in principle wrong with Theory 4. Chimpanzees really could have passed through a more humanoid, bipedal stage before reverting to quadrupedal apehood. As it happens, this very suggestion has been revived by John Gribbin and Jeremy Cherfas, in their two books, The Monkey Puzzle and The First Chimpanzee. They go so far as to suggest that chimpanzees are descended from gracile australopithecines (like Lucy), and gorillas from robust australopithecines (like ‘Dear Boy’). For such an in-your-face radical suggestion, they make a surprisingly good case. It centres on an interpretation of human evolution which has long been widely accepted, although not without controversy: people are juvenile apes who have become sexually mature. Or, putting it another way, we are like chimpanzees who have never grown up.

The Axolotl's Tale explains the theory, which is known as neoteny. To summarise, the axolotl is an overgrown larva, a tadpole with sex organs. In a classic experiment by Vilém Laufberger in Germany, hormone injections persuaded an  {86}  axolotl to grow into a fully adult salamander of a species that nobody had ever seen. More famously in the English-speaking world, Julian Huxley later repeated the experiment, not knowing it had already been done. In the evolution of the axolotl, the adult stage had been chopped off the end of the life cycle. Under the influence of experimentally injected hormone, the axolotl finally grew up, and an adult salamander was recreated, presumably never before seen. The missing last stage of the life cycle was restored.

The lesson was not lost on Julian's younger brother, the novelist Aldous Huxley. His After Many a Summer^* was one of my favourite novels when I was a teenager. It is about a rich man, Jo Stoyte, who resembles William Randolph Hearst and collects objets d'art with the same voracious indifference. His strict religious upbringing has left him with a terror of death, and he employs and equips a brilliant but cynical biologist, Dr Sigismund Obispo, to research how to prolong life in general and Jo Stoyte's life in particular. Jeremy Pordage, a (very) British scholar, has been hired to catalogue some eighteenth-century manuscripts recently acquired as a job lot for Mr Stoyte's library. In an old diary kept by the Fifth Earl of Gonister, Jeremy makes a sensational discovery which he imparts to Dr Obispo. The old Earl was hot on the trail of everlasting life (you have to eat raw fish guts), and there is no evidence that he ever died. Obispo takes the increasingly fretful Stoyte to England in quest of the Fifth Earl's remains... and finds him still alive at 200. The catch is that he has finally matured from the juvenile ape which all the rest of us are into a fully adult ape: quadrupedal, hairy, repellent, urinating on the floor while humming a grotesquely distorted vestige of a Mozart aria. The diabolical Dr Obispo, beside himself with gleeful laughter and evidently acquainted with Julian Huxley's work, tells Stoyte he can start on the fish guts tomorrow.

Gribbin and Cherfas are in effect suggesting that modern chimpanzees and gorillas are like the Earl of Gonister. They are humans (or australopithecines, orrorins or sahelanthropes) who have grown up and become quadrupedal apes again, like their, and our, more distant ancestors. I never thought the Gribbin/Cherfas theory was obviously silly. The new findings of very ancient hominids like Orrorin and Tournai, whose dates push up against our split with chimpanzees, could almost justify them in a sotto voce ‘We told you so’.

Even if we accept Orrorin and Tournai as bipedal, I would not choose with confidence between Theories 2, 3 and 4. And we mustn't forget Theory 1, that they walked on all fours and the problem goes away, which many people think is the most plausible. But of course these different theories make predictions about Concestor 1, our next stopping point. Theories 1,2, and 3 agree in assuming a chimpanzee-like Concestor 1, walking on all fours, but occasionally rising on the hind legs. Theory 4 by contrast differs in assuming a more humanoid Concestor 1. In narrating Rendezvous 1, I have been forced to make a decision between the theories. Somewhat reluctantly, I'll go with the majority, and assume a chimpanzee-like concestor. On to meet it!

Rotate 90 degrees

RENDEZVOUS 1 CHIMPANZEES

Between 5 and 7 million years ago, somewhere in Africa, we human pilgrims enjoy a momentous encounter. It is Rendezvous 1, our first meeting with pilgrims from another species. Two other species to be precise, for the common chimpanzee pilgrims and the pygmy chimpanzee or bonobo pilgrims have already joined forces with each other some 4 million years ‘before’ their rendezvous with us. The common ancestor we share with them, Concestor 1, is our 250,000-greats-grandparent — an approximate guess this, of course, like the comparable estimates that I shall be making for other concestors.

As we approach Rendezvous 1 then, the chimpanzee pilgrims are approaching the same point from another direction. Unfortunately we don't know anything about that other direction. Although Africa has yielded up some thousands of hominid fossils or fragments of fossils, not a single fossil has ever been found which can definitely be regarded as along the chimpanzee line of descent from Concestor 1. This may be because they are forest animals, and the leaf litter of forest floors is not friendly to fossils. Whatever the reason, it means that our chimpanzee pilgrims are searching blind. Their equivalent contemporaries of the Turkana Boy, of 1470, of Mrs Pies, Lucy, Little Foot, Dear Boy, and the rest of ‘our’ fossils — have never been found.

Nevertheless, in our fantasy the chimpanzee pilgrims meet us in some Pliocene forest clearing, and their dark brown eyes, like our less predictable ones, are fixed upon Concestor 1: their ancestor as well as ours. In trying to imagine the shared ancestor, an obvious question to ask is, is it more like modern chimpanzees or modern humans, is it intermediate, or completely different from either?

Notwithstanding the pleasing speculation that ended the previous section — which I would by no means rule out — the prudent answer is that Concestor 1 was more like a chimpanzee, if only because chimpanzees are more like the rest of the apes than humans are. Humans are the odd ones out among apes, both living and fossil. Which is only to say that more evolutionary change has occurred along the human line of descent from the common ancestor, than along the lines leading to the chimpanzees. We must not assume, as many laymen do, that our ancestors were chimpanzees. Indeed, the very phrase ‘missing link’ is suggestive of this misunderstanding. You still hear people saying things like, ‘Well, if we are descended from chimpanzees, why are there still chimpanzees around?’

So, when we and the chimpanzee/bonobo pilgrims meet at the rendezvous point, the likelihood is that the shared ancestor that we greet in that Pliocene clearing was hairy like a chimpanzee, and had a chimpanzee-sized brain.  {88}  Reluctantly to set aside the speculations of the previous chapter, it probably walked on its hands (knuckles) like a chimp, as well as its feet. It probably spent some time up trees, but also lots of time on the ground, maybe squat feeding as Jonathan Kingdon would say. All available evidence suggests that it lived in Africa, and only in Africa. It probably used and made tools, following local traditions as modern chimpanzees still do. It probably was omnivorous, sometimes hunting, but with a preference for fruit.

Bonobos have been seen to kill duikers, but hunting is more frequently documented for common chimpanzees, including highly co-ordinated group pursuits of colobus monkeys. But meat is only a supplement to fruit, which is the main diet of both species. Jane Goodall, who first discovered hunting and intergroup warfare in chimpanzees, was also the first to report their now famous habit of termite fishing, using tools of their own construction. Bonobos have not been seen to do this, but that may be because they have been studied less. Captive bonobos readily use tools. Common chimpanzees in different parts of Africa develop local traditions of tool use. Where Jane

[Graphics removed]

CONCESTOR 1

This reconstruction shows a male and female in an African forest. Concestor 1 probably practised knuckle-walking and occasional bipedality. It is likely to have lived in small groups, feeding mainly on fruit, and using some simple tools rather like chimpanzees today.

Goodall's animals on the east side of the range fish for termites, other groups to the west have developed local traditions of cracking nuts using stone or wood hammers and anvils. Some skill is required. You have to hit hard enough to break the kernel but not so hard as to pulp the nut itself. Although often spoken of as a new and exciting discovery, by the way, nut-cracking was mentioned by Darwin in Chapter 3 of The Descent of Man (1871):

It has often been said that no animal uses any tool; but the chimpanzee in a state of nature cracks a native fruit, somewhat like a walnut, with a stone.

The evidence cited by Darwin (a report by a missionary in Liberia in the 1843 issue of the Boston journal of Natural History) is brief and non-specific. It simply states that ‘the Troglodytes niger, or Black Orang of Africa’ is fond of a species of unidentified nut, which ‘they crack with stones precisely in the manner of human beings’.

The especially interesting thing about nutcracking, termite fishing and other such chimpanzee habits is that local groups have local customs, handed down locally. This is true culture. Local cultures extend to social habits and manners. For example, one local group in the Mahale Mountains in Tanzania has a particular style of social grooming known as the grooming hand clasp. The same gesture has been seen in another population in the Kibale forest in Uganda. But it has never been seen in Jane Goodall's intensively studied population at Gombe Stream. Interestingly, this gesture also spontaneously arose and spread among a captive group of chimpanzees.

If both species of modern chimpanzee used tools in the wild as we do, this would encourage us to think that Concestor 1 probably did too. I think it probably did — even though bonobos have not been seen using tools in the wild, they are adept tool-users in captivity. The fact that common chimpanzees use different tools in different areas, following local traditions, suggests to me that lack of such a tradition in a particular area should not be taken as negative evidence. After all, Jane Goodall's Gombe Stream chimpanzees haven't been seen to crack nuts. Presumably they would, if the West African nut-cracking tradition were introduced to them. I suspect that the same might be true of bonobos. Maybe they just haven't been studied enough in the wild. In any case, I think the indications are strong enough that Concestor 1 made and used tools. This idea is strengthened by the fact that tool use also occurs in wild orang utans, local populations again differing in ways that suggest local traditions.^*

The present-day representatives of the chimpanzee lineage are both forest apes, whereas we are savannah apes, more like baboons except, of course, that baboons are not apes at all but monkeys. Bonobos today are confined to the forests south of the great curve of the River Congo and north of its tributary the Kasai. Common chimpanzees inhabit a wider belt of the continent, north of the Congo, westward to the coast, and extending as far as the Rift Valley in the east.

As we shall see in the Cichlid's Tale, current Darwinian orthodoxy suggests that usually, in order for an ancestral species to split into two daughter species, there is an initial, accidental geographical separation between them. Without the geographical barrier, sexual mixing of the two gene pools keeps them  {91}  together. It is plausible that the great Congo river provided the barrier to gene flow which assisted the evolutionary divergence of the two chimpanzee species from each other, two or three million years ago. In the same way, it has been suggested that the Rift Valley, in the throes of its formation at the time, may have provided the barrier to gene flow which, further in the past, allowed our line to separate from that which gave rise to the chimpanzees.

This Rift Valley theory was proposed and supported by the distinguished Dutch primatologist Adriaan Kortlandt. It became better known when it was later espoused by the French palaeontologist Yves Coppens, and it is now widely called by the name Coppens gave it, East Side Story. Incidentally, I don't know what to make of the fact that, in his native France, Yves Coppens is widely cited as the discoverer of Lucy, even as the ‘father’ of Lucy. In the English-speaking world, this important discovery is universally attributed to Donald Johanson. East Side Story has a hard time dealing with Sahelanthropus (‘Tournai’) from Chad, thousands of miles to the west of the Rift Valley. Australopithecus bahrelghazali, a poorly known australopithecine also discovered in Chad, adds to the problem, although it is younger.

Whatever I say on this matter will soon be out of date when new fossils are discovered, so I'll hand over at this point to the bonobo and his tale.

The Bonobo's Tale

The bonobo, Pan paniscus, looks pretty much like a common chimpanzee, Pan troglodytes, and before 1929 they were not recognised as separate species. The bonobo, despite its other name of pygmy chimpanzee, which should be abandoned, is not noticeably smaller than the common chimpanzee. Its body proportions are slightly different, and so are its habits, and that is the cue for its brief tale. The primatologist Frans de Waal put it neatly: ‘The chimpanzee resolves sexual issues with power; the bonobo resolves power issues with sex...’ Bonobos use sex as a currency of social interaction, somewhat as we use money. They use copulation, or copulatory gestures, to appease, to assert dominance, to cement bonds with other troop members of any age or sex, including small infants. Paedophilia is not a hang-up with bonobos; all kinds of philia seem fine to them. De Waal describes how, in a group of captive bonobos that he watched, the males would develop erections as soon as a keeper approached at feeding time. He speculates that this is in preparation for sexually mediated food-sharing. Female bonobos pair off to practise so-called GG (genital-genital) rubbing.

One female facing another clings with arms and legs to a partner that, standing on both hands and feet, lifts her off the ground. The two females then rub their genital swellings laterally together, emitting grins and squeals that probably reflect orgasmic experiences.

The ‘Haight-Ashbury’ image of free-loving bonobos has led to a piece of wishful thinking among nice people, who perhaps came of age in the 1960s — or maybe  {92}  they are of the ‘medieval bestiary’ school of thought, in which animals exist only to point moral lessons to us. The wishful thinking is that we are more closely related to bonobos than to common chimpanzees. The Margaret Mead in us feels closer to this gentle role-model than to the patriarchal, monkey-butchering chimpanzee. Unfortunately, however, like it or not, we are exactly equally close to both species. This is simply because P. troglodytes and P. paniscus share a common ancestor which lived more recently than the ancestor they share with us. By the same token, molecular evidence suggests that chimpanzees and bonobos are more closely related to humans than they are to gorillas. From this it follows that humans are exactly as close to gorillas as chimpanzees and bonobos are. And we are exactly as close cousins of orang utans as chimpanzees, bonobos and gorillas are.

It does not follow from this that we resemble chimpanzees and bonobos equally. If chimpanzees have changed more than bonobos since the shared ancestor, Concestor 1, we might be more like bonobos than chimpanzees, or vice versa — and we shall probably find different things in common with both our Pan cousins, perhaps in roughly equal measure. They are equally closely related to us because they are linked to us via the same shared ancestor. This is the moral of the Bonobo's Tale, a simple moral and a very general one, which we shall meet again and again at other junctures of our pilgrimage.

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GORILLAS JOIN Phylogeny showing the gorillas diverging from the other African apes around 7 million years ago, as suggested by genetics. The right branch now represents the chimpanzees and humans (Concestor 1 is marked on the branch with a dot at 6 million years ago). The left branch represents the single genus of gorillas, now thought to comprise two species.

RENDEZVOUS 2 GORILLAS

The molecular clock tells us that Rendezvous 2, where the gorillas join us, again in Africa, is only a million years further into our pilgrimage than Rendezvous 1. Seven million years ago, North and South America were not joined, the Andes had not undergone their major uplift and the Himalayas only just so. Nevertheless the continents would have looked pretty much as now and the African climate, while less seasonal and slightly wetter, would have been similar. Africa was more thoroughly forested then than now — even the Sahara would have been wooded savannah at the time.

Unfortunately there are no fossils to bridge the gap between Concestors 2 and i, nothing to guide us in deciding whether Concestor 2, which is perhaps our 300,000-greats-grandparent, was more like a gorilla or more like a chimpanzee or, indeed, more like a human. My guess would be chimpanzee, but this is only because the huge gorilla seems more extreme, and less like the generality of apes. Don't let's exaggerate the unusualness of gorillas, however. They are not the largest apes that have ever lived. The Asian ape Gigantopithecus, a sort of giant orang utan, would have stood head and massive shoulders over the largest gorilla. It lived in China, and went extinct only recently, about half a million years ago, overlapping with Homo erectus and archaic Homo sapiens. This is so recent that some enterprising fantasists have gone so far as to suggest that the Yeti or Abominable Snowman of the Himalayas ... but I digress. Gigantopithecus presumably walked like a gorilla, probably on the knucldes of its hands and the soles of its feet as gorillas and chimpanzees do, and as orang utans, committed as they are to life up trees, do not.

It is a reasonable guess that Concestor 2 was also a knuckle-walker but that, like chimpanzees, it spent time in trees as well, especially at night. Natural selection under a tropical sun favours dark pigmentation as protection against ultraviolet rays, so if we had to guess at Concestor 2's colour we would presumably say black or dark brown. All apes except humans are hairy, so it would be surprising if Concestors 1 and 2 were not. Since chimpanzees, bonobos and gorillas are inhabitants of deep forest, it is plausible to locate Rendezvous 2 in a forest, in Africa, but there is no strong reason to guess any particular part of Africa.

Gorillas are not just giant chimpanzees, they are different in other respects which we need to think about in trying to reconstruct Concestor 2. Gorillas are entirely vegetarian. The males have harems of females. Chimpanzees are more promiscuous, and the differences in breeding systems have interesting consequences  {94}  on the size of their testes as we shall learn from the Seal's Tale. I suspect that breeding systems are evolutionarily labile, meaning easily changed. I don't see any obvious way to guess where Concestor 2 stood in this respect. Indeed, the fact that different human cultures today show a large range of breeding systems, from faithful monogamy to potentially very large harems, reinforces my reluctance to speculate about such matters for Concestor 2, and persuades me to bring my speculations as to its nature to a swift end.

Apes, perhaps especially gorillas, have long been potent generators — and victims — of human myths. The Gorilla's Tale considers our changing attitudes to our closest cousins.

The Gorilla's Tale

The rise of Darwinism in the nineteenth century polarised attitudes towards the apes. Opponents who might have stomached evolution itself balked with visceral horror at cousinship with what they perceived as low and revolting brutes, and desperately tried to inflate our differences from them. This was nowhere more true than with gorillas. Apes were ‘animals’; we were set apart. Worse, where other animals such as cats or deer could be seen as beautiful in their own way, gorillas and other apes, precisely because of their similarity to ourselves, seemed like caricatures, distortions, grotesques.

Darwin never missed an opportunity to put the other side, sometimes in little asides such as his charming observation in The Descent of Man that monkeys ‘smoke tobacco with pleasure’. T. H. Huxley, Darwin's formidable ally, had a robust exchange with Sir Richard Owen, the leading anatomist of the day, who claimed (wrongly as Huxley showed) that the ‘hippocampus minor’ was uniquely diagnostic of the human brain. Nowadays, scientists not only think we  {95}  resemble apes. We include ourselves within the apes, specifically the African apes. We emphasise, by contrast, the distinctness of apes, including humans, from monkeys. To call a gorilla or a chimpanzee a monkey is a solecism.

It has not always been so. In former times, apes were frequently lumped with monkeys, and some of the early descriptions confused apes with baboons, or with Barbary macaques, which indeed are still known as Barbary apes. More surprisingly, long before people thought in terms of evolution at all, and before apes were clearly distinguished from each other or from monkeys, great apes were often confused with humans. Agreeable as it would be to approve this apparent prescience of evolution, it unfortunately may owe more to racism. Early white explorers in Africa saw chimpanzees and gorillas as close kin only to black humans, not to themselves. Interestingly, tribes in both South East Asia and Africa have traditional legends suggesting a reversal of evolution as conventionally seen: their local great apes are regarded as humans who fell from grace. Orang utan means ‘man of the woods’ in Malay.

A picture of an ‘Ourang Outang’ by the Dutch Doctor Bontius in 1658 is, in T. H. Huxley's words, ‘nothing but a very hairy woman of rather comely aspect and with proportions and feet wholly human’. Hairy she is except, oddly, in one of the few places where a real woman is: her pubic region is conspicuously naked. Also very human are the pictures made, a century later, by Linnaeus's pupil Hoppius (1763). One of his creatures has a tail, but is otherwise wholly human, bipedal, and carries a walking stick. Pliny the Elder says that ‘the tailed species have even been known to play at draughts’ (American ‘checkers’).

One might have thought such a mythology would have prepared our civilisation for the idea of evolution when it arrived in the nineteenth century, and might even have accelerated its discovery. Apparently not. Instead, the picture is one of confusion between apes, monkeys and humans. This makes it hard to date the scientific discovery of each species of great ape, and it is often unclear which one is being discovered. The exception is the gorilla, which became known to science the most recently.

In 1847 an American missionary, Dr Thomas Savage, saw in the house of another missionary on the Gaboon river ‘a skull represented by the natives to be a monkey-like animal, remarkable for its size, ferocity and habits’. The unjust reputation for ferocity, later to be hyperbolised in the story of King Kong, comes through loud and clear in an article about the gorilla in the Illustrated London News published in the same year as the Origin of Species. This piece is replete with falsehoods of a quantity and magnitude that try even the high standards set by travellers’ tales of the time:

... a close inspection is almost an impossibility, especially as the moment it sees a man it attacks him. The strength of the adult male being prodigious, and the teeth heavy and powerful, it is said to watch, concealed in the thick branches of the forest trees, the approach of any of the human species, and, as they pass  {96}  under the tree, let down its terrible hind feet, furnished with an enormous thumb, grasp its victim round the throat, lift him from the earth, and, finally, drop him on the ground dead. Sheer malignity prompts the animal to this course, for it does not eat the dead man's flesh, but finds a fiendish gratification in the mere act of killing.

Savage believed the skull in the missionary's possession belonged ‘to a new species of Orang’. He later decided that his new species was none other than the ‘Pongo’ of earlier travellers’ tales in Africa. In naming it formally, Savage, with his anatomist colleague Professor Wyman, avoided Pongo and revived Gorilla, the name used by an ancient Carthaginian admiral for a race of wild hairy people which he claimed to have found on an island off the African coast. Gorilla has survived as both the Latin and common name for Savage's animal, while Pongo is now the Latin name of the orang utan of Asia.

Judging from its location, Savage's species must have been the western gorilla, Gorilla gorilla. Savage and Wyman put it in the same genus as the chimpanzees, and called it Troglodytes gorilla. By the rules of zoological nomenclature, Troglodytes had to be relinquished by both chimpanzee and gorilla because it had already been used for — of all things — the tiny wren. It survived as the specific name of the common chimpanzee, Pan troglodytes, while the former specific name of Savage's gorilla was promoted to become its generic name, Gorilla. The ‘mountain gorilla’ was ‘discovered’ — he shot it! — by the German Robert von Beringe as late as 1902. As we shall see, it is now regarded as a subspecies of the eastern gorilla, and the whole eastern species now — unfairly, one might think — bears his name: Gorilla beringei.

Savage did not believe his gorillas really were the race of islanders reported by the Carthaginian sailor. But the ‘pygmies’, originally mentioned by Homer and Herodotus as a legendary race of very small humans, were later assumed by seventeenth- and eighteenth-century explorers to be none other than the chimpanzees then being discovered in Africa. Tyson (1699) shows a drawing of a ‘Pygmie’ which, as Huxley says, is plainly a young chimpanzee although it, too, is depicted walking upright and carrying a walking stick. Now, of course, we use the word pygmy for small humans again.

This leads us back to the racism which, until relatively late in the twentieth century, was endemic in our culture. Early explorers often assigned the native peoples of the forests a closer affinity with chimpanzees, gorillas or orangs than with the explorers themselves. In the nineteenth century, after Darwin, evolutionists often regarded African peoples as intermediate between apes and Europeans, on the upward path to white supremacy. This is not only factually wrong. It violates a fundamental principle of evolution. Two cousins are always exactly equally related to any outgroup, because they are connected to that outgroup via a shared ancestor. For the reasons given in the Bonobo's Tale, all humans are exactly equally close cousins to all gorillas. Racism and speciesism, and our perennial confusion over how inclusively we wish to cast our moral and ethical net, are brought into sharp and sometimes uncomfortable focus in the history of our attitudes to our fellow humans, and our attitudes to apes — our fellow apes.^*

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RENDEZVOUS 3 ORANG UTANS

Molecular evidence puts Rendezvous 3 — where our ancestral pilgrimage is joined by the orang utans — at 14 million years ago, right in the middle of the Miocene Epoch. Although the world was starting to enter its current cool phase, the climate was warmer and the sea levels higher than at present. Coupled with minor differences in the positions of the continents, this led to the land between Asia and Africa, as well as much of south-east Europe, being intermittently submerged by sea. This bears, as we shall see, on our calculation of where Concestor 3, perhaps our two-thirds-of-a-million-greats-grandparent, might have lived. Did it live in Africa like 1 and 2, or Asia? As the common ancestor of ourselves and an Asian ape, we should be prepared to find it in either continent, and partisans of both are not hard to find. In favour of Asia is its richness of plausible fossils from around the right time, the mid-to-late Miocene. Africa, on the other hand, seems to be where the apes originated, before the beginning of the Miocene. Africa witnessed a great flowering of ape life in the early Miocene, in the form of proconsulids (several species of the early ape genus Proconsul) and others such as Afropithecus and Kenyapithecus. Our closest living relatives today, and all our post-Miocene fossils, are African.

But our special relationship to chimpanzees and gorillas has been known only for a few decades. Before that, most anthropologists thought we were the sister group to all the apes, and therefore equally close to African and Asian apes. The consensus favoured Asia as the home of our late Miocene ancestors, and some authorities even picked out a particular fossil ‘ancestor’, Ramapithecus. This animal is now thought to be the same as one previously called Sivapithecus which therefore, by the laws of zoological nomenclature, takes precedence. Ramapithecus should no longer be used — a pity because the name had become familiar. Whatever one feels about Sivapithecus/Ramapithecus as a human ancestor, many authorities agree that it is close to the line that gave rise to the orang utan and might even be the orang utan's direct ancestor. Gigantopithecus could be regarded as a kind of giant, ground-dwelling version of Sivapithecus. Several other Asian fossils occur from about the right time. Ouranopithecus and Dryopithecus seem almost to be jostling for the title of most plausible human ancestor of the Miocene. If only, it is tempting to remark, they were in the right continent. As we shall see, this ‘if only'just might turn out to be true.

If only the late Miocene apes were in Africa instead of Asia, we'd have a smooth series of plausible fossils linking the modern African apes all the way back to the early Miocene and the rich proconsulid ape fauna of Africa. When  {98}  molecular evidence established beyond any doubt our affinities with the African chimpanzees and gorillas, rather than with the Asian orangs, seekers of human ancestors reluctantly turned their backs on Asia. They assumed, in spite of the plausibility of the Asian apes themselves, that our ancestral line must lie in Africa right through the Miocene and concluded that, for some reason, our African ancestors had not fossilised after the early burgeoning of proconsulid apes in the early Miocene.

That's where things stood until 1998, when an ingenious piece of lateral thinking appeared in a paper called ‘Primate evolution — in and out of Africa’ by Caro-Beth Stewart and Todd R. Disotell. This tale, of back and forth traffic between Africa and Asia, will be told by the orang utan. Its conclusion will be that Concestor 3 probably lived in Asia after all.

But never mind, for the moment, where it lived. What did Concestor 3 look like? It is the common ancestor of the orang utans and all today's African apes, so it might resemble either or both of them. Which fossils might give us helpful clues? Well, looking at the family tree, the fossils known as Lufengpithecus, Oreopithecus, Sivapithecus, Dryopithecus and Ouranopithecus all lived around the right time or slightly later. Our best-guess reconstruction of Concestor 3 might combine elements of all five of these Asian fossil genera — but it would help if we could accept Asia as the location of the concestor. Let's listen to the Orang Utan's Tale and see what we think.

The Orang Utan's Tale

Perhaps we have been too ready to assume that our links with Africa go back a very long way. What if, instead, our ancestral lineage hopped sideways out of Africa around 20

FACING PAGE

CONCESTOR 3

A large quadrupedal ape which probably spent much of its time up in the trees, suspending itself from branches with its long arms. Its diet was mainly composed of fruit. Like all great apes it would have displayed considerable intelligence. It probably evolved in an Asian rainforest, as depicted here.

In and out of Africa Stewart and Disotell's family tree of African and Asian apes. Swollen areas represent dates known from fossils, while the lines linking these to the tree are inferred from parsimony analysis. Arrows represent inferred migration events. Adapted from Stewart and Disotell [273].

million years ago, flourished in Asia until around 10 million years ago, and then hopped back to Africa?

On this view, all the surviving apes, including the ones that ended up in Africa, are descended from a lineage that migrated out of Africa into Asia. Gibbons and orang utans are descendants of these migrants who stayed in Asia. Later descendants of the migrants returned to Africa, where the earlier Miocene apes had gone extinct. Back in their old ancestral home of Africa, these migrants then gave rise to gorillas, chimpanzees and bonobos, and us.

The known facts about the drifting of the continents and the fluctuations of sea levels are compatible. There were land bridges available across Arabia at the right times. The positive evidence in favour of the theory depends upon ‘parsimony’: an economy of assumptions. A good theory is one that needs to postulate little, in order to explain lots. (By this criterion, as I have often remarked elsewhere, Darwin's theory of natural selection may be the best theory of all time.) Here we are talking about minimising our assumptions about migration events. The theory that our ancestors stayed in Africa all along (no migrations) seemed, on the face of it, more economical with its assumptions than the theory that our ancestors moved from Africa into Asia (a first migration) and later moved back to Africa (a second migration).

But that parsimony calculation was too narrow. It concentrated on our own  {101}  lineage and neglected all the other apes, especially the many fossil species. Stewart and Disotell did a recount of the migration events, but they counted those that would be needed to explain the distribution of all the apes including fossils. In order to do this, you first have to construct a family tree on which you mark all the species about which you have sufficient information. The next step is to indicate, for each species on the family tree, whether it lived in Africa or Asia. On the diagram, which is taken from Stewart and Disotell's paper, Asian fossils are highlighted in black, African ones are in white. Not all the known fossils are there, but Stewart and Disotell did include all whose position on the family tree could be clearly worked out. They also drew in the Old World monkeys, who diverged from the apes around 25 million years ago (the most obvious difference between monkeys and apes, as we shall see, is that the monkeys retained their tails). Migration events are indicated by arrows.

Taking into account the fossils, the ‘hop to Asia and back again’ theory is now more parsimonious than the ‘our ancestors were in Africa all along’ theory. Leaving out the monkeys which, on both theories, account for two migration events from Africa to Asia, it need postulate only two ape migrations, as follows:

Conversely, the ‘our ancestors were in Africa all along’ theory demands six migration events to account for ape distributions, all from Africa to Asia, by ancestors of the following

1 Gibbons, around 18 million years ago

2 Oreopithecus, around 16 million years ago

3 Lufengpithecus, around 15 million years ago

4 Sivapithecus and orang utans, around 14 million years ago

5 Dryopithecus, around 13 million years ago

6 Ouranopithecus, around 12 million years ago

Of course all these migration counts are valid only if Stewart and Disotell have got the family tree right, based on anatomical comparisons. They think, for example, that among the fossil apes, Ouranopithecus is the closest cousin to the modern African apes (its branch is the last to come off the family tree in the diagram before the African apes). The next closest cousins, according to their anatomical assessments, are all Asian (Dryopithecus, Sivapithecus, etc.). If they have got the anatomy all wrong: if, for instance, the African fossil Kenyapithecus is actually closest to the modern African apes, then the migration counts would have to be done all over again.

The family tree was itself constructed on grounds of parsimony. But it is a  {102}  different land of parsimony. Instead of trying to minimise the number of geographical migration events we need to postulate, we forget about geography ana try to minimise the number of anatomical coincidences (convergent evolution) we need to postulate. Having got our family tree without regard to geography, we then superimpose the geographical information (the black and white coding on the diagram) to count migration events. And we conclude that it is most likely that the ‘recent’ African apes, that is gorillas, chimpanzees and humans, arrived from Asia.

Now here's an interesting little fact. A leading textbook of human evolution, by Richard G. Klein of Stanford University, gives a fine description of what is known of the anatomy of the main fossils. At one point Klein compares the Asian Ouranopithecus and the African Kenyapithecus and asks which most resembles our own close cousin (or ancestor) Australopithecus. Klein concludes that Australopithecus resembles Ouranopithecus more than it resembles Kenyapithecus. He goes on to say that, if only Ouranopithecus had lived in Africa, it might even make a plausible human ancestor. ‘On combined geographic-morphologic grounds’, however, Kenyapithecus is a better candidate. You see what is going on here? Klein is making the tacit assumption that African apes are unlikely to be descended from an Asian ancestor, even if the anatomical evidence suggests that they were. Geographical parsimony is being subconsciously allowed to pull rank over anatomical parsimony. Anatomical parsimony suggests that Ouranopithecus is a closer cousin to us than Kenyapithecus is. But, without being explicitly so called, geographical parsimony is assumed to trump anatomical parsimony. Stewart and Disotell argue that, when you take into account the geography of all the fossils, anatomical and geographical parsimony agree with each other. Geography turns out to agree with Klein's initial anatomical judgement that Ouranopithecus is closer to Australopithecus than Kenyapithecus is.

This argument may not be settled yet. It is a complicated business juggling anatomical and geographical parsimony. Stewart and Disotell's paper has unleashed a flourishing correspondence in the scientific journals, both for and against. As the available evidence stands at present, I think we should on balance prefer the ‘hop to Asia and back’ theory of ape evolution. Two migration events is more parsimonious than six. And there really do seem to be some telling resemblances between the late Miocene apes in Asia and our own line of African apes such as Australopithecus and chimpanzees. It is only a preference ‘on balance’, but it leads me to locate Rendezvous 3 (and Rendezvous 4) in Asia rather than Africa.

The moral of the Orang Utan's Tale is twofold. Parsimony is always in the forefront of a scientist's mind when choosing between theories, but it isn't always obvious how to judge it. And possessing a good family tree is often an essential first prerequisite to powerful further reasoning in evolutionary theory. But building a good family tree is a demanding exercise in itself. The ins and outs of it will be the concern of the gibbons, in the tale that they will tell us in melodious chorus after they join our pilgrimage at Rendezvous 4.

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RENDEZVOUS 4 GIBBONS

Rendezvous 4, where we are joined by the gibbons, occurs around 18 million years ago, probably in Asia, in the warmer and more wooded world of the early Miocene. Depending on which authority you consult, there are up to twelve modern species of gibbons. All live in South East Asia, including Indonesia and Borneo. Some authorities place them all in the genus Hylobates. The siamang used to be separated off, and people spoke of ‘gibbons and siamangs’. With the realisation that they divide into four groups, not two, this distinction has become obsolete, and I shall call them all gibbons.^*

Gibbons are small apes, and perhaps the finest arboreal acrobats that have ever lived. In the Miocene there were lots of small apes. Getting smaller and getting larger are easy changes to achieve in evolution. Just as Gigantopithecus and Gorilla got large independently of each other, plenty of apes, in the Miocene golden age of apes, got small. The pliopithecids, for instance, were small apes which flourished in Europe in the early Miocene and probably lived in a similar way to gibbons, without being ancestral to them. I suppose, for example, that they ‘brachiated’.

Brachia is the Latin for ‘arm’. Brachiation means using your arms rather than your legs to get about, and gibbons are spectacularly good at it. Their big grasping hands and powerful wrists are like upside-down seven-league boots, spring-loaded to slingshot the gibbon from branch to branch and from tree to tree. A gibbon's long arms, perfectly in tune with the physics of pendulums, are capable of hurling it across a sheer ten-metre gap in the canopy. My imagination finds high-speed brachiation more exciting even than flying, and I like to dream of my ancestors enjoying what must surely have been one of the great experiences life could offer. Unfortunately, current thinking doubts that our ancestry ever went through a fully gibbon-like stage, but it is reasonable to conjecture that Concestor 4, approximately our 1-million-greats-grandparent, was a small tree-dwelling ape with at least some proficiency in brachiation.

Among the apes, gibbons are also second only to humans in the difficult art of walking upright. Using its hands only to steady itself, a gibbon will use bipedal walking to travel along the length of a branch, whereas it uses brachiation to travel across from branch to branch. If Concestor 4 practised the same art and passed it on to its gibbon descendants, could some vestige of the skill have persisted in the brain of its human descendants too, waiting to resurface again in Africa? That is no more than a pleasing speculation, but it is true that apes in general have a tendency to walk bipedally from time to time. We can

[Graphics removed]

Upside-down seven-league boots

A pileated gibbon (Hylobates pileatus) demonstrating the art of brachiation.

also only speculate on whether Concestor 4 shared the vocal virtuosity of its gibbon descendants, and whether this might have presaged the unique versatility of the human voice, in speech and in music. Then again, gibbons are faithfully monogamous, unlike the great apes which are our closer relatives. Unlike, indeed, the majority of human cultures, in which custom and in several cases religion encourages (or at least allows) polygyny. We do not know whether Concestor 4 resembled its gibbon descendants, or its great ape descendants in this respect.^*

Let's summarise what we can guess about Concestor 4, making the usual weak assumption that it had a good number of the features shared by all its descendants, which means all the apes including us. It was probably more dedicated to life in the trees than Concestor 3, and smaller. If, as I suspect, it hung and swung from its arms, its arms were probably not so extremely specialised for brachiation as those of modern gibbons, and not so long. It probably had a gibbon-like face, with a short snout. It didn't have a tail. Or, to be more precise, its tail vertebrae were, as in all the apes, joined together in a short internal tail, the coccyx (pronounced koxix).

I don't know why we apes lost our tail. It is a subject that biologists discuss surprisingly little.^* Zoologists faced with this kind of conundrum often think comparatively. Look around the mammals, note where taillessness (or a very short tail) has independently cropped up, and try to make sense of it. I don't think anyone has done this systematically, and it would be a nice thing to undertake. Apart from apes, tail loss is found in moles, hedgehogs, the tailless tenrec Tenrec ecaudatus, guinea pigs, hamsters, bears, bats, koalas, sloths, agoutis and several others. Perhaps most interesting for our purposes, there are tailless monkeys, or monkeys with a tail so short it might as well not be there, as in a Manx cat.^* The Barbary macaque Macaca sylvanus is a tailless monkey and, perhaps in consequence, is often miscalled the Barbary ape. The ‘Celebes ape’ Macaca nigra is another tailless monkey. Jonathan Kingdon tells me it looks and walks just like a miniature chimpanzee. Madagascar has some tailless lemurs, such as the indri, and several extinct species including ‘koala lemurs’ (Megaladapis) and ‘sloth lemurs’, some of which were gorilla-sized.

Any organ which is not used will, other things being equal, shrink for reasons of economy if nothing else. Tails are used for a surprisingly wide variety of purposes among mammals.^* But here we must be especially concerned with animals who live up trees. Squirrel tails catch the air, so a ‘leap’ is almost like flying. Tree-dwellers often have long tails as counterweights, or as rudders for  {106}  leaping. Lorises and pottos, whom we shall meet at Rendezvous 8, creep about the trees, slowly stalking their prey, and they have extremely short tails. Their relatives the bushbabies, on the other hand, are energetic leapers, and they have long feathery tails. Tree sloths are tailless, like the marsupial koalas who might be regarded as their Australian equivalents, and both move slowly in the trees like lorises.

In Borneo and Sumatra, the long-tailed macaque lives up trees, while the closely related pig-tailed macaque lives on the ground and has a short tail. Monkeys that are active in trees usually have long tails. They run along the branches on all fours, using the tail for balance. They leap from branch to branch with the body in a horizontal position and the tail held out as a balancing rudder behind. Why, then, do gibbons, who are as active in trees as any monkey, have no tail? Maybe the answer lies in the very different way in which they move. All apes, as we have seen, are occasionally bipedal, and gibbons, when not brachiating, run along branches on their hind legs, using their long arms to steady themselves. It is easy to imagine a tail being a nuisance for a bipedal walker. My colleague Desmond Morris tells me that spider monkeys sometimes walk bipedally, and the long tail is obviously a major encumbrance. And when a gibbon projects itself to a distant branch it does so from a vertically hanging position, unlike the monkey's horizontal leaping posture. Far from being a steadying rudder streaming out behind, a tail would be a positive drag for a vertical brachiator like a gibbon or, presumably, Concestor 4.

That is the best I can do. I think zoologists need to give more attention to the puzzle of why we apes lost our tail. The a posteriori counterfactual engenders pleasing speculations. How would the tail have sat with our habit of wearing clothes, especially trousers? It gives a different urgency to the classic tailor's question, ‘Does Sir hang to the left or to the right?’

The Gibbon's Tale (written with Yan Wong)

Rendezvous 4 is the first time we greet a pilgrim band of more than a couple of already united species. Any more than that, and there can be problems with deducing relationships. These problems will become worse as our pilgrimage advances. How to solve them is the topic of the Gibbon's Tale.^*

We have seen that there are 12 species of gibbons, falling into four major groups. They are Bunopithecus (a group consisting of a single species, commonly known as the hoolock), Hylobates (six species, of which the best-known is the white-handed gibbon Hylobates lar), Symphalangus (the siamang), and Nomascus (four species of ‘crested’ gibbons). This tale explains how to build an evolutionary relationship, or phylogeny, relating the four groups.

Family trees can be ‘rooted’ or ‘unrooted’. When we draw a rooted tree, we know where the ancestor is. Most of the tree diagrams in this book are rooted. Unrooted trees, by contrast, have no sense of direction. They are often called  {107}  star diagrams, and there is no arrow of time. They don't start at one side of a page and end on the other. Here are three examples, which exhaust the possibilities for relating four entities.

At every fork in a tree, it makes no difference which is the left and which the right branch. And so far (though that will change later in the tale) no information is conveyed by the lengths of the branches. A tree diagram whose branch lengths are meaningless is known as a cladogram (an unrooted cladogram in this case). The order of branching is the only information conveyed by a cladogram: the rest is cosmetic. Try, for example, rotating either of the side forks about the horizontal line in the middle. It will make no difference to the pattern of relationships.

These three unrooted cladograms represent the only possible ways of connecting four species, as long as we restrict ourselves to connections via branches that only ever split in two (dichotomies). As with rooted trees, it is conventional to discount three-way splits (trichotomies) or more (polytomies) as temporary admissions of ignorance — ‘unresolved’.

Any unrooted cladogram turns into a rooted one the moment we specify the oldest point (the ‘root’) of the tree. Certain researchers — those we have relied upon for the tree at the start of this tale — have suggested the rooted cladogram of gibbons shown below, on the left. However, other researchers have suggested the rooted cladogram on the right.

In the first tree the crested gibbons, Nomascus, are distant relatives of all the other gibbons. In the second, it is the hoolock gibbon, Bunopithecus, who holds

this distinction. Despite their differences, both derive from the same unrooted tree (Tree A). The cladograms differ only in their rooting. The first is found by dangling the root of Tree A off the branch leading to Nomascus, the second by placing the root on the branch leading to Bunopithecus.

How do we ‘root’ a tree? The usual method is to extend the tree to include at least one — and preferably more than one — ‘outgroup’: a member of a group that is universally agreed beforehand to be only distantly related to all the others. In the gibbon tree, for example, orang utans or gorillas — or indeed elephants or kangaroos — could do duty as the outgroup. However uncertain we may be about relationships among gibbons, we know that the common ancestor of any gibbon with a great ape or an elephant is older than the common ancestor of any gibbon with any other gibbon: it is uncontroversial to place the root of a tree that includes the gibbons and the great apes somewhere between the two. It's easy to verify that the three unrooted trees I have drawn are the only possible dichotomous trees for four groups. For five groups there are 15 possible trees. But don't try to count the number of possible trees for, say, 20 groups. It is up in the hundreds of millions of millions of millions. The actual number is rises steeply with the number of groups to be classified, even the fastest computer can take forever. In principle, however, our task is simple. Of all possible trees we must choose that which best explains the similarities and differences of groups, between our groups.

How do we judge ‘best explains’? Infinitely rich similarities and differences present themselves when we look at a set of animals. But they are harder to count than you might think. Often one ‘feature’ is an inextricable part of another. If you count them as separate, you've really counted the same one twice. As an extreme example suppose there are four millipede species, A, B, C, and D. A and B resemble each other in all respects except that A has red legs and B has blue legs. C and D are the same as each other and very different from A and B, except that C has red legs while D has blue legs. If we count leg colour as a single ‘feature’ we correctly group AB apart from CD. But if we naively count each of 100 legs as separate, their colours will give a hundredfold boost to the number of features supporting the alternative grouping of AC as against BD. Everyone would agree that we have spuriously counted the same feature 100 times. It is ‘really’ only one feature, because a single embryological ‘decision’ determined the colour of all 100 legs simultaneously.

The same goes for left-right symmetry: embryology works in such a way that, with few exceptions, each side of an animal is a mirror image of the other. No zoologist would count each mirrored feature twice in making a cladogram, but non-independence isn't always so obvious. A pigeon needs a deep breastbone to attach the flight muscles. A flightless bird like a kiwi does not. Do we count deep breastbone and flapping wings as two separate features by which pigeons differ from kiwis? Or do we count them as only a single feature, on the grounds that the state of one character determines the other, or at least reduces its freedom to vary? In the case of the millipedes and the mirroring, the sensible answer is pretty obvious. In the case of the breastbones it isn't. Reasonable people can be found arguing on opposite sides.  {109} 

That was all about visible resemblances and differences. But visible features evolve only if they are manifestations of DNA sequences. Nowadays we can compare DNA sequences directly. As an added benefit, being long strings, DNA texts provide a lot more items to count and compare. Problems of the wing-and-breastbone variety are likely to be drowned out in the flood of data. Even better, many DNA differences will be invisible to natural selection and so provide a ‘purer’ signal of ancestry. As an extreme example, some DNA codes are synonymous: they specify exactly the same amino acid. A mutation that changes a DNA word to one of its synonyms is invisible to natural selection. But to a geneticist, such a mutation is no less visible than any other. The same goes for ‘pseudogenes’ (usually accidental duplicates of real genes) and for many other ‘junk DNA’ sequences, which sit in the chromosome but are never read and never used. Freedom from natural selection leaves DNA free to mutate in ways that leave highly informative traces for taxonomists. None of this alters the fact that some mutations do have real and important effects. Even if these are only the tips of icebergs, it is those tips that are visible to natural selection and account for all the visible and familiar beauties and complexities of life.

DNA too is far from immune to the problem of multiple counting — the molecular equivalent of the millipedes’ legs. Sometimes a sequence is duplicated many times throughout the genome. About half of human DNA consists of multiple copies of meaningless sequences, ‘transposable elements’, which maybe parasites that hijack the machinery of DNA replication to spread themselves about the genome. Just one of these parasitic elements, Alu, is present in over a million copies in most individuals, and we shall meet it again in the Howler Monkey's Tale. Even in the case of meaningful and useful DNA, there are a few cases where genes are present in dozens of identical (or near-identical) copies. But in practice multiple counting tends not to be a problem because duplicate DNA sequences are usually easy to spot.

As a better reason for caution, extensive regions of DNA occasionally show up enigmatic resemblances between comparatively unrelated creatures. Nobody doubts that birds are more closely related to turtles, lizards, snakes and crocodiles than to mammals (see Rendezvous 16). Nevertheless, the DNA sequences of birds and mammals have resemblances greater than one might expect given their distant relationship. Both have an excess of G-C pairings in their non-coding DNA. The G-C pairing is chemically stronger than the A-T one, and it may be that warm-blooded species (birds and mammals) need more tightly bound DNA. Whatever the reason, we should beware of allowing this G-C bias to persuade us of a close relationship between all warm-blooded animals. DNA seems to promise a Utopia for biological systematists, but we must be aware of such dangers: there is a lot that we still don't understand about genomes.

So, having taken the necessary invocation of caution, how can we use the information present in DNA? Fascinatingly, literary scholars use the same techniques as evolutionary biologists in tracing the ancestries of texts. And almost too good to be true — one of the best examples happens to be the work of the Canterbury Tales Project. Members of this international syndicate of  {110}  literary scholars have used the tools of evolutionary biology to trace the history of 85 different manuscript versions of The Canterbury Tales. These ancient manuscripts, hand-copied before the advent of printing, are our best hope of reconstructing Chaucer's lost original. As with DNA, Chaucer's text has survived through repeated copyings, with accidental changes perpetuated in the copies. By meticulously scoring the accumulated differences, scholars can reconstruct the history of copying, the evolutionary tree — for it really is an evolutionary process, consisting of a gradual accumulation of errors over successive generations. So similar are the techniques and difficulties in DNA evolution and literary text evolution, that each can be used to illustrate the other.

So, let's temporarily turn from our gibbons to Chaucer, and in particular four of the 85 manuscript versions of The Canterbury Tales: the ‘British Library’, ‘Christ Church’, ‘Egerton’, and ‘Hengwrt’ versions.^* Here are the first two lines of the General Prologue:

The first thing that we must do with either DNA or literary texts is to locate the similarities and differences. For this we have to ‘align’ them — not always an easy task, for texts can be fragmentary or jumbled and of unequal length. A computer is a great help when the going gets tough, but we don't need it to align the first two lines of Chaucer's General Prologue, which I have highlighted at the fourteen points where the scripts disagree.

Two places, the second and the fifth, have three variants rather than two. That makes a total of sixteen ‘differences’. Having compiled a list of differences we now work out which tree best explains them. There are many ways of doing this, and all can be used for animals as well as for literary texts. The simplest is to group the texts on the basis of overall similarity. This usually relies upon some variant on the following method. First we locate the pair of texts that are the most similar. We then treat this pair as a single averaged text, and put it alongside the remaining texts while we look for the next most similar pair. And so on, forming successive, nested groups until a tree of relationships is built up. These sorts of techniques — one of the most common is known as ‘neighbourjoining’ — are quick to calculate, but do not incorporate the logic of the evolutionary process. They are purely measures of similarity. For this reason, the  {111}  ‘cladist’ school of taxonomy, which is deeply evolutionary in its rationale (although not all its members realise it) prefers other methods, of which the earliest to be devised was the parsimony method.

Parsimony, as we saw in the Orang Utan's Tale, here means economy of explanation. In evolution, whether of animals or manuscripts, the most parsimonious explanation is the one that postulates the least quantity of evolutionary change. If two texts share a common feature, the parsimonious explanation is that they have jointly inherited it from a shared ancestor rather than that each evolved it independently. It is very far from an invariable rule, but it is at least more likely to be true than the opposite. The method of parsimony — at least in principle — looks over all possible trees and chooses the one that minimises the quantity of change.

When we are choosing trees for their parsimony, certain types of difference can't help us. Differences that are unique to a single manuscript, or a single species of animal, are uninformative. The neighbour-joining method uses them, but the method of parsimony ignores them completely. Parsimony relies upon informative changes: ones that are shared by more than one manuscript. The preferred tree is the one that uses shared ancestry to explain as many informative differences as possible. In our Chaucerian lines there are five informative differences to account for. Four split the manuscripts into

{British Library plus Egerton} versus {Christ Church plus Hengwrt}.

These are the differences highlighted by the first, third, seventh, and eighth red lines. The fifth, the virgule (diagonal stroke) highlighted by the twelfth red line, splits the manuscripts differently, into

{British Library plus Hengwrt} versus {Christ Church plus Egerton}.

These splits conflict with each other. We can draw no tree in which each change happens just once. The best we can do is the following (note that it is an un-rooted tree) which minimises the conflict, requiring only the virgule to appear or disappear twice.

Actually, in this case I haven't much confidence in our guess. Convergences or reversions are common in texts, especially when the meaning of the verse is not changed. A medieval scribe might have little compunction in changing a spelling, and even less in inserting or removing a punctuation mark such as a virgule. Better indicators of relationship would be changes such as the  {112}  reordering of words. The genetic equivalents are ‘rare genomic changes’: events such as large insertions, deletions, or duplications of DNA. We can explicitly acknowledge these by giving more or less weight to different types of change. Changes known to be common or unreliable are downweighted when counting up extra changes. Changes known to be rare, or reliable indicators of kinship, are given increased weighting. Heavy weighting to a change means we especially don't want to count it twice. The most parsimonious tree, then, is the one with the lowest overall weight.

The parsimony method is much used to find evolutionary trees. But if convergences or reversions are common — as with many DNA sequences and also in our Chaucerian texts — parsimony can be misleading. It is the notorious bugbear known as ‘long branch attraction’. Here's what this means.

Cladograms, whether rooted or unrooted, convey only the order of branching. Phylograms, or phylogenetic trees (Greek phylon = race/tribe/class), are similar but also use the length of branches to convey information. Typically branch lengths represent evolutionary distance: long branches represent a lot of change, short ones little change. The first line of The Canterbury Tales yields the following phylogram:

In this phylogram, the branches are not too different in length. But imagine what would happen if two of the manuscripts changed a lot, compared to the other two. The branches leading to these two would be drawn very long. And a proportion of the changes would not be unique. They would just happen to be identical to changes elsewhere on the tree, but (and now here is the point) especially to those on the other long branch. This is because long branches are where the most changes are anyway. With enough evolutionary changes, the ones that spuriously link the two long branches will drown out the true signal. Based upon a simple count of the number of changes, parsimony erroneously groups together the termini of especially long branches. The method of parsimony makes long branches spuriously ‘attract’ one another.

The problem of long branch attraction is an important headache for biological taxonomists. It rears its head whenever convergences and reversions are common, and unfortunately we cannot hope to avoid it by looking at more text. On the contrary, the more text we look at, the more erroneous similarities we find, and the stronger our conviction in the wrong answer. Such trees are said to lie in the dangerous-sounding ‘Felsenstein zone’, named after the distinguished  {113}  American biologist Joe Felsenstein. Unfortunately, DNA data are particularly vulnerable to long branch attraction. The main reason is that there are only four letters in the DNA code. If the majority of differences are single letter changes, independent mutation to the same letter by accident is extremely likely. This sets up a minefield of long branch attraction. Clearly we need an alternative to parsimony in these cases. It comes in the form of a technique known as likelihood analysis, which is increasingly favoured in biological taxonomy.

Likelihood analysis burns even more computer power than parsimony, because now the lengths of the branches matter. So we have vastly more trees to contend with because, in addition to looking at all possible branching patterns, we must also look at all possible branch lengths — a Herculean task. This means that, despite clever short cuts, today's computers can only cope with likelihood analysis involving small numbers of species.

‘Likelihood’ is not a vague term. On the contrary, it has a precise meaning. For a tree of a particular shape (remembering to include branch lengths), of all the possible evolutionary paths that could produce a phylogenetic tree of the same shape, only a tiny number would generate precisely those texts that we now see. The ‘likelihood’ of a given tree is the vanishingly small probability of ending up with the actual existing texts, rather than any of the other texts that could possibly have been generated by such a tree. Although the likelihood value for a tree is tiny, we can still compare one tiny value with another as a means of judgement.

Within likelihood analysis, there are various alternative methods of obtaining the ‘best’ tree. The simplest is to search for the single one that has the highest likelihood: the tree which is the most likely. Not unreasonably, this goes under the name ‘maximum likelihood’, but just because it is the single most likely tree doesn't mean that other possible trees aren't almost as likely. More recently it has been suggested that instead of believing in a single most likely tree, we should look at all possible trees, but give proportionally more credence to the more likely ones. This approach, an alternative to maximum likelihood, is known as Bayesian phylogenetics. If many likely trees agree on a particular branch point, then we calculate that it has a high probability of being correct. Of course, just as in maximum likelihood, we can't look at all possible trees, but there are computational shortcuts and they work pretty well.

Our confidence in the tree we finally choose will depend on our certainty that its various branches are correct, and it is common to place measures of this beside each branch point. Probabilities are automatically calculated when using the Bayesian method, but for others such as parsimony or maximum likelihood, we need alternative measures. A commonly used one is the ‘bootstrap’ method, which resamples different parts of the data repeatedly to see how much difference it makes to the final tree — how robust the tree is, in other words, to error. The higher the ‘bootstrap’ value, the more trustworthy the branch point, but even experts struggle to interpret exactly what a particular bootstrap value tells us. Similar methods are the ‘jackknife’, and the ‘decay index’. All are measures of how much we should believe each branch point on the tree.  {114} 

'By me was nothyng added ne mynusshyd' (Caxton's Preface). Unrooted phylogenetic tree of the first 250 lines of 24 different manuscript versions of The Canterbury Tales. This represents a subset of the manuscripts studied by the Canterbury Tales Project, whose abbreviations for the manuscripts are used here. The tree was constructed by parsimony analysis, and bootstrap values are shown on the branches. The four versions discussed are named in full.

Before we leave literature and return to biology, here is a summary diagram of the evolutionary relationships between the first 250 lines of 24 Chaucer manuscripts. It is a phylogram, in which not just the branching pattern but the lengths of the lines are meaningful. You can immediately read off which manuscripts are minor variants of each other, which are aberrant outliers. It is unrooted — it doesn't commit itself as to which of the 24 manuscripts is closest to the 'original'.

It's time to return to our gibbons. Over the years, many people have tried to work out gibbon relationships. Parsimony suggested four groups of gibbons. On the next page is a rooted cladogram based on physical characteristics.

This cladogram shows convincingly that the Hylobates species group together, as do the Nomascus ones. Both groupings have reasonably high bootstrap values (the numbers on the lines). But in several places the order of branching is unresolved. Even though it looks as though Hylobates and Bunopithecus form a group, the bootstrap value, 63, is unconvincing to those trained to read such runes. Morphological features do not suffice to resolve the tree.

For this reason, Christian Roos and Thomas Geissmann of Germany turned to molecular genetics, specifically to a section of mitochondrial DNA called the ‘control region’. Using DNA from six gibbons, they deciphered the sequences, lined them up letter-for-letter, and carried out neighbour-joining, parsimony, and maximum likelihood analyses on them. Maximum likelihood, which is the best of of the three methods at coping with long branch attraction, gave the most convincing result. Their final verdict on the gibbons is shown above, and you can see that it resolves the relationship between the four groups. The bootstrap values were enough to convince me that this was the tree to use for the phylogeny at the start of this chapter.

Gibbons ‘speciated’ — branched into their separate species — relatively recently. But as we look at more and more distantly related species, separated by longer and longer branches, even the sophisticated techniques of maximum likelihood and Bayesian analysis start to fail us. There can come a point where an unacceptably large proportion of similarities are coincidental. The DNA differences are then said to be saturated. No fancy techniques can recover the signal of ancestry, because any vestiges of relationship have been overwritten by the ravages of time. The problem is especially acute with neutral DNA differences. Strong natural selection keeps genes on the straight and narrow. In extreme cases, important functional genes can stay literally identical over hundreds of millions of years. But, for a pseudogene that never does anything, such lengths of time are enough to lead to hopeless saturation. In such cases, we need different data. The most promising idea is to use the rare genomic changes that I mentioned before — changes that involve DNA reorganisation rather than single letter changes. These being rare, indeed usually unique, coincidental resemblance is much less of a problem. And once found, they can reveal remarkable relationships, as we shall learn when our swelling pilgrim band is joined by the hippo, and we are bowled over by its whale of a surprising tale.

And now, an important afterthought on evolutionary trees, drawing in lessons from Eve's Tale and the Neanderthal's Tale. We might call it the gibbon's decline and fall of the species tree. We normally assume that we can draw a single evolutionary tree for a set of species. But Eve's Tale told us that different parts of DNA (and thus different parts of an organism) can have different trees. I think this poses an inherent problem with the very idea of species trees. Species are composites of DNA from many different sources. As we saw in Eve's  {116}  Tale and reiterated in the Neanderthal's Tale, each gene, in fact each DNA letter, takes its own path through history. Each piece of DNA, and each aspect of an organism, can have a different evolutionary tree.

An example of this comes up every day, but familiarity leads us to overlook its message. A Martian taxonomist shown only the genitals of a male human, a female human, and a male gibbon would have no hesitation in classifying the two males as more closely related to each other than either is to the female. Indeed, the gene determining maleness (called SRY) has never been in a female body, at least since long before we and the gibbons diverged. Traditionally, morphologists plead a special case for sexual characteristics, to avoid ‘nonsensical’ classifications. But identical problems arise elsewhere. We saw it previously with ABO blood groups, in Eve's Tale. My B-group gene relates me more closely to a B-group chimpanzee than an A-group human. And it is not just sex genes or blood groups, but all genes and characteristics which are susceptible to this effect, under certain circumstances. The majority of both molecular and morphological characteristics show chimps as our closest relatives. But a sizeable minority show that gorillas are instead, or that chimps are most closely related to gorillas and both are equally close to humans.

This should not surprise us. Different genes are inherited through different routes. The population ancestral to all three species will have been diverse — each gene having many different lineages. It is quite possible for a gene in humans and gorillas to be descended from one lineage, while in chimps it is descended from a more distantly related one. All that is needed is for anciently diverged genetic lineages to continue through to the chimp-human split so humans can descend from one and chimps from another.^*

So we have to admit that a single tree is not the whole story. Species trees can be drawn, but they must be considered a simplified summary of a multitude of gene trees. I can imagine interpreting a species tree in two different ways. The first is the conventional genealogical interpretation. One species is the closest relative of another if, out of all the species considered, it shares the most recent common genealogical ancestor. The second is, I suspect, the way of the future. A species tree can be seen as depicting the relationships among a democratic majority of the genome. It represents the result of a ‘majority vote’ among gene trees.

The democratic idea — the genetic vote — is the one that I prefer. In this book, all relationships between species should be interpreted in this way. All the phylogenetic trees I present should be viewed in this spirit of genetic democracy, from the relationships between apes to the relationships between the animals, plants, fungi and bacteria.

RENDEZVOUS 5 OLD WORLD MONKEYS

As we near this rendezvous and prepare to greet Concestor 5 — approximately our 1.5-million-greats-grandparent — we cross a momentous (if somewhat arbitrary) boundary. For the first time in our journey we leave one geological period, the Neogene, to enter an earlier one, the Palaeogene. The next time we do this will be to burst into the Cretaceous world of the dinosaurs. Rendezvous 5 is scheduled at about 25 million years ago, in the Palaeogene. More specifically it is in the Oligocéne Epoch of that Period, the last stop on our backward journey when the climate and vegetation of the world are recognisably similar to today's. Much further back, and we shall not find any evidence of the open grasslands that so typify our own Neogene Period, or the wandering herds of grazers that accompanied their spread. Twenty-five million years ago, Africa was completely isolated from the rest of the world, separated from the nearest piece of land — Spain — by a sea as wide as that which separates it from Madagascar today. It is on that gigantic island of Africa that our pilgrimage is about to be invigorated by a new influx of spirited and resourceful recruits, the Old World monkeys — the first pilgrims to arrive bearing tails.

Today, the Old World monkeys number just under 100 species, some of which have migrated out of their mother continent into Asia (see the Orang Utan's Tale). They are divided into two main groups: on the one hand are the colobus monkeys of Africa together with the langurs and proboscis monkeys of Asia; on the other hand are the mostly Asian macaques plus the baboons and guenons, etc. of Africa.

The last common ancestor of all surviving Old World monkeys lived some 11 million years later than Concestor 5, probably around 14 million years ago. The most helpful fossil genus for illuminating the period is Victoriapithecus, which is now known from more than a thousand fragments, including a splendid skull, from Maboko Island in Lake Victoria. All the Old World monkey pilgrims join hands around 14 million years ago to greet their own concestor, perhaps Victoriapithecus itself, or something like it. They then march on backwards to join the ape pilgrims at our own Concestor 5, 25 million years ago.

And what was Concestor 5 like? Perhaps a bit like the fossil genus Aegyptopithecus, which actually lived about 7 million years earlier. Concestor 5 itself, according to our usual rule of thumb, is more likely than not to have had the characteristics shared by its descendants, the catarrhines, defined as consisting of the apes and the Old World monkeys. For example (it's the feature that gives the catarrhines their name) Concestor 5 probably had narrow, downwards-facing

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Old World monkeys join This phylogeny of the 100 or so species of Old World monkey is generally accepted. The circles now visible at the tips of the branches indicate the number of known species in each group as an order of magnitude: no circle means 1-9 known species, a small width circle means 10-99, a larger circle, 100-999, etc.; each of the four groups here contain between 10 and 99 species.

nostrils, unlike the wide, sideways-facing nostrils of the New World monkeys, the platyrrhines. The females probably showed full menstruation, as is common among apes and Old World monkeys but not New World monkeys. It probably had an ear tube formed by the tympanic bone, unlike New World monkeys whose ear lacks a bony tube.

Did it have a tail? Almost certainly yes. Given that the most obvious difference between apes and monkeys is the presence or absence of the tail, we are tempted by the non sequitur that the divide of 25 million years ago corresponds to the moment at which the tail was lost. In fact, Concestor 5 was presumably tailed like virtually all other mammals, and Concestor 4 was tailless like all its descendants the modern apes. But we don't know at what point along the road leading from Concestor 5 to Concestor 4 the tail was lost. Nor is there any particular reason for us suddenly to start using the word ‘ape’ to signify the loss of the tail. The African fossil genus Proconsul, for example, can be called an ape rather than a monkey, because it lies on the ape side of the fork at Rendezvous 5. But the fact that it lies on the ape side of the fork tells us nothing about whether it had a tail. As it happens, the balance of the evidence suggests that, to quote the title of an authoritative recent paper, ‘Proconsul did not have a tail.’ But that in no way follows from the fact that it is on the ape side of the rendezvous divide.

What, then, should we call the intermediates between Concestor 5 and Proconsul before they lost their tail? A strict cladist would call them apes, because they lie on the ape side of the fork. A different kind of taxonomist would call them monkeys because they were tailed. Not for the first time, I say it is silly to become too worked up over names.

The Old World monkeys, Cercopithecidae, are a true clade, a group that includes all descendants of a single common ancestor. However ‘monkeys’ as a whole are not, because they include the New World monkeys, Platyrrhini. The Old World monkeys are closer cousins to apes, with whom they are united in the Catarrhini, than to New World monkeys. All apes and monkeys together constitute a natural clade, the Anthropoidea. ‘Monkeys’ constitutes an artificial (technically ‘paraphyletic’) grouping because it includes all the platyrrhines plus some of the catarrhines but excluding the ape portion of the catarrhines. It might be better to call the Old World monkeys tailed apes. Catarrhine, as I mentioned earlier, means ‘down nose’: the nostrils face downwards — in this respect we are ideal catarrhines. Voltaire's Dr Pangloss observed that ‘the nose is formed for spectacles, therefore we come to wear spectacles’. He could have added that our catarrhine nostrils are beautifully directed to keep out the rain. Platyrrhine means flat or broad nose. It is not the only diagnostic difference between these two great groups of primates, but it is the one that gives them their names. Let's press on to Rendezvous 6, and meet the platyrrhines.

RENDEZVOUS 6 NEW WORLD MONKEYS

Rendezvous 6, where the New World platyrrhine ‘monkeys’ meet us and our approximately 3-milIion-greats-grandparent, Concestor 6, the first anthropoid, is some 40 million years ago. It was a time of lush tropical forests — even Antarctica was at least partly green in those days. Although all platyrrhine monkeys now live in South or Central America, the rendezvous itself almost certainly did not take place there. My guess is that Rendezvous 6 is somewhere in Africa. A group of African primates with flat noses, who have left no surviving African descendants, somehow managed, in the form of a small founding population, to get across to South America. We don't know when this happened, but it was before 25 million years ago (when the first monkey fossils appear in South America) and after 40 million years ago (Rendezvous 6). South America and Africa were closer to each other than they are now, and sea levels were low, perhaps exposing a chain of islands across the gap from West Africa, convenient for island-hopping. The monkeys probably rafted across, perhaps on fragments of mangrove swamps that could support life as floating islands for a short while. Currents were in the right direction for inadvertent rafting. Another major group of animals, the hystricognath rodents, probably arrived in South America around the same time. Again probably they came from Africa, and indeed they are named after the African porcupine, Hystrix. Probably the monkeys rafted across the same island chain as the rodents, using the same favourable currents, though presumably not the same rafts.

Are all the New World primates descended from a single immigrant? Or was the island-hopping corridor used^* more than once by primates? What would constitute positive evidence for a double immigration? In the case of the rodents, there are still hystricognath rodents in Africa, including African porcupines, mole rats, dassie rats and cane rats. If it turned out that some of the South American rodents were close cousins of some African ones (say porcupines) while other South American rodents were closer cousins to other African ones (say mole rats) this would be good evidence that rodents more than once drifted to South America. That this is not the case is compatible with the view that rodents dispersed to South America only once, though it is not strong evidence. The South American primates, too, are all closer cousins to each other than they are to any African primate. Again this is compatible with the hypothesis of a single dispersal event, but again the evidence is not strong.

This is a good moment to repeat that the improbability of a rafting event is very far from being a reason for doubting that it happened. This sounds

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NEW WORLD MONKEYS JOIN The phylogeny of the 100 or so species of New World monkeys is somewhat disputed, but here we follow the modern consensus.

surprising. Usually, in everyday life, massive improbability is a good reason for thinking that something won't happen. The point about intercontinental rafting of monkeys, or rodents or anything else, is that it only had to happen once, and the time available for it to happen, in order to have momentous consequences, is way outside what we can grasp intuitively. The odds against a floating mangrove bearing a pregnant female monkey and reaching landfall in any one year may be ten thousand to one against. That sounds tantamount to impossible by the lights of human experience. But given 10 million years it becomes almost inevitable. Once it happened, the rest was easy. The lucky female gave birth to a family, which eventually became a dynasty, which eventually branched to become all the species of New World monkeys. It only had to happen once: great things then grew from small beginnings.

In any case, accidental rafting is not nearly so rare as you might think. Small animals are often seen on flotsam. And the animals aren't always small. The green iguana is typically a metre long and can be up to two metres. I quote from a note to Nature by Ellen J. Censky and others:

On 4 October 1995, at least 15 individuals of the green iguana, Iguana iguana, appeared on the eastern beaches of Anguilla in the Caribbean. This species did not previously occur on the island. They arrived on a mat of logs and uprooted trees, some of which were more than 30 feet long and had large root masses. Local fishermen say the mat was extensive and took two days to pile up on shore. They reported seeing iguanas on both the beach and on logs in the bay.

The iguanas were presumably roosting in trees on some other island, which were uprooted and sent to sea by a hurricane: either Luis, which had raged through the Eastern Caribbean on 4-5 September, or Marilyn, a fortnight later. Neither hurricane hit Anguilla. Censky and her colleagues subsequently caught or sighted green iguanas on Anguilla, and on an islet half a kilometre offshore. The population still survived on Anguilla in 1998 and included at least one reproductively active female.^*

I can't resist remarking how chilling this kind of ‘it only had to happen once’ logic becomes when you apply it to contingencies nearer home. The principle of nuclear deterrence, and the only remotely defensible justification for possessing nuclear weapons, is that nobody will dare risk a first strike, for fear of massive retaliation. What are the odds against a mistaken missile launch: a dictator who goes mad; a computer system that malfunctions; an escalation of threats that gets out of hand? The present leader of the largest nuclear power in the world (I am writing in 2003) thinks the word is ‘nucular’. He has never given any reason to suggest that his wisdom or his intelligence outperforms his literacy. He has demonstrated a predilection for ‘pre-emptive’ first strikes. What are the odds against a terrible mistake, initiating Armageddon? A hundred to one against, within any one year? I would be more pessimistic. We came awfully close in 1963, and that was with an intelligent President. In any case, what might happen in Kashmir? Israel? Korea? Even if the odds per year are as low as one in a hundred, a century is a very short time, given the scale of the disaster we are talking about. It only has to happen once.  {124} 

Let's return to a happier topic, the New World monkeys. As well as walking quadrupedally above branches, like many Old World monkeys, some New World monkeys suspend themselves like gibbons, and even brachi-ate. The tail is prominent in all the New World monkeys, and in the spider monkeys, woolly monkeys and howler monkeys it is prehensile, wielded like an extra arm. They can happily hang from the tail alone, or from any combination of arms, legs and tail. The tail doesn't have a hand at the end, but you almost believe it has, when you watch a spider monkey.^*

New World monkeys also include some spectacularly acrobatic leapers, as well as the only nocturnal anthropoids, the owl monkeys. Like owls and cats, owl monkeys have large eyes — the largest eyes of all the monkeys or apes. Pygmy marmosets are the size of a dormouse, smaller than any other anthropoid. The largest howler monkeys, however, are only about as big as a large gibbon. Howlers resemble gibbons, too, in being good at hanging and swinging from their arms, and in being very noisy — but where gibbons sound like New York police sirens in full cry, a troop of howler monkeys, with their resonating hollow bony voice boxes, remind me more of a ghost squadron of jet planes, roaring eerily through the treetops. As it happens, howler monkeys have a particular tale to tell us Old World monkeys — about the way we see colour, for they have independently arrived at the same solution.

Fifth arm

Black howler monkey (Alouatta caraya) demonstrating its prehensile tail.

The Howler Monkey's Tale (written with Yan Wong)

New genes aren't added to the genome out of thin air. They originate as duplicates of older genes. Then, over evolutionary time, they go their separate ways by mutation, selection and drift. We don't usually see this happening but, like detectives arriving on the scene after a crime, we can piece together what must have happened from the evidence that remains. The genes involved in colour vision provide a striking example. For reasons that will emerge, the howler monkey is especially well placed to tell the tale.

During their formative megayears, mammals were creatures of the night. The day belonged to the dinosaurs, who probably, if their modern relatives are any guide, had superb colour vision. So, we may plausibly imagine, did the  {125}  mammals’ remote ancestors, the mammal-like reptiles, who filled the days before the rise of the dinosaurs. But during the mammals’ long nocturnal exile, their eyes needed to snap up whatever photons were available, regardless of colour. Not surprisingly, for reasons of the kind that we shall examine in the Blind Cave Fish's Tale, colour discrimination degenerated. To this day most mammals, even those who have returned to live in the daylight, have rather poor colour vision, with only a two-colour system (‘dichromatic’). This refers to the number of different classes of colour-sensitive cells — ‘cones’ — in the retina. We catarrhine apes and Old World monkeys have three: red, green and blue, and are therefore trichromatic, but the evidence suggests that we regained a third class of cone, after our nocturnal ancestors lost it. Most other vertebrates, such as fish and reptiles but not mammals, have three-cone (trichromatic) or four-cone ftetrachromatic’) vision, and birds and turtles can be even more sophisticated. We'll come to the very special situation in the New World monkeys, and the even more special situation in the howler monkey, in a moment.

Interestingly, there is evidence that Australian marsupials differ from most mammals in having good trichromatic colour vision. Catherine Arrese and her colleagues, who discovered this in honey possums and dunnarts (it has also been demonstrated in wallabies), suggest that Australian (but not American) marsupials kept an ancestral reptilian visual pigment that the rest of the mammals lost. But mammals in general probably have the poorest colour vision among vertebrates. Most mammals see colour, if at all, only as well as a colourblind man. The notable exceptions are to be found among primates, and it is no accident that they, more than any other group of mammals, make use of bright colours in sexual display.

Unlike the Australian marsupials who perhaps never lost it, we can tell by looking at our relatives among the mammals that we primates did not retain trichromatic vision from our reptilian ancestors but rediscovered it — not once, but twice independently: first in the Old World monkeys and apes; and second in the New World howler monkeys, although not among the New World monkeys generally. Howler monkey colour vision is like that of apes, but different enough to betray its independent origin.

Why would good colour vision be so important that trichromacy evolved independently in New and Old World monkeys? A favoured suggestion is that it has to do with eating fruit. In a predominantly green forest, fruits stand out by their colours. This, in turn, is probably no accident. Fruits have probably evolved bright colours to attract frugivores, such as monkeys, who play the vital role of spreading and manuring their seeds. Trichromatic vision also assists in the detection of younger, more succulent leaves (often pale green, sometimes even red), against a background of darker green — but that is presumably not to the advantage of the plants.

Colour dazzles our awareness. Colour words are among the first adjectives that infants learn, and the ones they most eagerly tie to any noun that's going. It is hard to remember that the hues we perceive are labels for electromagnetic radiations of only slightly differing wavelengths. Red light has a wavelength around 700 billionths of a metre, violet around 420 billionths of a metre, but  {126}  the whole gamut of visible electromagnetic radiation that lies between these bounds is an almost ludicrously narrow window, a tiny fraction of the total spectrum whose wavelengths range from kilometres (some radio waves) down to fractions of a nanometre (gamma rays).

All eyes on our planet are set up in such a way as to exploit the wavelengths of electromagnetic radiation in which our local star shines brightest, and which pass through the window of our atmosphere. For an eye that has committed itself to biochemical techniques suitable for this loosely bounded range of wavelengths, the laws of physics impose sharper bounds to the portion of the electromagnetic spectrum that can be seen using those techniques. No animal can see far into the infrared. Those that come closest are pit vipers, who have pits in the head which, while in no sense focusing a proper image with infrared rays, allow these snakes to achieve some directional sensitivity to the heat generated by their prey. And no animal can see far into the ultraviolet although some, bees for instance, can see a bit further than we can. But on the other hand, bees can't see our red: for them it is infrared. All animals agree that ‘light’ is a narrow band of electromagnetic wavelengths lying somewhere between ultraviolet at the short end and infrared at the long end. Bees, people and snakes differ only slightly in where they draw the lines at each end of ‘light’.

An even narrower view is taken by each of the different kinds of light-sensitive cells within a retina. Some cones are slightly more sensitive towards the red end of the spectrum, others towards the blue. It is the comparison between cones that makes colour vision possible, and the quality of colour vision depends largely on how many different classes of cones there are to compare. Dichromatic animals have only two populations of cones interspersed with one another. Trichromats have three, tetrachromats four. Each cone has a graph of sensitivity, which peaks somewhere in the spectrum and fades away, not particularly symmetrically, on either side of the peak (see diagram below). Out beyond the edges of its sensitivity graph, the cell may be said to be blind.  {127} 

Suppose a cone's sensitivity peaks in the green part of the spectrum. Does this mean, if that cell is firing impulses towards the brain, that it is looking at a green object like grass or a billiard table? Emphatically not. It is just that the cell would need more red light (say) to achieve the same firing rate as a given amount of green light. Such a cell would behave identically towards bright red light or dimmer green light.^* The nervous system can tell the colour of an object only by comparing the simultaneous firing rates of (at least) two cells that favour different colours. Each one serves as a ‘control’ for the other. You can get an even better idea of the colour of an object by comparing the firing rate of three cells, all with different sensitivity graphs.

Colour television and computer screens, doubtless because they are designed for our trichromatic eyes, also work on a three-colour system. On a normal computer monitor, each ‘pixel’ consists of three dots placed too close together for the eye to resolve. Each dot always glows with the same colour — if you look at the screen at sufficient magnification you always see only the same three colours, usually red, green and blue although other combinations can do the job. Flesh tones, subtle shades — any hue you wish — can be achieved by manipulating the intensities with which these three primary colours glow.^*

Similarly, by comparing the firing rates from just three kinds of cones, our brains can perceive a huge range of hues. But most placental mammals, as already stated, are not trichromats but dichromats, with only two populations of cones in their retinas. One class peaks in the violet (or in some cases the ultraviolet), the other class peaks somewhere between green and red. In us trichromats, the short wavelength cones peak between violet and blue, and they are normally called blue cones. Our other two classes of cones can be called green cones and red cones. Confusingly, even the ‘red’ cones peak at a wavelength that is actually yellowish. But their sensitivity curve as a whole stretches into the red end of the spectrum. Even if they peak in the yellow, they still fire strongly in response to red light. This means that, if you subtract the firing rate of a ‘green’ cone from that of a ‘red’ cone, you'll get an especially high result when looking at red light. From now on I shall forget about peak sensitivities (violet, green and yellow) and refer to the three classes of cones as blue, green and red. In addition to cones, there are also rods: light-sensitive cells of a different shape from cones, which are especially useful at night and which are not used in colour vision at all. They'll play no further part in our story.

The chemistry and the genetics of colour vision are rather well understood. The main molecular actors in the story are opsins: protein molecules which serve as visual pigments sitting in the cones (and rods). Each opsin molecule works by attaching to, and encasing, a single molecule of retinal: a chemical derived from vitamin A.^* The retinal molecule has been forcibly kinked beforehand to fit it into the opsin. When hit by a single photon of light of an appropriate colour, the kink straightens out. This is the signal to the cell to fire a nervous impulse, which says to the brain ‘my kind of light here’. The opsin molecule is then recharged with another kinked retinal molecule, from a store in the cell.

Now, the important point is that not all opsin molecules are the same.  {128}  Opsins, like all proteins, are made under the influence of genes. DNA differences result in opsins that are sensitive to different colours, and this is the genetic basis of the two-colour or three-colour systems we have been talking about. Of course, since all genes are present in all cells, the difference between a red cone and a blue cone is not which genes they possess, but which genes they turn on. And there is some kind of rule that says that any one cone only turns on one class of gene.

The genes that make our green and red opsins are very similar to each other, and they are on the X chromosome (the sex chromosome of which females have two copies and males only one). The gene that makes the blue opsin is a bit different, and lies not on a sex chromosome but on one of the ordinary non-sex chromosomes called autosomes (in our case it is chromosome 7). Our green and red cells have clearly been derived from a recent gene duplication event, and much longer ago they must have diverged from the blue opsin gene in another duplication event. Whether an individual has dichromatic or trichromatic vision depends on how many distinct opsin genes it has in its genome. If it has, say, blue- and green-sensitive opsins but not red, it will be a dichromat.

That's the background to how colour vision works in general. Now, before we come to the special case of the howler monkey itself and how it became trichromatic, we need to understand the strange dichromatic system of the rest of the New World monkeys (some lemurs have it too, by the way, and not all New World monkeys do — for example, nocturnal owl monkeys have monochromatic vision). For the purposes of this discussion, ‘New World monkey’ temporarily excludes howler monkeys and other exceptional species. We'll come to the howler monkeys later.

First, set aside the blue gene as an unvarying fixture on an autosome, present in all individuals whether male or female. The red and green genes, on the X chromosome, are more complicated and will occupy our attention. Each X chromosome has only one locus where a red or a green^* allele might sit. Since a female has two X chromosomes, she has two opportunities for a red or green gene. But a male, with only one X chromosome, has either a red or a green gene but not both. So a typical male New World monkey has to be dichromatic. He has only two kinds of cones: blue plus either red or green. By our standards, all males are colourblind, but they are colourblind in two different ways; some males within a population lack green opsins, others lack red opsins. All have blue.

Females are potentially more fortunate. Having two X chromosomes, they could be lucky enough to have a red gene on one and a green gene on the other (plus the blue which again goes without saying). Such a female would be a trichromat^*. But an unlucky female might have two reds, or two greens, and would therefore be a dichromat. By our standards such females are colourblind, and in two ways, just like males.

A population of New World monkeys such as tamarins or squirrel monkeys, therefore, is an oddly complicated mixture. All males, and some females, are dichromats: colourblind by our standards but in two alternative ways. Some females, but no males, are trichromats, with true colour vision which is presumably similar to ours. Experimental evidence with tamarins searching for  {129}  food in camouflaged boxes showed that trichromatic individuals were more successful than dichromats. Perhaps foraging bands of New World monkeys rely on their lucky trichromat females to find food that most of them would otherwise miss. On the other hand, there is a possibility that the dichromats, either alone or in collusion with dichromats of the other kind, might have strange advantages. There are anecdotes of bomber crews in the Second World War deliberately recruiting one colourblind member because he could spot certain types of camouflage better than his otherwise more fortunate trichromat comrades. Experimental evidence confirms that human dichromats can indeed break certain forms of camouflage that fool trichromats. Is it possible that a troop of monkeys consisting of trichromats and two kinds of dichromats might collectively find a greater variety of fruits than a troop of pure trichromats? This might sound far-fetched, but it is not silly.

The red and the green opsin genes in New World monkeys constitute an example of a ‘polymorphism’. Polymorphism is the simultaneous existence, in a population, of two or more alternative versions of a gene, where neither is rare enough to be just a recent mutant. It is a well-established principle of evolutionary genetics that polymorphisms like this don't just happen without good reason. Unless something very special is going on, monkeys with the red gene will be either better off, or worse off, than monkeys with the green gene. We don't know which, but it is highly unlikely that they would be exactly equally good. And the inferior kind should go extinct.

A stable polymorphism in a population, then, indicates that something special is going on. What sort of thing? Two main suggestions have been made for polymorphisms in general, and either might apply to this case: frequency-dependent selection, and heterozygous advantage. Frequency-dependent selection happens when the rarer type is at an advantage, simply by virtue of being rarer. So, as the type which we had thought was ‘inferior’ starts to go extinct, it ceases to be inferior and bounces back. How could this be? Well, suppose ‘red’ monkeys are especially good at seeing red fruits while ‘green’ monkeys are especially good at seeing green fruits. In a population dominated by red monkeys, most of the red fruits will be already taken, and a lone green monkey, able to see green fruits, might be at an advantage — and vice versa. Even if that is not especially plausible, it is an example of the kind of special circumstance that can maintain both types in a population, without one of them going extinct. It is not hard to see that something along the lines of our ‘bomber crew’ theory might be the kind of special circumstance that maintains a polymorphism.

Turning now to heterozygous advantage, the classic example — cliché almost — is sickle-cell anaemia in humans. The sickling gene is bad, in that individuals with two copies of it (homozygotes) have damaged blood corpuscles that look like sickles, and suffer from debilitating anaemia. But it is good in that individuals with only one copy (hétérozygotes) are protected against malaria. In areas where malaria is a problem, the good outweighs the bad, and the siclding gene tends to spread through the population, in spite of the adverse effects on individuals unlucky enough to be homozygotes.^* Professor John Mollon and his colleagues, whose research is mainly responsible for uncovering the polymorphic  {130}  system of colour vision in New World monkeys, propose that the heterozygous advantage enjoyed by the trichromatic females is enough to favour the coexistence of the red and green genes in the population. But the howler monkey does it better, and this brings us to the teller of the tale itself.

Howler monkeys have managed to enjoy the virtues of both sides of the polymorphism, by combining them in one chromosome. They have done this by means of a lucky translocation. Translocation is a special kind of mutation. A chunk of chromosome somehow gets pasted into a different chromosome by mistake, or into a different place on the same chromosome. This seems to have happened to a lucky mutant ancestor of the howler monkeys, which consequently ended up with both a red gene and a green gene next door to one another on a single X chromosome. This monkey would have been well on its evolutionary way towards becoming a true trichromat, even if it was a male. The mutant X chromosome spread through the population until, now, all howler monkeys have it.

It was easy for howler monkeys to perform this evolutionary trick, because the three opsin genes were already knocking around the population in New World monkeys: it is just that, with the exception of a few lucky females, any one individual monkey had only two of them. When we apes and Old World monkeys independently did the same kind of thing, we did it differently. The dichromats from which we sprang were dichromats in only one way: there wasn't a polymorphism to take off from. Evidence suggests that the doubling-up of the opsin gene on the X chromosome in our ancestry was a true duplication. The original mutant found itself with two tandem copies of an identical gene, say two greens next door to each other on the chromosome, and it therefore was not a near-instant trichromat like the ancestral howler monkey mutant. It was a dichromat, with a blue and two green genes. The Old World monkeys became trichromats gradually in subsequent evolution, as natural selection favoured a divergence of the colour sensitivities of the two X opsin genes, towards green and red respectively.

When a translocation happens, it isn't just the gene of interest that is seen to move. Sometimes its travelling companions — its neighbours on the original chromosome who move with it to the new chromosome — can tell us something. And so it is in this case. The gene called Alu is well-known as a ‘transposable element’: a short, virus-like piece of DNA that replicates itself around the genome, as a sort of parasite, by subverting the cell's DNA replication machinery. Was Alu responsible for moving the opsin? It seems so. We find the ‘smoking gun’ when we look at the details. There are Alu genes at both ends of the duplicated region. Probably the duplication was an unintended by-product of parasitic reproduction. In some long-forgotten monkey of the Eocene Epoch, a genomic parasite near to the opsin gene tried to reproduce, accidentally replicated a much larger chunk of DNA than intended, and set us on the road to three-colour vision. Beware, by the way, of the temptation — it is all too common — to think that, because a genomic parasite seems, with hindsight, to have done us a favour, genomes therefore harbour parasites in the hope of future favours. That isn't how natural selection works.  {131} 

Whether engineered by Alu or not, mistakes of this kind still sometimes happen. When two X chromosomes line up, prior to crossing over, it is possible for them to line up incorrectly. Instead of lining the red gene on one chromosome with the corresponding red on the other, the similarity of the genes can confuse the lining-up process so that a red is lined up with a green. If crossing over then happens it is ‘unequal’: one chromosome could end up with an extra green (say) while the other X chromosome gets no green gene at all. Even if crossing over doesn't happen, a process called ‘gene conversion’ can take place, where a short sequence of one chromosome is converted to the matching sequence in the other. With misaligned chromosomes, a part of the red gene may be replaced by the equivalent part of the green gene, or vice versa. Both unequal crossing over and misaligned gene conversion can lead to red-green colourblindness.

Men suffer more frequently from red-green colourblindness than women (the suffering is not great, but it is still a nuisance and they presumably are deprived of aesthetic experiences enjoyed by the rest of us) because if they inherit one faulty X chromosome they do not have another to serve as a backup. Nobody knows whether they see blood and grass in the way the rest of us see blood, or in the way the rest of us see grass, or whether they see both in some completely different way. Indeed, it may vary from person to person. All we know is that people who are red-green colourblind think grass-like things are pretty much the same colour as blood-like things. In humans, dichromatic colourblindness afflicts about two per cent of males. Don't be confused, incidentally, by the fact that other kinds of red-green colourblindness are more common (affecting about eight per cent of males). These individuals are called anomalous trichromats: genetically they are trichromats, but one of their three kinds of opsins doesn't work.^*

Unequal crossing over doesn't always make things worse. Some X chromosomes end up with more than two opsin genes. The extra ones nearly always seem to be green rather than red. The record number is a staggering twelve extra green genes, arrayed in tandem. There is no evidence that individuals with extra green genes can see any better, but not all ‘green’ genes are exactly the same as each other — so it is theoretically possible for an individual to have not trichromatic vision but tetrachromatic or pentachromatic vision. I don't know that anybody has tested this.

It is possible that an uneasy thought has occurred to you. I have talked as though the acquisition, by mutation, of a new opsin automatically confers enhanced colour vision. But of course differences between the colour-sensitivities of cones are no earthly use unless the brain has some means of knowing which kind of cone is sending it messages. If it were achieved by genetic hard wiring — this brain cell is hooked up to a red cone, that nerve cell is hooked up to a green cone — the system would work, but it couldn't cope with mutations in the retina. How could it? How could brain cells be expected to ‘know’ that a new opsin, sensitive to a different colour, has suddenly become available and that a particular set of cones, in the huge population of cones in the retina, have turned on the gene for making the new opsin?  {132} 

It seems that the only plausible answer is that the brain learns. Presumably it compares the firing rates that originate in the population of cone cells in the retina and ‘notices’ that one sub-population of cells fires strongly when tomatoes and strawberries are seen; another sub-population when looking at the sky; another when looking at grass. This is a ‘toy’ speculation, but I suppose something like it enables the nervous system swiftly to accommodate a genetic change in the retina. My colleague Colin Blakemore, with whom I raised the matter, sees this problem as one of a family of similar problems that arise whenever the central nervous system has to accommodate itself to a change in the periphery.^*

The final lesson of the Howler Monkey's Tale is the importance of gene duplication. The red and the green opsin genes are clearly derived from a single ancestral gene that xeroxed itself to a different part of the X chromosome. Farther back in time, we may be sure, it was a similar duplication that separated the blue^* autosomal gene from what was to become the red/green X-chromo-somal gene. It is common for genes on completely different chromosomes to belong to the same ‘gene family’. Gene families have arisen by ancient DNA duplications followed by divergence of function. Various studies have found that a typical human gene has an average probability of duplication of about 0.1 to 1 per cent per million years. DNA duplication can be a piecemeal affair, or it can happen in bursts, for example when a newly virulent DNA parasite like Alu spreads throughout the genome, or when a genome is duplicated wholesale. (Entire-genome duplication is common in plants, and is postulated to have happened at least twice in our ancestry, during the origination of the vertebrates.) Regardless of when or how it happens, accidental DNA duplication is one of the major sources of new genes. Over evolutionary time, it isn't only genes that change, within genomes. Genomes themselves change.

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RENDEZVOUS 7 TARSIERS

We anthropoid pilgrims have arrived at Rendezvous 7, 58 million years ago in the dense and varied forests of the Palaeocene Epoch. There we greet a little evolutionary trickle of cousins, the tarsiers. We need a name for the clade that unites anthropoids and tarsiers, and it is haplorhines. The haplorhines consist of Concestor 7, perhaps our 6-million-greats-grandparent, and all its descendants: tarsiers, ‘monkeys’ and apes.

The first thing you notice about a tarsier is its eyes. Looking at the skull, it is almost the only thing there is to notice: a pair of eyes on legs pretty well sums up a tarsier. Each one of its eyes is as large as its entire brain, and the pupils open very wide too. The skull seen head-on seems to be wearing a pair of fashionably outsize, not to say giant, spectacles. Their huge size makes the eyes hard to rotate in their sockets but tarsiers, like some owls, are equal to the challenge. They rotate the whole head, on an extremely flexible neck, through nearly 360 degrees. The reason for their huge eyes is the same as in owls and night monkeys — tarsiers are nocturnal. They rely on moonlight, starlight and twilight, and need to sweep up every last photon they can.

Other nocturnal mammals have a tapetum lucidum — a reflecting layer behind the retina, which turns photons back in their tracks, so giving the retinal pigments a second chance to intercept them. It is the tapetum that makes it easy to spot cats and other animals at night.^* Shine a torch all around you. It will catch the attention of any animals in the vicinity, and they'll look straight at your light out of curiosity. The beam will be reflected back off the tapetum. Sometimes you can locate dozens of pairs of eyes with a single sweep of the torch. If electric light beams had been a feature of the environment in which animals evolved, they might well not have evolved a tapetum lucidum, as it is such a giveaway.

Tarsiers, surprisingly, have no tapetum lucidum. It has been suggested that their ancestors, along with other primates, passed through a diurnal phase and lost the tapetum. This is supported by the fact that tarsiers have the same weird system of colour vision as most of the New World monkeys. Several groups of mammals that were nocturnal in the time of the dinosaurs became diurnal when the death of the dinosaurs made it safe to do so. The suggestion is that the tarsiers subsequently returned to the night, but for some reason the evolutionary avenue of regrowing the tapetum was blocked to them. So they achieved the same result,^* of capturing as many photons as possible, by making their eyes very big indeed.  {134} 

The other descendants of Concestor 7, the ‘monkeys’ and apes, also lack a tapetum lucidum, not surprisingly given that they are all diurnal except the owl monkeys of South America. And the owl monkeys, like the tarsiers, have compensated by growing very large eyes — although not quite so large, in proportion to the head, as those of the tarsiers. We can make a good guess that Concestor 7 also lacked a tapetum lucidum and was probably diurnal. What else can we say about it?

Apart from being diurnal, it may have been quite tarsier-like. The reason for saying this is that there are some plausible fossils called the omomyids dating from about the right period. Concestor 7 might have been something like an omomyid, and the omomyids were quite tarsier-like. Their eyes were not so big as modern tarsiers’, but big enough to suggest that they were nocturnal. Perhaps Concestor 7 was a diurnal version of an omomyid, living in trees. Of its two descendant lineages, one stayed in the light and blossomed into the anthropoid monkeys and apes. The other reverted to the darkness and became the modern tarsiers.

Eyes apart, what is to be said about tarsiers? They are outstanding leapers, with long legs like frogs or grasshoppers. A tarsier can jump more then 3 metres horizontally and 1.5 metres vertically. They have been called furry frogs. It is probably no accident that they resemble frogs too in uniting the two bones of the lower legs, the tibia and the fibula, to make a single strong bone, the tibiofibula. All anthropoids have nails instead of claws, and tarsiers do too, with the curious exception of ‘grooming claws’ on the second and third toes.

We can't guess with any certainty where Rendezvous 7 takes place. But we might just note that North America is rich in early omomyid fossils of the right period, and that it was in those days firmly joined to Eurasia via what is now Greenland. Perhaps Concestor 7 was a North American.

RENDEZVOUS 8 LEMURS, BUSHBABIES AND THEIR KIN

Gathering the little leaping tarsiers into our pilgrimage, we head off back towards Rendezvous 8, where we are to be joined by the rest of the primates traditionally called prosimians: the lemurs, pottos, bushbabies and lorises. We need a name for those ‘prosimians’ that are not tarsiers. ‘Strepsirhines’ has become customary. It means ‘split nostril’ (literally comb nose). It is a slightly confusing name. All it means is that the nostril is shaped like a dog's. The rest of the primates, including us, are haplorhines (simple nose: our nostrils are each just a simple hole).

We haplorhine pilgrims, then, greet our strepsirhine cousins, of which the great majority are lemurs, at Rendezvous 8. Various dates have been suggested for this point. I have taken it as 63 million years into the past, a commonly accepted date and one just ‘before’ our passage back into the Cretaceous Period. Bear in mind, however, that a few researchers imagine this rendezvous even further back in time, during the Cretaceous itself. At 63 million years ago, the Earth's vegetation and climate had rebounded from their drastic disturbance when the Cretaceous — and the dinosaurs — came to an end (see ‘The Great Cretaceous Catastrophe’). The world was largely wet and forested, with at least the northern continents covered in a relatively restricted mix of deciduous conifers, and a scattering of flowering plant species.

Perhaps in the branches of a tree, we encounter Concestor 8, seeking fruit or maybe an insect. This most recent common ancestor of all surviving primates is approximately our 7-million-greats-grandparent. Fossils that might help us reconstruct what Concestor 8 was like include the large group called plesiadapiforms. They lived about the right time, and they have many of the qualities you would expect of the grand ancestor of all the primates. Not all of them, however, which makes their supposed position close to the primate ancestor controversial.

Of the living strepsirhines, the majority are lemurs, living exclusively in Madagascar, and we'll come to them in the tale that follows. The others divide into two main groups, the leaping bushbabies and the creeping lorises and pottos. When I was a child of three in Nyasaland (now Malawi) we had a pet bushbaby. Percy was brought in by a local African, and was probably an orphaned juvenile. He was tiny: small enough to perch on the rim of a glass of whisky, into which he would dip his hand and drink with evident enjoyment. He slept during the day, clasping the underside of a beam in the bathroom. When his ‘morning’ came (in the evening), if my parents failed to catch him in time

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LEMURS AND THEIR KIN JOIN The living primates can be divided into the lemurs and their kin, and the rest. The time of this divergence is debated — some experts place it as much as 20 million years earlier, with a consequent increase in the age of Concestors 9, 10, and 11. The five Madagascar lemur families (30 or so species) and the loris family (18 species) are known as ‘strepsirhines’. The order of branching within lemurs in this strepsirhine phylogeny remains controversial.

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(which was often, because he was extremely agile and a terrific leaper) he would race to the top of my mosquito net and urinate on me from above. When leaping, for example onto a person, he did not exhibit the common bushbaby habit of urinating on his hands first. On the theory that ‘urine washing’ is for scent-marking, this would make sense given that he was not an adult. On the alternative theory that the urine improves grip, it is less clear why he didn't do it.

I shall never know to which of the 17 species of bushbaby Percy belonged, but he was most certainly a leaper, not a creeper. The creepers are the pottos of Africa and the lorises of Asia. They move much more slowly — especially the ‘slow loris’ of the Far East, which is a stealth hunter, inching along a branch until within reach of prey, whereupon it lunges with great speed.

Bushbabies and pottos remind us that a tropical forest is a three-dimensional world like the sea. Seen from above the canopy, the green waves at its surface billow towards the horizon. Dive down into the darker green world beneath, and you pass through distinct layers, again as in the sea. The animals of the forest, like fish in the sea, find it as easy to move up and down as horizontally. But, also as in the sea, each species in practice specialises in making its living at a particular level. In the West African forests by night, the surface canopy is the province of the pygmy bushbabies hunting insects, and the fruit-eating pottos. Below the level of the canopy, the trunks of the trees are separated by gaps, and this is the domain of the needle-clawed bushbaby whose eponymous equipment enables it to cling to the trunks after leaping the gaps between them. Deeper still, in the understorey, the golden potto and the closely related angwantibo hunt caterpillars. At dawn, the nocturnal bushbabies and pottos give place to day-hunting monkeys, who parcel up the forest into similarly stratified layers. The same kind of stratification goes on in the South American forests, where as many as seven species of (marsupial) possum can be found, each at its own level.

The lemurs are descended from those early primates who happened to find themselves marooned in Madagascar during the time when monkeys were evolving in Africa. Madagascar is a large enough island to serve as a laboratory for natural experiments in evolution. The tale of Madagascar will be told by one of the lemurs, by no means the most typical of them, the aye-aye Daubentonia. I don't remember much from the discourse on lemurs that Harold Pusey — wise and learned warhorse of the lecture hall — gave to my generation of Oxford zoologists, but I do remember the haunting refrain with which he concluded almost every sentence about lemurs: ‘Except Daubentonia.’ ‘EXCEPT Daubentonia!’ Despite appearances, Daubentonia, the aye-aye, is a perfectly respectable lemur, and lemurs are the most famous inhabitants of the great island of Madagascar. The Aye-Aye's Tale is about Madagascar, textbook showcase of biogeographical natural experiments, a tale not just of lemurs but of all of Madagascar's peculiar — in the original sense of the word — fauna and flora.  {139} 

The Aye-Aye's Tale

A British politician once described a rival (who later went on to become their party leader) as having ‘something of the night’ about him. The aye-aye conveys a similar impression, and indeed it is wholly nocturnal — the largest primate to be so. It has disconcertingly wide-set eyes in a ghostly pale face. The fingers are absurdly long: the fingers of an Arthur Rackham witch. ‘Absurd’ only by human standards, however, for we may be sure those fingers are long for a good reason: aye-ayes with shorter fingers would be penalised by natural selection, even if we don't know why. Natural selection is a strong enough theory to be predictive in this fashion, now that science no longer needs convincing of its truth.

One finger, the middle finger, is unique. Hugely long and thin, even by aye-aye standards, it is used specifically to make holes in dead wood and lever out grubs. Aye-ayes detect prey in wood by drumming with the same long finger, and listening for the changes in tone that betray an insect underneath.^* That isn't quite all they use the long middle finger for. At Duke University, which surely has the largest collection of lemurs outside Madagascar, I have seen an aye-aye, with great delicacy and precision, insert the long middle finger up its own nostril — in quest of what, I don't know. The late Douglas Adams wrote a wonderful chapter about the aye-aye in last Chance to See, his travel book about his journeys with the zoologist Mark Carwardine.

The aye-aye is a nocturnal lemur. It is a very strange-looking creature that seems to have been assembled from bits of other animals. It looks a little like a large cat with a bat's ears, a beaver's teeth, a tail like a large ostrich feather, a middle finger like a long dead twig and enormous eyes that seem to peer past you into a totally different world which exists just over your left shoulder... Like virtually everything that lives on Madagascar, it does not exist anywhere else on earth.

What wonderfully pithy writing, how sadly missed its author. Adams and Carwardine's purpose in Last Chance to See was to call attention to the plight of endangered species. The 30 or so surviving species of lemurs are relicts of a much larger fauna that survived up until Madagascar was invaded by destructive humans about 2,000 years ago.

Madagascar is a fragment of Gondwana (see page 237) which became separated from what is now Africa about 165 million years ago, and finally separated from what became India about 90 million years ago. This order of events may seem surprising but, as we shall see, once India had shaken itself free of Madagascar it moved away unusually fast by the sub-lorisoid standards of plate tectonics.  {140} 

Setting aside bats (which presumably flew in) and human introductions, Madagascar's terrestrial inhabitants are descendants either of the ancient Gondwana fauna and flora, or of rare immigrants rafted in with improbable good luck from elsewhere. It is a natural botanical and zoological garden, which houses about five per cent of all the plant and animal land species in the world, more than 80 per cent of them being found nowhere else. Yet, notwithstanding this astonishing richness of species, it is also remarkable for the number of major groups that are totally absent. Unlike Africa or Asia, Madagascar has no native antelopes, no horses or zebras, no giraffes, no elephants, no rabbits, no elephant shrews, no members of the cat or the dog family: none of the expected African fauna at all^*. There are bushpigs which seem to have arrived quite recently, perhaps introduced by humans. (We shall return to the aye-aye and the other lemurs at the end of the tale.)

Madagascar has three members of the mongoose family, which are clearly related to each other and must have arrived in the form of a single founder species from Africa, and subsequently branched. Of these, the most famous is the fossa, a sort of giant mongoose the size of a beagle but with a very long tail. Its smaller relatives are the falanouc, and the fanaloka whose Latin name, confusingly, is Fossa fossa^*

There is a group of peculiarly Madagascan rodents, nine genera in all, united in one subfamily, the Nesomyinae. These include a burrowing giant rat-like form, a tree-climber, a tufted-tail ‘marsh rat’ and a jumping jerboa-like form. It  {141}  has long been controversial whether these peculiarly Madagascan rodents result from a single immigration event, or several. If there was a single founder, it would mean that its descendants, since arriving in Madagascar, evolved to fill all these different rodent niches: a very Madagascan story. Recent molecular evidence shows that a couple of species on the African mainland are more closely related to some Madagascan rodents than some Madagascan rodents are to each other. This might seem to indicate multiple immigration from Africa. However, a closer look at the evidence supports a more surprising hypothesis. It seems that all the Madagascan rodents are descended from a single founder who arrived, not from Africa but from India. If this is right, the affinities with two African rodents would indicate further rafting from Madagascar to Africa. The ancestors of the African species came from India, via Madagascar. It is as though the Indian Ocean favours rafting in a westerly direction. And once again we mustn't forget that India would have been closer to Madagascar when the immigration happened.

Six out of the eight species of baobab tree are unique to Madagascar, and its count of 130 species of palm trees dwarfs the number found in the whole of Africa. Some authorities think chameleons originated there. Certainly, two-thirds of the world's species of chameleons are native to Madagascar. And there is a peculiarly Madagascan family of shrew-like animals, the tenrecs. Once classified in the Order Insectivora, they are nowadays placed with the Afrotheria whom we shall meet at Rendezvous 13. They probably arrived on Madagascar as two different founder populations from Africa, before any other mammals. They have now diversified into 27 species, including some that resemble hedgehogs, some that resemble shrews, and one that lives largely underwater like a water shrew. The resemblances are convergent — independently evolved, in typical Madagascan fashion. Madagascar being isolated, there were no ‘true’ hedgehogs and no ‘true’ water shrews. So tenrecs, who had the good fortune to be on the spot, evolved to become the local equivalents of hedgehogs and water shrews.

Madagascar has no monkeys or apes at all, and that set the scene for the lemurs themselves. By lucky chance, some time later than 63 million years ago, a founder population of early strepsirhine primates accidentally found their way to Madagascar. As usual, we have no idea how this happened. The evolutionary split (Rendezvous 8, at 63 Mya) was later than Madagascar's geographical separation from Africa (165 Mya) and India (88 Mya), so we can't say the lemurs’  {142}  ancestors were Gondwanan residents sitting there all along. In several places in this book I have used ‘rafting’ as a kind of shortened code for ‘fluke sea-crossing by some means unknown, of great statistical improbability, which only had to happen once, and which we know must have happened at least once because we see the later consequences’. I should add that ‘great statistical improbability’ is in there for form's sake. The evidence, as we saw at Rendezvous 6, is actually that ‘rafting’ in this general sense is commoner than intuition would expect. The classic example is the swift recolonisation of the remnants of Krakatoa after it was abruptly destroyed by a catastrophic volcanic event.^*

In Madagascar, the consequences of the lucky rafting were dramatic and delightful: lemurs great and small, ranging in size from the pygmy mouse lemur, smaller than a hamster, to the recently extinct Archaeoindris, which was heavier than a large silverback gorilla and looked like a bear; familiar lemurs like the ring-tailed, with their long, striped, hairy-caterpillar tails wafting in the air as the troop runs along the ground; or the indri (opposite) or the dancing sifaka which may be the most bipedally accomplished primate after ourselves.

And of course there is the aye-aye, teller of this tale. The world will be a sadder place when the aye-aye goes extinct, as I fear it may. But a world without Madagascar would be not just sadder — it would be impoverished. If you wiped out Madagascar, you would destroy only about a thousandth of the world's total land area, but fully four per cent of all species of animals and plants.

For a biologist, Madagascar is the Island of the Blest. Along our pilgrim voyage, it is the first of five large — in some cases very large indeed — islands, whose isolation, at crucial junctures in Earth history, radically structured the diversity of mammals. And not just mammals. Something similar happens with insects, birds, plants and fish, and when we are eventually joined by more distant pilgrims we shall find other islands playing the same role — not all of them dry land islands. The Cichlid's Tale will persuade us that each of the great African lakes is its own watery Madagascar, and cichlid fishes are its lemurs.

The islands or island continents that have shaped the evolution of mammals are, in the order we shall visit them, Madagascar, Laurasia (the great northern continent which was once isolated from its southern counterpart, Gondwana), South America, Africa, and Australia. Gondwana itself might be added to the list, for, as we shall discover at Rendezvous 15, it too bred its own unique fauna, before it broke up into all our Southern Hemisphere continents. The Aye-Aye's Tale has shown us the faunistic and floristic extravagance of Madagascar. Laurasia is the ancient home, and Darwinian proving-ground, of the huge influx of pilgrims we shall meet at Rendezvous 11, the laurasiatheres. At Rendezvous 12 we shall be joined by a strange band of pilgrims, the xenarthrans, who served their evolutionary apprenticeship on the then island continent of South America, and who will tell us the tale of the others who shared it. At Rendezvous 13 we find the afrotheres, another hugely varied group of mammals, whose diversity was honed on the island continent of Africa. Then, at Rendezvous 14 it is the turn of Australia and the marsupials. Madagascar is the microcosm which sets the pattern — large enough to follow it, small enough to display it in exemplary clarity.

THE GREAT CRETACEOUS CATASTROPHE

Rendezvous 8, where our pilgrims meet the lemurs 63 million years ago, is our last rendezvous ‘before’, in our backward journey, we burst through the 65 million year barrier, the so-called K/T boundary, which separates the Age of Mammals from the much longer Age of Dinosaurs that preceded it.^* The K/T was a watershed in the fortunes of the mammals. They had been small, shrew-like creatures, nocturnal insectivores, their evolutionary exuberance held down under the weight of reptilian hegemony for more than 100 million years. Suddenly the pressure was released and, in a geologically very short time, the descendants of those shrews expanded to fill the ecological spaces left by the dinosaurs.

What caused the catastrophe itself? A controversial question. At the time there was extensive volcanic activity in India, spewing out lava flows covering well over a million square kilometres (the ‘Deccan Traps’) which must have had a radical effect on the climate. However, a variety of evidence is building a consensus that the final deathblow was more sudden and more drastic. It seems that a projectile from space — a large meteorite or comet — hit Earth. Detectives proverbially reconstruct events from cigar ash and footprints. The ash in this case is a worldwide layer of the element iridium at just the right place in the geological strata. Iridium is normally rare in the Earth's crust but common in meteorites. The sort of impact we are talking about would have pulverised the

The Earth at the time of the K/T extinction [257]. The position of the Chicxulub bolide impact is shown. By the end of the Cretaceous, Laurasia and Gondwana had broken up into continental shapes broadly familiar to us today, though Europe was still a large island and India, now separated from Madagascar, was making its rapid way towards Asia. The climate was warm and mild, even in the polar regions, as it was throughout the Mesozoic Era, partly as a result of the pattern of warm ocean currents.

incoming bolide, and scattered its remains as dust throughout the atmosphere, from which it would eventually have rained down all over the Earth's surface. The footprint — 100 miles wide and 30 miles deep — is a titanic impact crater, Chicxulub, at the tip of the Yucatan peninsula in Mexico. The location is marked on the map opposite, which also illustrates the disposition of the continents, oceans and shallow seas at the time.

Space is full of moving objects, travelling in random directions and at a great variety of speeds relative to one another. There are many more ways in which objects can be travelling at high speeds relative to us than low speeds. So, most of the objects that hit our planet are travelling very fast indeed. Fortunately, most of them are small and burn up in our atmosphere as ‘shooting stars’. A few are large enough to retain some solid mass all the way to the planet's surface. And, once in a few tens of millions of years, a very large one catastrophically collides with us. Because of their high velocity relative to Earth, these massive objects release an unimaginably large quantity of energy when they collide. A gunshot wound is hot because of the velocity of the bullet. A colliding meteorite or comet is likely to be travelling even faster than a high-velocity rifle bullet. And where the rifle bullet weighs only ounces, the mass of the celestial projectile that ended the Cretaceous and slew the dinosaurs was measured in gigatons. The noise of the impact, thundering round the planet at a thousand kilometres per hour, probably deafened every living creature not burned by the blast, suffocated by the wind-shock, drowned by the 150-metre tsunami that raced around the literally boiling sea, or pulverised by an earthquake a thousand times more violent than the largest ever dealt by the San Andreas fault. And that was just the immediate cataclysm. Then there was the aftermath — the global forest fires, the smoke and dust and ash which blotted out the sun in a two-year nuclear winter that lolled off most the plants and stopped dead the world's food chains.

No wonder all the dinosaurs, with the notable exception of the birds, perished — and not just the dinosaurs, but about half of all other species too, particularly the marine ones.^* The wonder is that any life at all survives these cataclysmic visitations. By the way, the one that ended the Cretaceous and the dinosaurs is not the biggest — that honour falls to the mass extinction that marks the end of the Permian, about a quarter of a billion years ago, in which some 95 per cent of all species went extinct. Recent evidence suggests that an even larger comet or meteorite was responsible for that mother of all extinctions. We are uneasily aware that a similar catastrophe could hit us at any moment. Unlike the dinosaurs in the Cretaceous, or the pelycosaurian (mammallike) reptiles in the Permian, astronomers would give us several years’ warning, or at least months. But this would not be a blessing for, at least with present-day technology, there is nothing we could do to prevent it. Fortunately, the odds that this will happen in any particular person's lifetime are, by normal actuarial standards, negligible. At the same time, the odds that it will happen in some unfortunate individuals’ lifetime are near certainty. Insurance companies are just not used to thinking that far ahead. And the unfortunate individuals concerned will probably not be human, for the statistical likelihood is that we shall be extinct before then anyway.  {145} 

A rational case can be mounted that humanity should start research into defensive measures now, to bring the technology up to the point where, if a credible warning were sounded, there would be time to put measures into effect. Present-day technology could only minimise the impact, by storing a suitable balance of seeds, domestic animals, machines including computers and databases full of accumulated cultural wisdom, in underground bunkers with privileged humans (now there's a political problem). Better would be to develop so-far only dreamed-of technologies to avert the catastrophe by diverting or destroying the intruder. Politicians who invent external threats from foreign powers, in order to scare up economic or voter support for themselves, might find that a potentially colliding meteor answers their ignoble purpose just as well as an Evil Empire, an Axis of Evil, or the more nebulous abstraction ‘Terror’, with the added benefit of encouraging international co-operation rather than divisiveness. The technology itself is similar to the most advanced ‘star wars’ weapons systems, and to that of space exploration itself. The mass realisation that humanity as a whole shares common enemies could have incalculable benefits in drawing us together rather than, as at present, apart.

Evidently, since we exist, our ancestors survived the Permian extinction, and later the Cretaceous extinction. Both catastrophes, and the others that have also occurred, must have been extremely unpleasant for them, and they survived by the skin of their teeth, possibly deaf and blind but just capable of reproducing, otherwise we wouldn't be here. Perhaps they were hibernating at the time, and didn't wake up until after the nuclear winter that is thought to follow such catastrophes. And then, in the fullness of evolutionary time, they reaped the benefits. In the case of the Cretaceous survivors, there were now no dinosaurs to eat them, no dinosaurs to compete with them. You might think there was a down side: no dinosaurs for them to eat. But few mammals were large enough, and few dinosaurs small enough, to make that much of a loss. There can be no doubt that the mammals flowered massively after the K/T, but the form of the flowering and how it relates to our rendezvous points is debatable. Three ‘models’ have been suggested, and now is the time to discuss them. The three shade into each other, and I shall present them in their extreme forms only for simplicity. For reasons of clarity, as I believe, I shall change their usual names to the Big Bang Model, the Delayed Explosion Model, and the Non-explosive Model. There are parallels in the controversy over the so-called Cambrian Explosion, to be discussed in the Velvet Worm's Tale.

Of the three models, the evidence, especially molecular evidence but increasingly fossil evidence too, seems to favour the Delayed Explosion Model. Most of the major splits in the mammal family tree go way back, deep into dinosaur times. But most of those mammals that coexisted with dinosaurs were pretty similar to each other, and remained so until the removal of the dinosaurs freed them to explode into the Age of Mammals. A few members of those major lineages haven't changed much since those early times, and they consequently resemble each other, even though the common ancestors that they share are extremely ancient. Eurasian shrews and tenrec shrews, for example, are very similar to each other, probably not because they have converged from different starting points but because they haven't changed much since primitive times. Their shared ancestor, Concestor 13, is thought to have lived about 105 million years ago, nearly as long before the K/T boundary as the K/T is before the present.

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RENDEZVOUS 9 COLUGOS AND TREE SHREWS

Rendezvous 9 occurs 70 million years into the past, still in the time of the dinosaurs and before the flowering of mammalian diversity properly began. Actually, the flowering of flowers themselves had only just begun. Flowering plants, while diverse, had been previously restricted to disturbed habitats such as those uprooted by elephantine dinosaurs or ravaged by fire, but by now had gradually evolved to include a range of forest-canopy trees and understorey bushes. Concestor 9, which was something like our 10-million-greats-grand-parent, was the common ancestor we share with a pair of squirrel-like mammal groups. Well, one of them is squirrel-like and the other more like a flying squirrel. They are the 18 species of tree shrews and the two species of colugos or ‘flying lemurs’, all from South East Asia.

The tree shrews are all very similar to each other, and are placed in the family Tupaiidae. Most live like squirrels, in trees, and some species resemble squirrels even down to having long, fluffy, aerodynamic tails. The resemblance, however, is superficial. Squirrels are rodents. Tree shrews are certainly not rodents. As to what they are, well, that is partly what the next tale will be about. Are they shrews, as their common name would suggest? Are they primates, as certain authorities have long thought? Or are they something else altogether? The pragmatic solution has been to place them in their own, uncertainly placed, mammalian order, the Scandentia (Latin scandere = to climb). But in seeking concestor points, we cannot avoid the problem so easily. The Colugo's Tale contains my justification — or apology? — for the solution I have adopted, which is to unite the colugos and the tree shrews ‘before’ they join our pilgrimage.

Colugos have long been known as flying lemurs, prompting the obvious put-down: they neither fly nor are lemurs. Recent evidence suggests that they are closer to lemurs than was realised even by those responsible for the misnomer. And, while they don't have powered flight like a bat or a bird, they are adept gliders. The two species, Cynocephalus volans the Philippine colugo, and C. variegatus, the Malayan colugo, have a whole order to themselves, the Dermoptera. It means ‘wings of skin’. Like the flying squirrels of America and Eurasia, the more distantly related flying scaly-tailed squirrels of Africa, and the marsupial gliders of Australia and New Guinea, colugos have a single large flap of skin, the patagium, which works a bit like a controlled parachute. Unlike that of the other gliders, the colugo's patagium embraces the tail as well as the limbs, and it extends right to the tips of the fingers and toes. Colugos are also, with a ‘wing’ span of 70 centimetres, larger than any of those other gliders.  {148}  Colugos can glide more than 70 metres through the forest at night, to a distant tree, with little loss of height.

The fact that the patagium stretches right to the tip of the tail, and to the tips of the fingers and toes, suggests that the colugos are more deeply committed to the gliding way of life than other mammalian gliders. And indeed, they are pretty inept on the ground. They more than make up for it in the air, where their huge parachute gives them the run of large areas of forest at high speed. This necessitates good stereoscopic vision for steering accurately at night towards a target tree, avoiding fatal collisions, and then making a precision landing. And indeed they have large stereoscopic eyes, excellent for night vision.

Colugos and tree shrews have unusual reproductive systems, but in very different directions. Colugos resemble marsupials in that their young are born early in embryonic development. Having no marsupial pouch, the mother presses the patagium into service. The tail region of the patagium is folded forwards to form a makeshift pouch in which the (usually single) young sits. The mother often hangs upside down from a branch like a sloth, and the patagium then looks and feels like a hammock for the baby.

To be a baby colugo peeping over the edge of a warm, furry hammock sounds appealing. A baby tree shrew, on the other hand, receives perhaps less maternal care than any other baby mammal. The mother tree shrew, at least in several of the species, has two nests, one in which she herself lives, the other in which the babies are deposited. She visits them only to feed them, and then only for the briefest possible time, between five and ten minutes. And she visits them for this brief feed only once in every 48 hours. In the meantime, with no mother to keep them warm as any other baby mammal would have, the little tree shrews need to heat themselves from their food. To this end, the mother's milk is exceptionally rich.  {149} 

The affinities of the tree shrews and the colugos, to each other and to the rest of the mammals, are subject to dispute and uncertainty. There is a lesson in that very fact, and it is the lesson of the Colugo's Tale.

The Colugo's Tale

The colugo could tell a tale of nocturnal gliding through the forests of South East Asia. But for the purposes of our pilgrimage it has a more down-to-earth tale to tell, whose moral is a warning. It is the warning that our apparently tidy story of concestors, rendezvous points, and the sequence in which pilgrims join us, is heavily subject to disagreement and revision as new research is done. The phylogeny diagram at Rendezvous 9 shows one recently supported view. According to this view, which I am provisionally accepting here, the pilgrims we primates greet at Rendezvous 9 are an already united band consisting of the colugos and the tree shrews. A few years ago, the colugos would not have entered into this picture. Orthodox taxonomy would have had the tree shrews alone joining the primates at this rendezvous: the colugos would have joined us further down the road, not even very close.

There is no guarantee that our present picture will stay settled. New evidence may resurrect our previous view, or it may prompt a completely different one. Some researchers even think the colugos are closer to the primates than the tree shrews are. If they are right, Rendezvous 9 is where we primates are joined by the colugos. We'd have to wait for the tree shrews at Rendezvous 10, and the numbering of concestors from then on would need to be increased by one. But that is not the view I have adopted. Doubt and uncertainty may seem rather unsatisfactory as the moral for a tale, but it is an important lesson that must be taken on board before our pilgrimage to the past proceeds much further. The lesson will apply to many other rendezvous.

I could have signalled my uncertainty by having multi-way splits (‘polytomies’: see the Gibbon's Tale) in my phylogenetic trees. This is the solution adopted by certain authors, notably Colin Tudge in his masterly phylogenetic summary of all life on earth, The Variety Of Life. But having polytomies on some branches risks giving false confidence in the others. The revolution in mammalian systematics involving the laurasiatheres and afrotheres (Rendezvous 11 to 13) happened after Tudge's book was published, as recently as 2000, and so some areas of his classification which he considered resolved have now been transformed. Were he to bring out a new edition, it would surely be radically changed. Very possibly the same will happen with this book, and it isn't just the colugos and tree shrews. The position of tarsiers (Rendezvous 7), and the grouping of lampreys with hagfishes (Rendezvous 22) are unsure. The affinities of the afrotheres (Rendezvous 13) and the coelacanths (Rendezvous 19) are still slightly unsure. The ordering of our rendezvous with cnidarians and ctenophores (Rendezvous 28 and 29) could be the wrong way round.

Other rendezvous, such as that with the orang utans, are as near certain as it  {150}  is possible to be, and there are many more in that happy category. There are also some borderline cases. So, rather than make what comes close to a subjective judgement about which groups deserve fully resolved trees and which do not, I have nailed my more-or-less uncertain colours to the mast in 2004, explaining the doubts in the text whenever possible (apart from a single rendezvous, number 37, where the order is so unsure that even the experts are not willing to hazard a guess). In the fullness of time, I fear that some (but relatively few, I hope) of my rendezvous points and their phylogenies will turn out to be wrong, in the light of new evidence.^*

Earlier systems of taxonomy that were not tied to the evolution-standard might be controversial, in the way that matters of taste or judgement are controversial. A taxonomist might argue that, for reasons of convenience in exhibiting museum specimens, tree shrews should be grouped with shrews and colugos with flying squirrels. In such judgements there is no absolutely right answer. The phyletic taxonomy adopted in this book is different. There is a correct tree of life, but we don't yet know what it is. There is still room for human judgement, but it is judgement about what will eventually turn out to be the undisputable truth. It is only because we haven't looked at enough details yet, especially molecular details, that we are still unsure what that truth is. The truth really is hanging up there waiting to be discovered. The same cannot be said for judgements of taste or of museum convenience.

RENDEZVOUS 10 RODENTS AND RABBITKIND

Rendezvous 10 occurs 75 million years into our journey. It is here that our pilgrims are joined — overwhelmed, rather — by a teeming, scurrying, gnawing, whisker-quivering plague of rodents. For good measure, we also greet at this point the rabbits, including the very similar hares and jack-rabbits, and the rather more distant pikas. Rabbits were once classified as rodents, because they also have very prominent gnawing teeth at the front — indeed they outpoint the rodents, with an extra pair. They were then separated off, and are still placed in their own order, Lagomorpha, as opposed to Rodentia. But modern authorities group the lagomorphs together with the rodents in a ‘cohort’ called Glires. In the terms of this book, the lagomorph pilgrims and the rodent pilgrims joined up with each other ‘before’ the whole lot of them joined our pilgrimage. Concestor 10 is approximately our 15-million-greats-grandparent. It is the latest ancestor we share with a mouse, but the mouse is connected to it through a very much larger number of greats, because of short generation times.

Rodents are one of the great success stories of mammaldom. More than 40 per cent of all mammal species are rodents, and there are said to be more individual rodents in the world than all other mammals combined. Rats and mice have been the hidden beneficiaries of our own Agricultural Revolution, and they have travelled with us across the seas to every land in the world. They devastate our granaries and our health. Rats and their cargo of fleas were responsible for the Black Death and the Great Plague (both outbreaks of bubonic plague), they have spread typhus, and have been blamed for more human deaths in the second millennium than all wars and revolutions put together. When even the four horsemen are laid low by the apocalypse, it will be rats that scavenge their remains, rats that will swarm like lemmings over the ruins of civilisation. And, by the way, lemmings are rodents, too — northern voles who, for reasons that are not entirely clear, build up their populations to plague proportions in so-called ‘lemming years’, and then indulge in frantic — though not wantonly suicidal as is falsely alleged — mass migrations.

Rodents are gnawing machines. They have a pair of very prominent incisor teeth at the front, perpetually growing to replace massive wear and tear. The gnawing masseter muscles are especially well developed in rodents. They don't have canine teeth, and the large gap or diastema that separates their incisors from their back teeth improves the efficiency of their gnawing. Rodents can gnaw their way through almost anything. Beavers fell substantial trees by gnawing through their trunks. Mole rats live entirely underground, tunnelling

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FACING PAGE RODENTS AND RABBITS JOIN Experts generally accept that the 70 or so species of rabbit relatives and the approximately 2,000 rodents (two-thirds of which are in the mouse family) group together. Recent genetic studies place this group as the sister to the primates, colugos, and tree shrews. Parts of the branching order within the rodents are not entirely established, but a phylogeny similar to this is supported by most molecular data. IMAGES, LEFT TO RIGHT: capybara (Hydrochaeris hydrochaeris); Cape mole rat (Georychus capensis); Cape porcupine (Hystrix africaeaustralis); red squirrel (Sciurus vulgaris); common dormouse (Muscardinus aveltanarius); springhare (Pedetes capensis); European beaver (Castor fiber); bank vole (Clethrionomys glareolus); northern birch mouse (Sicista betulina); Arctic hare (Lepus orcticus); American pika (Ochotona princeps).

not with their front paws like moles, but purely with their incisor teeth.^* Different species of rodents have penetrated the deserts of the world (gundis, gerbils), the high mountains (marmots, chinchillas), the forest canopy (squirrels, including flying squirrels), rivers (water voles, beavers, capybaras), rainforest floor (agoutis), savannah (maras, springhares), and Arctic tundra (lemmings).

Most rodents are mouse-sized, but they range up through marmots, beavers, agoutis and maras to the sheep-sized capybaras of the South American waterways. Capybaras are prized for meat, not just because of their large size but because, bizarrely, the Roman Catholic Church traditionally deemed them honorary fish for Fridays, presumably because they live in water. Large as they are, modern capybaras are dwarfed by various giant South American rodents that went extinct only quite recently. The giant capybara, Protohydrochoerus, was the size of a donkey. Telicomys was an even larger rodent the size of a small rhinoceros which, like the giant capybara, went extinct at the time of the Great American Interchange, when the Isthmus of Panama ended South America's island status. These two groups of giant rodents were not particularly closely related to each other, and seem to have evolved their gigantism independently.

A world without rodents would be a very different world. It is less likely to come to pass than a world dominated by rodents and free of people. If nuclear war destroys humanity and most of the rest of life, a good bet for survival in the short term, and for evolutionary ancestry in the long term, is rats. I have a post-Armageddon vision. We and all other large animals are gone. Rodents emerge as the ultimate post-human scavengers. They gnaw their way through New York, London and Tokyo, digesting spilled larders, ghost supermarkets and human corpses and turning them into new generations of rats and mice, whose racing populations explode out of the cities and into the countryside. When all the relics of human profligacy are eaten, populations crash again, and the rodents turn on each other, and on the cockroaches scavenging with them. In a period of intense competition, short generations perhaps with radioactively enhanced mutation-rates boost rapid evolution. With human ships and planes gone, islands become islands again, with local populations isolated save for occasional lucky raftings: ideal conditions for evolutionary divergence. Within 5 million years, a whole range of new species replace the ones we know. Herds of giant grazing rats are stalked by sabre-toothed predatory rats.^* Given enough time, will a species of intelligent, cultivated rats emerge? Will rodent historians and scientists eventually organise careful archaeological digs (gnaws?) through the strata of our long-compacted cities, and reconstruct the peculiar and temporarily tragic circumstances that gave ratkind its big break?

The Mouse's Tale

Of all the thousands of rodents, the house mouse, Mus musculus, has a special tale to tell because it has become the second most intensively studied mammal species after our own. Much more than the proverbial guinea pig, the mouse is a main staple of medical, physiological and genetic laboratories the world over. In particular, the mouse is one of very few mammals apart from ourselves whose genome has so far been completely sequenced.

Two things about these recently sequenced genomes have sparked unwarranted surprise. The first is that mammal genomes seem rather small: of the order of 30,000 genes or maybe even less. And the second is that they are so similar to each other. Human dignity seemed to demand that our genome should be much larger than that of a tiny mouse. And shouldn't it be absolutely larger than 30,000 genes anyway?

This last expectation has led people, including some who should know better, to deduce that the ‘environment’ must be more important than we thought, because there aren't enough genes to specify a body. That really is a breathtakingly naive piece of logic. By what standard do we decide how many genes you need to specify a body? This kind of thinking is based on a subconscious assumption which is wrong: the assumption that the genome is a kind of blueprint, with each gene specifying its own little piece of body. As the Fruit Fly's Tale will tell us, it is not a blueprint, but something more like a recipe, a computer program, or a manual of instructions for assembly.

If you think of the genome as a blueprint, you might expect a big, complicated animal like yourself to have more genes than a little mouse, with fewer cells and a less sophisticated brain. But, as I said, that isn't the way genes work. Even the recipe or instruction-book model can be misleading unless it is properly understood. My colleague Matt Ridley develops a different analogy which I find beautifully clear, in his book Nature via Nurture. Most of the genome that we sequence is not the book of instructions, or master computer program, for building a human or a mouse, although parts of it are. If it were, we might indeed expect our program to be larger than the mouse's. But most of the genome is more like the dictionary of words available for writing the book of instructions — or, we shall soon see, the set of subroutines that are called by the master program. As Ridley says, the list of words in David Copperfield is almost the same as the list of words in The Catcher in the Rye. Both draw upon the vocabulary of an educated native speaker of English. What is completely different about the two books is the order in which those words are strung together.

When a person is made, or when a mouse is made, both embryologies draw upon the same dictionary of genes: the normal vocabulary of mammal embryologies. The difference between a person and a mouse comes out of the different orders with which the genes, drawn from that shared mammalian vocabulary, are deployed, the different places in the body where this happens, and its timing. All this is under the control of particular genes whose business it is to turn other genes on, in complicated and exquisitely timed cascades. But such controlling genes constitute only a minority of the genes in the genome.  {155} 

Don't misunderstand ‘order’ as meaning the order in which the genes are strung out along the chromosomes. With notable exceptions, which we shall meet in the Fruit Fly's Tale, the order of genes along a chromosome is as arbitrary as the order in which words are listed in a vocabulary — usually alphabetical but, especially in phrase books for foreign travel, sometimes an order of convenience: words useful in airports; words useful when visiting the doctor; words useful for shopping, and so on. The order in which genes are stored on chromosomes is unimportant. What matters is that the cellular machinery finds the right gene when it needs it, and it does this using methods that are becoming increasingly understood. In the Fruit Fly's Tale, we'll return to those few cases, very interesting ones, where the order of genes arranged on the chromosome is non-arbitrary in something like the foreign phrase-book sense. For now, the important point is that what distinguishes a mouse from a man is mostly not the genes themselves, nor the order in which they are stored in the chromosomal ‘phrase-book’, but the order in which they are turned on: the equivalent of Dickens or Salinger choosing words from the vocabulary of English and arranging them in sentences.

In one respect the analogy of words is misleading. Words are shorter than genes, and some writers have likened each gene to a sentence. But sentences aren't a good analogy, for a different reason. Different books are not put together by permuting a fixed repertoire of sentences. Most sentences are unique. Genes, like words but unlike sentences, are used over and over again in different contexts. A better analogy for a gene than either a word or a sentence is a toolbox subroutine in a computer.

The computer I happen to be familiar with is the Macintosh, and it is some years since I did any programming so I am certainly out of date with the details. Never mind — the principle remains, and it is true of other computers too. The Mac has a toolbox of routines stored in ROM (Read Only Memory) or in System files permanently loaded at start-up time. There are thousands of these toolbox routines, each one doing a particular operation, which is likely to be needed, over and over again, in slightly different ways, in different programs. For example the toolbox routine called ObscureCursor hides the cursor from the screen until the next time the mouse is moved. Unseen to you, the Obscure-Cursor ‘gene’ is called every time you start typing and the mouse cursor vanishes. Toolbox routines lie behind the familiar features shared by all programs on the Mac (and their imitated equivalents on Windows machines): pulldown menus, scrollbars, shrinkable windows that you can drag around the screen with the mouse, and many others.

The reason all Mac programs have the same ‘look and feel’ (that very similarity famously became the subject of litigation) is precisely that all Mac programs, whether written by Apple, or by Microsoft, or by anybody else, call the same toolbox routines. If you are a programmer who wishes to move a whole region of the screen in some direction, say following a mouse drag, you would be wasting your time if you didn't invoke the ScrollRect toolbox routine. Or if you want to place a check mark by a pulldown menu item, you would be mad to write your own code to do it. Just write a call of Checkltem into your program, and the  {156}  job is done for you. If you look at the text of a Mac program, whoever wrote it, in whatever programming language and for whatever purpose, the main thing you'll notice is that it consists largely of invocations of familiar, built-in toolbox routines. The same repertoire of routines is available to all programmers. Different programs string calls of these routines together in different combinations and sequences.

The genome, sitting in the nucleus of every cell, is the toolbox of DNA routines available for performing standard biochemical functions. The nucleus of a cell is like the ROM of a Mac. Different cells, for example liver cells, bone cells and muscle cells, string ‘calls’ of these routines together in different orders and combinations when performing particular cell functions including growing, dividing, or secreting hormones. Mouse bone cells are more similar to human bone cells than they are to mouse liver cells — they perform very similar operations and need to call the same repertoire of toolbox routines in order to do so. This is the kind of reason why all mammal genomes are approximately the same size as each other — they all need the same toolbox.

Nevertheless, mouse bone cells do behave differently from human bone cells; and this too will be reflected in different calls to the toolbox in the nucleus. The toolbox itself is not identical in mouse and man, but it might as well be identical without in principle jeopardising the main differences between the two species. For the purpose of building mice differently from humans, what matters is differences in the calling of toolbox routines, more than differences in the toolbox routines themselves.

The Beaver's Tale

A ‘phenotype’ is that which is influenced by genes. That pretty much means everything about a body. But there is a subtlety of emphasis which flows from the word's etymology. Phaino is Greek for ‘show’, ‘bring to light’, ‘make appear’, ‘exhibit’, ‘uncover’, ‘disclose’, ‘manifest’. The phenotype is the external and visible manifestation of the hidden genotype. The Oxford English Dictionary defines it as ‘the sum total of the observable features of an individual, regarded as the consequence of the interaction of its genotype with its environment’ but it precedes this definition by a subtler one: ‘A type of organism distinguishable from others by observable features.’

Darwin saw natural selection as the survival and reproduction of certain types of organism at the expense of rival types of organism. ‘Types’ here doesn't mean groups or races or species. In the subtitle of The Origin of Species, the much misunderstood phrase ‘preservation of favoured races’ most emphatically does not mean races in the normal sense. Darwin was writing before genes were named or properly understood, but in modern terms what he meant by ‘favoured races’ was ‘possessors of favoured genes’.

Selection drives evolution only to the extent that the alternative types owe  {157}  their differences to genes. If the differences are not inherited, differential survival has no impact on future generations. For a Darwinian, phenotypes are the manifestations by which genes are judged by selection. When we say that a beaver's tail is flattened to serve as a paddle, we mean that genes whose phenotypic expression included a flattening of the tail survived by virtue of that phenotype. Individual beavers with the fiat-tailed phenotype survived as a consequence of being better swimmers; the responsible genes survived inside them, and were passed on to new generations of flat-tailed beavers.

At the same time, genes that expressed themselves in huge, sharp incisor teeth capable of gnawing through wood also survived. Individual beavers are built by permutations of genes in the beaver gene pool. Genes have survived through generations of ancestral beavers because they have proved good at collaborating with other genes in the beaver gene pool, to produce phenotypes that flourish in the beaver way of life.

At the same time again, alternative co-operatives of genes are surviving in other gene pools, making bodies that survive by prosecuting other life trades: the tiger co-operative, the camel co-operative, the cockroach co-operative, the carrot co-operative. My first book, The Selfish Gene, could equally have been called The Co-operative Gene without a word of the book itself needing to be changed. Indeed, this might have saved some misunderstanding (some of a book's most vocal critics are content to read the book by title only). Selfishness and cooperation are two sides of a Darwinian coin. Each gene promotes its own selfish welfare, by co-operating with the other genes in the sexually stirred gene pool which is that gene's environment, to build shared bodies.

But beaver genes have special phenotypes quite unlike those of tigers, camels or carrots. Beavers have lake phenotypes, caused by dam phenotypes. A lake is an extended phenotype. The extended phenotype is a special kind of phenotype, and it is the subject of the rest of this tale, which is a brief summary of my book of that title. It is interesting not only in its own right but because it helps us to understand how conventional phenotypes develop. It will turn out that there is no great difference of principle between an extended phenotype like a beaver lake, and a conventional phenotype like a flattened beaver tail.

How can it possibly be right to use the same word, phenotype, on the one hand for a tail of flesh, bone and blood, and on the other hand for a body of still water, stemmed in a valley by a dam? The answer is that both are manifestations of beaver genes; both have evolved to become better and better at preserving those genes; both are linked to the genes they express by a similar chain of embryological causal links. Let me explain.

The embryological processes by which beaver genes shape beaver tails are not known in detail, but we know the kind of thing that goes on. Genes in every cell of a beaver behave as if they ‘know’ what kind of cell they are in. Skin cells have the same genes as bone cells, but different genes are switched on in the two tissues. We saw this in the Mouse's Tale. Genes, in each of the different kinds of cells in a beaver's tail, behave as if they ‘know’ where they are. They cause their respective cells to interact with each other in such a way that the whole tail assumes its characteristically hairless flattened form. There are  {158}  formidable difficulties in working out how they ‘know’ which part of the tail they are in, but we understand in principle how these difficulties are overcome; and the solutions, like the difficulties themselves, will be of the same general kind when we turn to the development of tiger feet, camel humps and carrot leaves.

They are also of the same general kind in the development of the neuronal and neurochemical mechanisms that drive behaviour. Copulatory behaviour in beavers is instinctive. A male beaver's brain orchestrates, via hormonal secretions into the blood, and via nerves controlling muscles tugging on artfully hinged bones, a symphony of movements. The result is precise co-ordination with a female, who herself is moving harmoniously in her own symphony of movements, equally carefully orchestrated to facilitate the union. You may be sure that such exquisite neuromuscular music has been honed and perfected by generations of natural selection. And that means genes. In beaver gene pools, genes survived whose phenotypic effects on the brains, the nerves, the muscles, the glands, the bones, and the sense organs of generations of ancestral beavers improved the chances of those very genes passing through those very generations to arrive in the present.

Genes ‘for’ behaviour survive in the same kind of way as genes ‘for’ bones, and skin. Do you protest that there aren't ‘really’ any genes for behaviour; only genes for the nerves and muscles that make the behaviour? You are still wrecked among heathen dreams. Anatomical structures have no special status over behavioural ones, where ‘direct’ effects of genes are concerned. Genes are ‘really’ or ‘directly’ responsible only for proteins or other immediate biochemical effects. All other effects, whether on anatomical or behavioural phenotypes, are indirect. But the distinction between direct and indirect is vacuous. What matters in the Darwinian sense is that differences between genes are rendered as differences in phenotypes. It is only differences that natural selection cares about. And, in very much the same way, it is differences that geneticists care about.

Remember the ‘subtler’ definition of phenotype in the Oxford English Dictionary: ‘A type of organism distinguishable from others by observable features’. The key word is distinguishable. A gene ‘for’ brown eyes is not a gene that directly codes the synthesis of a brown pigment. Well, it might happen to be, but that is not the point. The point about a gene ‘for’ brown eyes is that its possession makes a difference to eye colour when compared with some alternative version of the gene — an ‘allele’. The chains of causation that culminate in the difference between one phenotype and another, say between brown and blue eyes, are usually long and tortuous. The gene makes a protein which is different from the protein made by the alternative gene. The protein has an enzymatic effect on cellular chemistry, which affects X which affects Y which affects Z which affects... a long chain of intermediate causes which affects... the phenotype of interest. The allele makes the difference when its phenotype is compared with the corresponding phenotype, at the end of the correspondingly long chain of causation that proceeds from the alternative allele. Gene differences cause phenotypic differences. Gene changes cause phenotypic changes. In Darwinian  {159}  evolution alleles are selected, vis-a-vis alternative alleles, by virtue of the differences in their effects on phenotypes.

The beaver's point is that this comparison between phenotypes can happen anywhere along the chain of causation. All intermediate links along the chain are true phenotypes, and any one of them could constitute the phenotypic effect by which a gene is selected: it only has to be ‘visible’ to natural selection, nobody cares whether it is visible to us. There is no such thing as the ‘ultimate’ link in the chain: no final, definitive phenotype. Any consequence of a change in alleles, anywhere in the world, however indirect and however long the chain of causation, is fair game for natural selection, so long as it impinges on the survival of the responsible allele, relative to its rivals.

Now, let's look at the embryological chain of causation leading to dam-building in beavers. Dam-building behaviour is a complicated stereotypy, built into the brain like a fine-tuned clockwork mechanism. Or, as if to follow the history of clocks into the electronic age, dam-building is hard-wired in the brain. I have seen a remarkable film of captive beavers imprisoned in a bare, unfurnished cage, with no water and no wood. The beavers enacted, ‘in a vacuum’, all the stereotyped movements normally seen in natural building behaviour when there is real wood and real water. They seem to be placing virtual wood into a virtual dam wall, pathetically trying to build a ghost wall with ghost sticks, all on the hard, dry, flat floor of their prison. One feels sorry for them: it is as if they are desperate to exercise their frustrated dam-building clockwork.

Only beavers have this kind of brain clockwork. Other species have clockwork for copulation, scratching and fighting, and so do beavers. But only beavers have brain clockwork for dam-building, and it must have evolved by slow degrees in ancestral beavers. It evolved because the lakes produced by dams are useful. It is not totally clear what they are useful for, but they must have been useful for the beavers who built them, not just any old beavers. The best guess seems to be that a lake provides a beaver with a safe place to build its lodge, out of reach for most predators, and a safe conduit for transporting food. Whatever the advantage it must be a substantial one, or beavers would not devote so much time and effort to building dams. Once again, note that natural selection is a predictive theory. The Darwinian can make the confident prediction that, if dams were a useless waste of time, rival beavers who refrained from building them would survive better and pass on genetic tendencies not to build. The fact that beavers are so anxious to build dams is very strong evidence that it benefited their ancestors to do so.

Like any other useful adaptation, the dam-building clockwork in the brain must have evolved by Darwinian selection of genes. There must have been genetic variations in the wiring of the brain which affected dam-building. Those genetic variants that resulted in improved dams were more likely to survive in beaver gene pools. It is the same story as for all Darwinian adaptations. But which is the phenotype? At which link in the chain of causal links shall we say the genetic difference exerts its effect? The answer, to repeat it, is all links where a difference is seen. In the wiring diagram of the brain? Yes, almost certainly. In  {160}  the cellular chemistry that, in embryonic development, leads to that wiring? Of course. But also behaviour — the symphony of muscular contractions that is behaviour — this too is a perfectly respectable phenotype. Differences in building behaviour are without doubt manifestations of differences in genes. And, by the same token, the consequences of that behaviour are also entirely allowable as phenotypes of genes. What consequences? Dams, of course. And lakes, for these are consequences of dams. Differences between lakes are influenced by differences between dams, just as differences between dams are influenced by differences between behaviour patterns, which in turn are consequences of differences between genes. We may say that the characteristics of a dam, or of a lake, are true phenotypic effects of genes, using exactly the logic we use to say that the characteristics of a tail are phenotypic effects of genes.

Conventionally, biologists see the phenotypic effects of a gene as confined within the skin of the individual bearing that gene. The Beaver's Tale shows that this is unnecessary. The phenotype of a gene, in the true sense of the word, may extend outside the skin of the individual. Birds’ nests are extended phenotypes. Their shape and size, their complicated funnels and tubes where these exist, all are Darwinian adaptations, and so must have evolved by the differential survival of alternative genes. Genes for building behaviour? Yes. Genes for wiring up the brain so it is good at building nests of the right shape and size? Yes. Genes for nests of the right shape and size? Yes, by the same token, yes. Nests are made of grass or sticks or mud, not bird cells. But the point is irrelevant to the question of whether differences between nests are influenced by differences between genes. If they are, nests are proper phenotypes of genes. And nest differences surely must be influenced by gene differences, for how else could they have been improved by natural selection?

Artefacts like nests and dams (and lakes) are easily understood examples of extended phenotypes. There are others where the logic is a little more... well, extended. For example, parasite genes can be said to have phenotypic expression in the bodies of their hosts. This can be true even where, as in the case of cuckoos, they don't live inside their hosts. And many examples of animal communication — as when a male canary sings to a female and her ovaries grow — can be rewritten in the language of the extended phenotype. But that would take us too far from the beaver, whose tale will conclude with one final observation. Under favourable conditions the lake of a beaver can span several miles, which may make it the largest phenotype of any gene in the world.

RENDEZVOUS 11 LAURASIATHERES

Eighty-five million years ago, in the hot-house world of the Upper Cretaceous, we greet Concestor 11, approximately our 25-million-greats-grandparent. Here we are joined by a much more diverse band of pilgrims than the rodents and rabbits who swelled our party at Rendezvous 10. Zealous taxonomists recognise their shared ancestry by giving them a name, Laurasiatheria, but it is seldom used because, in truth, this is a miscellaneous bunch. The rodents are all built to the same toothy design and have proliferated and diversified, presumably because it works so well. ‘Rodents’ therefore really means something strong; it unites animals that have much in common. ‘Laurasiatheria’ is as awkward as it sounds. It unites highly disparate mammals which have only one thing in common: their pilgrims all joined up with each other ‘before’ they join us. They all hail, originally, from the old northern continent of Laurasia.

And what a diverse crew these laurasian pilgrims are, some of them flying, some of them swimming, many of them galloping, half of them nervously looking over their shoulder for fear of being eaten by the other half. They belong to seven different orders, the Pholidota (pangolins), Carnivora (dogs, cats, hyenas, bears, weasels, seals, etc.), the Perissodactyla (horses, tapirs and rhinos), Cetartiodactyla (antelopes, deer, cattle, camels, pigs, hippos and... well, we'll come to the surprise member of this group later), Microchiroptera and Megachiroptera (respectively small and big bats) and Insectivora (moles, hedgehogs and shrews, but not elephant shrews or tenrecs: we have to wait for Rendezvous 13 to meet them).

Carnivora is an irritating name because, after all, it simply means meat-eater, and meat-eating has been invented literally hundreds of times independently in the animal kingdom. Not all carnivores are Carnivora (spiders are carnivores and so was the hoofed Andrewsarchus, the largest meat-eater since the end of the dinosaurs) and not all Carnivora are carnivores (think of the gentle giant panda, eating almost nothing but bamboo). Within the mammals the order Carnivora does appear to be a genuinely monophyletic clade: that is, a group of animals, all descended from a single concestor who would have been classified as one of them. Cats (including lions, cheetahs and sabretooths), dogs (including wolves, jackals and Cape hunting dogs), weasels and their kind, mongooses and their kind, bears (including pandas), hyenas, wolverines, seals, sea lions and walruses, all are members of the laurasiatherian order Carnivora, and all are descended from a concestor which would have been placed in the same order.

Rotate 90 degrees

LAURASIATHERES JOIN In the early 2000s, genetic studies led to a revolution in mammalian taxonomy. According to this new view, there are four major groups of placental mammal. One is our current band (mostly consisting of rodents and primates). Consistently found to be its closest relative is another major group, the 2,000 or so species of laurasiathere. The laurasiathere phylogeny drawn here is considered reasonably certain by proponents of this new classification.

Carnivores and their prey need to outrun each other, and it is not surprising that the demands of fleetness have pushed them in similar evolutionary directions. You need long legs for running, and the great laurasiatherian herbivores and carnivores have, independently and in different ways, added extra length to their legs by commandeering bones which, in us, are inconspicuously buried within the hands (metacarpals) or feet (metatarsals). The ‘cannon-bone’ of a horse is the enlarged third metacarpal (or metatarsal) fused together with two tiny ‘splint’ bones that are vestiges of the second and fourth metacarpal (metatarsal). In antelopes and other even-toed ungulates, the cannon-bone is a fusion of the third and fourth metacarpal (metatarsal). Carnivores, too, have elongated their metacarpals and metatarsals, but these five bones have stayed separate instead of fusing together or disappearing altogether, as in horses, cattle and the rest of the so-called ungulates.

Unguis is Latin for nail, and ungulates are animals that walk on their nails — hooves. But the ungulate way of walking has been invented several times and ungulate is a descriptive term rather than a respectable taxonomic name. Horses, rhinos and tapirs are odd-toed ungulates. Horses walk on a single toe, the middle one. Rhinos and tapirs walk on the middle three, as did early horses and some atavistically mutant horses today. Even-toed or cloven-hoofed ungulates walk on two toes, the third and fourth. The convergent resemblances between the two-toed cattle family and the one-toed horse family are modest compared to the convergent resemblances of both, separately, to certain extinct South American herbivores. A group called the litopterns independently, and earlier, ‘discovered’ the horse habit of walking on a single middle toe. Their leg skeletons are almost identical to those of horses. Other South American herbivores, among the so-called notoungulates, independently discovered the cattle/antelope habit of walking on toes three and four. Such stunning resemblances really did fool a senior Argentinian zoologist in the nineteenth century, who thought that South America was the evolutionary nursery of many of our great groups of mammals. In particular, he believed that litopterns were early relatives of the true horse (perhaps with a little national pride that his country might have been the cradle of that noble animal).

The laurasiathere pilgrims now joining us include small animals as well as the large ungulates and carnivores. Bats are remarkable for all sorts of reasons. They are the only surviving vertebrates to put up any sort of competition to birds in flight, and very impressive aerobats they are. With nearly a thousand species, they far outnumber all other orders of mammals except rodents. And bats have perfected sonar (the sound equivalent of radar) to a higher degree than any other group of animals, including human submarine designers.^*

The other main group of small laurasiatheres are the so-called insectivores. The order Insectivora includes shrews, moles, hedgehogs and other small, snouty creatures which eat insects and small terrestrial invertebrates like worms, slugs and centipedes. As with Carnivora, I shall use a capital letter to denote the taxonomic group, Insectivora, as opposed to insectivore with a small i, which means just anything that eats insects. So, a pangolin (or scaly anteater) is an insectivore but not an Insectivore. A mole is an Insectivore, which actually  {164}  eats insects. As I have already remarked, it is a pity the early taxonomists used names like Insectivora and Carnivora, which are only loosely correlated to the descriptions of preferred diet with which they are so readily confused.

Related to carnivores like dogs, cats and bears are the seals, sea lions and walruses. We shall soon hear the Seal's Tale, which is about mating systems. I find seals interesting for another reason, too: they have moved into the water, and have modified themselves in that direction to about half the extent that dugongs have, or whales have. And that reminds me — there is one other major group of laurasiatheres that we haven't dealt with. On to the Hippo's Tale, for a real surprise.

The Hippo's Tale

When I was a schoolboy studying Greek, I learned that hippos meant ‘horse’ and potamos ‘river’. Hippopotamuses were river horses. Later, when I gave up Greek and read Zoology, I was not too disconcerted to learn that hippopotamuses weren't close to horses after all. Instead, they were classified firmly with pigs, in the middle of the even-toed ungulates or artiodactyls. I have now learned something so shocking that I am still reluctant to believe it, but it looks as though I am going to have to. Hippos’ closest living relatives are whales. The even-toed ungulates include whales! Whales, needless to say, don't have hooves at all, whether odd- or even-toed. Indeed, they don't have toes, so it might be less confusing if we adopt the scientific name, artiodactyls (which is actually just the Greek for even-toed, so the change doesn't help much). For completeness, I should add that the equivalent name for the horse order is Perissodactyla (Greek  {165}  for uneven-toed). Whales, it would now seem from strong molecular evidence, are artiodactyls. But since they previously had been placed in the order Cetacea, and since Artiodactyla was also a well-established name, a new composite has been coined: Cetartiodactyla. Whales are wonders of the world. They include the largest organisms that have ever moved. They swim with up-and-down movements of the spine derived from the mammalian gallop, as opposed to the side to side wave motion of the spine of a swimming fish or a running lizard.^* The front limbs are used for steering and stabilising. There are no externally visible hind limbs at all, but some whales have small vestigial pelvic and leg bones buried deep in their bodies. It would not be too hard to believe that whales are closer cousins to even-toed ungulates than they are to any other mammals. A bit strange, perhaps, but not shocking to accept that some remote ancestor branched to the left and went to sea to give rise to the whales, while it branched to the right to give all the even-toed ungulates. What is shocking is that, according to the molecular evidence, whales are deeply embedded within the even-toed ungulates. Hippos are closer cousins to whales than hippos are to anything else including other even-toed ungulates such as pigs.^* On their backward journey, the hippo pilgrims and the whale pilgrims unite with each other ‘before’ the two of them join the ruminants, and then the other even-toed ungulates such as pigs. Whales are the surprise inclusion that I coyly referred to when I introduced the cetartiodactyls at Rendezvous it. ft is known as the Whippo Hypothesis.

All this supposes that we believe the testimony of the molecules.^* What do the fossils say? To my initial surprise, the new theory fits quite nicely. Most of the great orders of mammals (though not the subdivisions within them) — go a long way back into the age of dinosaurs, as we saw in connection with the Great Cretaceous Catastrophe. Rendezvous 10 (with the rodents and rabbits) and Rendezvous 11 (the one we have just reached) both took place during the Cretaceous Period at the height of the dinosaur regime. But mammals in those days were all rather small, shrew-like creatures, whether their respective descendants were destined to become mice or hippos. The real growth of mammal diversity started suddenly after the dinosaurs went extinct 65.5 million years ago. It was then that the mammals were able to blossom into all economic trades vacated by the dinosaurs. Large body size was just one thing that became possible for mammals only when the dinosaurs were gone. The process of divergent evolution was swift, and a huge range of mammals, of all sizes and shapes, roamed the land within 5 million years of ‘liberation’. Five to ten million years later, in the late Palaeocene to early Eocene Epoch, there are abundant fossils of even-toed ungulates.  {166} 

Another 5 million years later, in the early to middle Eocene, we find a group called the archaeocetes (see picture opposite). The name means ‘old whales’, and most authorities accept that among these animals are to be found the ancestors of modern whales. An early one of these, Pakicetus from Pakistan, seems to have spent at least some of its time on land. Later ones include the unfortunately named Basilosaurus (unfortunate, not because of Basil but because saurus means lizard: when first discovered, Basilosaurus was thought to be a marine reptile, and the rules of naming rigidly enforce priority, even though we now know better).^* Basilosaurus had an immensely long body, and would have been a good candidate for the giant sea serpent of legend, if only it were not long extinct. Around the time that whales were represented by the likes of Basilosaurus, the contemporary hippo ancestors may have been members of a group called the anthracotheres, some reconstructions of which make them look quite like hippos.

Returning to the whales, what of the antecedents of the archaeocetes, before they re-invaded the water? If the molecules are right that whales’ closest affinities are with hippos, we might be tempted to seek their ancestors among fossils which show some evidence of herbivory. On the other hand, no modern whale or dolphin is herbivorous. The completely unrelated dugongs and manatees, by the way, show that it is perfectly possible for a purely marine mammal to have a purely herbivorous diet. Whales eat either planktonic Crustacea (baleen whales); fish or squid (dolphins and most toothed whales); or large prey such as seals (killer whales). This has led people to look for whale ancestors among carnivorous land mammals, beginning with Darwin's own speculation, sometimes ridiculed though I have never understood why:

In North America the black bear was seen by Hearne swimming for hours with widely open mouth, thus catching, like a whale, insects in the water. Even in so extreme a case as this, if the supply of insects were constant, and if better adapted competitors did not already exist in the country, I can see no difficulty in a race of bears being rendered, by natural selection, more and more aquatic in their structure and habits, with larger and larger mouths, till a creature was produced as monstrous as a whale (Origin of Species, 1859, p 184).

As an aside, this suggestion of Darwin illustrates an important general point about evolution. The bear seen by Hearne was evidently an enterprising individual, feeding in an unusual way for its species. I suspect that major new departures in evolution often start in just such a way, with a piece of lateral thinking by an individual who discovers a new and useful trick, and learns to perfect it. If the habit is then imitated by others, including perhaps the individual's own children, there will be a new selection pressure set up. Natural selection will favour genetic predispositions to be good at learning the new trick, and much will follow. I suspect that something like this is how ‘instinctive’ feeding habits such as tree-hammering in woodpeckers, and mollusc-smashing in thrushes and sea otters, got their start.^*

For a long time, people looking over the available fossils for a plausible antecedent to the archaeocetes have favoured the mesonychids, a large group of land mammals that flourished in the Palaeocene Epoch, just after the extinction  {167}  of the dinosaurs. The mesonychids seem to have been largely carnivorous, or omnivorous like Darwin's bear, and they fit with what we all — before the coming of the hippo theory — thought a whale ancestor ought to be. An additionally nice thing about the mesonychids is that they had hooves. They were hoofed carnivores, perhaps a bit like wolves but running on hooves!^* Could they, then, have given rise to the even-toed ungulates, as well as to the whales? Unfortunately, the idea doesn't fit with the hippo theory specifically. Even though the mesonychids seem to be cousins of today's even-toed ungulates (and there are reasons for believing this over and above their hooves) they are no closer to hippos than they are to all the rest of the cloven-hoofed animals. We keep coming back to the molecular shocker: whales are not just cousins of all the artiodactyls, they are buried within the artiodactyls, closer to hippos than hippos are to cows and pigs.

Gathering all this together, we can sketch a forward chronology as follows. Molecular evidence puts the split between camels (plus llamas) and the rest of the artiodactyls at 6 5 million years, more or less exactly when the last dinosaurs died. Don't imagine, by the way, that the shared ancestor looked anything like a camel. In those days, all mammals looked more or less like shrews. But 65 million years ago, the ‘shrews’ that were going to give rise to camels split from the ‘shrews’ that were going to give rise to all the rest of the artiodactyls. The split between pigs and the rest (mostly ruminants) took place 60 million years ago. The split between ruminants and hippos took place about 55 million years ago. Then the whale lineage split off from the hippo lineage not long afterwards, say about 54 million years ago, which gives time for primitive whales such as the semi-aquatic Pakicetus to have evolved by 50 million years ago. Toothed whales and baleen whales parted company much later, around 34 million years ago, around the time when the earliest baleen whale fossils are found.

Perhaps I was exaggerating a little when I implied that a traditional zoologist like me should be positively upset at the discovery of the hippo-whale connection. But let me try to explain why I was genuinely disconcerted when I first read about it a few years ago. It wasn't just that it was different from what I had learned as a student. That wouldn't have worried me at all, in fact I would have found it positively exhilarating. What worried me, and still does to some extent, was that it seemed to undermine all generalisations that one might wish to make about groupings of animals. The life of a molecular taxonomist is too short to allow a pairwise comparison of every species with every other species. Instead what one does is take two or three whale species, say, and assume that they are representative of whales as a group. It is tantamount to the assumption that the whales are a clade, sharing a common ancestor which is not shared by the other animals with which one is making the comparison. It is assumed not to matter, in other words, which whale you take to stand for all. Similarly, lacking the time to test every species of rodent, say, or artiodactyl, we might take blood^* from a rat, and from a cow. It doesn't matter which artiodactyl you take to compare with the representative whale because, yet again, we assume that the artiodactyls are a good clade, so it doesn't make any difference whether we take a cow, a pig, a camel or a hippo.  {168} 

But now we are told that it does matter. Camel blood and hippo blood really will give a different comparison with whale blood because hippos are closer cousins to whales than they are to camels. See where this lands us. If we can't trust the artiodactyls to hang together as a group, represented by any one of their number, how can we be sure that any group will hang together? Can we even assume that hippos hang together, such that it doesn't matter whether we choose a pygmy hippo or a common hippo for comparison with whales? What if whales are closer to pygmy hippos than to common hippos? Actually we probably can rule that out, because fossil evidence suggests that the two hippo genera split apart about as recently as our split from chimpanzees, and that really does leave too little time to evolve all the different kinds of whales and dolphins.

It is more problematical whether all the whales hang together. On the face of it, the toothed whales and the baleen whales might well represent two entirely separate returns to the sea from the land. Indeed, that very possibility has often been advocated. The molecular taxonomists who demonstrated the hippo connection very wisely did take DNA from both a toothed whale and a baleen whale. They found that the two whales are indeed much closer cousins to each other than they are to a hippo. But again, how do we know that ‘the toothed whales’ hang together as a group? And the same for ‘the baleen whales’? Maybe all the baleen whales are related to a hippo except the minke whale, which is related to a hamster. No, I don't believe that, and I really do think the baleen whales are a united clade, sharing a common ancestor which is not shared by anything that is not a baleen whale. But can you see how the hippo/whale discovery shakes the confidence?

We could regain our confidence if we could think of a good reason why whales might be special in this respect. If whales are glorified artiodactyls, they are artiodactyls that suddenly took off, evolutionarily speaking, leaving the rest of the artiodactyls behind. Their closest cousins, the hippos, remained relatively static, as normal, respectable artiodactyls. Something happened in the history of the whales that made them flip into evolutionary overdrive. They evolved so much faster than all the rest of the artiodactyls that their origin within that group was obscured, until molecular taxonomists came along and uncovered it. So, what is special about the history of the whales?

When you write it down like that, the solution leaps off the page. Leaving the land and becoming wholly aquatic was a bit like going into outer space. When we go into space we are weightless (not, by the way, because we are a long way from the Earth's gravity, as many people think, but because we are in free fall like a parachutist before he pulls the ripcord). A whale floats. Unlike a seal or a turtle, which still comes on land to breed, a whale never stops floating. It never has to contend with gravity. A hippo spends time in the water, but it still needs stout, treetrunk-like legs and strong leg muscles for the land. A whale doesn't need legs at all, and indeed it doesn't have any. Think of a whale as what a hippo would like to be if only it could be freed from the tyranny of gravity. And of course there are so many other odd things about living the whole time in the sea that it comes to seem far less surprising that whale evolution should have  {169}  spurted as it did, leaving hippos behind, stranded on land and stranded in the middle of the artiodactyls. This suggests that I was unduly alarmist a few paragraphs back.

Much the same thing happened in the other direction, 300 million years earlier, when our fish ancestors emerged from the water onto the land. If whales are glorified hippos, we are glorified lungfish. The emergence of legless whales from within the middle of the artiodactyls, leaving the rest of the artiodactyls ‘behind’, should not seem more surprising than the emergence of four-legged land animals from one particular group offish, leaving those fish ‘behind’. That, at any rate, is how I rationalise the hippo-whale connection, and recover my lost zoological composure.

Epilogue to the Hippo's Tale

Zoological composure be blowed. My attention was drawn to the following while this book was in its final stages of preparation. In 1866, the great German zoologist Ernst Haeckel drew up a schematic evolutionary tree of mammals. I had often seen the full tree reproduced in histories of zoology, but I had never  {170}  before noticed the position of the whales and hippos in Haeckel's scheme. Whales are ‘Cetacea’, as today, and Haeckel presciently placed them close to the artiodactyls. But the real stunner is where he put the hippos. He called them by the unflattering name ‘Obesa’ and he classified them not in the artiodactyls but as a tiny twig on the branch leading to Cetacea.^* Haeckel classified hippos as the sister group to the whales: hippos, in his vision, were more closely related to whales than they were to pigs, and all three were more closely related to each other than to cows.

... there is no new thing under the sun. Is there anything whereof it may be said, See, this is new? It hath been already of old time, which was before us.

ECCLESIASTES 1, 9-10

The Seal's Tale

Most wild animal populations have approximately equal numbers of males and females. There's a good Darwinian reason for this, which was clearly seen by the great statistician and evolutionary geneticist R. A. Fisher. Imagine a population in which the numbers were unequal. Now, individuals of the rarer sex will on average have a reproductive advantage over individuals of the commoner sex. This is not because they are in demand and have an easier time finding a mate (although that might be an additional reason). Fisher's reason is a deeper one, with a subtle economic slant. Suppose there are twice as many males as females in the population. Now, since every child born has exactly one father and one mother, the average female must, all other things being equal, have twice as many children as the average male. And vice versa if the population sex ratio is reversed. It is simply a question of allocating the available posterity among the available parents. So, any general tendency for parents to favour sons rather than daughters, or daughters rather than sons, will immediately be counteracted by natural selection for the opposite tendency. The only evolutionarily stable sex ratio is 50/50.

But it isn't quite that simple. Fisher spotted an economic subtlety in the logic. What if it costs twice as much to rear a son, say, as to rear a daughter, presumably because males are twice as big? Well, now, the reasoning changes. The choice that faces a parent is no longer, ‘Shall I have a son or a daughter?’ It is now, ‘Shall I have a son or — for the same price — two daughters?’ The balanced sex ratio in the population is now twice as many females as males. Parents who favour sons on the grounds that males are rare, will see their advantage precisely undermined by the extra cost of making males. Fisher divined that the true sex ratio equalised by natural selection is not the ratio of numbers of males to numbers of females. It is the ratio of economic spending on rearing sons to economic spending on rearing daughters. And what does economic spending mean? Food? Time? Risk? Yes, in practice all these are likely to be important, and for Fisher the agent doing the spending was always  {171}  parents. But economists use a more general expression of cost, which they call opportunity cost. The true cost to a parent of making a child is measured in lost opportunities to make other children. This opportunity cost was named Parental Expenditure by Fisher. Under the name Parental Investment, Robert L. Trivers, a brilliant intellectual successor to Fisher, used the same idea to elucidate sexual selection. Trivers was also the first to understand clearly the fascinating phenomenon of parent-offspring conflict, in a theory that has been carried further in startling directions by the equally brilliant David Haig.

As ever, and at the risk of boring those of my readers not handicapped by a little learning in philosophy, I once again must stress that the purposeful language I have used is not to be treated literally. Parents do not sit down and discuss whether to have a son or a daughter. Natural selection favours, or disfavours, genetic tendencies to invest food or other resources in such a way as to lead eventually to equal or unequal parental expenditure on sons and daughters, over the whole of a breeding population. In practice this will often amount to equal numbers of males and females in the population.

But what about those cases where a minority of males holds the majority of females in harems? Does this violate Fisher's expectations? Or those cases where males parade in front of females in a ‘lek’, and the females look them over and choose their favourite? Most females have the same favourite, so the end result is the same as for a harem: polygyny — disproportionate access to a majority of females by a privileged minority of males. That minority of males ends up fathering most of the next generation, with the rest of the males hanging about as bachelors. Does polygyny violate Fisher's expectations? Surprisingly, no. Fisher still expects equal investment in sons and daughters, and he is right. Males may have a lower expectation of reproducing at all, but if they do reproduce they reproduce in spades. Females are unlikely to have no children but they are also unlikely to have very many. Even under conditions