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 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 at all. Ever since, the purpose of sex has been an open question, and it has been called the queen of evolutionary problems.1
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 cliché 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 exhaustion 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. 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.”2
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.”3 There might be a few holes in existing theories, said the cynics, but do not expect us 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.
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.”4
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 60,000 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 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.5
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 Weismann, 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 furnishing material for the operation of natural selection,” Weismann called sex.6 It speeds up evolution.
Graham Bell, an English biologist working in Montreal, has 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 vicar, 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.7
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 into Weismann’s argument, Fisher’s book in 19308 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 pooling their resources. If one man invented a steam engine 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.10
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.11
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 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.”12 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 discrete 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 Hamlet 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, understanding 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.13
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 spirit and charity. It also seemed to explain animal altruism. Bees die as 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.14
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.15 The ones who had confused species and individual, such as Julian Huxley, 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.17
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 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.18
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 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 méans. 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.”20 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 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.21
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 appendixes, it no longer served a purpose but was not easily got rid of.22
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 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 of the situation is being overlooked.”24 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 libidinous 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?25
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: 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.26
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 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 repaired.27
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.”28 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 rainbow trout and domestic chicken are “triploid”—plus a single parrot that turned up a few years ago.29 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.30
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 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.31
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.32
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.
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.33
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 outpopulated 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 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.34
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.35
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 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.36
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 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.37
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, conversely, 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 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.40
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.41
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.42
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.”43
And Kondrashov’s theory suffers from the same flaw as all genetic-repair theories and the Vicar of Bray himself: It works too 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.44
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.