About the Author
MATT R I D L E Y is
the author of Nature Via Nurture: Genes, Experience, and What Makes Us Human; the critically acclaimed national bestseller Genome: The Autobiography of a Species in 23
Chapters; The Origins of Virtue: Human Instincts and the Evolution of Cooperation; and the New York Times Notable Book The Red Queen: Sex and the Evolution of Human Nature. His books have been short-listed for six literary awards, including the Los Angeles Times Book Prize. Formerly a scientist, journalist, and a national newspaper columnist, he is a visiting professor at Cold Spring Harbor Laboratory in New York and the chairman of the International Centre for Life in Newcastle, England:
THE RED QUEEN
Sex and the Evolution of
Human Nature
MATT RIDLEY
Perennial
An Imprint of HarperCollinsPublishers For Matthew
This book was first published in Great Britain in 1993 by Penguin Books Ltd: 1t is here reprinted by arrangement with Penguin Putnam.
THE RED QUEEN: Copyright © 1993 by Matt Ridley: All rights reserved: Printed in the United States of America: No part of this book may be used or reproduced in any manner whatsoever without written permission except in the case of brief quotations embodied in critical articles and reviews.
For information address Penguin Putnam, 375 Hudson Street, New York, NY 10014:
HarperCollins books may be purchased for educational, business, or sales promotional use: For information please write: Special Markets Department, HarperCollins Publishers 1nc., to East 53rd Street, New York, NY
10022:
First Perennial edition published 2003.
Library of Congress Cataloging-in-Publication Data Ridley, Matt.
The red queen : sex and the evolution of human nature / Matt Ridley.—1st Perennial ed:
p: cm.
Originally published: London: Viking, 1 993 : Includes bibliographical references and index: ISBN 0 - 06 -0 55 6 57-9
1: Human evolution. z. Social evolution: 3: Sex 1: Title: GN365.9•R53 2.003
599 . 93 '8 -dc21
2003 04335 6
04 05 o6 07 o8 09 RRD 12. 11 to 9 8
CONTENTS
Acknowledgments ::: vii
Chapter 1 ::: HUMAN NATURE ::: I
Chapter 2 ::: THE•ENIGMA ::: 23
Chapter 3
::: THE POWER OF PARASITES ::: 53
Chapter 4 ::: GENETIC MUTINY AND GENDER ::: 89
Chapter 5
::: THE PEACOCK'S TALE ::: 129
Chapter 6 ::: POLYGAMY AND THE NATURE OF MEN ::: 171 Chapter 7 ::: MONOGAMY AND THE NATURE OF WOMEN ::: 209
Chapter 8 ::: SEXING THE MIND ::: 245
Chapter 9 ::: THE USES OF BEAUTY ::: 277
Chapter to ::: THE INTELLECTUAL CHESS GAME ::: 307
Epilogue ::: THE SELF-DOMESTICATED APE ::: 345
Notes ::: 351
Bibliography ::: 369
Index ::: 395
. ACKNOWLEDGMENTS
This book is crammed with original ideas—very few of them my own. Science writers become accustomed to the feeling that they are intellectual plagiarists, raiding the minds of those who are too busy to tell the world about their discoveries. There are scores of people who could have written each chapter of my book better than I. My consolation is that few could have written all the chapters.
My role has been to connect the patches of others ' research together into a quilt.
But I remain deeply indebted and grateful to all those whose minds I raided. I have interviewed more than sixty people in the course of researching this book and have never met with anything but courtesy, patience, and infectious curiosity about the world. Many became friends. I am especially grateful to those whom I interviewed repeatedly and at length until I had almost picked their minds clean: Laura Betzig, Napoleon Chagnon, Leda Cosmides, Helena Cronin, Bill Hamilton, Laurence Hurst, Bobbi Low, Andrew Pomiankowski, Don Symons, and John Tooby.
Among those who agreed to interviews in person or by telephone, I would like to thank Richard Alexander, Michael Bailey, Alexandra Basolo, Graham Bell, Paul Bloom, Monique Borgehoff Mulder, Don Brown, Jim Bull, Austin Burt, David Buss, Tim Clutton-Brock, Bruce Ellis, John Endler, Bart Gledhill, David Goldstein, Alan Grafen,
Tim
Guilford,
David
Haig,
Dean
Hamer,
Kristen Hawkes, Elizabeth Hill, Kim Hill, Sarah Hrdy, William Irons, William James, Charles Keckler, Mark Kirkpatrick, Jochen Kumm, Curtis Lively, John Maynard Smith, Matthew Meselson, Geoffrey
::: viii :::
ACKNOWLEDGMENTS
Miller, Anders Moller, Atholl McLachlan, Jeremy Nathans, Magnus Nordborg, Elinor Ostrom, Sarah Otto, Kenneth Oye, Margie Profet, Tom Ray, Michael Ryan, Dev Singh, Robert Smuts, Randy Thornhill, Robert Trivers, Leigh Van Valen, Fred Whitam, George Williams, Margo Wilson, Richard Wrangham, and Marlene Zuk.
My sincere thanks also to those who corresponded with me or sent me their papers and books: Christopher Badcock, Robert Foley, Stephen Frank, Valerie Grant, Toshikazu Hasegawa, Doug Jones, Egbert Leigh, Daniel Perusse, Felicia Pratto, and Edward Tenner.
Other minds I raided more subtly, even surreptitiously.
Among those who have given advice or helped to clear my thoughts in many conversations are Alun Anderson, Robin Baker, Horace Barlow, Jack Beckstrom, Rosa Beddington, Mark Bellis, Roger Bing-ham, Mark Boyce, John Browning, Stephen Budiansky, Edward Carr, Geoffrey Carr, Jeremy Cherfas, Alice Clarke, Nico Colchester, Charles Crawford, Francis Crick, Martin Daly, Kurt Darwin, Marian Dawkins, Richard Dawkins, Andrew Dobson, Emma Duncan, Peter Garson, Anthony Gottlieb, John Hartung, Peter Hudson, Anya Hurlbert, Mark Flinn, Archie Fraser, Steven Gaulin, Charles Godfray, Joel Heinen, Nigella Hillgarth, Michael Kinsley, Richard Ladle, Richard Machalek, Seth Masters, Patrick McKim, Graeme Mitchison, Oliver Morton, Randolph Nesse, Paul Neuburg, Paul Newton, Linda Partridge, Marion Petrie, Steve Pinker, Mike Polioudakis, Jeanne Regalski, Peter Richerson, Mark Ridley (being mistaken for whom has been a great benefit to me), Alan Rogers, Vincent Sarich, Terry Sejnowski, Miranda Seymour, Rachel Smolker, Beverly Strassmann, Jeremy Taylor, Nancy Thornhill, David Wilson, Edward Wilson, Adrian Wooldridge, and Bob Wright.
Several people helped even further by reading drafts of chapters and commenting on them: Their advice was time-consuming to them but immensely valuable to me: Laura Betzig, Mark Boyce, Helena Cronin, Richard Dawkins, Laurence Hurst, Geoffrey Miller, and Andrew Pomiankowski. I owe a special debt to Bill Hamilton, to whom I returned again and again for inspiration at the early stages of this project:
ACKNOWLEDGMENTS
::: IX :::
My agents, Felicity Bryan and Peter Ginsberg, were unfailingly encouraging and constructive at all stages: My editors at Penguin and Macmillan, Ravi Mirchandani, Judith Flanders, Bill Rosen, and especially Carrie Chase, were efficient, kind, and inspired.
My wife, Anya Hurlbert, read the entire book, and her advice and support throughout have been invaluable.
Lastly, thanks to the red squirrel that sometimes scratched at my window while I wrote: I still don ' t know which sex it was.
Chapter 1
HUMAN NATURE
The most curious part of the thing was, that the trees and the
other things round them never changed their places at all: howev-
er fast they went, they never seemed to pass anything: "I wonder
if all the things move along with us?" thought poor puzzled
Alice: And the Queen seemed to guess her thoughts, for she cried,
"Faster! Don't try to talk!"
—Lewis Carroll, Through the Looking-Glass When a surgeon cuts into a body, he knows what he will find inside. If he is seeking the patient 's stomach, for example, he does not expect to find it in a different place in every patient. All people have stomachs, all human stomachs are roughly the same shape, and all are found in the same place. There are differences, no doubt.
Some people have unhealthy stomachs; some have small stomachs; some have slightly misshapen stomachs. But the differences are tiny compared with the similarities. A vet or a butcher could teach the surgeon about a much greater variety of different stomachs: big, multichambered cow stomachs; tiny mouse stomachs; somewhat human looking pig stomachs. There is, it is safe to say, such a thing as the typical human stomach, and it is different from a nonhuman stomach.
It is the assumption of this book that there is also, in the same way, a typical human nature. It is the aim of this book to seek it: Like the stomach surgeon, a psychiatrist can make all sorts of basic assumptions when a patient lies down on the couch. He can assume that the patient knows what it means to love, to envy, to trust, to think, to speak, to fear, to smile, to bargain, to covet, to dream, to remember, to sing, to quarrel, to lie. Even if the person were from a newly discovered continent, all sorts of assumptions about his or her mind and nature would still be valid. When, in the 1930s , contact was made with New Guinea tribes hitherto cut off from the outside world and ignorant of its existence, they were found to smile and frown as unambiguously as any Westerner, despite 100,000 years of separation since they last shared a com-
::: 4 :::
The Red Queen
mon ancestor: The "smile" of a baboon is a threat; the smile of a man is a sign of pleasure: It is human nature the world over: That is not to deny the fact of culture shock. Sheeps ' eye-ball soup, a shake of the head that means yes, Western privacy, circumcision rituals, afternoon siestas, religions, languages, the difference in smiling frequency between a Russian and an American waiter in a restaurant—there are myriad human particulars as well as human universals: Indeed, there is a whole discipline, cultural anthropology, that devotes itself to the study of human cultural differences. But it is easy to take for granted the bedrock of similarity that underlies the human race—the shared peculiarities of being human.
This book is an inquiry into the nature of that human nature: Its theme is that it is impossible to understand human nature without understanding how it evolved, and it is impossible to understand how it evolved without understanding how human sexuality evolved. For the central theme of our evolution has been sexual.
Why sex? Surely there are features of human nature other than this one overexposed and troublesome procreative pastime: True enough, but reproduction is the sole goal for which human beings are designed; everything else is a means to that end: Human beings inherit tendencies to survive, to eat, to think, to speak, and so on: But above all they inherit a tendency to reproduce: Those of their predecessors that reproduced passed on their characteristics to their offspring; those that remained barren did not: Therefore, anything that increased the chances of a person reproducing successfully was passed on at the expense of anything else. We can confidently assert that there is nothing in our natures that was not carefully "chosen" in this way for its ability to contribute to eventual reproductive success:
This seems an astonishingly hubristic claim: It seems to deny free will, ignore those who choose chastity, and portray human beings as programmed robots bent only on procreation: It seems to imply that Mozart and Shakespeare were motivated only by sex: Yet I know of no other way that human nature can have HUMAN NATURE
::: 5 :::
developed except by evolution, and there is now overwhelming evidence that there is no other way for evolution to work except by competitive reproduction. Those strains that reproduce persist; those that do not reproduce die out. The ability to reproduce is what makes living things different from rocks: Besides, there is nothing inconsistent with free will or even chastity in this view of life. Human beings, I believe, thrive according to their ability to take initiatives and exercise individual talent: But free will was not created for fun; there was a reason that evolution handed our ancestors the ability to take initiatives, and the reason was that free will and initiative are means to satisfy ambition, to compete with fellow human beings, to deal with life 's emergencies, and so eventually to be in a better position to reproduce and rear children than human beings who do not reproduce. Therefore, free will itself is any good only to the extent that it contributes to eventual reproduction.
Look at it another way: If a student is brilliant but terrible in examinations—if, say, she simply collapses with nervousness at the very thought of an exam—then her brilliance will count for
nothing in a course that 'is tested by a single examination at the end of the term. Likewise, if an animal is brilliant at survival, has an efficient metabolism, resists all diseases, learns faster than its competitors, and lives to a ripe old age, but is infertile, then its superior genes are simply not available to its descendants. Everything can be inherited except sterility. None of your direct ancestors died childless. Consequently, if we are to understand how human nature evolved, the very core of our inquiry must be reproduction, for reproductive success is the examination that all human genes must pass if they are not to be squeezed out by natural selection: Hence I am going to argue that there are very few features of the human psyche and nature that can be understood without reference to reproduction: I begin with sexuality itself. Reproduction is not synonymous with sex; there are many asexual ways to reproduce. But reproducing sexually must improve an individual 's reproductive success or else sex would not persist: I end with intelligence, the most human of all features. It is increasingly hard to
::: 6 :::
The Red Queen
understand how human beings came to be so clever without considering sexual competition.
What was the secret that the serpent told Eve? That she could eat a certain fruit? Pah. That was a euphemism. The fruit was carnal knowledge, and everybody from Thomas Aquinas to Milton knew it. How did they know it? Nowhere in Genesis is there even the merest hint of the equation: Forbidden fruit equals sin equals sex. We know it to be true because there can only be one thing so central to mankind. Sex.
OF NATURE AND NURTURE
The idea that we were designed by our past was the principal insight of Charles Darwin. He was the first to realize that you can abandon divine creation of species without abandoning the argument from design. Every living thing is "designed " quite unconsciously by the selective reproduction of its own ancestors to suit a particular life-style. Human nature was as carefully designed by natural selection for the use of a social, bipedal, originally African ape as human stomachs were designed for the use of an omnivorous African ape with a taste for meat.
That starting point will already have irritated two kinds of people. To those who believe that the world was made in seven days by a man with a long beard and that therefore human nature cannot have been designed by selection but by an Intelligence, I merely bid a respectful good day. We have little common ground on which to argue because I share few of your assumptions. As for those who protest that human nature did not evolve, but was invented de novo by something called "culture, " I have more hope: I think I can persuade you that our views are compatible. Human nature is a product of culture, but culture is also a product of human nature, and both are the products of evolution. This does not mean that I am going to argue that it is "all in our genes. " Far from it. I am vigorously going to challenge the notion that anything psychological is purely genetic, and equally vigorously challenge the assumption HUMAN NATURE
::: 7 :::
that anything universally human is untainted by genes. But our
" culture" does not have to be the way it is. Human culture could be very much more varied and surprising than it is: Our closest relatives, the chimpanzees, live in promiscuous societies in which females seek as many sexual partners as possible and a male will kill the infants of strange females with whom he has not mated. There is no human society that remotely resembles this particular pattern: Why not? Because human nature is different from chimp nature: If this is so, then the study of human nature must have profound implications for the study of history, sociology, psychology, anthropology, and politics. Each of those disciplines is an attempt to understand human behavior, and if the underlying universals of human behavior are the product of evolution, then it is vitally important to understand what the evolutionary pressures were. Yet I have gradually come to realize that almost all of social science proceeds as if 1859, the year of the publication of the Origin of Species, had never happened; it does so quite deliberately, for it insists that human culture is a product of our own free will and invention. Society is not the product of human psychology, it asserts, but vice versa:
That sounds reasonable enough, and it would be splendid for those who believe in social engineering if it were true, but it is simply not true: Humanity is, of course, morally free to make and remake itself infinitely, but we do not do so. We stick to the same monotonously human pattern of organizing our affairs: If we were more adventurous, there would be societies without love, without ambition, without sexual desire, without marriage, without art, without grammar, without music, without smiles—and with as many unimaginable novelties as are in that list. There' would be societies in which women killed each other more often than men, in which old people were considered more beautiful than twenty-year-olds, in which wealth did not purchase power over others, in which people did not discriminate in favor of their own friends and against strangers, in which parents did not love their own children: I am not saying, like those who cry, "You can't change human nature, you know, " that it is futile to attempt to outlaw, say,
::: 8 :::
The Red Queen
racial persecution because it is in human nature. Laws against racism do have an effect because one of the more appealing aspects of human nature is that people calculate the consequences of their actions: But I am saying that even after a thousand years of strictly enforced laws against racism, we will not one day suddenly be able to declare the problem of racism solved and abolish the laws secure in the knowledge that racial prejudice is a thing of the past. We assume, and rightly, that a Russian is just as human after two generations of oppressive totalitarianism as his grandfather was before him. But why, then, does social science proceed as if it were not the case, as if people 's natures are the products of their societies?
It is a mistake that biologists used to make, too. They believed that evolution proceeded by accumulating the changes that individuals gathered during their lives. The idea was most clearly formulated by Jean-Baptiste Lamarck, but Charles Darwin someti mes used it, too: The classic example is a blacksmith 's son supposedly inheriting his father 's acquired muscles at birth: We now know that Lamarckism cannot work because bodies are built from cakelike recipes, not architectural blueprints, and it is simply impossible to feed information back into the recipe by changing the cake:' But the first coherent challenge to Lamarckism was the work of a German follower of Darwin named August Weismann, who began to publish his ideas in the 1880s: 2 Weismann noticed something peculiar about most sexual creatures: Their sex cells—
eggs and sperm—remained segregated from the rest of the body from the moment of their birth: He wrote: "I believe that heredity depends upon the fact that a small portion of the effective substance of the germ, the germ-plasm, remains unchanged during the development of the ovum into an organism, and that this part of the germ-plasm serves as a foundation from which germ-cells of the new organism are produced. There is, therefore, continuity of the germ-plasm from one generation to another. "; In other words, you are descended not from your mother but from her ovary. Nothing that happened to her body or her mind in her life could affect your nature (though it could affect your nurture, of course—an extreme example being that her addiction to HUMAN NATURE
::: 9:::
drugs or alcohol might leave you damaged in some nongenetic way at birth). You are born free of sin. Weismann was much ridiculed for this in his lifetime and little believed. But the discovery of the gene and of the DNA from which it is made and of the cipher in which DNA's message is written have absolutely confirmed his suspicion.
The germ-plasm is kept separate from the body.
Not until the 1970s were the-full implications of this realized. Then Richard Dawkins of Oxford University effectively invented the notion that because bodies do not replicate themselves but are grown, whereas genes do replicate themselves, it inevitably follows that the body is merely an evolutionary vehicle for the gene, rather than vice versa. If genes make their bodies do things that perpetuate the genes (such as eat, survive, have sex, and help rear children), then the genes themselves will be perpetuated. So other kinds of bodies will disappear: Only bodies that suit the survival and perpetuation of genes will remain:
Since then, the ideas of which Dawkins was an early champion have changed biology beyond recognition. What was still—
despite Darwin—essentially a descriptive science has become a study of function: The difference is crucial. Just as no engineer would dream of describing a car engine without reference to its function (to turn wheels), so no physiologist would dream of describing a stomach without reference to its function (to digest food). But before, say, 1970, most students of animal behavior and virtually all students of human behavior were content to describe what they found without reference to a function. The gene-centered view of the world changed this for good. By 1980 no detail of animal courtship mattered unless it could be explained in terms of the selective competition of genes. And by 1990 the notion that human beings were the only animals exempt from this logic was beginning to look ever more absurd. If man has evolved the ability to override his evolutionary imperatives, then there must have been an advantage to his genes in doing so. Therefore, even the emanci-pation from evolution that we so fondly imagine we have achieved must itself have evolved because it suited the replication of genes.
Inside my skull is a brain that was designed to exploit the
::: 10 :::
The Red Queen
conditions of an African savanna between 3 million and 1 00,000
years ago: When my ancestors moved into Europe (I am a white European by descent) about 100,000 years ago, they quickly evolved a set of physiological features to suit the sunless climate of northern latitudes: pale skin to prevent rickets, male beards, and a circulation relatively resistant to frostbite. But little else changed: Skull size, body proportions, and teeth are all much the same in me as they were in my ancestors 100,000 years ago and are much the same as they are in a San tribesman from southern Africa: And there is little reason to believe that the gray matter inside the skull changed much, either: For a start, 100,000 years is only three thousand generations, a mere eye blink in evolution, equivalent to a day and a half in the life of bacteria. Moreover, until very recently the life of a European was essentially the same as that of an African. Both hunted meat and gathered plants. Both lived in social groups: Both had children dependent on their parents until their late teens: Both used stone, bone, wood, and fiber to make tools: Both passed wisdom down with complex language. Such evolutionary novelties as agriculture, metal, and writing arrived less than three hundred generations ago, far too recently to have left much imprint on my mind.
There is, therefore, such a thing as a universal human nature, common to all peoples: If there were descendants of Homo erectus still living in China, as there were a million years ago, and those people were as intelligent as we are, then truly they could be said to have different but still human natures.' They might perhaps have no lasting pair bonds of the kind we call marriage, no concept of romantic love, and no involvement of fathers in parental care.
We could have some very interesting discussions with them about such matters. But there are no such people: We are all one close family, one small race of the modern Homo sapiens people who lived in Africa until 100,000 years ago, and we all share the nature of that beast.
Just as human nature is the same everywhere, so it is recognizably the same as it was in the past: A Shakespeare play is about motives and predicaments and feelings and personalities that are instantly familiar. Falstaff 's bombast, Iago 's cunning, Leontes ' s HUMAN NATURE
::: I1 :::
jealousy, Rosalind 's strength, and Malvolio ' s embarrassment have not changed in four hundred years. Shakespeare was writing about the same human nature that we know today. Only his vocabulary (which is nurture, not nature) has aged. When I watch Anthony and Cleopatra, I am seeing a four-hundred-year-old interpretation of a two-thousand-year-old history. Yet it never even occurs to me that love was any different then from what it is now: It is not necessary to explain to me why Anthony falls under the spell of a beautiful woman. Across time just as much as across space, the fundamentals of our nature are universally and idiosyncratically human.
THE INDIVIDUAL IN SOCIETY
Having argued that all human beings are the same, that this book is about their shared human nature, I shall now seem to argue the opposite. But I am not being inconsistent.
Human beings are individuals. All individuals are slightly different. Societies that treat their constituent members as identical pawns soon run into trouble. Economists and sociologists who believe that individuals will usually act in their collective rather than their particular interests ( "From each according to his ability, to each according to his needs " ' versus "Devil take the hindmost") are soon confounded: Society is composed of competing individuals as surely as markets are composed of competing merchants; the focus of economic and social theory is, and must be, the individual.
Just as genes are the only things that replicate, so individuals, not societies, are the vehicles for genes. And the most formidable threats to reproductive destiny that a human individual faces come from other human individuals.
It is one of the remarkable things about the human race that no two people are identical. No father is exactly recast in his son; no daughter is exactly like her mother; no man is his brother 's double, and no woman is a carbon copy of her sister—unless they are that rarity, a pair of identical twins. Every idiot can be father or mother to a genius—and vice versa. Every face and every set of fin-
::: 112
:::
The Red Quern
gerprints is effectively unique: Indeed, this uniqueness goes further in human beings than in any other animal. Whereas every deer or every sparrow is self-reliant and does everything every other deer or sparrow does, the same is not true of a man or a woman, and has not been for thousands of years. Every individual is a specialist of some sort, whether he or she is a welder, a housewife, a playwright, or a prostitute: In behavior, as in appearance, every human individual is unique.
How can this be? How can there be a universal, species-specific human nature when every human being is unique? The solution to this paradox lies in the process known as sex. For it is sex that mixes together the genes of two people and discards half of the mixture, thereby ensuring that no child is exactly like either of its parents: And it is also sex that causes all genes to be contributed eventually to the pool of the whole species by such mixing. Sex causes the differences between individuals but ensures that those differences never diverge far from a golden mean for the whole species.
A simple calculation will clarify the point: Every human being has two parents, four grandparents, eight great-grandparents, sixteen great-great-grandparents, and so on: A mere thirty generations back—in, roughly, A.D. 1066—you had more than a billion direct ancestors in the same generation (2 to the power of 30): Since there were fewer than a billion people alive at that time in the whole world, many of them were your ancestors two or three times over. If, like me, you are of British descent, the chances are that almost all of the few million Britons alive in 1066, including King Harold, William the Conqueror, a random serving wench, and the meanest vassal (but excluding all well-behaved monks and nuns), are your direct ancestors: This makes you a distant cousin many times over of every other Briton alive today except the children of recent immigrants: All Britons are descended from the same set of people a mere thirty generations ago. No wonder there is a certain uniformity about the human (and every other sexual) species. Sex imposes it by its perpetual insistence on the sharing of genes.
If you go back further still, the different human races soon HUMAN NATURE
::: 13 :::
merge. Little more than three thousand generations back, all of our ancestors lived in Africa, a few million simple hunter-gatherers, completely modern in physiology and psychology.' As a result, the genetic differences between the average members of different races are actually tiny and are mostly confined to a few genes that affect skin color, physiognomy, or physique. Yet the differences between any two individuals, of the same race or of different races, can still be large. According to one estimate, only 7 percent of the genetic differences between two individuals can be attributed to the fact that they are of different race; 85 percent of the genetic differences are attributable to mere individual variation, and the rest is tribal or national. In the words of one pair of scientists: "What this means is that the average genetic difference between one Peruvian farmer and his neighbor, or one Swiss villager and his neighbor, is twelve times greater than the difference between the 'average genotype ' of the Swiss population and the 'average genotype ' of the Peruvian population: "'
It is no harder to explain than a game of cards. There are aces and kings and twos and threes in any deck of cards. A lucky player is dealt a high-scoring hand, but none of his cards is unique: Elsewhere in the room are others with the same kinds of cards in their hands. But even with just thirteen kinds of cards, every hand is different and some are spectacularly better than others: Sex is merely the dealer, generating unique hands from the same monotonous deck of genetic cards shared by the whole species.
But the uniqueness of the individual is only the first of the implications of sex for human nature. Another is that there are, in fact, two human natures: male and female: The basic asymmetry of gender leads inevitably to different natures for the two genders, natures that suit the particular role of each gender. For example, males usually compete for access to females, rather than vice versa.
There are good evolutionary reasons for this, and there are clear evolutionary consequences, too; for instance, men are more aggressive than women.
A third implication of sex for human natures is that every other human being alive today is a potential source of genes for
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The Red Queen
your children. And we are descended from only those people who sought the best genes, a habit we inherited from them. Therefore, if you spot somebody with good genes, it is your inherited habit to seek to buy some of those genes; or, put more prosaically, people are attracted to people of high reproductive and genetic potential—the healthy, the fit, and the powerful. The consequences of this fact, which goes under the name of sexual selection, are bizarre in the extreme, as will become clear in the rest of this book: OURS TO REASON WHY?
To speak of the " purpose" of sex or of the function of a particular human behavior is: shorthand. I do not imply some teleological goal-seeking or the existence of a great designer with an aim in mind: Still less will I be implying foresight or consciousness on the part of "sex " itself or of mankind: I merely refer to the astonishing power of adaptation, so well appreciated by Charles Darwin and so little understood by his modern critics: For I must confess at once that I am an "adaptationist, " which is a rude word for somebody who believes that animals and plants, their body parts and their behaviors, consist largely of designs to solve particular problems.'
Let me explain: The human eye is " designed " to form an image of the visual world on its retina; the human stomach is
" designed " to digest food; it is perverse to deny such facts: The only question is how they came to be "designed " for their jobs.
And the only answer that has stood the test of time and scrutiny is that there was no designer. Modern people are descended mainly from those people whose eyes and stomachs were better at those jobs than other people 's. Small, random improvements in the ability of stomachs to digest and of eyes to see were thus inherited, and small diminishments in ability were not inherited because the owners, equipped with poor digestion or poor vision, did not live so long or breed so well:
We human beings find the notion of engineering design quite easy to grasp and have little difficulty seeing the analogy with HUMAN NATURE
::: 15 :::
the design of an eye: But we seem to find it harder to grasp the idea of "designed " behavior, mainly because we assume that purposeful behavior is evidence of conscious choice: An example might help to clarify what I mean: There is a little wasp that injects its eggs into whitefly aphids, where they grow into new wasps by eating the whitefly from the inside out: Distressing but true: If one of these wasps, upon poking its tail into a whitefly, discovers that the aphid is already occupied by a young wasp, then she does something that seems remarkably intelligent: She withholds sperm from the egg she is about to lay and lays an unfertilized egg inside the wasp larva that is inside the whitefly. (It is a peculiarity of wasps and ants that unfertilized eggs develop into males, while all fertilized ones develop into females.) The "intelligent" thing that the mother wasp has done is to recognize that there is less to eat inside an already-occupied whitefly than in virgin territory: Her egg will therefore grow into a small, stunted wasp. And in her species, males are small, females large. So it was "clever " of her to "choose " to make her offspring male when she "knew " it was going to be small: But of course this is nonsense: She was not "clever "; she did not " choose " and she " knew " not what she did: She was a minuscule wasp with a handful of brain cells and absolutely no possibility of conscious thought: She was an automaton, carrying out the simple instructions of her neural program: If whitefly occupied,
withhold sperm: Her program had been designed by natural selection over millions of years: Wasps that inherited a tendency to withhold sperm when they found their prey already occupied had more successful offspring than those that did not. Yet in exactly the same way that natural selection had "designed" an eye, as if for the "purpose " of seeing, so natural selection had produced behavior that seemed designed to suit the wasp ' s purposes:'
This "powerful illusion of deliberate design"' is so fundamental a notion and yet so simple that it hardly seems necessary to repeat it. It has been much more fully explored and explained by Richard Dawkins in his wonderful book The Blind Watchmaker:"
Throughout this book I will assume that the greater the degree of complexity there is in a behavior pattern, genetic mechanism, or
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The Red Queen
psychological attitude, the more it implies a design for a function.
Just as the complexity of the eye forces us to admit that it is designed to see, so the complexity of sexual attraction implies that it is designed for genetic trade.
In other words, I believe that it is always worth asking the question why. Most of science is the dry business of discovering how the universe works, how the sun shines, or how plants grow.
Most scientists live their lives steeped in how questions, not why questions. But consider for a moment the difference between the question "Why do men fall in love? " and the question "How do men fall in love? " The answer to the second will surely turn out to be merely a matter of plumbing. Men fall in love through the effects of hormones on brain cells and vice versa, or some such physiological effect. One day some scientist will know exactly how the brain of a young man becomes obsessed with the image of a particular young woman, molecule by molecule. But the why question is to me more interesting because the answer gets to the heart of how human nature came to be what it is.
Why has that man fallen in love with that woman? Because she's pretty. Why does pretty matter? Because human beings are a mainly monogamous species and so males are choosy about their mates (as male chimpanzees are not); prettiness is an indication of youth and health, which are indications of fertility: Why does that man care about fertility in his mate? Because if he did not, his genes would be eclipsed by those of men who did. Why does he care about that? He does not, but his genes act as if they do. Those who choose infertile mates leave no descendants. Therefore, everybody is descended from men who preferred fertile women, and every person inherits from those ancestors the same preference.
Why is that man a slave to his genes? He is not: He has free will.
But you just said he 's in love because it is good for his genes: He 's free to ignore the dictates of his genes. Why do his genes want to get together with her genes anyway? Because that 's the only way they can get into the next generation; human beings have two sexes that 'must breed by mixing their genes. Why do human beings have two sexes? Because in mobile animals hermaphrodites are less good HUMAN NATURE
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at doing two things at once than males and females are at each doing his or her own thing. Therefore, ancestral hermaphroditic animals were outcompeted by ancestral sexed animals: But why only two sexes? Because that was the only way to settle a long-running genetic dispute between sets of genes: What? I 'll explain later. But why does she need him? Why don ' t her genes just go ahead and make babies without waiting for his input? That is the most fundamental why question of all, and the one with which the next chapter begins:
In physics, there is no great difference between a why question and a how question. How does the earth go around the sun?
By gravitational attraction. Why does the earth go around the sun?
Because of gravity. Evolution, however, causes biology to be a very different game because it includes contingent history. As anthropologist Lionel Tiger has put it, "We are perforce in some sense constrained, goaded, or at least affected by the accumulated impact of selective decisions made over thousands of generations.' Gravity is gravity however history deals its dice. A peacock is a showy peacock because at some point in history ancestral peahens stopped picking their mates according to mundane utilitarian criteria and instead began to follow a fashion for preferring elaborate display.
Every living creature is a product of its past. When a neo-Darwinian asks, "Why? " he is really asking, "How did this come about? "
He is a historian.
OF CONFLICT AND COOPERATION
One of the peculiar features of history is that time always erodes advantage: Every invention sooner or later leads to a counterinven-tion. Every success contains the seeds of its own overthrow. Every hegemony comes to an end. Evolutionary history is no different.
Progress and success are always relative: When the land was unoc-cupied by animals, the first amphibian to emerge from the sea could get away with being slow, lumbering, and fishlike, for it had no enemies and no competitors. But if a fish were to take to the
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The Red Queen
land today, it would be gobbled up by a passing fox as surely as a Mongol horde would be wiped out by machine guns. In history and in evolution, progress is always a futile, Sisyphean struggle to stay in the same relative place by getting ever better at things: Cars move through the congested streets of London no faster than horse-drawn carriages did a century ago. Computers have no effect on productivity because people learn to complicate and repeat tasks that have been made easier:"
This concept, that all progress is relative, has come to be known in biology by the name of the Red Queen, after a chess piece that Alice meets in Through the Looking-Glass, who perpetually runs without getting very far because the landscape moves with her: It is an increasingly influential idea in evolutionary theory, and one that will recur throughout the book. The faster you run, the more the world moves with you and the less you make progress. Life is a chess tournament in which if you win a game, you start the next game with the handicap of a missing pawn.
The Red Queen is not present at all evolutionary events.
Take the example of a polar bear, which is equipped with a thick coat of white fur: The coat is thick because ancestral polar bears better survived to breed if they did not feel the cold: There was a relatively simple evolutionary progression: thicker and thicker fur, warmer and warmer bears. The cold did not get worse just because the bear 's insulation got thicker: But the polar bear 's fur is white for a different reason: camouflage. White bears can creep up on seals much more easily than brown bears can: Presumably, once upon a time, it was easy to creep up on Arctic seals because they feared no enemies on the ice, just as present-day Antarctic seals are entirely fearless on the ice. In those days, proto—polar bears had an easy time catching seals. But soon nervous, timid seals tended to live longer than trusting ones, so gradually seals grew more and more wary: Life grew harder for bears. They had to creep up on the seals stealthily, but the seals could easily see them coming—until one day (it may not have been so sudden, but the principle is the same) by chance mutation a bear had cubs that were white instead of brown. They thrived and multiplied because the seals did not see HUMAN NATURE
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them coming. The seal 's evolutionary effort was for nothing; they were back where they started. The Red Queen was at work: In the world of the Red Queen, any evolutionary progress will be relative as long as your foe is animate and depends heavily on you or suffers heavily if you thrive, like the seals and the bears.
Thus the Red Queen will be especially hard at work among predators and their prey, parasites and their hosts, and males and females of the same species. Every creature on earth is in a Red Queen chess tournament with its parasites (or hosts), its predators (or prey), and, above all, with its mate.
Just as parasites depend on their hosts and yet make them suffer, and just as animals exploit their mates and yet need them, so the Red Queen never appears without another theme being sounded: the theme of intermingled cooperation and conflict. The relationship between a mother and her child is fairly straightforward: Both are seeking roughly the same goal—the welfare of themselves and each other. The relationship between a man and his wife 's lover or between a woman and her rival for a promotion is also fairly straightforward: Both want the worst for each other. One relationship is all about cooperation, the other all about conflict. But what is the relationship between a woman and her husband? It is cooperation in the sense that both want the best for the other: But why?
In order to exploit each other. A man uses his wife to produce children for him. A woman uses her husband to make and help rear her children. Marriage teeters on the line between a cooperative venture and a form of mutual exploitation—ask any divorce lawyer. Successful marriages so submerge the costs under mutual benefits that the cooperation can predominate; unsuccessful ones do not: This is one of the great recurring themes of human history, the balance between cooperation and conflict. It is the obsession of governments and families, of lovers and rivals. It is the key to economics. It is, as we shall see, one of the oldest themes in the history of life, for it is repeated right down to the level of the gene itself. And the principal cause of it is sex. Sex, like marriage, is a cooperative venture between two rival sets of genes. Your body is the scene of this uneasy coexistence.
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The Red Queen
TO CHOOSE
One of Charles Darwin 's more obscure ideas was that animals '
mates can act like horse breeders, consistently selecting certain types and so changing the race: This theory, known as sexual selection, was ignored for many years after Darwin 's death and has only recently come back into vogue: Its principal insight is that the goal of an animal is not just to survive but to breed. Indeed, where breeding and survival come into conflict, it is breeding that takes precedence; for example, salmon starve to death while breeding.
And breeding, in sexual species, consists of finding an appropriate partner and persuading it to part with a package of genes. This goal is so central to life that it has influenced the design not only of the body but of the psyche. Simply put, anything that increases reproductive success will spread at the expense of anything that does not—even if it threatens survival.
Sexual selection produces the appearance of purposeful
" design " as surely as natural selection does( Just as a stag is designed by sexual selection for battle with sexual rivals and a peacock is designed for seduction, so a man 's psychology is designed to do things that put his survival at risk but increase his chances of acquiring or retaining one or more high-quality mates: Testosterone itself, the very elixir of masculinity, increases susceptibility to infectious disease. The more competitive nature of men is a consequence of sexual selection: Men have evolved to live dangerously because success in competition or battle used to lead to more or better sexual conquests and more surviving children. Women who live dangerously merely put at risk those children they already have.
Likewise, the intimate connection between female beauty and female reproductive potential (beautiful women are almost by definition young and healthy; compared with older women, they are therefore both more fertile, and have a longer reproductive life ahead of them) is a consequence of sexual selection acting on both men's psyches and women 's bodies: Each sex shapes the other.
Women have hourglass-shaped bodies because men have preferred them that way: Men have an aggressive nature because women have HUMAN NATURE
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preferred them that way (or have allowed aggressive men to defeat other men in contests over women—it amounts to the same thing).
Indeed, this book will end with the astonishing theory that the human intellect itself is a product of sexual rather than natural selection, for most evolutionary anthropologists now believe that big brains contributed to' reproductive success either by enabling men to outwit and outscheme other men (and women to outwit and outscheme other women) or because big brains were originally used to court and seduce members of the other sex.
Discovering and describing human nature and how it differs from the nature of other animals is as interesting a task as any that science has faced; it is on a par with the quest for the atom, the gene, and the origin of the universe. Yet science has consistently shied away from the task: The greatest "experts " our species has produced on the subject of human nature were people like Buddha and Shakespeare, not scientists or philosophers. The biologists stick to animals; those who try to cross the line (as Harvard 's Edward Wilson did in his book Sociobiology in 1975) are vilified with accusa-tions of political motives." Meanwhile, human scientists proclaim that animals are irrelevant to the study of human beings and that there is no such thing as a universal human nature. The consequence is that science, so coldly successful at dissecting the Big Bang and DNA, has proved spectacularly inept at tackling what the philosopher David Hume called the greatest question of all: Why is human nature what it is?
Chapter 2
THE ENIGMA
Birth after birth the line unchanging runs,
And fathers live transmitted in their sons;
Each passing year beholds the unvarying kinds,
The same their manners, and the same their minds:
Till, as erelong successive buds decay,
And insect-shoals successive pass away,
Increasing wants the pregnant parent vex
With the fond wish to form a softer sex. . .
—Erasmus Darwin, " The Temple of Nature"
Zog the Martian steered her craft carefully into its new orbit and prepared to reenter the hole in the back of the planet, the one that had never been seen from Earth: She had done it many times before and was not so much nervous as impatient to be home. It had been a long stay on Earth, longer than most Martians made, and she looked forward to a long argon bath and a glass of cold chlorine. It would be good to see her colleagues again. And her children. And her husband—she caught herself and laughed. She had been on Earth so long she had even begun to think like an earthling. Husband indeed! Every Martian knew that no Martian had a husband.
There was no such thing as sex on Mars. Zog thought with pride of the report in her knapsack: " Life on Earth: The Reproduction Enigma Solved. " It was the finest thing she had ever done; promotion could not be denied her now, whatever Big Zag said.
A week later, Big Zag opened the door of the Earthstudy Inc. committee room and asked the secretary to send Zog in: Zog entered and sat in the seat assigned to her: Big Zag avoided her eyes as she cleared her throat and began.
" Zog, this committee has read your report carefully, and we are all, I think I can say, impressed with its thoroughness. You have certainly made an exhaustive survey of reproduction on Earth.
Moreover, with the possible exception of Miss Zeeg here, we are all agreed that you have made an overwhelming case for your hypothesis. I consider it now beyond doubt that life on Earth reproduces in the way you describe, using this strange device called 'sex. ' Some of the committee are less happy with your conclusion that many of
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The Red Queen
the peculiar facets of the earthling species known as human beings are a consequence of this sex thing: jealous love, a sense of beauty, male aggression, even what they laughingly call intelligence. " The committee chuckled sycophantically at this old joke. "But," said Big Zag suddenly and loudly, looking up from the paper in front of her,
" we have one major difficulty with your report. We believe you have entirely failed to address the most interesting issue of all. It is a three-letter question of great simplicity. " Big Zag 's voice dripped sarcasm: "Why?"
Zog stammered: "What do you mean, why?"
" I mean why do earthlings have sex? Why don 't they just clone themselves as we do? Why do they need two creatures to have one baby? Why do males exist? Why? Why? Why? "
" Oh," said Zog quickly, "I tried to answer that question, but I got nowhere. I asked some human beings, people who had studied the subject for years, and they did not know. They had a few suggestions, but each person 's suggestion was different. Some said sex was a historical accident. Some said it was a way of fending off disease. Some said it was about adapting to change and evolving faster. Others said it was a way of repairing genes. But basically they did not know. "
"Did not know?" Big Zag burst out. "Did not know? The most essential peculiarity in their whole existence, the most intriguing scientific question anybody has ever asked about life on Earth, and they don't know: Zod save us! "
What is the purpose of sex? At first glance the answer seems obvious to the point of banality. But a second glance brings a different thought. Why must a baby be the product of two people? Why not three, or one? Need there be a reason at all?
About twenty years ago a small group of influential biologists changed their ideas about sex. From considering it logical, inevitable, and sensible as a means of reproduction, they switched almost overnight to the conclusion that it was impossible to explain why it had not disappeared altogether. Sex seemed to make no sense THE ENIGMA
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at all: Ever since, the purpose of sex has been an open question, and it has been called the queen of evolutionary problems.'
But dimly, through the confusion, a wonderful answer is taking shape. To understand it requires you to enter a looking-glass world, where nothing is what it seems. Sex is not about reproduction, gender is not about males and females, courtship is not about persuasion, fashion is not about beauty, and love is not about affection. Below the surface of every banality and cliche there lies irony, cynicism, and profundity.
In 1858, the year Charles Darwin and Alfred Russel Wallace gave the first plausible account of a mechanism for evolution, the Victorian brand of optimism known as "progress " was in its prime. It is hardly surprising that Darwin and Wallace were immediately interpreted as having given succor to the god of progress.
Evolution's immediate popularity (and it was popular) owed much to the fact that it was misunderstood as a theory of steady progress from amoeba to man, a ladder of self-improvement.
As the end of the second millennium approaches, mankind is in a different mood. Progress, we think, is about to hit the buffers of overpopulation, the greenhouse effect, and the exhaus-tion of resources. However fast we run, we never seem to get anywhere: Has the industrial revolution made the average inhabitant of the world healthier, wealthier, and wiser? Yes, if he is German. No, if he is Bangladeshi. Uncannily (or, a philosopher would have us believe, predictably), evolutionary science is ready to suit the mood. The fashion in evolutionary science now is to scoff at progress; evolution is a treadmill, not a ladder.
PREGNANT VIRGINS
For people, sex is the only way to have babies, and that, plainly enough, is its purpose. It was only in the last half of the nineteenth century that anybody saw a problem with this. The problem was that there seemed to be all sorts of better ways of reproducing.
Microscopic animals split in two. Willow trees grow from cuttings.
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The Red Queen
Dandelions produce seeds that are clones of themselves. Virgin greenfly give birth to virgin young that are already pregnant with other virgins. August Weismann saw this clearly in 1889. "The significance of amphimixis [sex], he wrote, "cannot be that of making multiplication possible, for multiplication may be effected without amphimixis in the most diverse ways—by division of the organism into two or more, by budding, and even by the production of unicellular germs. "'
Weismann started a grand tradition. From that day to this, at regular intervals, the evolutionists have declared that sex is a
" problem," a luxury that should not exist. There is a story about an early meeting of the Royal Society in London, attended by the king, at which an earnest discussion began about why a bowl of water weighed the same with a goldfish in it as it did without. All sorts of explanations were proffered and rejected. The debate became quite heated. Then the king suddenly said, " I doubt your premise." He sent for a bowl of water and a fish and a balance: The experiment was done. The bowl was put on the balance, and the fish was added; the bowl 's weight increased by exactly the weight of the fish: Of course.
The tale is no doubt apocryphal, and it is not fair to suggest that the scientists you will meet in these pages are quite such idiots as to assume a problem exists when it does not. But there is a small similarity. When a group of scientists suddenly said that they could not explain why sex existed and they found the existing explanations unsatisfactory, other scientists found this intellectual sensitivity absurd. Sex exists, they pointed out; it must confer some kind of advantage. Like engineers telling bumblebees they could not fly, biologists were telling animals and plants they would be better off breeding asexually. "A problem for this argument, "
wrote Lisa Brooks of Brown University, "is that many sexual organisms seem to be unaware of the conclusion. "' There might be a few holes in existing theories, said the cynics, but do not expect is to give you a Nobel Prize for plugging them. Besides, why must sex have a purpose? Maybe it is just an evolutionary accident that reproduction happens that way, like driving on one side of the road.
THE ENIGMA
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Yet lots of creatures do not have sex at all or do it in some generations and not others: The virgin greenfly ' s great-great-granddaughter, at the end of the summer, will be sexual: She will mate with a male greenfly and have young that are mixtures of their parents. Why does she bother? For an accident, sex seems to have hung on with remarkable tenacity: The debate has refused to die.
Every year produces a new crop of explanations, a new collection of essays, experiments, and simulations. Survey the scientists involved now and virtually all will agree that the problem has been solved; but none will agree on the solution: One man insists on hypothesis A, another on hypothesis B, a third on C, a fourth on all of the above. Could there be a different explanation altogether? I asked John Maynard Smith, one of the first people to pose the question
" Why sex?," whether he still thought some new explanation was needed. "No. We have the answers. We cannot agree on them, that is all. "'
OF SEX AND FREE TRADE
A brief genetic glossary is necessary before we proceed. Genes are biochemical recipes written in a four-letter alphabet called DNA, recipes for how to make and run a body. A normal human being has two copies of each of 30,000 genes in every cell in his or her body.
The total complement of 6o,000 human genes is called the
" genome," and the genes live on twenty-three pairs of ribbonlike objects called "chromosomes? ' When a man impregnates a woman, each one of his sperm contains one copy of each gene, 30,000 in all, on twenty-three chromosomes. These are added to the 30,000
single genes on twenty-three chromosomes in the woman 's egg to make a complete human embryo with 30,000 pairs of genes and twenty-three pairs of chromosomes.
A few more technical terms are essential, and then we can discard the whole jargon-ridden dictionary of genetics. The first word is "meiosis," which is simply the procedure by which the male selects the genes that will go into a sperm or the female selects the
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The Rtd Queen
genes that will go into an egg. The man may choose either the 30,000 genes he inherited from his father or the seventy-five thousand he inherited from his mother or more likely, a mixture. During meiosis something peculiar happens. Each of the 23 pairs of chromosomes is laid alongside it opposite number. Chunks of one set are swapped with chunks of the other in a procedure called
" recombination." One whole set is then passed on to the offspring to be married with a set from the other parent—a procedure known as "outcrossing."
Sex is recombination plus outcrossing; this mixing of genes is its principal feature. The consequence is that the baby gets a thorough mixture of its four grandparents ' genes (because of recombination) and its two parents' genes (because of outcrossing). Between them, recombination and outcrossing are the essential procedures of sex. Everything else about it—gender, mate choice, incest avoidance, polygamy, love, jealousy—are ways of doing outcrossing and recombination more effectively or carefully.
Put this way, sex immediately becomes detached from reproduction. A creature could borrow another 's genes at any stage in its life. Indeed, that is exactly what bacteria do. They simply hook up with each other like refueling bombers, pass a few genes through the pipe, and go their separate ways. Reproduction they do later, by splitting in half.'
So sex equals genetic mixing. The disagreement comes when you try to understand why genetic mixing is a good idea. For the past century or so, traditional orthodoxy held that genetic mixing is good for evolution because it helps create variety, from which natural selection can choose. It does not change genes—even Weis-manri, who did not know about genes and referred vaguely to "ids,"
realized that—but it throws together new combinations of genes.
Sex is a sort of free trade in good genetic inventions and thus greatly increases the chances that they will spread through a species and the species will evolve. "A source of individual variability fur-nishing material for the operation of natural selection, " Weismann called sex.' It speeds up evolution.
Graham Bell, an English biologist working in Montreal, has THE ENIGMA
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dubbed this traditional theory the "Vicar of Bray " hypothesis after a fictional sixteenth-century cleric who was quick to adapt to the prevailing religious winds, switching between Protestant and Catholic rites as the ruling monarch changed. Like the flexible vic-ar, sexual animals are said to be adaptable and quick to change. The Vicar of Bray orthodoxy survived for almost a century; it still survives in biology textbooks. The precise moment when it was first questioned is hard to pin down for sure. There were doubts as far back as the 1920s. Only gradually did it dawn on modern biologists that the Weismann logic was profoundly flawed. It seems to treat evolution as some kind of imperative, as if evolving were what species exist to do—as if evolving were a goal imposed on existence.'
This is, of course, nonsense. Evolution is something that happens to organisms. It is a directionless process that sometimes makes an animal 's descendants more complicated, sometimes simpler, and sometimes changes them not at all: We are so steeped in notions of progress and self-improvement that we find it strangely hard to accept this. But nobody has told the coelacanth, a fish that lives off Madagascar and looks exactly like its ancestors of 300
million years ago, that it has broken some law by not "evolving. "
The notion that evolution simply cannot go fast enough, and its corollary that a coelacanth is a failure because it did not become a human being, is easily refuted. As Darwin noticed, mankind has intervened dramatically to speed up evolution, producing hundreds of breeds of dogs, from chihuahuas to St. Bernards, in an evolutionary eye blink: That alone is evidence that evolution was not going as fast as it could. Indeed, the coelacanth, far from being a flop, is rather a success: It has stayed the same—a design that persists without innovation, like a Volkswagen beetle. Evolving is not a goal but a means to solving a problem.
Nonetheless, Weismann 's followers, and especially Sir Ronald Fisher and Hermann Muller, could escape the teleology trap by arguing that evolution, if not preordained, was at least essential.
Asexual species were at a disadvantage and would fail in competition with sexual species. By incorporating the concept of the gene
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Tbt Red Queen
into Weismann 's argument, Fisher 's book in 1930 8 and Muller's in 19329 laid out a seemingly watertight argument for the advantages of sex, and Muller even went as far as to declare the problem emphatically solved by the new science of genetics. Sexual species shared their newly invented genes among all individuals; asexual ones did not. So sexual species were like groups of inventors pool-ing their resources. If one man invented a steam erigine and another a railway, then the two could come together. Asexual ones behaved like groups of jealous inventors who never shared their knowledge, so that steam locomotives were used on roads and horses dragged carts along railways.
In 1965, James Crow and Motoo Kimura modernized the Fisher-Muller logic by demonstrating with mathematical models how rare mutations could come together in sexual species but not in asexual ones. The sexual species does not have to wait for two rare events in the same individual but can combine them from different individuals: This, they said, would grant the sexual species an advantage over the asexual ones as long as there were at least one thousand individuals in the sexual ones. All was hunky-dory. Sex was explained, as an aid to evolution, and modern mathematics was adding new precision. The case could be considered closed.'°
MANKIND'S GREATEST RIVAL IS MANKIND
So it might have remained were it not for a voluminous and influential publication by a Scottish biologist named V. C. Wynne Edwards that had appeared a few years before, in 1962. Wynne Edwards did biology an enormous service by exposing a gigantic fallacy that had systematically infected the very heart of evolutionary theory since Darwin 's day. He exposed the fallacy not to demolish it but because he believed it to be true and important. But in so doing he made it explicit for the first time."
The fallacy persists in the way many laymen speak of evolution. We talk blithely among ourselves about evolution being a question of the "survival of the species. " We imply that species THE ENIGMA
::: 33 ::•
compete with each other, that Darwin 's "struggle for existence " is between dinosaurs and mammals, or between rabbits and foxes, or between men and neanderthals. We borrow the imagery of nation-states and football teams: Germany against France, the home team against its rivals.
Charles Darwin, too, slipped occasionally into this way of thinking: The very subtitle of On the Origin of Species refers to the
" preservation of favored races.' But his main focus was on the individual, not the species. Every creature differs from every other; some survive or thrive more readily than others and leave more young behind; if those changes are heritable, gradual change is inevitable. Darwin 's ideas were later fused with the discoveries of Gregor Mendel, who had proved that heritable features came in dis-crete packages, which became known as genes, forming a theory that was able to explain how new mutations in genes spread through a whole species.
But there lay buried beneath this theory an unexamined dichotomy. When the fittest are struggling to survive, with whom are they competing? With other members of their species or with members of other species?
A gazelle on the African savanna is trying not to be eaten by cheetahs, but it is also trying to outrun other gazelles when a cheetah attacks. What matters to the gazelle is being faster than other gazelles, not being faster than cheetahs. (There is an old story of a philosopher who runs when a bear charges him and his friend: "It's no good, you 'll never outrun a bear, " says the logical friend: "I don't have to, " replies the philosopher: " I only have to outrun you. ") In the same way, psychologists sometimes wonder why people are endowed with the ability to learn the part of Ham-let or understand calculus when neither skill was of much use to mankind in the primitive conditions where his intellect was shaped.
Einstein would probably have been as hopeless as anybody in working out how to catch a woolly rhinoceros: Nicholas Humphrey, a Cambridge psychologist, was the first to see clearly the solution to this puzzle: We use our intellects not to solve practical problems but to outwit each other: Deceiving people, detecting deceit, under-
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The Red Queen
standing people 's motives, manipulating people—these are what the intellect is used for. So what matters is not how clever and crafty you are but how much more clever and craftier you are than other people. The value of intellect is infinite. Selection within the species is always going to be more important than selection between the species."
Now this may seem a false dichotomy. After all, the best thing an individual animal can do for its species is to survive and breed. Often, however, the two imperatives will be in conflict. Suppose the individual is a tigress whose territory has recently been invaded by another tigress. Does she welcome the intruder and discuss how best they can cohabit the territory, sharing prey? No, she fights her to the death, which from the point of view of the species is unhelpful. Or suppose the individual is an eaglet of a rare species anxiously watched by conservationists in its nest. Eaglets often kill their younger brothers and sisters in the nest. Good for the individual, bad for the species.
Throughout the world of animals, individuals are fighting individuals, whether of the same species or of another. And indeed, the closest competitor a creature is ever likely to meet is a member of its own species. Natural selection is not going to pick genes that help gazelles survive as a species but hurt the chances of individuals—because such genes will be wiped out long before they can show their benefits. Species are not fighting species as nations battle other nations.
Wynne Edwards believed fervently that animals often did things for the species, or at least for the group in which they lived.
For example, he thought that seabirds chose not to breed when their numbers were high in order to prevent too much pressure on the food supply. The result of Wynne Edwards 's book was that two factions formed: the group selectionists, who argued that much of animal behavior was informed by the interests of the group, not the individual, and the individual selectionists, who argued that individual interests always triumphed. The group selectionist argument is inherently appealing—we are immersed in the ethic of team spir-it and charity. It also seemed to explain animal altruism. Bees die as THE ENIGMA
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they sting, trying to save the hive; birds warn each other of predators or help to feed their young siblings; even human beings are prepared to die in acts of selfless heroism to save others ' lives. But as we shall see, the appearance is misleading. Animal altruism is a myth. Even in the most spectacular cases of selflessness it turns out that animals are serving the selfish interests of their own genes—if sometimes being careless with their bodies.
THE REDISCOVERY OF THE INDIVIDUAL
If you attend a meeting of evolutionary biologists somewhere in America, you might be lucky and spot a tall, gray-whiskered, smiling man bearing a striking resemblance to Abraham Lincoln, standing rather diffidently at the back of the crowd. He will probably be surrounded by a knot of admirers, hanging on his every word—for he is a man of few words. A whisper will go around the room:
"George is here." You will sense from people's reactions the presence of greatness.
The man in question is George Williams, who has been a quiet, bookish professor of biology at the State University of New York at Stony Brook on Long Island for most of his career. He has done no memorable experiments and has made no startling discovery. Yet he is the progenitor of a revolution in evolutionary biology almost as profound as Darwin 's. In 1966, irritated by Wynne Edwards and other exponents of group selection, he spent a summer vacation writing a book about how he thought evolution worked. Called Adaptation and Natural Selection, that book still towers over biology like a Himalayan peak. It did for biology what Adam Smith had done for economics: It explained how collective effects could flow from the actions of self-interested individuals."
In the book Williams exposed the logical flaws in group selection with unanswerable simplicity. The few evolutionists who had stuck to individual selection all along, such as Ronald Fisher, J. B. S. Haldane, and Sewall Wright, were vindicated." The ones who had confused species and individual, such as Julian Huxley,
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The Red Queen
were eclipsed. 16 Within a few years of Williams 's book, Wynne Edwards was effectively defeated, and almost all biologists agreed that no creature could ever evolve the ability to help its"species at the expense of itself. Only when the two interests coincided would it act selflessly.
This was disturbing. It seemed at first to be a very cruel and heartless conclusion to reach, particularly in a decade when economists were tentatively celebrating the discovery that the ideal of helping society could persuade people to pay high taxes to support welfare. Society, they said, need not be based on tempering the greed of individuals but on appealing to their better natures. And here were biologists coming to exactly the opposite conclusion about animals, depicting a harsh world in which no animal ever sacrificed its own ambition to the need of the team or the group: Crocodiles would eat one another 's babies even on the brink of extinction.
Yet that was not what Williams said. He knew full well that individual animals often cooperate and that human society is not a ruthless free-for-all. But he also saw that cooperation is nearly always between close relatives—mothers and children, sister worker bees—or that it is practiced where it directly or eventually benefits the individual. The exceptions are few indeed. This is because where selfishness brings higher rewards than altruism, selfish individuals leave more descendants, so altruists inevitably become extinct. But where altruists help their relatives, they are helping those who share some of their genes, including whatever genes had caused them to be altruistic. So without any conscious intention on the part of individuals, such genes spread."
But Williams realized that there was one troubling exception to this pattern: sex. The traditional explanation for sex, the Vicar of Bray theory, was essentially group selectionist. It demanded that an individual altruistically share its genes with those of another individual when breeding because if it did not, the species would not innovate and would, a few hundred thousand years later, be outcompeted by other species that did. Sexual species, it said, were better off than asexual species.
But were sexual individuals better off than asexual ones? If THE ENIGMA
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not, sex could not be explained by the Williams " selfish " school of thought. Therefore, either there was something wrong with the selfish theories and true altruism could indeed emerge, or the traditional explanation of sex was wrong. And the more Williams and his allies looked, the less sense sex seemed to make for the individual as opposed to the species.
Michael Ghiselin of the California Academy of Sciences in San Francisco was at the time engaged in a study of Darwin 's work and was struck by Darwin 's own insistence on the primacy of the struggle between individuals rather than the struggle between groups: But Ghiselin, too, began thinking about how sex seemed such an exception to this. He posed the following question: How could a gene for sexual reproduction spread at the expense of an asexual gene? Suppose all members of a species were asexual but one day one pair of them invented sex. What benefit would it bring? And if it brought no benefit, why would it spread? And if it could not spread, why were so many species sexual? Ghiselin could not see how the new sexual individuals could possibly leave behind more offspring than the old asexual ones. Indeed, surely they would leave fewer because, unlike their rivals, they had to waste time finding each other, and one of them, the male, would not produce babies at all.1e
John Maynard Smith, an engineer-turned-geneticist at the University of Sussex in England, with a penetrating and somewhat playful mind that had been trained by the great neo-Darwinist J. B. S. Haldane, answered Ghiselin 's question without solving his dilemma. He said that a sexual gene could spread only if it doubled the number of offspring an individual could have, which seemed absurd. Suppose, he said, turning Ghiselin 's thought around, that in a sexual species one day a creature decides to forgo sex and put all of its genes into its own offspring, taking none from its mate. It would then have passed twice as many genes on to the next generation as its rivals had. Surely it would be at a huge advantage. It would contribute twice as much to the next generation and would soon be left in sole possession of the genetic patrimony of the species.19
Imagine a Stone Age cave inhabited by two men and two
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The Red Queen
women, one of them a virgin. One day the virgin gives birth "asexually " to a baby girl that is essentially her identical twin. (She becomes, in the jargon, a "parthenogen. ") It could happen in several ways—for example, by a process called "automixis, " in which an egg is, roughly speaking, fertilized by another egg. The cave woman has another daughter two years later by the same means. Her sister, meanwhile, has had a son and a daughter by the normal method.
There are now eight people in the cave. Next, the three young girls each have two children and the first generation dies off. Now there are ten people in the cave, but five of them are parthenogens. In two generations the gene for parthenogenesis has spread from one-quarter to one-half of the population. It will not be long before men are extinct.
This is what Williams called the cost of meiosis and Maynard Smith called the cost of males. For what dooms the sexual cave people is simply that half of them are men, and men do not produce babies. It is true that men do occasionally help in child rearing, killing woolly rhinos for dinner or whatever, but even that does not really explain why men are necessary. Suppose that the asexual women at first gave birth only when they had intercourse.
Again there are precedents. There are grasses that only set seed when fertilized by pollen from a related species, but the seed inherits no genes from the pollen. It is called " pseudogamy. "'° In this case the men in the cave would have no idea that they are being genetically excluded and would treat the asexual babies as their own, serving woolly rhino meat to them just as they would to their own children.
This thought-experiment illustrates the numerically huge advantage a gene that makes its owner asexual has. Logic such as this set Maynard Smith, Ghiselin, and Williams to wondering what compensating advantage of sex there must be, given that every mammal and bird, most invertebrate animals, most plants and fungi, and many protozoa are sexual.
For those who think that to talk about the "cost of sex " is merely to illustrate how absurdly pecuniary we have become, and who reject the whole logic of this argument as specious, I offer the THE ENIGMA
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following challenge. Explain hummingbirds—not how they work but why they exist at all. If sex had no cost, hummingbirds would not exist. Hummingbirds eat nectar, which is produced by flowers to lure pollinating insects and birds. Nectar is a pure gift by the plant of its hard-won sugar to the hummingbird, a gift given only because the hummingbird will then carry pollen to another plant.
To have sex with another plant, the first plant must bribe the pollen carrier with nectar. Nectar is therefore a pure, unadulterated cost incurred by the plant in its quest for sex. If sex had no cost, there would be no hummingbirds. 2'
Williams was inclined to conclude that perhaps his logic was good, but for animals like us the practical problems were simply insurmountable. In other words, getting from being sexual to being asexual would indeed confer advantages, but it would be just too difficult to achieve. About this time sociobiologists were beginning to fall into a trap of being too readily enamored of
" adaptationist" arguments—just-so stories, as Stephen Jay Gould of Harvard called them. Sometimes, he pointed out, things were the way they were for accidental reasons. Gould 's own example is of the triangular space between two cathedral arches at right angles, known as a spandrel, which has no function but is simply the by-product of putting a dome on four arches. The spandrels between the arches on St. Mark 's Basilica in Venice were not there because somebody wanted spandrels. They were there because there is no way to put two arches next to each other without producing a space in between. The human chin may be such a spandrel; it has no function but is the inevitable result of having jaws. Likewise the fact that blood: is red is surely a photochemical accident, not a design feature. Perhaps sex was a spandrel, an evolutionary relic of a time when it served a purpose. Like chins or little toes or appendix-es, it no longer served a purpose but was not easily got rid of. 31
Yet this argument for sex is pretty unconvincing because quite a few animals and plants have abandoned sex or have it only occasionally. Take the average lawn. The grass in it never has sex—
unless you forget to cut it, at which point it grows flower heads.
And what about water fleas? For many generations in a row water
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The Red Queen
fleas are asexual: They are all female, they give birth to other females, they never mate. Then as the pond fills up with water fleas, some start to give birth to males, which mate with other females to produce "winter " eggs that lie on the bottom of the pond and regenerate when the pond is flooded again. Water fleas can turn sex on and off again, which seems to prove that it has some immediate purpose beyond helping evolution to happen. It is worth an individual water flea 's while to have sex at least in certain seasons.
So we are left with an enigma. Sex serves the species but at the expense of the individual. Individuals could abandon sex and rapidly outcompete their sexual rivals. But they do not. Sex must therefore in some mysterious manner "pay its way" for the individual as well as for the species. How?
PROVOCATION BY IGNORANCE
Until the mid-1970s the debate that Williams had started remained an arcane and obscure one: And the protagonists sounded fairly confident in their attempts to resolve the dilemma. But in the mid-1970s two crucial books changed that forever by throwing down a gauntlet that other biologists could not resist picking up.
One book was by Williams himself, the other by Maynard Smith. 23
" There is a kind of crisis at hand in evolutionary biology, " wrote Williams melodramatically. But whereas Williams 's book, Sex and
Evolution, was an ingenious account of several possible theories of sex—an attempt to defuse the crisis—Maynard Smith 's book, The
Evolution of Sex, was very different: It was a counsel of despair and
,
bafflement. Again and again Maynard Smith came back to the enormous price of sex: the twofold disadvantage—two parthenogenetic virgins can have twice as many babies as one woman and one man: Again and again he declared it insurmountable by current theories.
" I fear the reader may find these models insubstantial and unsatisfactory," he wrote. "But they are the best we have. " And in a separate paper: "One is left with the feeling that some essential feature THE ENIGMA
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of the situation is being overlooked."" By insisting that the problem was emphatically not solved, Maynard Smith 's book had an electrifying impact: It was an unusually humble and honest gesture.
Attempts to explain sex have since proliferated like libidi-nous rabbits: They present an unusual spectacle to the observer of science: Most of the time scientists are groping around in a barrel of ignorance trying to find a fact or a theory or to discern a pattern where none had been seen before. But this was a rather different game. The fact—sex—was well known. To explain it—to give sex an advantage—was not sufficient. The proffered explanation had to be better than others: It is like the gazelle running faster than other gazelles rather than running faster than cheetahs. Theories of sex are a dime a dozen, and most are "right" in the sense of making logical sense: But which is most right?"
In the pages that follow you will meet three kinds of scientists. The first is a molecular biologist, muttering about enzymes and exonucleolytic degradation. He wants to know what happens to the DNA of which genes are made. His conviction is that sex is all about repairing DNA or some such molecular engineering. He does not understand equations, but he loves long words, usually ones he and his colleagues have invented: The second is a geneticist, all mutations and Mendelism. He will be obsessed with describing what happens to genes during sex. He will demand experiments, such as depriving organisms of sex for many generations to see what happens: Unless you stop him, he will start writing equations and talking of "linkage disequilibria: " The third is an ecologist, all parasites and polyploidy: He loves comparative evidence: which species has sex and which does not: He knows a plethora of extraneous facts about the arctic and the tropics. His thinking is a little less rigorous than others, his language a little more colorful: His natural habitat is the graph, his occupation the computer simulation.
Each of these characters champions a type of explanation for sex. The molecular biologist is essentially talking about why sex was invented, which is not necessarily the same question as what sex achieves today, the question the geneticist prefers to address.
The ecologist, meanwhile, is asking a slightly different question:
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Th'e Red Queen
Under what circumstances is sex better than asex? An analogy might be the reasons for the invention of computers. The historian (like the molecular biologist) will insist they were invented to crack the codes used by German submarine commanders. But they are not used for that today. They are used to do repetitive tasks more efficiently and quickly than people can (the geneticist's answer). The ecologist is interested in why computers have replaced telephone operators but not, say, cooks. All three may be
" right" on different levels.
THE MASTER-COPY THEORY
The leader of the molecular biologists is Harris Bernstein of the University of Arizona. His argument is that sex was invented to repair genes. The first hint of this was the discovery that mutant fruit flies unable to 'repair genes are unable to "recombine " them, either. Recombination is the essential procedure in sex, the mixing of genes from the two grandparents of the sperm or egg. Knock out genetic repair, and sex stops, too.
Bernstein noticed that the tools the cell uses for sex are the same as it uses to repair genes. But he has been unable to convince the geneticists or the ecologists that repair is more than the original, long superseded purpose of the machinery sex uses. The geneticists say the machinery of sex did indeed evolve from the machinery of gene repair, but that is not the same thing as saying sex exists today to repair genes. After all, human legs are the descendants of fishes ' fins, but they are designed nowadays for walking, not swimming."
A quick digression into molecules is necessary here. DNA, the stuff of genes, is a long, thin molecule that carries information in a simple alphabet of four chemical "bases," like Morse code with two kinds of dots and two kinds of dashes. Call these bases "letters" : A, C, G, and T. The beauty of DNA is that each letter is complementary to another, meaning that it prefers to align itself opposite that other letter. Thus A pairs with T and vice versa, C
THE ENIGMA
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with G and vice versa. This means there is an automatic way of copying DNA: by going along the strand of the molecule, stitching together another from the complementary letters. The sequence AAGTTC becomes, on the complementary strand, TTCAAG; copy that and you get the original sequence back again. Every gene normally consists of a strand of DNA and its complementary copy closely entwined in the famous double helix. Special enzymes move up and down the strands, and where they find a break, repair it by reference to the complementary strand. DNA is continually being damaged by sunlight and chemicals. If it were not for the repair enzymes, it would quite quickly become meaningless gobbledygook.
But what happens when both strands are damaged at the same place? This can be quite common—for example, when the two strands get fused together like a spot of glue on a closed zipper. The repair enzymes have no way of knowing what to repair the DNA to: They need a template of what the gene used to look like: Sex provides it: It introduces a copy of the same gene from another creature (outcrossing) or from another chromosome (recombination) in the same creature. Repair can now refer to a fresh template: Of course, the fresh template may also be damaged at the same place, but the chances of that are small. A shopkeeper adding up a list of prices makes sure he has it right the first time by simply repeating the task. His reasoning is that he is unlikely to make the same mistake twice.
The repair theory is supported by some good circumstantial evidence. For example, if you expose a creature to damaging ultraviolet light, it generally fares better if it is capable of recombination than if it is not, and it fares better still if it has two chromosomes in its cells. If a mutant strain appears that eschews recombination, it proves to be especially susceptible to damage by ultraviolet light: Moreover, Bernstein can explain details that his rivals cannot—for example, the curious fact that just before dividing its chromosome pairs in two to make an egg, a cell will double the number and then dispose of three-quarters of the proceeds. In the repair theory, this is to find, and convert to a "common currency, " the errors that are to be repaird.''
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The Red Queen
Nonetheless, the repair theory remains inadequate to the task it has set itself: It is silent on outcrossing. Indeed, if sex is about getting spare copies of genes, it would be better to get them'
from relatives rather than seek out unrelated members of the species: Bernstein says outcrossing is a way of masking mutations, but this amounts to no more than a restatement of the reason why inbreeding is a bad thing; and sex is the cause of inbreeding, not the consequence:
Moreover, every argument that the repair people give for recombination is merely an argument for keeping backup copies of genes, and there is a far simpler way of doing that than swapping them at random between chromosomes. It is called "diploidy: "ZB An egg or a sperm is "haploid"—it has one copy of each gene. A bacterium or a primitive plant, such as moss, is the same. But most plants and nearly all animals are diploid, meaning they have two copies of every gene, one from each parent: A few creatures, especially plants that are descended from natural hybrids or have been selected by man for large size, are "polyploid." Most hybrid wheat, for example, is " hexaploid "; it has six copies of each gene: In yams, female plants are "octoploid " or hexaploid, males all "tetraploid "
—a discrepancy that renders yams sterile. Even some strains of rain-bow trout and domestic chicken are "triploid "—plus a single parrot that turned up a few years ago: 1° Ecologists have begun to suspect that polyploidy in plants is a sort of alternative to sex: At high altitudes and high latitudes many plants seem to abandon sex in favor of asexual polyploidy:3°
But by mentioning ecologists we are getting ahead of ourselves: The point at issue is gene repair: If diploid creatures were to indulge in a little recombination between chromosomes every time their cells divided as the body grew, there would be plenty of opportunity for repair: But they do not: They recombine their genes only at the final peculiar division called meiosis that leads to the formation of an egg or a sperm. Bernstein has an answer for this: He says that there is another, more economical way to repair damage to genes during ordinary cell division, which is to allow the fittest cells to survive: There is no need for repair at that stage THE ENIGMA
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because the undamaged cells will soon outgrow the damaged ones.
Only when producing germ cells, which go out to face the world alone, need you check for errors."
The verdict on Bernstein: unproven. Certainly the tools of sex seem to be derived from the tools of repair, and certainly recombination achieves some gene repair. But is it the purpose of sex? Probably not.
CAMERAS AND RATCHETS
The geneticists, too, are obsessed with damaged DNA. But whereas the molecular biologists concentrate on the damage that is repaired, the geneticists talk about the damage that cannot be repaired. They call this "mutation. "
Scientists used to think of mutations as rare events. But in recent years they have gradually come to realize how many mutations happen. They are accumulated at the rate of about one hundred per genome per generation in mammals. That is, your children will have one hundred differences from you and your spouse in their genes as a result of random copying errors by your enzymes or as a result of mutations in your ovaries or testicles caused by cosmic rays. Of those one hundred, about ninety-nine will not matter: they will be so-called silent or neutral mutations that do not affect the sense of genes. That may not seem many, given that you have seventy-five thousand pairs of genes and that many of the changes will be tiny and harmless or will happen in silent DNA between genes. But it is enough to lead to a steady accumulation of defects and, of course, a steady rate of invention of new ideas."
The received wisdom on mutations is that most of them are bad news and a good proportion kill their owners or inheritors (cancer starts as one or more mutations), but that occasionally among the bad there is a good mutation, a genuine improvement.
The sickle cell anemia mutation, for example, can be fatal to those who have two copies of it, but the mutation has actually increased in some parts of Africa because it gives immunity to malaria.
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The Red Queen
For many years geneticists concentrated on good mutations and viewed sex as a way of distributing them among the population, like the " cross-fertilization " of good ideas in universities and industries: Just as technology needs "sex" to bring in innovations from outside, so an animal or plant that relies on only its own inventions will be slow to innovate: The solution is to beg, borrow, or steal the inventions of other animals and plants, to get hold of their genes in the way that companies copy one another 's inventions. Plant breeders who try to combine high yield, short stems, and disease resistance in rice plants are acting like manufacturers with access to many different inventors. Breeders of asexual plants must wait for the inventions to accumulate slowly within the same lineage: One of the reasons the common mushroom has changed very little over the three centuries that it has been in cultivation is that mushrooms are asexual, and so no selective breeding has been possible."
The most obvious reason to borrow genes is to benefit from the ingenuity of others as well as yourself. Sex brings together mutations, constantly rearranging genes into new combinations until fortuitous synergy results. One ancestor of a giraffe, for example, might have invented a longer neck while another invented longer legs: The two together were better than either alone: But this argument confuses consequence with cause. Its advantages are far too remote; they will appear after a few generations, by which time any asexual competitor will long ago have out-populated its sexual rivals. Besides, if sex is good at throwing together good combinations of genes, it will be even better at breaking them up. The one thing you can be sure about sexual creatures is that their offspring will be different from them, as many a Caesar, Bourbon, and Plantagenet discovered to their disappointment: Plant breeders much prefer varieties of wheat or corn that are male-sterile and produce seeds without sex because it enables them to be sure their good varieties will breed true.
It is almost the definition of sex that it breaks up combinations of genes. The great cry of the geneticists is that sex reduces
" linkage disequilibria: " What they mean is that if it were not for THE ENIGMA
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recombination, genes that are linked together—such as those for blue eyes and blond hair—would always be linked together, and nobody would ever have blue eyes and brown hair, or blond hair and brown eyes. Thanks to sex, the moment the fabled synergy is found, it is lost again: Sex disobeys that great injunction: "If it ain't broke, don 't fix it." Sex increases randomness."
In the late 1980s there was one last revival of interest in theories of "good" mutation: Mark Kirkpatrick and Cheryl Jenkins were interested not in two separate inventions but in the ability to invent the same thing twice. Suppose, for example, that blue eyes double fertility, so that people with blue eyes have twice as many children as people with brown eyes. And suppose that at first everybody has brown eyes. The first mutation in a brown-eyed person to blue eyes will have no effect because blue eyes are a recessive gene, and the dominant brown-eye gene on the person 's other chromosome will mask it: Only when the blue-eye genes of two of the descendants of the original mutant person come together will the great benefit of blue eyes be seen. Only sex would allow the people to mate and the genes to meet. This so-called segregation theory of sex is logical and uncontroversial. It is indeed one of the advantageous consequences of sex. Unfortunately, it is far too weak an effect to be the main explanation for sex 's prevalence. Mathematical models reveal that it would take five thousand generations to do its good work and asex would long since have won the game."
In recent years the geneticists have turned away from good mutations and begun to think about bad ones: Sex, they suggest, is a way of getting rid of bad mutations. This idea also has its origins in the 1960s, with Hermann Muller, one of the fathers of the Vicar of Bray theory Muller, who spent much of his career at the University of Indiana, published his first scientific paper on genes in 1911, and a veritable flood of ideas and experiments followed in the succeeding decades. In 1964 he had one of his greatest insights; it has come to be known as "Muller 's ratchet: " A simplified example of it goes like this: There are ten water fleas in a tank, only one of which is entirely free of mutations; the others all have one or several minor defects.
On average only five of the water fleas in each generation manage to
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The Red Queen
breed before they are eaten by a fish: The defect-free flea has a one-in-two chance of not breeding. So does the flea with the most defects, of course, but there is a difference: Once the defect-free flea is dead, the only way for it to be re-created is for another mutation to correct the mutation in a flea with a defect—a very unlikely possibility. The one with two defects can be re-created easily by a single mutation in a water flea with one defect anywhere among its genes.
In other words, the random loss of certain lines of descent will mean that the average number of defects gradually increases. Just as a ratchet turns easily one way but cannot turn back, so genetic defects inevitably accumulate. The only way to prevent the ratchet from turning is for the perfect flea to have sex and pass its defect-free genes to other fleas before it dies. i6
Muller 's ratchet applies if you use a photocopier to make a copy of a copy of a copy of a document. With each successive copy the quality deteriorates. Only if you guard the unblemished original can you regenerate a clean copy. But suppose the original is stored with the copies in a file and more copies are made when there is only one left in the file. You are just as likely to send out the original as to send out a copy. Once the original is lost, the best copy you can make is less good than it was before. But you can always make a worse copy just by copying the worst copy you have.
Graham Bell of McGill University has disinterred a curious debate that raged among biologists at the turn of the century about whether sex had a rejuvenating effect. What intrigued these early biologists was if and why a population of protozoa kept in a tank with sufficient food but given no chance to have sex inevitably fell into a gradual decline in vigor, size, and rate of (asexual) reproduction. Reanalyzing the experiments, Bell found some clear examples of Muller 's ratchet at work. Bad mutations gradually accumulated in the protozoa deprived of sex. The process was accelerated by the habit of this one group of protozoa, the ciliates, of keeping its germ-line genes in one place and keeping copies of them elsewhere for everyday use. The method of reproducing the copies is hasty and inaccurate, so defects accumulate especially fast there. During sex, one of the things the creatures do is throw away their copies THE ENIGMA
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and create new ones from the germ-line originals. Bell compares it with a chair maker who copies the last chair he made, errors and all, and returns to his original design only occasionally. Sex therefore does indeed have a rejuvenating effect: It enables these little animals to drop all the accumulated errors of an especially fast asexual ratchet whenever they have sex."
Bell's conclusion was a curious one. If a population is small (less than 10 billion) or the number of genes in the creature is very large, the ratchet has a severe effect on an asexual lineage. This is because it is easier to lose the defect-free class in a smaller population. So those creatures with larger genomes and relatively smaller populations (10 billion is twice as many people as there are on Earth) will be ratcheted into trouble fairly quickly. But those with few genes and vast populations are all right. Bell reckons that being sexual was a prerequisite for being big (and therefore few), or, con-versely, sex is unnecessary if you stay small. 38
Bell calculated the amount of sex—or, rather, of recombination—that is needed to halt the ratchet; for smaller creatures, less sex is necessary. Water fleas need to have sex only once every several generations. Human beings need to have sex in every generation: Moreover, as James Crow at the University of Wisconsin in Madison has suggested, Muller's ratchet may explain why budding is a relatively rare way of reproducing—especially among animals. Most asexual species still go to the trouble of growing their offspring from single cells (eggs). Why? Crow suggests it is because defects that would be fatal in a single cell can be easily smuggled into a bud. 39
If the ratchet is a problem only for big creatures, why do so many small ones have sex? Besides, to halt the ratchet requires only occasional episodes of sex; it does not require so many animals to abandon asexual reproduction altogether: Aware of these difficulties, in 1982 Alexey Kondrashov of the Research Computer Center in Poschino, near Moscow, came up with a theory that is a sort of reverse Muller 's ratchet. He argued that in an asexual population, every time a creature dies because of a mutation it gets rid of that mutation but no more. In a sexual population some of the creatures born have lots of mutations and some have few: If the ones with
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The Red Queen
lots of mutations die, then sex keeps throwing the ratchet into reverse, purging mutations: Since most mutations are harmful, this gives sex a great advantage.'°
But why purge mutations in this way rather than correct more of them by better proofreading? Kondrashov has an ingenious explanation of why this makes sense: The cost of making proofreading mechanisms perfect gets rapidly higher as you get nearer to perfection; in other words, it is like the law of diminishing returns: Allowing some mistakes through but having sex to purge them out may be cheaper:
Matthew Meselson, a distinguished molecular biologist, has come up with another explanation that expands on Kondrashov 's idea: Meselson suggests that "ordinary " mutations that change one letter for another in the genetic code are fairly innocuous because they can be repaired, but insertions—whole chunks of DNA that jump into the middle of genes—cannot be reversed so easily: These "selfish " insertions tend to spread like an infection, but sex defeats them, since sex segregates them into certain individuals whose deaths purge them from the population:"
Kondrashov is prepared to stand by an empirical test of his idea: He says that if the rate of deleterious mutations turns out to be more than one per individual per generation, then he is happy; if it proves to be less than one, then his idea is in trouble: The evidence so far is that the deleterious mutation rate teeters on the edge: It is about one per individual per generation in most creatures: But even supposing it is high enough, all that proves is that sex can perhaps play a role in purging mutations: It does not say that is why sex persists.' Z
Meanwhile, there are defects in the theory: It fails to explain how bacteria—of which some species rarely have sex and others not at all—nonetheless suffer from mutation at a low rate and make fewer proofreading mistakes when copying DNA: As one of Kondrashov 's critics put it, sex is "a cumbersome strange tool to have evolved for a housekeeping role: ""
And Kondrashov 's theory suffers from the same flaw as all genetic-repair theories and the Vicar of Bray himself: It works too THE ENIGMA
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slowly. Pitted against a clone of asexual individuals, a sexual population must inevitably be driven extinct by the clone 's greater productivity unless the clone 's genetic drawbacks can appear in time. It is a race against time. For how long? Curtis Lively of the University of Indiana has calculated that for every tenfold increase in population size, the advantage of sex is granted six more generations to show its effects or sex will lose the game. If there are a million individuals, sex has forty generations before it goes extinct; if a billion, it has eighty. Yet the genetic repair theories all require thousands of generations to do their work. Kondrashov's is certainly the fastest theory, but it is probably not fast enough."
There is still no purely genetic theory to explain sex that attracts wide support. An increasing number of students of evolution believe that the solution to the great enigma of sex lies in ecology, not genetics.
Chapter 3
THE POWER OF
PARASITES
The chessboard is the world; the pieces are the phenomena of the universe; the rules of the game are what we call the laws of Nature: The player on the other side is hidden from us: We know that his play is always fair, just, and patient: But also we know, to our cost, that he never overlooks a mistake or makes the small-est allowance for ignorance:
—Thomas Henry Huxley
Even for microscopic animals, the bdelloid rotifers are peculiar.
They live in any kind of fresh water, from puddles in your gutter to hot springs by the Dead Sea and ephemeral ponds on the Antarctic continent. They look like animated commas driven by what appear to be small waterwheels at the front of the body, and when their watery home dries up or freezes, they adopt the shape of an apostrophe and go to sleep. This apostrophe is known as a "tun," and it is astonishingly resistant to abuse. You can boil it for an hour or freeze it to within I degree of absolute zero—that is, to -272
degrees Centigrade—for a whole hour: Not only does it fail to dis-integrate, it does not even die: Tuns blow about the globe as dust so easily that rotifers are thought to travel regularly between Africa and America: Once thawed out, the tun quickly turns back into a rotifer, paddles its way about the pond with its bow wheels, eating bacteria as it goes, and within a few hours starts producing eggs that hatch into other rotifers. A bdelloid rotifer can fill a medium-sized lake with its progeny in just two months.
But there is another odd thing about bdelloids besides their feats of endurance and fecundity. No male bdelloid rotifer has ever been seen. As far as biologists can tell, every single member of every one of all five hundred species of bdelloid in the world is a female. Sex is simply not in the bdelloid repertoire.
It is possible that bdelloid rotifers mix others ' genes with their own by eating their dead comrades and absorbing some of their genes, or something bizarre like that,' but recent research by Matthew Meselson and David Welch suggests that they just never
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do have sex. They have found that the same gene in two different individuals can be up to 30 percent different at points that do not affect its function—a level of difference that implies bdelloids gave up sex between 40 million and 80 million years ago.'
There are many other species in the world that never have sex, from dandelions and lizards to bacteria and amoebas, but the bdelloids are the only example of a whole order of animal that entirely lacks the sexual habit: Perhaps as a result the bdelloids all look rather alike, whereas their relatives, the monogonont rotifers, tend to be much more varied; they cover the whole range of shapes of punctuation marks: Nonetheless, the bdelloids are a living rebuke to the conventional wisdom of biology textbooks—that without sex, evolution can barely happen and species cannot adapt to change: The existence of the bdelloid rotifers is, in the words of John Maynard Smith, " an evolutionary scandal: "'
THE ART OF BEING SLIGHTLY DIFFERENT
Unless a genetic mistake happens, a baby bdelloid rotifer is identical to its mother: A human baby is not identical CO its mother: That is the first consequence of sex: Indeed, according to most ecologists, it is the purpose of sex:
In 1966, George Williams exposed the logical flaw at the heart of the textbook explanation of sex: He showed how it required animals to ignore short-term self-interest in order to further the survival and evolution of their species, a form of self-restraint that could have evolved only under very peculiar circumstances: He was very unsure what to put in its place. But he noticed that sex and dispersal often seem to be linked. Thus, grass grows asexual runners to propagate locally but commits its sexually produced seeds to the wind to travel farther. Sexual aphids grow wings; asexual ones do not: The :suggestion that immediately follows is that if your young are going to have to travel abroad, then it is better that they vary because abroad may not be like home.'
Elaborating on that idea was the main activity throughout THE POWER OF PARASITES
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the 1970s of ecologists interested in sex. In 1971, in his first attack on the problem, John Maynard Smith suggested that sex was needed for those cases in which two different creatures migrate into a new habitat in which it helps to combine both their characters.' Two years later Williams returned to the fray and suggested that if most of the young are going to die, as most who try their luck as travelers will, then it may be the very fittest ones that will survive. It therefore matters not one bit how many young of average quality a creature has. What counts is having a handful of young that are exceptional. If you want your son to become pope, the best way to achieve this is not to have lots of identical sons but to have lots of different sons in the hope that one is good, clever, and religious enough.'
The common analogy for what Williams was describing is a lottery. Breeding asexually is like having lots of lottery tickets all with the same number. To stand a chance of winning the lottery, you need lots of different tickets. Therefore, sex is useful to the individual rather than the species when the offspring are likely to face changed or unusual conditions.
Williams was especially intrigued by creatures such as aphids and monogonont rotifers, which have sex only once every few generations. Aphids multiply during the summer on a rose-bush, and monogonont rotifers multiply in a street puddle. But when the summer comes to an end, the last generation of aphids or of monogonont rotifers is entirely sexual: It produces males and females that seek each other out, mate, and produce tough little young that spend the winter or the drought as hardened cysts awaiting the return of better conditions. To Williams this looked like the operation of his lottery. While conditions were favorable and predictable, it paid to reproduce as fast as possible—asexually.
When the little world came to an end and the next generation of aphid or rotifer faced the uncertainty of finding a new home or waited for the old one to reappear, then it paid to produce a variety of different young in the hope that one would prove ideal.
Williams contrasted the "aphid-rotifer model " with two others: the strawberry-coral model and the elm-oyster model.
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Strawberry plants and the animals that build coral reefs sit in the same place all their lives, but they send out runners or coral branches so that the individual and its clones gradually spread over the surrounding space: However, when they want to send their young much farther away, in search of a new, pristine habitat, the strawberries produce sexual seeds and the corals produce sexual larvae called "planulae." The seeds are carried away by birds; the planulae drift for many days on the ocean currents: To Williams, this looked like a spatial version of the lottery: Those who travel far-thest are most likely to encounter different conditions, so it is best that they vary in the hope that one or two of them will suit the place they reach. Elm trees and oysters, which are sexual, produce millions of tiny young that drift on breezes or ocean currents until a few are lucky enough to land in a suitable place and begin a new life. Why do they do this? Because, said Williams, both elms and oysters have saturated their living space already. There are few clearings in an elm forest and few vacancies on an oyster bed. Each vacancy will attract many thousands of applicants in the form of new seeds or larvae: Therefore, it does not matter that your young are good enough to survive. What matters is whether they are the very best. Sex gives variety, so sex makes a few of your offspring exceptional and a few abysmal, whereas asex makes them all average:'
THE TANGLED BANK
Williams's proposition has reappeared in many guises over the years, under many names and with many ingenious twists. In general, however, the mathematical models suggest that these lottery models only work if the prize that rewards the right lottery ticket is indeed a huge jackpot. Only if a very few of the dispersers survive and do spectacularly well does sex pay its way. In other cases, it does not.'
Because of this limitation, and because most species are not necessarily producing young that will migrate elsewhere, few ecolo-THE POWER OF PARASITES
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gists wholeheartedly adopted lottery theories. But it was not until Graham Bell in Montreal asked, like the apocryphal king and the goldfish, to see the actual evidence for the pattern the lottery model was designed to explain that the whole edifice tumbled down: Bell set out to catalog species according to their ecology and their sexuality: He was trying to find the correlation between ecological uncertainty and sexuality that Williams and Maynard Smith had more or less assumed existed. So he expected to find that animals and plants were more likely to be sexual at higher latitudes and altitudes (where weather is more variable and conditions harsher); in fresh water rather than the sea (because fresh water varies all the time, flooding, drying up, heating up in summer, freezing in winter, and so on, whereas the sea is predictable); among weeds that live in disturbed habitats; and in small creatures rather than large ones.
He found exactly the opposite. Asexual species tend to be small and live at high latitudes and high altitudes, in fresh water or disturbed ground. They live in unsaturated habitats where harsh, unpredictable conditions keep populations from reaching full capacity.
Indeed, even the association between sex and hard times in aphids and rotifers turns out to be a myth. Aphids and monogonont rotifers both turn sexual not when winter or drought threaten but when overcrowding affects the food supply. You can make them turn sexual in the laboratory just by letting them get too crowded.
Bell's verdict on the lottery model was scathing: "Accepted, at least as a conceptual foundation, by the best minds which have contemplated the function of sexuality, it seems utterly to fail the test of comparative analysis. "'
Lottery models predict that sex should be most common where in fact it is rarest—among highly fecund, small creatures in changeable environments. On the contrary, here sex is the exception; but in big, long-lived,: slow-breeding creatures in stable environments sex is the rule:
This was a bit unfair toward Williams, whose "elm-oyster model " had at least predicted that fierce competition between saplings for space was the reason elms were sexual: Michael Ghiselin developed this idea further in 1974 and made some telling
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analogies with economic trends. As Ghiselin put it, "In a saturated economy, it pays to diversify. " Ghiselin suggested that most creatures compete with their brothers and sisters, so if everybody is a little different from their brothers and sisters, then more can survive. The fact that your parents thrived doing one thing means that it will probably pay to do something else because the local habitat might well be full already with your parents ' friends or relatives doing their thing.'°
Graham Bell has called this the "tangled bank" theory, after the famous last paragraph of Charles Darwin's Origin of Species: "It is interesting to contemplate an entangled bank, clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other and dependent upon each other in so complex a manner, have all been produced by laws acting around us:"
Bell used the analogy of a button maker who has no competitors and has already supplied buttons to most of the local market. What does he do? He could either continue selling replace-ments for buttons or he could diversify the range of his buttons and try to expand the market by encouraging his customers to buy all sorts of different kinds of buttons. Likewise, sexual organisms in saturated environments, rather than churning out more of the same offspring, would be better off varying them a bit in the hope of producing offspring that could avoid the competition by adapting to a new niche: Bell concluded from his exhaustive survey of sex and asex in the animal kingdom that the tangled bank was the most promising of the ecological theories for sex.' Z
The tangled bankers had some circumstantial evidence for their idea, which came from crops of wheat and barley. Mixtures of different varieties generally yield more than a single variety does; plants transplanted to different sites generally do worse than in their home patches, as if genetically suited to their home ground; if allowed to compete with one another in a new site, plants derived from cuttings or tillers generally do worse than plants derived from sexual seed, as if sex provides some sort of variable advantage."
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The trouble is, all these results are also predicted by rival theories just as plausibly. Williams wrote: "Fortune will be benevo-lent indeed if the inference from one theory contradicts that of another."" This is an especially acute problem in the debate. One scientist gives the analogy of somebody trying to decide what makes his driveway wet: rain, lawn sprinklers, or flooding from the local river. It is no good turning on the sprinkler and observing that it wets the drive or watching rain fall and seeing that it wets the drive." To conclude anything from such observations would be to fall into the trap that philosophers call " the fallacy of affirming the consequent. " Because sprinklers can wet the drive does not prove that they did wet the drive. Because the tangled bank is consistent with the facts does not prove it is the cause of the facts.
It is hard to find dedicated enthusiasts of tangled banks these days. Their main trouble is a familiar one: If it ain' t broke, why does sex need to fix it? An oyster that has grown large enough to breed is a great success, in oyster terms. Most of its siblings are dead: If, as tangled bankers assume, the genes had something to do with that, then why must we automatically assume that the combination of genes that won in this generation will be a flop in the next? There are ways around this difficulty for tangled bankers, but they sound a bit like special pleading: It is easy enough to identify an individual case where sex would have some advantage, but to raise it to a general principle for every habitat of every mammal and bird, for every coniferous tree, a principle that can give a big enough advantage to overcome the fact that asex is twice as fecund as sex—nobody can quite bring himself to do that: There is a more empirical objection to the tangled bank theory. Tangled banks predict a greater interest in sex in those animals and plants that have many small offspring that then compete with one another than among the plants and animals that have few large young. Superficially, the effort devoted to sex has little to do with how small the offspring are. Blue whales, the biggest animals, have huge young—each may weigh five tons or more. Giant sequoias, the biggest plants, have tiny seeds, so small that the ratio of their weight to the weight of the tree is the same as the ratio of
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the tree to the planet Earth. 16 Yet both are sexual creatures. By contrast, an amoeba, which splits in half when it breeds, has an enormous " young" as big as "itself: " Yet it never has sex.
A student of Graham Bell 's named Austin Burt went out and looked at the real world to see if the tangled bank fitted the facts. He looked not at whether mammals have sex but at how much recombination goes on among their genes. He measured this quite easily by counting the number of "crossovers " on a chromosome: These are spots where, quite literally, one chromosome swaps genes with another: What Burt found was that among mammals the amount of recombination bears no relation to the number of young, little relation to body size, and close relation to age at maturity: In other words, long-lived, late-maturing mammals do more genetic mixing regardless of their size or fecundity than short-lived, early maturing mammals: By Burt 's measure, man has thirty crossovers, rabbits ten, and mice three. Tangled-bank theories would predict the opposite:"
The tangled bank also conflicted with the evidence from fossils: In the 1970s evolutionary biologists realized that species do not change much. They stay exactly the same for thousands of generations, to be suddenly replaced by other forms of life. The tangled bank is a gradualist idea: If tangled banks were true, then species would gradually drift through the adaptive landscape, changing a little in every generation, instead of remaining true to type for millions of generations. A gradual drifting away of a species from its previous form happens on small islands or in tiny populations precisely because of effects somewhat analogous to Muller ' s ratchet: the chance extinction of some forms and the chance prosperity of other, mutated forms: In larger populations the process that hinders this is sex itself, for an innovation is donated to the rest of the species and quickly lost in the crowd. In island populations sex cannot do this precisely because the population is so inbred: 18
It was Williams who first pointed out that a huge false assumption lay, and indeed still, lies, at the core of most popular treatments of evolution. The old concept of the ladder of progress THE POWER OF PARASITES
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still lingers on in the form of a teleology: Evolution is good for species, and so they strive to make it go faster. Yet it is stasis, not change, that is the hallmark of evolution. Sex and gene repair and the sophisticated screening mechanisms of higher animals to ensure that only defect-free eggs and sperm contribute to the next generation—all these are ways of preventing change. The coelacanth, not the human, is the triumph of genetic systems because it has remained faithfully true to type for millions of generations despite endless assaults on the chemicals that carry its heredity: The old
"Vicar of Bray " model of sex, in which sex is an aid to faster evolution, implies that organisms would prefer to keep their mutation rate fairly high—since mutation is the source of all variety—and then do a good job of sieving out the bad ones: But, as Williams put it, there is no evidence yet found that any creature ever does anything other than try to keep its mutation rate as low as possible.
It strives for a mutation rate of zero: Evolution depends on the fact that it fails. 19
Tangled banks work mathematically only if there is a sufficient advantage in being odd: The gamble is that what paid off in one generation will not pay off in the next and that the longer the generation, the more this is so—which implies that conditions keep changing.
THE RED QUEEN
Enter, running, the Red Queen. This peculiar monarch became part of biological theory twenty years ago and has been growing ever more important in the years since then: Follow me if you will into a dark labyrinth of stacked shelves in an office at the University of Chicago, past ziggurats of balanced books and three-foot Babels of paper. Squeeze between two filing cabinets and emerge into a Sty-gian space the size of a broom cupboard, where sits an oldish man in a checked shirt and with a gray beard that is longer than God 's but not so long as Charles Darwin 's. This is the Red Queen's first prophet, Leigh Van Valen, a single-minded student of evolution.
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One day in 1973, before his beard was so gray, Van Valen was searching his capacious mind for a phrase to express a new discovery he had made while studying marine fossils. The discovery was that the probability a family of animals would become extinct does not depend on how long that family has already existed. In other words, species do not get better at surviving (nor do they grow feeble with age, as individuals do). Their chances of extinction are random.
The significance of this discovery had not escaped Van Valen, for it represented a vital truth about evolution that Darwin had not wholly appreciated. The struggle for existence never gets easier. However well a species may adapt to its environment, it can never relax, because its competitors and its enemies are also adapting to their niches., Survival is a zero-sum game. Success only makes one species a more tempting target for a rival species. Van Valen's mind went back to his childhood and lit upon the living chess pieces that Alice encountered beyond the looking glass. The Red Queen is a formidable woman who runs like the wind but never seems to get anywhere:
" Well, in our country," said Alice, still panting a little, " you'd generally get to somewhere else—if you ran very fast for a long time as we've been doing: "
" A slow sort of country! " said the Queen. " Now, here,
you see, it takes all the running you can do to keep in the same place: If you want to get to somewhere else, you must run at least twice as fast as that! "20
"A new evolutionary law, " wrote Van Valen, who sent a man-uscript to each of the most prestigious scientific journals, only to see it rejected. Yet his claim was justified. The Red Queen has become a great personage in the biological court. And nowhere has she won a greater reputation than in theories of sex. 11
Red Queen theories hold that the world is competitive to the death. It does keep changing. But did we not just hear that species are static for many generations and do not change? Yes. The THE POWER OF PARASITES
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point about the Red Queen is that she runs but stays in the same place. The world keeps coming back to where it started; there is change but not progress.
Sex, according to the Red Queen theory, has nothing to do with adapting to the inanimate world—becoming bigger or better camouflaged or more tolerant of cold or better at flying—but is all about combating the enemy that fights back.
Biologists have persistently overestimated the importance of physical causes of premature death rather than biological ones. In virtually any account of evolution, drought, frost, wind, or starvation looms large as the enemy of life. The great struggle, we are told, is to adapt to these conditions. Marvels of physical adaptation—the camel's hump, the polar bear 's fur, the rotifer 's boil-resistant tun—
are held to be among evolution' s greatest achievements. The first ecological theories of sex were all directed at explaining this adapt-ability to the physical environment. But with the tangled bank, a different theme has begun to be heard, and in the Red Queen 's march it is the dominant tune. The things that kill animals or prevent them from reproducing are only rarely physical factors. Far more often other creatures are involved—parasites, predators, and competitors.
A water flea that is starving in a crowded pond is the victim not of food shortage but of competition: Predators and parasites probably cause most of the world 's deaths, directly or indirectly. When a tree falls in the forest, it has usually been weakened by a fungus. When a herring meets its end, it is usually in the mouth of a bigger fish or a in a net. What killed your ancestors two centuries or more ago?
Smallpox, tuberculosis, influenza, pneumonia, plague, scarlet fever, diarrhea. Starvation or accidents may have weakened people, but infection killed them. A few of the wealthier ones died of old age or 22
cancer or heart attacks, but not many.
The "great war " of 1914—18 killed 25 million people in four years. The influenza epidemic that followed killed 25 million in four months.23 It was merely the latest in a series of devastating plagues to hit the human species after the dawn of civilization.
Europe was laid waste by measles after A:D. 165, by smallpox after A.D. 251, by bubonic plague after 1348, by syphilis after 1492, and
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by tuberculosis after 1800." And those are just the epidemics.
Endemic diseases carried away additional vast numbers of people.
Just as every plant is perpetually under attack from insects, so every animal is a seething mass of hungry bacteria waiting for an opening. There may be more bacterial than human cells in the object you proudly call " your " body. There may be more bacteria in and on you as you read this than there are human beings in the whole world.
Again and again in recent years evolutionary biologists have found themselves returning to the theme of parasites. As Richard Dawkins put it in a recent paper: "Eavesdrop [over] morning coffee at any major centre of evolutionary theory today, and you will find 'parasite ' to be one of the commonest words in the language.
Parasites are touted as the prime movers in the evolution of sex, promising a final solution to that problem of problems."
Parasites have a deadlier effect than predators for two reasons. One is that there are more of them. Human beings have no predators except great white sharks and one another, but they have lots of parasites: Even rabbits, which are eaten by stoats, weasels, foxes, buzzards, dogs, and people, are host to far more fleas, lice, ticks, mosquitoes, tapeworms, and uncounted varieties of protozoa, bacteria, fungi, and viruses. The myxomatosis virus has killed far more rabbits than have foxes. The second reason, which is the cause of the first, is that parasites are usually smaller than their hosts, while predators are usually larger. This means that the parasites live shorter lives and pass through more generations in a given time than their hosts. The bacteria in your gut pass through six times as many generations during your lifetime as people have passed through since they were apes.26 As a consequence, they can multiply faster than their hosts and control or reduce the host population: The predator merely follows the abundance of its prey.
Parasites and their hosts are locked in a close evolutionary embrace: The more successful the parasite 's attack (the more hosts it infects or the more resources it gets from each), the more the host 's chances of survival will depend on whether it can invent a defense. The better the host defends, the more natural selection will promote the parasites that can overcome the defense. So the THE POWER OF PARASITES
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advantage will always be swinging from one to the other: The more dire the emergency for one, the better it will fight: This is truly the world of the Red Queen, where you never win, you only gain a temporary respite.
BATTLES OF WIT
It is also the inconstant world of sex. Parasites provide exactly the incentive to change genes every generation that sex seems to demand: The success of the genes that defended you so well in the last generation may be the best of reasons to abandon these same gene combinations in the next. By the time the next generation comes around, the parasites will have surely evolved an answer to the defense that worked best in the last generation: It is a bit like sport: In chess or in football, the tactic that proves most effective is soon the one that people learn to block easily. Every innovation in attack is soon countered by another in defense.
But of course the usual analogy is an arms race, America builds an atom bomb, so Russia does, too. America builds missiles; so must Russia: Tank after tank, helicopter after helicopter, bomber after bomber, submarine after submarine, the two countries run against each other, yet stay in the same place: Weapons that would have been invincible twenty years before are now vulnerable and obsolete. The bigger the lead of one superpower, the harder the other tries to catch up: Neither dares step off the treadmill while it can afford to stay in the race. Only when the economy of Russia collapses does the arms race cease (or pause):"
These arms race analogies should not be taken too seriously, but they do lead to some interesting insights. Richard Dawkins and John Krebs raised one argument derived from arms races to the level of a "principle": the " life-dinner principle. " A rabbit running from a fox is running for its life, so it has the greater evolutionary incentive to be fast: The fox is merely after its dinner: True enough, but what about a gazelle running from a cheetah? Whereas foxes eat things other than rabbits, cheetahs eat only gazelles. A slow gazelle might never be unlucky enough to meet a cheetah, but a slow chee-
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tah that never catches anything dies. So the downside is greater for the cheetah. As Dawkins and Krebs put it, the specialist will usually win the race."
Parasites are supreme specialists, but arms race analogies are less reliable for them. The flea that lives in the cheetah 's ear has what economists call an " identity of interest " with the cheetah: If the cheetah dies, the flea dies. Gary Larson once drew a cartoon of a flea walking through the hairs on a dog 's back carrying a placard that read: THE END OF THE DOG IS NEAR: The death of the dog is bad news for the flea, even if the flea hastened it. The question of whether parasites benefit from harming their hosts has vexed para -
sitologists for many years. When a parasite first encounters a new host (myxomatosis in European rabbits, AIDS in human beings, plague in fourteenth-century Europeans) it usually starts off as extremely virulent and gradually becomes less so. But some diseases remain fatal, while others quickly become almost harmless: The explanation is simple: The more contagious the disease, and the fewer resistant hosts there are around, the easier it will be to find a new host. So contagious diseases in unresistant populations need'
not worry about killing their hosts, because they have already moved on. But when most potential hosts are already infected or resistant, and the parasite has difficulty moving from host to host, it must take care not to kill its own livelihood: In the same way an industrial boss who pleads with his workers, " Please don't strike or the company will go bust, " is likely to be more persuasive if unem-ployment is high than if the workers already have other job offers.
Yet, even where virulence declines, the host is still being hurt by the parasite and is still under pressure to improve its defenses, while the parasite is continually trying to get around those defenses and sequester more resources to itself at the host 's expense.'
ARTIFICIAL VIRUSES
Startling proof of the fact that parasites and hosts are locked in evolutionary arms races has come from a surprising source: the innards of computers: In the late 1980s evolutionary biologists THE POWER OF PARASITES
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began to notice a new discipline growing among their more computer-adept colleagues called artificial life: Artificial life is a hubristic name for computer programs that are designed to evolve through the same process of replication, competition, and selection as real life: They are, in a sense, the ultimate proof that life is just a matter of information and that complexity can result from directionless competition, design from randomness.
If life is information and life is riddled with parasites, then information, too, should be vulnerable to parasites. When the history of computers comes to be written, it is possible that the first program to earn the appellation "artificially alive " will be a deceptively simple little two-hundred-line program written in 1983 by Fred Cohen, a graduate student at the California Institute of Technology. The program was a "virus" that would insinuate copies of itself into other programs in the same way a real virus insinuates copies of itself into other hosts. Computer viruses have since become a worldwide problem. It begins to look as if parasites are inevitable in any system of life.'
But Cohen's virus and its pesky successors were created by people. It was not until Thomas Ray, a biologist at the University of Delaware, conceived an interest in artificial life that computer parasites first appeared spontaneously. Ray designed a system called Tierra that consisted of competing programs that were constantly being filled by mutation with small errors. Successful programs would thrive at one another 's expense: The effect was astonishing. Within Tierra, programs began to evolve into shorter versions of themselves. Programs that were seventy-nine instructions long began to replace the original eighty-instruction programs: But then suddenly there appeared versions of the program just forty-five instructions long: They borrowed half of the code they needed from longer programs. These were true parasites. Soon a few of the longer programs evolved what Ray called immunity to parasites: One program became impregnable to the attentions of one parasite by concealing part of: itself. But the parasites were not beaten. A mutant parasite appeared in the soup that could find the concealed lines."
And so the arms race escalated: Sometimes when he ran the
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computer, Ray was confronted with spontaneously appearing hyperparasites, social hyperparasites, and cheating hyper-hyperparasites—all within an evolving system of (initially) ridiculous simplicity. He had discovered that the notion of a host-parasite arms race is one of the most basic and unavoidable consequences of evolution."
Arms race analogies are flawed, though. In a real arms race, an old weapon rarely regains its advantage. The day of the longbow will not come again. In the contest between a parasite and its host, it is the old weapons, against which the antagonist has forgotten how to defend, that may well be the most effective. So the Red Queen may not stay in the same place so much as end up where she started from, like Sisyphus, the fellow condemned to spend eternity rolling a stone up a hill in Hades only to see it roll down again.
There are three ways for animals to defend their bodies against parasites. One is to grow and divide fast enough to leave them behind. This is well known to plant breeders, for example: The tip of the growing shoot into which the plant is putting all its resources is generally free of parasites. Indeed, one ingenious theory holds that sperm are small specifically so they have no room to carry bacteria with them to infect eggs." A human embryo indulges in a frenzy of cell division soon after it is fertilized, perhaps to leave behind any viruses and bacteria stuck in one of the compart-ments. The second defense is sex, of which more anon. The third is an immune system, used only by the descendants of reptiles. Plants and many insects and amphibians have an additional method: chemical defense. They produce chemicals that are toxic to their pests.
Some species of pests then evolve ways of breaking down the tox-ins, and so on. An arms race has begun.
Antibiotics are chemicals produced naturally by fungi to kill their rivals: bacteria. But when man began to use antibiotics, he found that, with disappointing speed, the bacteria were evolving the ability to resist the antibiotics. There were two startling things about antibiotic resistance in pathogenic bacteria. One, the genes for resistance seemed to jump from one species to another, from harmless gut bacteria to pathogens, by a form of gene transfer not THE POWER OF PARASITES
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unlike sex. And two, many of the bugs seemed to have the resistance genes already on their chromosomes; it was just a matter of reinventing the trick of switching them on. The arms race between bacteria and fungi has left many bacteria with the ability to fight antibiotics, an ability they no longer " thought they would need "
when inside a human gut.
Because they are so short-lived compared with their hosts, parasites can be quicker to evolve and adapt. In about ten years, the genes of the AIDS virus change as much as human genes change in 10 million years. For bacteria, thirty minutes can be a lifetime.
Human beings, whose generations are an eternal thirty years long, are evolutionary tortoises.
PICKING DNA'S LOCKS
Evolutionary tortoises nonetheless do more genetic mixing than evolutionary hares. Austin Burt's discovery of a correlation between generation length and amount of recombination is evidence of the Red Queen at work. The longer your generation time, the more genetic mixing you need to combat your parasites." Bell and Burt also discovered that the mere presence of a rogue parasitic chromosome called a "B-chromosome" is enough to induce extra recombination (more genetic mixing) in a species." Sex seems to be an essential part of combating parasites. But how?
Leaving aside for the moment such things as fleas and mosquitoes, let us concentrate on viruses, bacteria, and fungi, the causes of most diseases. They specialize in breaking into cells—either to eat them, as fungi and bacteria do, or, like viruses, to subvert their genetic machinery for the purpose of making new viruses: Either way, they must get into cells. To do that they employ protein molecules that fit into other molecules on cell surfaces; in the jargon, they "bind. " The arms races between parasites and their hosts are all about these binding proteins. Parasites invent new keys; hosts change the locks. There is an obvious group-selectionist argument here for sex: At any one time a sexual species will have
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lots of different locks; members of an asexual one will all have the same locks. So a parasite with the right key will quickly exterminate the asexual species but not the sexual one: Hence, the well-known fact: By turning our fields over to monocultures of increasingly inbred strains of wheat and maize, we are inviting the very epidemics of disease that can only be fought by the pesticides we are forced to use in ever larger quantities. i6
The Red Queen 's case is both subtler and stronger than that, though: It is that an individual, by having sex, can produce offspring more likely to survive than an individual that produces clones of itself: The advantage of sex can appear in a single generation: This is because whatever lock is common in one generation will produce among the parasites the key that fits it: So you can be sure that it is the very lock not to have a few generations later, for by then the key that fits it will be common: Rarity is at a premium.
Sexual species can call on a sort of library of locks that is unavailable to asexual species. This library is known by two long words that mean roughly the same thing: heterozygosity and polymorphism: They are the things that animals lose when their lineage becomes inbred. What they mean is that in the population at large (polymorphism) and in each individual as well (heterozygosity) there are different versions of the same gene at any one time. The
" polymorphic" blue and brown eyes of Westerners are a good example: Many brown-eyed people carry the recessive gene for blue eyes as well; they are heterozygous. Such polymorphisms are almost as puzzling as sex to true Darwinists because they imply that one gene is as good as the other. Surely, if brown eyes were marginally better than blue (or, more to the point, if normal genes were better than sickle-cell-anemia genes), then one would gradually have driven the other extinct. So why on earth are we stuffed full of so many different versions of genes? Why is there so much heterozygosity?
In the case of sickle-cell anemia it is because the sickle gene helps to defeat malaria, so the heterozygotes (those with one normal gene and one sickle gene) are better off than those with normal genes where malaria is common, whereas the homozygotes (those with two normal genes or two sickle genes) suffer from malaria and anemia respectively."
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This example is so well worn from overuse in biology textbooks that it is hard to realize it is not just another anecdote but an example of a common theme. It transpires that many of the most notoriously polymorphic genes, such as the blood groups, the histocompatibility antigens and the like, are the very genes that affect resistance to disease—the genes for locks: Moreover, some of these polymorphisms are astonishingly ancient; they have persisted for geological eons: For example, there are genes that have several versions in mankind, and the equivalent genes in cows also have several versions. But what is bizarre is that the cows have the very same versions of the genes as mankind. This means that you might have a gene that is more like the gene of a certain cow than it is like the equivalent gene in your spouse: This is considerably more astonishing than it would be to discover that the word for, say, "meat" was viande in France, fleisch in Germany, viande again in one uncontacted Stone Age village in New Guinea, and fleisch in a neighboring village.
Some very powerful force is at work ensuring that most versions of each gene survive and that no version changes very much. 3B
That force is almost certainly disease: As soon as a lock gene becomes rare, the parasite key gene that fits it becomes rare, so that lock gains an advantage: In a case where rarity is at a premium, the advantage is always swinging from one gene to another, and no gene is ever allowed to become extinct. To be sure, there are other mechanisms that can favor polymorphism: anything that gives rare genes a selective advantage over common genes: Predators often give rare genes a selective advantage by overlooking rare forms and picking out common forms. Give a bird in a cage some concealed pieces of food, most of which are painted red but a few painted green; it will quickly get the idea that red things are edible and will initially overlook green things: J: B. S Haldane was the first to realize that parasitism, even more than predation, could help to maintain polymorphism, especially if the parasite 's increased success in attacking a new variety of host goes with reduced success against an old variety—which would be the case with keys and locks:'°
The key and lock metaphor deserves closer scrutiny: In flax, for example, there are twenty-seven versions of five different genes that confer resistance to a rust fungus: twenty-seven versions of
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five locks. Each lock is fitted by several versions of one key gene in the rust. The virulence of the rust fungus attack is determined by how well its five keys fit the flax 's five locks. It is not quite like real keys and locks because there are partial fits: The rust does not have to open every lock before it can infect the flax. But the more locks it opens, the more virulent its effects.°
THE SIMILARITY BETWEEN SEX AND VACCINATION
At this point the alert know-it-alls among you will be seething with impatience at my neglect of the immune system. The normal way to fight a disease, you may point out, is not to have sex but to produce antibodies, by vaccination or whatever. The immune system is a fairly recent invention in geological terms. It started in the reptiles perhaps 300 million years ago. Frogs, fish, insects, lobsters, snails, and water fleas do not have immune systems. Even so, there is now an ingenious theory that marries the immune system with sex in an overarching Red Queen hypothesis. Hans Bremermann of the University of California at Berkeley is its author, and he makes a fascinating case for the interdependence of the two: The immune system, he points out, would not work without sex."
The immune system consists of white blood cells that come in about 10 million different types. Each type has a protein lock on it called an "antibody," which corresponds to a key carried by a bacterium called an "antigen: " If a key enters that lock, the white cell starts multiplying ferociously in order to produce an army of white cells to gobble up the key-carrying invader, be it a flu virus, a tuberculosis bacterium, or even the cells of a transplanted heart.
But the body has a problem. It cannot keep armies of each antibody-lock ready to immobilize all types of keys because there is simply no room for millions of different types, each represented by millions of individual cells. So it keeps only a few copies of each white cell. As soon as one type of white cell meets the antigen that fits its locks, it begins multiplying. Hence the delay between the onset of flu and the immune response that cures it.
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Each lock is generated by a sort of random assembly device that tries to maintain as broad a library of kinds of lock as it can, even if some of the keys that fit them have not yet been found in parasites: This is because the parasites are continually changing their keys to try to find ones that fit the host 's changing locks: The immune system is therefore prepared. But this randomness means that the host is bound to produce white cells that are designed to attack its own cells among the many types it invents.
To get around this, the host 's own cells are equipped with a password, which is known as a major histocompatibility antigen. This stops the attack. (Please excuse the mixed metaphor—keys and locks and passwords; it does not get any more mixed.) To win, then, the parasite must do one of the following: infect somebody else by the time the immune response hits (as flu does), conceal itself inside host cells (as the AIDS virus does), change its own keys frequently (as malaria does), or try to imitate whatever password the host 's own cells carry that enable them to escape attention. Bilharzia parasites, for example, grab password molecules from host cells and stick them all over their bodies to camouflage themselves from passing white cells. Trypanosomes, which cause sleeping sickness, keep changing their keys by switching on one gene after another. The AIDS virus is craftiest of all.
According to one theory, it seems to keep mutating so that each generation has different keys. Time after time the host has locks that fit the keys and the virus gets suppressed. But eventually, after perhaps ten years, the virus 's random mutation hits upon a key that the host does not have a lock for. At that point the virus has won.
It has found the gap in the repertoire of the immune system ' s locks and runs riot. In essence, according to this theory, the AIDS virus evolves until it finds a chink in the body 's immune armor.42
Other parasites try to mimic the passwords carried by the host: The selective pressure is on all pathogens to mimic the passwords of their hosts. The selective pressure is on all hosts to keep changing the password. This, according to Bremermann, is where sex comes in:
The histocompatibility genes, which determine more than
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the passwords but are themselves responsible for susceptibility to disease, are richly polymorphic. There are over one hundred versions of each histocompatibility gene in the average population of mice, and even more in human beings. Every person carries a unique combination, which is why transplants between people other than identical twins are rejected unless special drugs are taken. And without sexual outbreeding, it is impossible to maintain that polymorphism.
Is this conjecture or is there proof? In 1991, Adrian Hill and his colleagues at Oxford University produced the first good evidence that the variability of histocompatibility genes is driven by disease: They found that one kind of histocompatibility gene, HLA-Bw53, is frequent where malaria is common and very rare elsewhere. Moreover, children ill with malaria generally do not have HLA-Bw53. That may be why they are
And in an extraordinary
discovery made by Wayne Potts of the University of Florida at Gainesville, house mice appear to choose as mates only those house mice that have different histocompatibility genes from their own.
They do this by smell. This preference maximizes the variety of genes in mice and makes the young mice more disease-resistant."
WILLIAM HAMILTON AND PARASITE POWER
That sex, polymorphism, and parasites have something to do with one another is an idea with many fathers. With characteristic pre-science, J: B. S: Haldane got most of the way there: "I wish to suggest that [heterozygosity] may play a part in disease resistance, a particular race of bacteria or virus being adapted to individuals of a certain range of biochemical constitutions, while the other constitutions are relatively resistant. " Haldane wrote that in 1949, four years before the structure of DNA was elucidated." An Indian colleague of Haldane's, Suresh Jayakar, got even closer a few years later.46 Then the idea lay dormant for many years, until the late 1970s when five people came up with the same notion independently of one another within the space of a few years: John Jaenike of THE POWER OF PARASITES
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Rochester, Graham Bell of Montreal, Hans Bremermann of Berkeley, John Tooby of Harvard, and Bill Hamilton of Oxford:"
But it was Hamilton who pursued the connection between sex and disease most doggedly and became most associated with it.
In appearance, Hamilton was an almost implausibly perfect example of the absentminded professor as he stalked through the streets of Oxford, deep in thought, his spectacles attached umbilically to a string around his neck, his eyes fixed on the ground in front of him.
His unassuming manner and relaxed style of writing and storytelling were deceptive. Hamilton had a habit of being at the right place in biology at the right time. In the 196os he molded the theory of kin selection—the idea that much of animal cooperation and altruism is explained by the success of genes that cause animals to look after close relatives because they share many of the same genes. Then in 1967 he stumbled on the bizarre internecine warfare of the genes that we shall meet in chapter 4. By the 198os he was anticipating most of his colleagues in pronouncing reciprocity as the key to human cooperation: Again and again in this book we will find we are treading in Hamilton's footsteps! 8
With the help of two colleagues from the University of Michigan, Hamilton built a computer model of sex and disease, a slice of artificial life. It began with an imaginary population of two hundred creatures. They happened to be rather like humans—each began breeding at fourteen, continued until thirty-five or so, and had one offspring every year. But the computer then made some of them sexual—meaning two parents had to produce and rear each child— and some of them asexual: Death was random: As expected, the sexual race quickly became extinct every time they ran the computer. In a game between sex and asex, asex always won, other things being equal: ;9
Next, they introduced several species of parasites, two hundred of each, whose power depended on "virulence genes " matched by "resistance genes" in the hosts. The least resistant hosts and the least virulent parasites were killed in each generation: Now the asexual race no longer had an automatic advantage. Sex often won the game, mostly if there were lots of genes that determined resistance and virulence in each creature.
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What kept happening in the model, as expected, was that resistance genes that worked got more common, then virulence genes that undid those resistance genes got more common in turn, so those resistance genes grew rare again, followed by the virulence genes. As Hamilton put it, "Antiparasite adaptations are in constant obsolescence: " But instead of the unfavored genes being driven to extinction, as happened to the asexual species, once rare, they stopped getting rarer; they could therefore be brought back. " The essence of sex in our theory, " wrote Hamilton, "is that it stores genes that are currently bad but have promise for reuse. It continually tries them in combination, waiting for the time when the focus of disadvantage has moved elsewhere. " There is no permanent ideal of disease resistance, merely the shifting sands of impermanent obsolescence:'°
When it runs the simulations, Hamilton's computer screen fills with a red transparent cube inside which two lines, one green and one blue, chase each other like fireworks on a slow-exposure photograph: What is happening is that the parasite is pursuing the host through genetic "space," or, to put it more precisely, each axis of the cube represents different versions of the same gene, and the host and the parasite keep changing their gene combinations.
About half the time the host eventually ends up in one corner of the cube, having run out of variety in its genes, and stays there.
Mutation mistakes are especially good at preventing it from doing that, but even without them it will do so spontaneously. What happens is entirely unpredictable even though the starting conditions are ruthlessly "deterministic"—there is no element of chance.
Sometimes the two lines pursue each other on exactly the same steady course around the edge of the cube, gradually changing one gene for fifty generations, then another, and so on. Sometimes strange waves and cycles appear. Sometimes there is pure chaos: The two lines just fill the cube with colored spaghetti. It is strangely alive.'
Of course the model is hardly the real world; it no more clinches the argument than building a model of a battleship proves that a real battleship will float: But it helps identify the conditions THE POWER OF PARASITES
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under which the Red Queen is running forever: A hugely simplified version of a human being and a grotesquely simplified version of a parasite will continually change their genes in cyclical and random ways, never settling, always running, but never going anywhere, eventually coming back to where they started—as long as they both have sex.52
SEX AT ALTITUDE
Hamilton's disease theory makes many of the same predictions as Alexey Kondrashov 's mutation theory, which we met in the last chapter. To return to the analogy of the lawn sprinkler and the rainstorm, both can explain how the driveway got wet: But which is correct? In recent years ecological evidence has begun to tip the scales Hamilton's way. In certain habitats, mutation is common and diseases rare—mountaintops, for example, where there is much more ultraviolet light of the type that damages genes and causes mutations: So if Kondrashov is right, sex should be more common on mountaintops. It is not. Alpine flowers are often among the most asexual of flowers. In some groups of flowers, the ones that live near the tops of mountains are asexual, while those that live lower down are sexual. In five species of Townsendia, the alpine daisy, the asexuals are all found at higher altitudes than the sexuals. In Townsendia condensata, which lives only at very high altitudes, only one sexual population has ever been found, and that was the one nearest sea level."
There are all sorts of explanations of this that have little to do with parasites, of course: The higher you go, the colder it gets, and the less you can rely on insects to pollinate a sexual flower. But if Kondrashov were right, such factors should be overwhelmed by the need to fight mutation. And the altitude effect is mirrored by a latitude effect: In the words of one textbook: " There are ticks and lice, bugs and flies, moths, beetles, grasshoppers, millipedes, and more, in all of which males disappear as one moves from the tropics toward the poles. ""
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Another trend that fits the parasite theory is that most asexual plants are short-lived annuals. Long-lived trees face a particular problem because their parasites have time to adapt to their genetic defenses—to evolve. For example, among Douglas firs infested by scale insects (which are amorphous blobs of insectness that barely even look like animals), the older trees are more heavily infested than the younger ones. By transplanting scale insects from one tree to another, two scientists were able to show that this is an effect of better-adapted insects, not weaker old trees. Such trees would do their offspring no favors by having identical young, on whom the well-adapted insects would immediately descend. Instead, the trees are sexual and have different young."
Disease might almost put a sort of limit on longevity: There is little point in living much longer than it takes your parasites to adapt to you. How yew trees, bristlecone pines, and giant sequoias get away with living for thousands of years is not clear, but what is clear is that, by virtue of chemicals in their bark and wood, they are remarkably resistant to decay. In the Sierra Nevada mountains of California lie the trunks of fallen sequoias, partly covered by the roots of huge pine trees that are hundreds of years old, yet the wood of the sequoia stumps is hard and true. f6
In the same vein it is tempting to speculate that the peculiar synchronized flowering of bamboo might have something to do with sex and disease. Some bamboos flower only once every 121
years, and they do so at exactly the same moment all over the world, then die. This gives their young all sorts of advantages: They do not have living parents to compete with, and the parasites are wiped out when the bamboo parent plants die. (Their predators have problems, too; flowering causes a crisis for pandas.)"
Moreover, it is a curious fact that parasites themselves are often sexual, despite the enormous inconvenience this causes. A bil-harzia worm inside a human vein cannot travel abroad to seek a mate, but if it encounters a genetically different worm, infected on a separate occasion, they have sex. To compete with their sexual hosts, parasites, too, need sex.
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SEXLESS SNAILS
But these are all hints from natural history, not careful scientific experiments. There is also a small amount of more direct evidence in favor of the parasite theory of sex. By far the most thorough study of the Red Queen was done in New Zealand by a soft-spoken American biologist named Curtis Lively who became intrigued by the evolution of sex when told to write an essay on the subject as a student: He soon abandoned his other research, determined to solve the problem of sex.
He went to New Zealand and examined water snails from streams and lakes and found that in many populations there are no males and the females give birth as virgins, but in other populations the females mate with males and produce sexual offspring. So he was able to sample the snails, count the males, and get a rough measure of the predominance of sex: His prediction was that if the Vicar of Bray was right and snails needed sex to adjust to changes, he would find more males in streams than in lakes because streams are changeable habitats; if the tangled bank was right and competition between snails was the cause of sex, he would find more males in lakes than in streams because lakes are stable, crowded habitats; if the Red Queen was right, he would find more males where there were more parasites.58
There were more males in lakes. About 1 2 percent of snails in the average lake are male, compared to 2 percent in the average stream. So the Vicar of Bray is ruled out. But there are also more parasites in lakes, so the Red Queen is not ruled out: Indeed, the closer he looked, the more promising the Red Queen seemed to be.
There were no highly sexual populations without parasites. 59
But Lively could not rule out the tangled bank, so he returned to New Zealand and repeated his survey, this time intent on finding out whether the snails and their parasites were genetically adapted to each other: He took parasites from one lake and tried to infect snails from another lake on the other side of the Southern Alps. In every case the parasites were better at infecting snails from their own lake. At first this sounds like bad,news for the Red Queen, but Lively realized it was not: It is a very host cen-
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tered view to expect greater resistance in the home lake. The parasite is constantly trying to outwit the snail 's defenses, so it is likely to be only one molecular step behind the snail in changing its keys to suit the snail ' s locks. Snails from another lake have altogether different locks. But since the parasite in question, a little creature called Microphallus, actually castrates the snail, it grants enormous relative success to the snails with new locks. Lively is now doing the crucial experiment in the laboratory—to see whether the presence of parasites actually prevents an asexual snail from displacing a sexual one. b°
The case of the New Zealand snails has done much to satisfy critics of the Red Queen, but they have been even more impressed by another of Lively 's studies—of a little fish in Mexico called the topminnow. The topminnow sometimes hybridizes with a similar fish to produce a triploid hybrid (that is, a fish that stores its genes in triplicate, like a bureaucrat). The hybrid fish are inca -
pable of sexual reproduction, but each female will as a virgin produce clones of herself as long as she receives sperm from a normal fish. Lively and Robert Vrijenhoek of Rutgers University in New Jersey caught topminnows in each of three different pools and
,counted the number of cysts caused by black spot disease, a form of worm infection. The bigger the fish, the more black spots. But in the first pool, Log pool, the hybrids had far more spots than the sexual topminnows, especially when large. In the second pool, Sandal pool, where two different asexual clones coexisted, those from the more common clone were the more parasitized; the rarer clones and the sexual topminnows were largely immune. This was what Lively had predicted, reasoning that the worms would adjust their keys to the most common locks in the pond, which would be those of the most common clone. Why? Because a worm would always have a greater chance of encountering the most common lock than any other lock. The rare clone would be safe, as would the sexual topminnows, each of which had a different lock.
But even more intriguing was the third pool, Heart pool.
This pool had dried up in a drought in 1976 and had been recolonized two years later by just a few topminnows: By 1983 all the THE POWER OF PARASITES
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topminnows there were highly inbred, and the sexual ones were more susceptible to black spots than the clones in the same pool.
Soon more than 95 percent of the topminnows in Heart pool were asexual clones. This, too, fits the Red Queen theory, for sex is no good if there is no genetic variety: It 's no good changing the locks if there is only one type of lock available. Lively and Vrijenhoek introduced some more sexual female topminnows into the pool as a source of new kinds of lock. Within two years the sexual topminnows had become virtually immune to black spot, which had now switched to attacking the hybrid clones. More than 80 percent of the topminnows in the pool were sexual again. So all it took for sex to overcome its twofold disadvantage was a little bit of genetic variety."
The topminnow study beautifully illustrates the way in which sex enables hosts to impale their parasites on the horns of a dilemma. As John Tooby has pointed out, parasites simply cannot keep their options open. They must always "choose. " In competition with one another they must be continually chasing the most common kind of host and so poisoning their own well by encouraging the less common type of host. The better their keys fit the locks of the host, the quicker the host is induced to change its locks."
Sex keeps the parasite guessing. In Chile, where introduced European bramble plants became a pest, rust fungus was introduced to control them. It worked against an asexual species of bramble and failed against a sexual species. And when mixtures of different varieties of barley or wheat do better than pure stands of one variety (as they do), roughly two-thirds of the advantage can be accounted for by the fact that mildew spreads less easily through the mixture than through a pure stand."
THE SEARCH FOR INSTABILITY
The history of the Red Queen explanation of sex is an excellent example of how science works by synthesizing different approaches to a problem. Hamilton and others did not pluck the idea of para-
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sites and sex from thin air: They are the beneficiaries of three separate lines of research that have only now converged. The first was the discovery that parasites can control populations and cause them to go in cycles: This was hinted at by Alfred Lotka and Vito Volterra in the 1920s and fleshed out by Robert May and Roy Anderson in London in the 1970s. The second was the discovery by J. B. S: Haldane and others in the 1940s of abundant polymorphism, the curious phenomenon that for almost every gene there seemed to be several different versions, and something was keeping one from driving out all the others: The third was the discovery by Walter Bodmer and other medical scientists of how defense agaii*t parasites works—the notion of genes for resistance providing a sort of lock-and-key system. Hamilton put all three lines of inquiry together and said: Parasites are in a constant battle with hosts, a battle that is fought by switching from one resistance gene to another; hence the battery of different versions of genes: None of this would work without sex."
In all three fields the breakthrough was to abandon notions of stability: Lotka and Volterra were interested in knowing whether parasites could stably control populations of hosts; Haldane was interested in what kept polymorphisms stable for so long. Hamilton was different. "Where others seem to want stability I always hope to find, for the benefit of my idea of sex, as much change and motion . . . as I can get.""
The main weakness of the theory remains the fact that it requires some kind of cycles of susceptibility and resistance; the advantage should always be swinging back and forth like a pendu-lum, though not necessarily with such regularity: 66 There are some examples of regular cycles in nature: Lemmings and other rodents often grow abundant every three years and rare in between: Grouse on Scottish moors go through regular cycles of abundance and scarcity, with about four years between peaks, and this is caused by a parasitic worm: But chaotic surges, such as locust plagues, or much more steady growth or decline, such as in human beings, are more normal: It remains possible that versions of the genes for resistance to disease do indeed show cycles of abundance and scarcity: But nobody has looked. b7
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THE RIDDLE OF THE ROTIFER
Having explained why sex exists, I must now return to the case of the bdelloid rotifers, the tiny freshwater creatures that never have sex at all—a fact that John Maynard Smith called a "scandal. " For the Red Queen theory to be right, the bdelloids must in some manner be immune from disease; they must have an alternative antiparasite mechanism to sex: That way they could:be exceptions that prove the rule rather than embarrass it:
As it happens, the rotifer scandal may be on the verge of a solution. But in the best traditions of the science of sex, it could still go either way. Two new theories to explain the sexlessness of bdelloid rotifers point to two different explanations.
The first is Matthew Meselson 's: He thinks that genetic insertions—jumping genes that insert copies of themselves into parts of the genome where they do not belong—are for some reason not a problem for rotifers. They do not need sex to purge them from their genes. It 's a Kondrashov-like explanation, though with a touch of Hamilton: (Meselson calls insertions a form of venereal genetic infection:) 68 The second is a more conventional Hamilton-ian idea: Richard Ladle of Oxford University noticed that there are groups of animals capable of drying out altogether without dying—losing about 90 percent of their water content. This requires remarkable biochemical skill. And none of them have sex.
They are tardigrades, nematodes, and bdelloid rotifers: Some rotifers, remember, dry themselves out into little "tuns " and blow around the world in dust: This is something ,sexual monogonont rotifers cannot do (although their eggs can). Ladle thinks that drying yourself out may be an effective antiparasite strategy, a way of purging the parasites from your body. He cannot yet explain exactly why the parasites mind being dried out more than their hosts do; viruses are little more than molecular particles, in any case, and so could surely survive a good drying. But he seems to be on to something. Those nematode or tardigrade species that do not dry out are sexual. Those that can dry out are all female:'
The Red Queen has by no means conquered all her rivals: Pockets of resistance remain. Genetic repair diehards hold out in
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places like Arizona, Wisconsin, and Texas. Kondrashov 's banner still attracts fresh followers. A few lonely tangled bankers snipe from their laboratories. John Maynard Smith pointedly calls himself a pluralist still. Graham Bell says he has abandoned the "mono-lithic confidence " (in the tangled bank) that infused his book The
Masterpiece of Nature, but has not become an undoubting Red Queen-er. George Williams still hankers after his notion that sex is a historical accident that we are stuck with. Joe Felsenstein maintains that the whole argument was misconceived, like a discussion of why goldfish do not add to the weight of the water when added to a bowl. Austin Burt takes the surprising view that the Red Queen and the Kondrashov mutation theory are merely detailed vindications of Weismann's original.idea that sex supports the variation needed to speed up evolution—that we have come full circle. Even Bill Hamilton concedes that the pure Red Queen probably needs some variation in space as well as time to make her work. Hamilton and Kondrashov met for the first time in Ohio in July 1992 and agreed convivially to differ until more evidence was in. But scientists always say that: Advocates never concede defeat. I believe that a century hence biologists will look back and declare that the Vicar of Bray fell down a tangled bank and was slain by the Red Queen. 7°
Sex is about disease. It is used to combat the threat from parasites. Organisms need sex to keep their genes one step ahead of their parasites. Men are not redundant after all; they are woman 's insurance policy against her children being wiped out by influenza and smallpox (if that is a consolation). Women add sperm to their eggs because if they did not, the resulting babies would be identically vulnerable to the first parasite that picked their genetic locks.
Yet before men begin to celebrate their new role, before the fireside drum-beating sessions incorporate songs about pathogens, let them tremble before a new threat to the purpose of their existence. Let them consider the fungus. Many fungi are sexual, but they do not have males. They have tens of thousands of different sexes, all physically identical, all capable of mating on equal terms, but all incapable of mating with themselves!' Even among animals there are many, such as the earthworm, that are hermaphrodites. To THE POWER OF PARASITES
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be sexual does not necessarily imply the need for sexes, let alone for just two sexes, let alone for two sexes as different as men and women. Indeed, at first sight, the most foolish system of all is two sexes because it means that fully 50 percent of the people you meet are incompatible as breeding partners. If we were hermaphrodites, everybody would be a potential partner. If we had ten thousand sexes, as does the average toadstool, 99 percent of those we meet would be potential partners. If we had three sexes, two-thirds would be available. It turns out that the Red Queen 's solution to the problem of why people are sexual is only the beginning of a long story:
Chapter 4
GENETIC MUTINY AND
GENDER
The turtle lives
'twixt plated decks
Which practically conceal its sex:
I think it clever of the turtle
In such a fix to be so fertile:
—Ogden Nash
In the Middle Ages, the archetypal British village owned one common field for grazing cattle. Every villager shared the common and was allowed to graze as many cattle on it as he wanted. The result was that the common was often overgrazed until it could support only a few cattle. Had each villager been encouraged to exercise a little restraint, the common could have supported far more cattle than it did.
This " tragedy of the commons" ' has been repeated again and again throughout the history of human affairs. Every sea fishery that has ever been exploited is soon overfished and its fishermen driven into penury. Whales, forests, and aquifers have been treated in the same way. The tragedy of the commons is, for economists, a matter of ownership: The lack of a single ownership of the commons or the fishery means that everybody shares equally in the cost of overgrazing or overfishing. But the individual who grazes one too many cows or the fisherman who catches one too many netfuls still gets the whole of the reward of that cow or netful. So he reaps the benefits privately and shares the costs publicly. It is a one-way ticket to riches for the individual and a one-way ticket to poverty for the village. Individually rational behavior leads to a collectively irrational outcome. The free-rider wins at the expense of the good citizen.
Exactly the same problem plagues the world of the genes. It is, oddly, the reason that boys are different from girls.
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WHY ARE PEOPLE NOT HERMAPHRODITES?
None of the theories discussed so far explains why there are two separate genders:' Why is every creature not a hermaphrodite, mixing its genes with those of others, but avoiding the cost of maleness by being a female, too? For that matter, why are there two genders at all, even in hermaphrodites? Why not just give each other parcels of genes, as equals? "Why sex? " makes no sense without
" why sexes? " As it happens, there is an answer. This chapter is about perhaps the strangest of all the Red Queen theories, the one that goes under the unprepossessing name of " intragenomic conflict: " Translated, it is about harmony and selfishness, about conflicts of interest between genes inside bodies, about free-rider genes and outlaw genes: And it claims that many of the features of a sexual creature arose as reactions to this conflict, not to be of use to the individual: It "gives an unstable, interactive, and historical character to the evolutionary process."'
The thirty thousand pairs of genes that make and run the average human body find themselves in much the same position as seventy-five thousand human beings inhabiting a small town.
Just as human society is an uneasy coexistence of free enterprise and social cooperation, so is the activity of genes within a body.
Without cooperation, the town would not be a community. Everybody would lie and cheat and steal his way to wealth at the expense of everybody else, and all social activities—commerce, government, education, sport—would grind to a mistrustful halt: Without cooperation between the genes, the body they inhabit could not be used to transmit those genes to future generations because it would never get built.
A generation ago, most biologists would have found that paragraph baffling: Genes are not conscious and do not choose to cooperate; they are inanimate molecules switched on and off by chemical messages: What causes them to work in the right order and create a human body is some mysterious biochemical program, not a democratic decision: But in the last few years the revolution begun by Williams, Hamilton, and others has caused more and GENETIC MUTINY AND GENDER
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more biologists to think of genes as analogous to active and cunning individuals. Not that genes are conscious or driven by future goals—no serious biologist believes that—but the extraordinary teleological fact is that evolution works by natural selection, and natural selection means the enhanced survival of genes that enhance their own survival: Therefore, a gene is by definition the descendant of a gene that was good at getting into future generations. A gene that does things that enhance its own survival may be said, teleologically, to be doing them because they enhance its survival.
Cooperating to build a body is as effective a survival "strategy " for genes as cooperating to run a town is a successful social strategy for human beings.
But society is not all cooperation; a measure of competitive free enterprise is inevitable. A gigantic experiment called communism in a laboratory called Russia proved that. The simple, beautiful suggestion that society should be organized on the principle "from each according to his ability, to each according to his need " proved disastrously unrealistic because each did not see why he should share the fruits of his labors with a system that gave him no reward for working harder: Enforced cooperation of the Communist kind is as vulnerable to the selfish ambitions of the individual as a free-for-all would be. Likewise, if a gene has the effect of enhancing the survival of the body it inhabits but prevents that body from breeding or is never itself transmitted through breeding, then that gene will by definition become extinct and its effect will disappear.
Finding the right balance between cooperation and competition has been the goal and bane of Western politics for centuries.
Adam Smith recognized that the economic needs of the individual are better met by unleashing the ambitions of all individuals than by planning to meet those needs in advance. But even Adam Smith could not claim that free markets produce Utopia. Even the most libertarian politician today believes in the need to regulate, oversee, and tax the efforts of ambitious individuals so as to ensure that they do not satisfy their ambitions entirely at the expense of others. In the words of Egbert Leigh, a biologist at the Smithsonian Tropical Research Institute, "Human intelligence has yet to design
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The Red Queen
a society where free competition among the members works for the good of the whole. "' The society of genes faces exactly the same problem. Each gene is descended from a gene that unwittingly jos-tled to get into the next generation by whatever means was in its power. Cooperation between them is marked, but so is competition.
And it is that competition that led to the invention of gender.
As life emerged from the primeval soup several billion years ago, the molecules that caused themselves to be replicated at the expense of others became more numerous. Then some of those molecules discovered the virtues of cooperation and specialization, so they began to -assemble in groups called chromosomes to run machines called cells that could replicate these chromosomes efficiently. In just the same way little groups of agriculturalists joined with blacksmiths and carpenters to form cooperative units called villages. The chromosomes then discovered that several kinds of cells could merge to form a supercell, just as villages began to group together as tribes. This was the invention of the modern cell from a team of different bacteria. The cells then grouped together to make animals and plants and fungi, great big conglomerates of conglomerates of genes, just as tribes merged into countries and countries into empires.'
None of this would have been possible for society without laws to enforce the social interest over the individual, selfish drive; it was the same with genes. A gene has only one criterion by which posterity judges it: whether it becomes an ancestor of other genes.
To a large extent it must achieve that at the expense of other genes, just as a man acquires wealth largely by persuading others to part with it (legally or illegally). If the gene is on its own, all other genes are its enemies—every man for himself. If the gene is part of a coalition, then the coalition shares the same interest in defeating a rival coalition, just as employees of Hertz share the same interest in its thriving at the expense of Avis.
This broadly describes the world of viruses and bacteria.
They are disposable vehicles for simple teams of genes, each team highly competitive with other teams but with largely harmonious relations among team members. For reasons that will soon become GENETIC MUTINY AND GENDER
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apparent, this harmony breaks down when bacteria merge to become cells and cells merge to become organisms. It has to be reasserted by laws and bureaucracies.
And even at the bacterial level it does not entirely hold true. Consider the case of a new, supercharged mutant gene that appears in a bacterium. It is superior to all other genes of its type, but its fate is determined largely by the quality of its team. It is like a brilliant engineer finding himself employed by a doomed, small firm or a brilliant athlete stuck on a second-rate team: Just as the engineer or the athlete seeks a transfer, so we might expect that bacterial genes would have invented a way to transfer themselves from one bacterium to another:
They have. It is called "conjugation, " and it is widely agreed to be a form of sex itself. Two bacteria simply connect to each other by a narrow pipe and shunt some copies of genes across. Unlike sex, it has nothing to do with reproduction, and it is a relatively rare event. But in every other respect it is sex. It is genetic trade.
Donal Hickey of the University of Ottawa and Michael Rose of the University of California at Irvine were the first to suggest in the early 1980s that bacterial "sex" was invented not for the bacteria but for the genes—not for the team but for the players.' It was a case of a gene achieving its selfish end at the expense of its teammates, abandoning them for a better team: Their theory is not a full explanation of why sex is so common throughout the animal and plant kingdoms; it is not a rival to the theories discussed heretofore. But it does suggest how the whole process got itself started. It suggests an origin for sex:
From the point of view of an individual gene, then, sex is a way to spread laterally as well as vertically: If a gene were able to make its owner-vehicle have sex, therefore, it would have done something to its own advantage (more properly, it would be more likely to leave descendants if it could), even if it were to the disadvantage of the individual: Just as the rabies virus makes the dog want to bite anything, thus subverting the dog to its own purpose of spreading to another dog, so a gene might make its owner have sex just to get into another lineage.
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The Red Queen
Hickey and Rose are especially intrigued by genes called transposons, or jumping genes, that seem to be able to cut themselves our of chromosomes and stitch themselves back into other chromosomes. In 1980 two teams of scientists simultaneously came to the conclusion that the transposons seemed to be examples of "selfish " or parasitic DNA, which spreads copies of itself at the expense of other genes: Instead of looking for some reason that transposons exist for the benefit of the individual, as scientists had done before, they simply saw it as bad for the individual and good for the transposons.' Muggers and outlaws do not exist for the benefit of society but to its detriment and for the benefit of themselves. Perhaps transposons were, in Richard Dawkins 's words,
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