The Red Queen

" outlaw genes. "8 Hickey then noticed that transposons were much more common among outbreeding sexual creatures than among inbreeding or asexual ones. He ran some mathematical models which showed that parasitic genes would do well even if they had a bad effect on the individual they inhabited. He even found some cases of parasitic genes of yeast that spread quickly in sexual species and slowly in asexual ones. Such genes were on "plasmids,"

or separate little loops of DNA, and it turns out that in bacteria such plasmids actually provoke the very act of conjugation by which they spread: They are like rabies viruses making dogs bite one another: The line between a rogue gene and an infectious virus is a blurred one.'

NOBODY IS DESCENDED FROM ABEL

Despite this little rebellion, life is fairly harmonious in the bacterial team. Even in a more complicated organism such as an amoeba, formed by an agglomeration of ancestral bacteria sometime in the distant past,'° there is little difference between the interests of the team and the individual members. But in more complicated creatures the opportunities for genes to thrive at the expense of their fellows are greater.

The genes of animals and plants turn out to be full of half-GENETIC MUTINY AND GENDER

::: 97 :::

suppressed mutinies against the social harmony: In some female flour beetles there exists a gene called Medea that kills those off-•

spring that do not inherit it:" It is as if the gene booby-traps all the female 's young and defuses only those that it itself inhabits. Whole selfish chromosomes called B chromosomes exist that do nothing but ensure their transmission to the next generation by invading every egg the insect makes.' Another insect, a scale insect, has an even more bizarre genetic parasite: When its eggs are fertilized, sometimes more than one sperm penetrates the egg. If this happens, one of the sperm fuses with the egg's nucleus in the normal way; the spare sperm hang around and begin dividing as the egg divides: When the creature matures, the parasitic sperm cells eat out its gonads and replace them with themselves. So the insect produces sperm or eggs that are barely related to itself, an astonishing piece of genetic cuckoldry:"

The greatest opportunity for selfish genes comes during sex: Most animals and plants are diploid: Their genes come in pairs: But diploidy is an uneasy partnership between two sets of genes, and when partnerships end, things often get acrimonious.

The partnerships end with sex: During meiosis, the central genetic procedure of sex, the paired genes are separated to make haploid sperm and eggs: Suddenly each gene has an opportunity to be selfish at its partner 's expense: If it can monopolize the eggs or sperm, it thrives and its partner does not.'

This opportunity has been explored in recent years by a group of young biologists, prominent among them Steve Frank of the University of California at Irvine, and Laurence Hurst, Andrew Pomiankowski, David Haig, and Alan Grafen at Oxford University.

Their logic goes like this: When a woman conceives, her embryo gets only half of her genes: They are the lucky ones; the unlucky other half languish in obscurity in the hope of another toss of the coin when she next breeds. For, to recapitulate, you have twenty-three pairs of chromosomes, twenty-three from your father and twenty-three from your mother. When you make an egg or a sperm, you pick one from each pair to give a total of twenty-three chromosomes: You could give all the ones you inherited from your mother

::: 98 :::

The Red Queen

or all the ones from your father, or more likely a mixture of the two. Now a selfish gene that loaded the dice so that it stood a better than fifty-fifty chance of getting into the embryo might do rather well. Suppose it simply killed off its opposite number, the one that came from the other grandparent of the embryo.

Such a gene exists. On chromosome two of a certain kind of fruit fly there is a gene called "segregation distorter, " which simply kills all sperm containing the other copy of chromosome two.

The fly therefore produces half as much sperm as normal. But all of the sperm contains the segregation distorter gene, which has thereby ensured a monopoly of the fly 's offspring."

Call such a gene Cain: Now it so happens that Cain is Abel's virtually identical twin, so he cannot kill his brother without killing himself. This is because the weapon he uses against Abel is merely a destructive enzyme released into the cell—a chemical weapon, as it were. His only hope is to attach to himself a device that protects him—a gas mask (though it in fact consists of a gene that repels the destructive enzyme). The "mask of Cain " protects him from the gas he uses against Abel. Cain becomes an ancestor, and Abel does not. Thus a gene for chromosomal fratricide will spread as surely as a murderer will inherit the Earth. Segregation distorters and other fratricidal genes go under the general name of

" meiotic drive " because they drive the process of meiosis, the division of the partnerships, into a biased outcome."

Meiotic-drive genes are known in flies and mice and a few other creatures, but they are rare. Why? For the same reason that murder is rare. The interest of the other genes has been reasserted through laws. Genes, like people, have other things to do than kill each other. Those genes that shared Abel 's chromosome and died with him would have survived had they invented some technique to foil Cain. Or, to put it another way, genes that foil meiotic drivers will spread as surely as meiotic drivers will spread. A Red Queen race is the result:

David Haig and Alan Grafen believe that such a response is indeed common and that it consists of a sort of genetic scrambling, the swapping of chunks of chromosomes. If a chunk of chromo-GENETIC MUTINY AND GENDER

::: 99 :::

some lying next to Abel suddenly swapped places with the chunk lying next to Cain, then the mask of Cain would be unceremoni-ously removed from Cain 's chromosome and plonked onto Abel 's.

The result: Cain would commit suicide, and Abel would live happily ever after:"

This swapping is called "crossing over: " It happens between virtually all pairs of chromosomes in most species of animal and plant. It achieves nothing except a more thorough mixing of the genes—which is what most people thought its purpose was before Haig and Grafen suggested otherwise. But Haig and Grafen are implying that crossing over need not serve any such function; it is merely a piece of intracellular law enforcement. In a perfect world policemen would not exist because people would never commit murder. Policemen were not invented because they adorn society but because they prevent the disruption of society. So, according to the Haig-Grafen theory, crossing over polices the division of chromosomes to keep it fair.

This is not, by its nature, the sort of theory that lends itself to easy confirmation. As Haig remarks, in a dry Australian manner, crossing over is like an elephant repellent. You know it 's working because you don ' t see any elephants."

Cain genes survive in mice and flies by hugging their masks close to them so that they are not likely to be parted by crossing over. But there is one pair of chromosomes that is especially plagued by Cain genes, the " sex chromosomes," because these peculiar chromosomes do not engage in crossing over. In people and many other animals, gender is determined by genetic lottery. If you receive a pair of X chromosomes from your parents, you become a female; if you receive an X and a Y, you become a male (unless you are a bird, spider, or butterfly, in which case it is the other way around): Because Y chromosomes contain the genes for determining maleness, they are not compatible with Xs and do not cross over with them. Consequently, a Cain gene on an X chromosome can safely kill the Y chromosome and not risk suicide. It biases the sex ratio of the next generation in favor of females, but that is a cost borne by the whole population equally, whereas the benefit

::: 100 :::

The Red Queen

of monopolizing the offspring is received by the Cain gene itself—just as in the case of free-riders causing the tragedy of the commons."

I N PRAISE OF UNILATERAL DISARMAMENT

By and large, however, the common interest of the genes prevails over the ambitions of the outlaws. As Egbert Leigh has put it, "a parliament of genes" asserts its will. Yet the reader may be getting restless: "This little tour of the cellular bureaucracy, " he says, "fun though it was, has brought us no closer to the question asked at the beginning of the chapter—why there are two genders. "''°

Have patience: The road we have chosen—to seek conflicts between sets of genes—leads to the answer. For gender itself may prove to be a piece of cellular bureaucracy: A male is defined as the gender that produces sperm or pollen: small, mobile, multitudi-nous gametes. A female produces few, large, immobile gametes called eggs. But size is not the only difference between male and female gametes. A much more significant difference is that there are a few genes that come only from the mother: In 1981 two scientists at Harvard whose perspicacity we will reencounter throughout the book, Leda Cosmides and John Tooby, pieced together the history of an even more ambitious genetic rebellion against this parliament of genes, one that forced the evolution of animals and plants into strange new directions and resulted in the invention of two genders.''

So far I have treated all genes as similar in their pattern of inheritance. But this is not quite accurate. When a sperm fertilizes an egg, it donates just one thing to that egg: a bagful of genes called a nucleus. The rest of it stays outside the egg. A few of the father 's genes are left behind because they are not in the nucleus at all; they are in little structures called "organelles. " There are two main kinds of organelles, mitochondria, which use oxygen to extract energy from food, and chloroplasts (in plants), which use sunlight to make food from air and water. These organelles are GENETIC MUTINY AND GENDER

::: 1 01 :::

almost certainly the descendants of bacteria that lived inside cells and were "domesticated " because their biochemical skills were of use to the host cells. Being descendants of free-living bacteria, they came with their own genes, and they still have many of these genes: Human mitochondria, for example, have thirty-seven genes of their own: To ask, "Why are there two genders? " is to ask, "Why are organelle genes inherited through the maternal line? " ' Why not just let the sperm 's organelles into the egg, too? Evolution seems to have gone to extraordinary lengths to keep the father 's organelles out: In plants a narrow constriction prevents the father 's organelles from passing into the pollen tube: In animals the sperm is given a sort of strip search as it enters the egg to remove all the organelles: Why should this be?

The answer lies in the exception to this rule: an alga called

Chlamydomonas that has two genders called plus and minus rather than male and female: In this species the two parents ' chloroplasts engage in a war of attrition that destroys 95 percent of them: The 5 percent remaining are those of the plus parent, which by force of sheer numbers overwhelm the minus ones.' This war impoverishes the whole cell. The nuclear genes take the same dim view of it as the prince takes in Romeo and Juliet of the war between two of his subjects:

Rebellious subjects, enemies to peace,

Profaners of this neighbour-stained steel, —

Will they not hear? What, ho! you men, you beasts, That quench the fire ofyour pernicious rage With purple fountains issuing from your veins, On pain of torture, from those bloody hands

Throw your mistemper'd weapons to the ground,

And hear the sentence ofyour moved prince:

Three civil brawls, bred of an airy word, By thee, Old Capulet, and Montague, Have thrice disturb'd the quiet of our streets:

::: If ever you disturb our streets again, Your lives shall pay the forfeit of the peace:

::: IO2:::

The Red Queen

As the prince soon discovers, even this severe sentence is insufficient to suppress the quarrel. Had he followed the example of the nuclear genes, he would have killed all the Montagues. The nuclear genes of both father and mother between them arrange that the organelles of the male are slaughtered. It is an advantage (to the male nucleus, not to the male organelles) to be of the type that allows its organelles to be killed, so that a viable offspring results.

So owners of docile, suicidal organelles (in the minus gender) would proliferate. Soon any deviation from a ratio of fifty-fifty killers and victims would benefit the rarer type and cause the ratio to correct itself. Two genders have been invented: killer, which provides the organelles, and victim, which does not.

Laurence Hurst of Oxford uses these arguments to predict that two genders are a consequence of sex by fusion. That is, where sex consists of the fusing of two cells, as in Chlamydomonas and most animals and plants, you find two genders. Where it consists of "conjugation "—the formation of a pipe between the two cells and the transfer of a nucleus of genes down the pipe—and there is no fusion of cells, then there is no conflict and no need for killer and victim genders. Sure enough, in those species with sex by conjugation, such as ciliated protozoa and mushrooms, there are many different genders: In those species with sex by fusion, there are almost invariably two genders. In one especially satisfying case there is a "hypotrich" ciliate that can have sex in either fashion.

When it has fusion sex, it behaves as if it had two genders: When it has conjugation sex, there are many genders: In 1991, just as he was putting the finishing touches on this tidy story, Hurst came across a case that seemed to contradict it: a form of slime-mold that has thirteen genders and fusion sex: But he delved deeper and discovered that the thirteen genders were arranged in a hierarchy. Gender thirteen always contributes the organelles, whomever it mates with. Gender twelve contributes them only if it mates with gender eleven and downward. And so on: This works just as well as having two genders but is a great deal more complicated: 2"

GENETIC MUTINY AND GENDER

::: 103 :::

SAFE SEX TIPS FOR SPERM

Along with most of the animal and plant kingdoms, we practice fusion sex and we have two genders. But it is a much modified form of fusion sex: Males do not submit their organelles to be slaughtered; they leave them behind at the border: The sperm carries just a nucleus cargo, a mitochondrial engine, and a flagellum propeller. The sperm-making cells go to great lengths to strip off the rest of the cytoplasm before the sperm is complete and redigest it at some expense. Even the propeller and engine are jettisoned when the sperm meets the egg; only the nucleus travels farther.

Hurst explains this by raising once again the matter of disease. 2$ Organelles are not the only genetic rebels inside cells; bacteria and viruses are there as well. And exactly the same logic applies to them as to organelles. When cells fuse, the rival bacteria in each engage in a struggle to the death. If a bacterium living happily inside an egg suddenly finds its patch invaded by a rival carried by a sperm, it will have to compete, and that might well mean abandoning its latency and manifesting itself as disease. There is ample evidence that diseases are reawakened by other "rival" infections.

For example, the virus that causes AIDS, known as HIV, infects human brain cells but lies dormant there: If, however, cytomegalovirus, an entirely different kind of virus, infects a brain cell already infected with HIV, then the effect is to reawaken the HIV virus, which proliferates rapidly. This is one of the reasons HIV seems more likely to go on to cause AIDS if the infected person gets a second, complicating infection: Also, one of the features of AIDS is that all sorts of normally innocuous bacteria and viruses, such as Pneumocystis, or cytomegalovirus or herpes, which live calmly inside many of our bodies, can suddenly become virulent and aggressive during the progression of AIDS. This is partly because AIDS is a disease of the immune system, and immune sur-veillance of these diseases is therefore lifted, but it also makes evolutionary sense. If your host is going to die, you had better multiply as fast as possible. So-called opportunist infections there-

::: 104:::

The Red Queen

fore hit you when you are down: Incidentally, one scientist has suggested that the cross-reactivity of the immune system (infection with one strain causes immune resistance to another strain of the same species of parasite) might be the parasite's way of slamming the door on rival members of its species once it is inside. 36

If it pays a parasite to go for broke when a rival appears, then it pays a host to prevent cross-infection with two strains of parasite. And nowhere is the risk of cross-infection greater than during sex. A sperm fusing with an egg risks bringing its cargo of bacteria and viruses as well; their arrival would awaken the egg 's own parasites and cause a battle for possession that would leave the egg sick or dead: To avoid this, therefore, the sperm tries to avoid bringing into the egg material that might harbor bacteria or viruses. It passes just the nucleus into the egg: Safe sex indeed: Proof of this theory will be hard to come by, but suggestive support comes from Paramecium, a protozoan that mates by conjugation—passing spare nuclei through a narrow tube: The procedure is hygienic in the sense that only the nuclei travel through the tube: Two paramecia stay linked for only two minutes or so; any longer and cytoplasm would also pass through the tube: The tube is too narrow even for the nucleus, which only just squeezes through: And it may be no accident that Paramecium and its relatives are the only creatures that possess such tiny nuclei, which are used as stores of genes ( "coding vaults " they have been called) and from which larger, working copies are made for everyday use."

DECISION TIME

Gender, then, was invented as a means of resolving the conflict between the cytoplasmic genes of the two parents. Rather than let such conflict destroy the offspring, a sensible agreement was reached: All the cytoplasmic genes would come from the mother, none from the father. Since this made the father 's gametes smaller, they could specialize in being more numerous and mobile the better to find eggs. Gender is a bureaucratic solution to an antisocial habit.

GENETIC MUTINY AND GENDER

::: 1 05 :::

This explains why there are two genders, one with small gametes, the other with large ones: But it does not explain why every creature cannot have both genders on board: Why are people not hermaphrodites? Were I a plant, the question might not arise: Most plants are hermaphrodites: There is a general pattern for mobile creatures to be " dioecious " (with separate genders) and ses-sile creatures, such as plants and barnacles, to be hermaphroditic: This makes a sort of ecological sense. Given that pollen is lighter than seed, a flower that produces only seed can have only local offspring: One that also produces pollen can generate plants that spread far and wide: A la* of diminishing returns applies to seed but not to pollen.

But it does not explain why animals took a different route: The answer lies in those muttering organelles left behind at the gate when the sperm entered the egg: In a male any gene in an organelle is in a cul-de-sac because it will be left behind by the sperm. All of the organelles in your body and all of the genes in them came from your mother; none came from your father: This is bad news for the genes, whose life 's work, remember, is to pass into the next generation: Every man is a dead end for organelle genes.

Not surprisingly, there is a "temptation " for such genes to invent solutions to their difficulty (that is, those that do solve the problem spread at the expense of those that do not): The most attractive solution for an organelle gene in a hermaphrodite is to divert all of the owner 's resources into female and away from male reproduction.

This is not pure fantasy. Hermaphrodites are in a state of constant battle against rebellious organelle genes trying to destroy their male parts: Male-killer genes have been found in more than 140 species of plant: They grow flowers, but the male anthers are stunted or withered: Seed but no pollen is produced: Invariably the cause of this sterility is a gene that lies inside an organelle, not a nuclear gene: By killing the anthers, the rebellious gene diverts more of the plant' s resources into female seed, through which it can be inherited. The nucleus has no such bias toward females; indeed, if the rebels are achieving their aims in many members of the species, the nucleus would benefit greatly from being the only

::: 106 :::

The Red Queen

plant on the block capable of producing pollen: So wherever they appear, male-sterility genes are soon , blocked by nuclear fertility restorers: In maize, for example, there are two male-sterility organelle genes, each suppressed by a separate nuclear restorer. In tobacco there are no less than eight such pairs of genes. By hybridizing different strains of maize, plant breeders can release the male-sterile genes from nuclear suppression because the sup-pressor from one parent no longer recognizes the rebel from the other. They wish to do this because a field of male-sterile maize cannot fertilize itself. By planting a different, male-fertile strain among it, the breeders can collect hybrid seed. And hybrid seed, benefiting from the mysterious boost known as hybrid vigor, out-yields both its parents: Male-sterile/female-fertile strains of sun-flower, sorghum, cabbage, tomato, maize, and other crops are a mainstay of farmers all over the world. 38

It is easy to spot when male-sterile genes are at work. The plants have two types: hermaphrodite and female. Such populations of plants are known as gynodioecious; androdioecious plants, with males and hermaphrodites only, are almost unknown. In wild thyme, for example, about half the plants are usually 'female, the rest hermaphrodites. The only way to explain the fact that they have stopped halfway along the one-way street is to posit a continuing battle between the organelles ' male-killer genes and nuclear fertility restorer genes. Under certain conditions the battle will reach a stalemate; any further advance by one side gives the other an advantage and the ability to force it back: The more common male-killers get, the more restorer genes will be favored, and vice-versa."

The same logic does not apply to animals, many of which are not hermaphrodites. It pays an organelle gene to kill males only if by doing so some energy or resource is diverted to the sisters of the killed males; hence, male-killing is rarer. In hermaphroditic plants. if the male function dies, the female function of the plant grows more vigorously or produces more seed. But a male-killer gene in, say, a mouse, by killing the males in a brood, does not benefit those mice's sisters at all. Killing males because they are evolutionary culs-de-sac for organelles would be pure spite.'°

Consequently, the battle is resolved rather differently in GENETIC MUTINY AND GENDER

::: I07:::

animals. Imagine a population of happy hermaphroditic mice.

There arrives in its midst a mutation, which happens to kill male gonads (testes). It spreads because females that have the gene do rather well: They have twice as many babies because they put no effort into making sperm. Soon the population consists of hermaphrodites and females, the latter possessing the male-killing gene: It is possible for the species to escape back to hermaphroditism by suppressing the male-killer gene, as many plants have obviously done, but it is just as likely that something else will happen before a mutation that causes the suppression can appear and take effect.

Maleness is a rather rare commodity at this stage. The few remaining hermaphroditic mice are at a premium because only they can produce the sperm that the all-female mice still need. The rarer they get, the better they do. No longer does it pay to have the male-killing mutation: Rather, the reverse. What would really pay the nuclear genes would be a female-killer gene so that one of the hermaphrodites could give up its female function altogether and concentrate on selling sperm to the rest. But if such a female-killing gene appeared, then the remaining hermaphrodites, which lack both the female-killer and the male-killer genes, are no longer at a premium. They are competing with pure males and pure females: Most of the sperm on offer comes complete with female-killer genes, and most of the eggs available to fertilize come complete with male-killer genes, so their offspring are constantly forced to specialize. The genders are separated."

The answer to the question "Would you not avoid paying the cost of maleness by being a hermaphrodite?" is simple: Yes, but there is no way to get there from here. We are stuck with two genders:

THE CASE OF THE 1MMACULATE TURKEYS

By separating their genders, animals ended the first mutiny of the organelles: But it was a temporary victory. The organelle genes renewed their mutiny, this time with the "aim " of driving all males

::: 108 :::

The Red Queen

into extinction and leaving the species all-female. This might seem to be a suicidal ambition because a male-less sexual species would become extinct in one generation, taking all of its genes with it, but there are two reasons this does not faze the organelles. First, they can and do convert the species into a parthenogenetic species, able to give virgin birth without sperm—in effect, they try to abolish sex—and second, they behave like cod fishermen or whale hunters or the grazers of commons. They seek short-term competitive advantage even when it leads to long-term suicide: A rational whale hunter does not spare the last pair of whales so that they. can breed; he kills them before his rival does and banks the proceeds: Likewise, an organelle does not spare the last male lest the species become extinct, for it faces extinction anyway if it is in a male: Consider a ladybird beetle 's brood. If the male eggs die, the female eggs in the brood eat them and get a free meal as a result.

Not surprisingly, there are male-killing genes at work in ladybirds, flies, butterflies, wasps, and bugs—about thirty species of insects have been studied so far—if and only if the young in a brood are in competition with one another: Those male-killing genes are not in organelles, however, but in bacteria that live inside the insects '

cells: Those bacteria, like the organelles, are excluded from sperm but not from eggs: 32

In animals such genes are called sex-ratio distorters: In at least twelve species of small parasitic wasps called Trichogramma, a bacterial infection makes the female produce only female young even from unfertilized eggs: Since all wasps have a peculiar system of sex determination in which unfertilized eggs become male, this does not condemn the race to extinction and helps the bacterium get into the next generation via the cytoplasm of the egg: The whole species becomes parthenogenetic for as many generations as the bacterium is there: Treat the wasps with an antibiotic and, to and behold, two genders reappear among the offspring. Penicillin cures virgin birth:"

In the 1950s scientists at an agricultural research center in Beltsville, Maryland, noticed that some turkey eggs began to develop without being fertilized: Despite heroic efforts by the scientists, GENETIC MUTINY AND GENDER

::: 109:::

these virgin-born turkeys rarely progressed beyond the stage of simple embryos. But the scientists did notice that vaccinating the fowl against fowl pox with a live virus increased the proportion of eggs likely to begin developing without sperm, from I—2 percent to 3—16 percent: By selective breeding and the use of three live viruses they were able to produce a strain of Pozo Gray turkeys nearly half of whose eggs would begin to develop without sperm: 34

If turkeys, why not people? Laurence Hurst has pursued an obscure hint of a gender-altering parasite among human beings. In a small French scientific journal there appeared in 1946 an astonishing story: A woman came to the attention of a doctor in Nancy when she was having her second child; her first, a daughter, had died in infancy: She 'expressed no surprise on learning that the second child was also a daughter: In her family, she said, no sons were ever born.

Her tale was this: She was the ninth daughter of a sixth daughter: Her mother had no brothers, nor did she. Her eight sisters had thirty-seven daughters and no sons: Her five aunts had eighteen daughters and no sons. In all, seventy-two women had 35

been born in two generations of her family and not one man: That such a thing should happen by chance is possible but amazingly unlikely: less than one chance in a thousand billion billion: The two French scientists who described the case, R. Lienhart and H. Vermelin, also ruled out selective spontaneous abortion of males on the grounds that there were no signs of it: Indeed, many of the women were unusually fecund: One had twelve daughters, two had nine, and one had eight: Instead, the scientists conjectured that the woman and her relatives contained some kind of cytoplasmic gene that feminized every embryo it infected, regardless of the sex chromosomes present. (There is no evidence, incidentally, that virgin birth was involved. The woman 's eldest sister was a celibate nun and childless:)

The case of Madame B, as she was described, is tantalizing in the extreme. Did her daughters and nieces have only daughters?

Did her first cousins? Is there still, in Nancy, an ever-growing dynasty of women, so that the city 's sex ratio will soon be unbal-

::: 110 :::

The Red Queen

anced? Was the explanation proffered by the French doctors the right one? If so, what was the gene and wherein did it live? It might have been in a parasite or in an organelle. How did it work? We may never know:

THE ALPHABETICAL BATTLE OF THE LEMMINGS

With the exception of some female inhabitants of the city of Nancy, the gender of a human being is determined by his or her sex chromosomes: When you were conceived, your mother 's egg was chased by two kinds of your father 's sperm, one containing an X

chromosome and one containing a Y chromosome: Whichever got there first decided your gender: Among mammals, birds, most other animals, and many plants, this is the usual way of going about things: Gender is determined genetically, by sex chromosomes: Those with an X and a Y are male, those with two Xs are female.

But even the invention of sex chromosomes and their success in largely suppressing the rebellion of cytoplasmic genes did not succeed in making life harmonious in the society of genes. The sex chromosomes themselves began to have an interest in the gender of their owners ' children. In man, for instance, the genes that control gender are on the Y chromosome. Half of a man 's sperm are X carriers and half are Y carriers. To father a daughter, the man must fertilize his mate with an X carrier. In doing so he passes none of the Y's genes to her: From the Y ' s point of view, his daughter is unrelated to him. Therefore, a Y gene that causes the death of all the man 's X-bearing sperm and ensures its own monopoly of the man' s children will thrive at the expense of all other kinds of Y genes: That all those children are sons and the species will therefore go extinct matters not in the least to the Y; he has no foresight.

This phenomenon of the " driving Y " was first predicted by Bill Hamilton in

He saw it as a powerful danger that was

1967."

liable to drive species extinct suddenly and silently. He wondered what prevented it from happening, if anything did: One solution GENETIC MUTINY AND GENDER

::: III :::

was to gag the Y chromosome, removing all but its gender-determining role: Indeed, Y chromosomes are kept in a kind of house arrest most of the time: Only a few of their genes are expressed, and the rest are entirely silent. In many species gender is determined not by the Y chromosome but by the ratio of the number of X chromosomes to the number of ordinary chromosomes. One X

fails to masculinize a bird, two succeed; and in most birds, the Y

chromosome has withered away altogether.

The Red Queen is at work. Far from settling down to a fair and reasonable way of determining gender, nature has to face an infinite series of rebellions: It suppresses one only to find it has opened the way to another: For this reason gender determination is a mechanism full of, in the words of Cosmides and Tooby, "meaningless complexity manifesting unreliability, aberrations, and (from the individual 's point of view) waste." "

But if the Y chromosome can drive, so can the X. The lemming is a fat arctic mouse famous among cartoonists for apocryphally throwing itself off cliffs in hordes: It is famous among biologists for its tendency to explode in numbers and then collapse again when overcrowding has destroyed its food supply. But it is notable for another reason: It has a peculiar way of determining the gender of its babies: It has three sex chromosomes, W, X, and Y. XY

is a male; XX, WX, and WY are all females. YY cannot survive at all: What has happened is that a mutant form of driving X chromosome, W, has appeared that overrules the masculinizing power of the Y The result is an excess of females. Since this puts males at a premium, you might expect that males would soon evolve the ability to produce more Y-bearing than X-bearing sperm, but they have not done so. Why? At first biologists thought it had something to do with population explosions during which an excess of daughters is a good idea, but recently they have determined that this is unnecessary: The female-biased sex ratio is stable for genetic, not ecological, reasons:"

A male that produces only Y sperm can mate with an XX

female and produce all sons (XY) or with a WX female and produce half sons and half daughters or with a WY female. In the last

::: 1 12 :::

The Red Queen

case he has only WY daughters because YY sons die: The net result, therefore, is that if he mates with one of each, he will have as many daughters as sons, and all his daughters will be WY

females, who can have only daughters: So, far from restoring the sex ratio to equality by producing only Y sperm, he has kept it unbalanced toward females: The case of the lemming demonstrates that even the invention of sex chromosomes did not prevent mutinous chromosomes from altering the sex ratio."

LOTTERY OR CHOICE?

Not all animals have sex chromosomes: Indeed, it is hard to see why so many do. They make gender a pure lottery, governed by an arbitrary convention with the sole advantage of (usually) keeping the sex ratio at fifty-fifty: If the first sperm to reach your mother 's egg carried a Y chromosome, you are a male; if it carried an X chromosome, you are a female. There are at least three different and better ways to determine your gender.

The first, for sedentary creatures, is to choose the gender appropriate to your sexual opportunities. For example, be a different gender from your neighbor because he or she will probably turn out to be your mate. A slipper limpet, which delights in the Latin name Crepidula fornicata, begins life as a male and becomes a female when it ceases peregrinating and settles on a rock; another male lands on it, and gradually it, too, turns female; a third male lands, and so on, until there is a tower of ten or more slipper limpets, the bottom ones being female, the top ones male. A similar method of gender determination is employed by certain reef fish: The shoal consists of lots of females and a single large male: When he dies, the largest female simply changes gender. The blue-headed wrasse changes gender from female to male when it reaches a certain size.'"

This sex change makes good sense from the fish' s point of view because there is a basic difference between the risks and rewards of being male or female: A large female fish can lay only a few more eggs than a small one, but a large male fish, by fighting GENETIC MUTINY AND GENDER

::: 113 :::

for and winning a harem of females, can have a great many more offspring than a small male. Conversely, a small male does worse than a small female because he fails to win a mate at all. Therefore, among polygamists the following strategy often appears: If small, be female; if large, be male:"

There is a lot to be said for such stratagems. It is profitable to be a female while growing up and get some breeding done, and then change sex and hit the jackpot as a polygamist male once you are big enough to command a harem: Indeed, the surprise is that more mammals and birds do not adopt this system: Half-grown male deer spend years in a state of celibacy awaiting the chance to breed, while their sisters produce a fawn a year.

A second way of determining gender is to leave it to the environment. In some fish, shrimp, and reptiles, gender is determined by the temperature at which the egg is incubated. Among turtles, warm eggs hatch into females; among alligators, warm eggs hatch into males; among crocodiles, warm and cool eggs hatch into females, intermediate ones into males: (Reptiles are the most adventurous sex determiners of all: Many lizards and snakes use genetic means, but whereas XY iguanas become male and XX

female, XY snakes become female and XX male:) Atlantic silverside fish are even more unusual: Those in the North Atlantic determine their gender by genes as we do; those farther south use the temperature of the water to set the gender of the embryo. p2

This environmental method seems a peculiar way of going about it: It means that unusually warm conditions can lead to too many male alligators and too few females. It leads to "intersexes,"

animals that are neither one thing nor the other: 43 Indeed, no biologist has a watertight explanation for why alligators, crocodiles, and turtles employ this technique: The best one is that it is all size related: The warm eggs hatch as larger babies than the cool ones. If being large is more of an advantage to males than females (true of crocodiles, in which males compete for females) or vice versa (true of turtles, in which large females lay more eggs than small ones, whereas small males are just as capable of fertilizing females as large ones), then it would pay to make warm eggs hatch

::: 114:::

The Red Queen

as the gender that most benefits from being large." A clearer example of the same phenomenon is the case of a nematode worm that lives inside an insect larva. Its size is set by the size of the insect; once it has eaten all of its home and host, it grows no more. But whereas a big female worm can lay more eggs, a big male worm cannot fertilize more females. So big worms tend to become female and small ones male.' :

A third way of determining gender is for the mother to choose the sex of each child. One way of achieving this is peculiar to monogonont rotifers, bees, and wasps: Their eggs become female only if fertilized: Unfertilized eggs hatch into males (which means that males are haploid and have only one set of genes to the females ' two. Again, this makes some sort of sense. It means that a female can found a dynasty even if she never meets a male. Since most wasps are parasites that live inside other insects, this may help a single female who happens on an insect host to start a colony without waiting for a male to arrive. But haplodiploidy is vulnerable to certain kinds of genetic mutiny. For example, in a wasp called Nasonia, there is a rare supernumerary chromosome called PSR, inherited through the male line, that causes any female egg in which it finds itself to become a male by the simple expedient of getting rid of all the father 's chromosomes except itself.

Reduced to just the haploid maternal complement of chromosomes, the egg develops into a male. PSR is found where females predominate and has the advantage that it is in the rare, and therefore sought-after, gender.'

This, briefly, is the theory of sex allocation: Animals choose the appropriate gender for their circumstances unless forced to rely on the genetic lottery of sex chromosomes: But in recent years biologists have begun to realize that the genetic lottery of sex chromosomes is not incompatible with sex allocation. If they could distinguish between X and Y sperm, even birds and mammals could bias the sex ratios of their offs pring, and they would be selected to do so in exactly the same way as crocodiles and nematodes—to produce more of the gender that most benefits from being bigger when the offspring are likely to be big."

GENETIC MUTINY AND GENDER

::: 115 :::

PRIMOGENITURE AND PRIMATOLOGY

In the course of the neo-Darwinian revolution of the 1960s and 1970s, Britain and America each produced a grand old revolutionary whose intellectual dominance remains secure to this day: John Maynard Smith and George Williams, respectively: But each country also produced a brilliant young Turk whose precocious intellect exploded on the world of biology like a flare: Britain 's prodigy was Bill Hamilton, whom we have already met: America ' s was Robert Trivers, who as a Harvard student in the early 1970s conceived a whole raft of new ideas that proved far ahead of his time: Trivers is a legend in biology, as he is the first ingenuously to confirm: Unconventional to the point of eccentricity, he divides his time between watching lizards in Jamaica and thinking in a redwood grove near Santa Cruz, California: One of his most provocative ideas, conceived jointly with fellow student Dan Willard in 1973, may hold the key to understanding one of the most potent and yet simple questions a human being ever asks: "Is it a boy or a girl?"'

If you include Barbara and Jenna Bush, daughters of the forty-third president of the United States, it is a curious statistical fact that all the presidents have between them had ninety sons and only sixty-three daughters. A sex ratio of 6o percent male in such a large sample is markedly different from the population at large, though how it came about nobody can guess—probably by pure chance. Yet presidents are not alone. Royalty, aristocrats, and even well-off American settlers have all consistently produced slightly more sons than daughters. So do well-fed opossums, hamsters, coypus, and high-ranking spider monkeys. The Trivers-Willard theory links these diverse facts.49

Trivers and Willard realized that the same general principle of sex allocation, which determines the gender of nematodes and fish, applies even to those creatures that cannot change sex but that take care of their young: They predicted that animals would be found to have some systematic control over the sex ratio of their own young: Think of it as a competition to have the most grandchildren. If males are polygamous, a successful son can give you far

::: 116 :::

The Red Queen

more grandchildren than a successful daughter, and an unsuccessful son will do far worse than an unsuccessful daughter because he will fail to win any mates at all: A son is a high-risk, high-reward reproductive option compared with a daughter: A mother in good condition gives her offspring a good start in life, increasing the chances of her sons ' winning harems as they mature: A mother in poor condition is likely to produce a feeble son who will fail to mate at all, whereas her daughters can join harems and reproduce even when not in top condition: So you should have sons if you have reason to think they will do well and daughters if you have reason to think they will do poorly—relative to others in the population:'°

Therefore, said Trivers and Willard, especially in polygamous animals, parents in good condition probably have male-biased litters of young; parents in poor condition probably have female-biased litters: Initially this was scoffed at as farfetched conjecture, but gradually it has received grudging respect and empirical support.

Consider the case of the Venezuelan opossum, a marsupial that looks like a large rat and lives in burrows. Steven Austad and Mel Sunquist of Harvard were intent on disproving the Trivers-Willard theory: They trapped and marked forty virgin female opossums in their burrows in Venezuela: Then they fed 125 grams of sardines to each of twenty opossums every two days by leaving the sardines outside the burrows, no doubt to the delight and astonish-ment of the opossums: Every month thereafter they trapped the animals again, opened their pouches, and sexed their babies. Among the 256 young belonging to the mothers who had not been fed sardines, the ratio of males to females was exactly one to one: Among the 270 from mothers who had been fed sardines, the sex ratio was nearly I:4 to I: Well-fed opossums are significantly more likely to have sons than poorly fed ones."

The reason? The well-fed opossums had bigger babies; bigger males were much more likely to win a harem of females in later life than smaller males: Bigger females were not much more likely to have more babies than small females: Hence, the mother opossums were investing in the gender most likely to reward them with many grandchildren.

GENETIC MUTINY AND GENDER

::: 117:::

Opossums are not alone. Hamsters reared in the laboratory can be made to have female-biased litters by keeping them hungry during adolescence or pregnancy. Among coypus (large aquatic rodents), females in good condition give birth to male-biased litters; those in poor condition give birth to female-biased litters. In white-tailed deer, older mothers or yearlings in poor condition have female fawns more often than by chance alone: So do rats kept in conditions of stress. But in many ungulates (hoofed animals), stress or poor habitat has the opposite effect, inducing a male-biased sex ratio.52

Some of these effects can be easily explained by rival theories. Because males are often bigger than females, male embryos generally grow faster and are more of a strain on the mother.

Therefore, it pays a hungry hamster or a weak deer to miscarry a male-biased litter and retain a female-biased one: Moreover, proving biased sex ratios at birth is not easy, and there have been so many negative results that some scientists maintain the positive ones are merely statistical flukes. (If you toss: a coin long enough, sooner or later you will get twenty heads in a row.) But neither explanation can address the opossum study and others like it. By the late 1980s many biologists were convinced that Trivers and Willard were right at least some of the time:"

The most intriguing results, however, were those that concerned social status. Tim Clutton-Brock of Cambridge University studied red deer on the island of Rhum off the Scottish coast. He found that the mother 's condition had little effect on the gender of her calves, but her rank within the social group did have an effect: Dominant females were slightly more likely to have sons than daughters:"

Clutton-Brock's results alerted primatologists,who had long suspected biased sex ratios in various species of monkey. In the Peruvian spider monkeys studied by Meg Symington, there was a clear association between rank and gender of offspring: Of twenty-one offspring born to lowest-ranked females, twenty-one were female; of eight born to highest-ranked females, six were male; those in the middle ranks had an equal sex ratio."

::: 118 :::

The Red Queen

But an even greater surprise was in store when other monkeys revealed their gender preferences. Among baboons, howler monkeys, rhesus macaques, and bonnet macaques, the opposite preference prevailed: high-ranking females gave birth to female offspring, and low-ranking females give birth to male offspring. In the eighty births to twenty female Kenyan baboons studied by Jeanne Altmann of the University of Chicago, the effect was so pronounced that high-ranking females were twice as likely to have daughters as low-ranking ones. Subsequent studies have come to less clear conclusions, and a few scientists believe that the monkey results are explained by chance. But one intriguing hint suggests otherwise."

Symington 's spider monkeys preferred sons when dominant, whereas the other monkeys preferred daughters. This may be no accident: In most monkeys (including howlers, baboons, and macaques) males leave the troop of their birth and join another at puberty—so-called male-exogamy: In spider monkeys the reverse applies: Females leave home. If a monkey leaves the troop it is born into, it has no chance to inherit its mother 's rank: Therefore, high-ranking females will have young of whatever gender stays at home in order to pass on the high rank to them. Low-ranking females will have young of whatever gender leaves the troop in order not to saddle the young with low rank. Thus high-ranking howlers, baboons, and macaques have daughters; high-ranking spider monkeys have sons."

This is a highly modified Trivers-Willard effect, known in the trade as a local-resource competition model. 58 High rank leads to a sex bias in favor of the gender that does not leave at puberty.

Could it possibly apply to human beings?

DOMINANT WOMEN HAVE SONS?

Mankind is an ape. Of the five species of ape, three are social, and in two of those, chimpanzees and gorillas, it is the females that leave the home troop. In the chimpanzees of Gombe Stream in Tan-GENETIC MUTINY AND GENDER

::: 119 :::

zania studied by Jane Goodall, young males born to senior females tend to rise to the top faster than males born to junior females.

Therefore, female apes of high social status "should "—according to the Trivers-Willard logic—have male young and those of low social status "should " have female young." Now men are not excessively polygamous, so the rewards of large size to men is not great: big men do not necessarily win more wives, and big boys do not necessarily become big men. But humans are a highly social species whose society is nearly always stratified in some way. One of the prime, indeed, ubiquitous perquisites of high social status in human males, as in male chimpanzees, is high reproductive success.

Wherever you look, from tribal aborigines to Victorian English-men, high-status males have had—and mostly still do have—more children than low-status ones. And the social status of males is very much inherited, or rather passed on from parent to child, whereas females generally leave home when they marry. I am not implying that the tendency for the female to travel to the male 's home when she marries is instinctive, natural, inevitable, or even desirable, but I am noting that it has been general. Cultures in which the opposite happens are rare. So human society, like ape society but unlike most monkey society, is a female-exogamous patriarchy, and sons inherit their father 's (or mother 's) status more than daughters inherit their parents ' status. Therefore, says Trivers-Willard, it would pay dominant fathers and high-ranking mothers, or both, to have sons and subordinates to have daughters: Do they?

The short answer is that nobody knows. American presidents, European aristocrats, various royals, and a few other elites have been suspected of having male-biased progeny at birth. In racist societies, subject races seem to be slightly more likely to have daughters than sons. But the subject is too fraught with potential complicating factors for any such statistics to be reliable. For example, merely by ceasing to breed once they have a boy—which those interested in dynastic succession might do—people would have male-biased sex ratios at birth. However, there certainly are no studies showing reliably unbiased sex ratios. And there is one tantalizing study from New Zealand that hints at what might be found

::: 120 :::

The Red Queen

if anthropologists and sociologists cared to look into the matter. b°

As early as 1966, Valerie Grant, a psychiatrist at the University of Auckland in New Zealand, noticed an apparent tendency for women who subsequently gave birth to boys to be more emotionally independent and dominating than those who gave birth to girls: She tested the personalities of eighty-five women in the first trimester of pregnancy using a standard test designed to distinguish "dominant " from "subordinate " personalities—whatever that may mean.

Those who later gave birth to daughters averaged 1:3 5 on the dominance scale (from 0 to 6): Those who later gave birth to sons averaged 2.26, a highly significant difference. The interesting thing about Grant' s work is that she began before the Trivers-Willard theory was published, in the 1960s. "I arrived at the idea quite independently of any study in any of the areas in which such a notion might reasonably arise, " she told me, "For me the idea arose out of an unwillingness to burden women with the responsibility for the 'wrong ' sex child." b" Her work remains the only hint that maternal social rank affects the gender of children in the way that the Trivers-Willard-Symington theory would predict. If it proves to be more than a chance result, it immediately leads to the question of how people are unconsciously achieving something that they , have been consciously striving to achieve for generations unnumbered:

SELLING GENDER

Almost no subject is more steeped in myth and lore than the business of choosing the gender of children. Aristotle and the Talmud both recommended placing the bed on a north-south axis for those wanting boys. Anaxagoras 's belief that lying on the right side during sex would produce a boy was so influential that centuries later some French aristocrats had their left testicles amputated. At least posterity had its revenge on Anaxagoras, a Greek philosopher and client of Pericles: He was killed by a stone dropped by a crow, no doubt a retrospective reincarnation of some future French marquis who cut off his left testicle and had six girls in a row."

GENETIC MUTINY AND GENDER

::: 12.1 :::

It is a subject that has always drawn charlatans like blow-flies to a carcass: The old wives ' tales that have answered the pleas of fathers for centuries are mostly ineffective: The Japanese Sex Selection Society promotes the use of calcium to increase the chances of having a son—with little effect: A book published in 1991 by two French gynecologists claimed precisely the opposite: that a diet rich in potassium and sodium but poor in calcium and magnesium gives a woman an 80 percent chance of conceiving a son if consumed for six weeks before fertilization: A company offering Americans "gender kits " for $50 was driven into bankruptcy after the regulators claimed it was deceiving the consumer:"

The more modern and scientific methods are somewhat more reliable. They all rely on trying to separate in the laboratory Y-bearing (male) sperm from X-bearing (female) sperm based on the fact that the latter possess 3.5 percent more DNA. The widely licensed technique invented by an American scientist, Ronald Ericsson, claims a 70 percent success rate from forcing the sperm to swim through albumen, which supposedly slows down the heavier X-bearing sperm more than it does the Y-bearing sperm, thus separating them. By contrast, Larry Johnson of the United States Department of Agriculture has developed a technique that works efficiently (about 70 percent male offspring and 90 percent female:) It dyes the sperm DNA with a fluorescent dye and then allows the sperm to swim in Indian file past a detector: According to the brightness of the sperm 's fluorescence, the detector sorts them into two channels: The Y-bearing sperm, having smaller amounts of DNA, are slightly less brightly fluorescent: The detectors can sort sperm at ►oo,000 a second: Early concerns that the dyes might cause genetic damage have been largely allayed by animal experiments and this technique is now being used in the United States, mostly by people who wish to " balance the family"—have a girl after a string of boys, or vice versa:

Curiously, if humans were birds, it would be much easier to alter the chances of having young of one gender or the other because in birds the mother determines the gender of the embryo, not the father: Female birds have X and Y chromosomes (or some-

::: 122 :::

The Red Queen

times just one X), while male birds have two Xs. So a female bird can simply release an egg of the desired gender and let any sperm fertilize it. Birds do make use of this facility. Bald eagles and some other hawks often give birth to females first and males second.

This enables the female to get a head start on the male in the nest, which enables it to grow larger (and female hawks are always larger than males). Red-cockaded woodpeckers raise twice as many sons as daughters and use spare sons as nannies for subsequent broods.

Among zebra finches, as Nancy Burley of the University of California at Santa Cruz discovered, " attractive" males mated with "unattractive " females usually have more sons than daughters, and vice versa. Attractiveness in this species can be altered by the simple expedient of putting red (attractive) or green (unattractive) bands on the male 's legs, and black (attractive) or light blue (unattractive) on the female 's legs. This makes them more or less desirable to other zebra finches as mates."

But we are not birds: The only way to be certain of rearing a boy is to kill a girl child at birth and start again, or to use amnio-centesis to identify the gender of the fetus and then abort it if it 's a girl. These repugnant practices are undoubtedly on offer in various parts of the world. The Chinese, deprived of the chance to have more than one child, killed more than 250,000 girls after birth between 1979 and 1984.66 In some age groups in China, there are 122 boys for every 100 girls. In one recent study of clinics in Bombay, of 8,000 abortions, 7,997 were of female fetuses."

It is possible that selective spontaneous abortion also explains much of the animal data. In the case of the coypu, studied by Morris Gosling of the University of East Anglia, females in good condition miscarry whole litters if they are too female-biased, and they start again. Magnus Nordborg of Stanford University, who has studied the implications of sex-selective infanticide in China, believes that such biased miscarriage could .explain the baboon data. But it seems a wasteful way to proceed: 68

There are many well-established natural factors that bias the sex ratio of human offspring, proving that it is at least possible. The most famous is the returning-soldier effect. During and GENETIC MUTINY AND GENDER

::: 123 :::

immediately after major wars, more sons are born than usual in the belligerent countries as if to replace the men that died. (This would make little sense; the men born after wars will mate with their contemporaries, not with those widowed by the war). Older fathers are more likely to have girls, but older mothers are more likely to have boys. Women with infectious hepatitis or schizophre-nia have slightly more daughters than sons: So do women who smoke or drink. So did women who gave birth after the thick London smog of 1952. So do the wives of test pilots, abalone divers, clergymen, and anesthetists. In parts of Australia that depend on rainfall for drinking water, there is a clear drop in the proportion of sons born 320 days after a heavy storm fills the dams and churns up the mud. Women with multiple sclerosis have more sons, as do women who consume small amounts of arsenic."

Finding the logic in this plethora of statistics is beyond most scientists at this stage. William James of the Medical Research Council in London has for some years been elaborating a hypothesis that hormones can influence the relative success of X

and Y sperm: There is a good deal of circumstantial evidence that high levels of the hormone gonadotrophin in the mother can increase the proportion of daughters and that testosterone in the father can increase the proportion of sons.'°

Indeed, Valerie Grant 's theory suggests a hormonal explanation for the returning-soldier effect: that during wars women adopt more dominant roles, which affects their hormone levels and their tendency to have sons. Hormones and social status are closely related in many species; and so, as we have seen, are social status and sex ratio of offspring. How the hormones work, nobody knows, but it is possible that they change the consistency of the mucus in the cervix or even that they alter the acidity of the vagina. Putting baking soda in the vagina of a rabbit was proved to affect the sex ratio of its babies as early as 1932."

Moreover, a hormone theory would tackle one of the most persistent objections to the Trivers-Willard theory: that there seems to be no genetic control of the sex ratio. The failure of animal breeders to produce a strain that can bias the gender of its off-

::: 124:::

The Red Quern

spring is glaring: It is not for want of trying: As Richard Dawkins put it: "Cattle breeders have had no trouble in breeding for high milk yield, high beef production, large size, small size, hornless-ness, resistance to various diseases, and fearlessness in fighting bulls: It would obviously be of immense interest to the dairy industry if cattle could be bred with a bias toward producing heifer calves rather than bull calves: All attempts to do this have singular-ly failed."'

The poultry industry is even more desperate to learn how to breed chickens that lay eggs that hatch into chicks of only one gender: At present it employs teams of highly trained Koreans, who guard a close secret that enables them to sex day-old chicks at great speed (though a computer program may soon match them"): They travel all over the world plying their peculiar trade. It is hard to believe that nature is simply unable to do what the Korean experts can do so easily.

Yet this objection is easily answered once the hormonal theory is taken into account. Munching enchiladas in sight of the Pacific Ocean one day, Robert Trivers explained to me why the failure to breed sex-biased animals is entirely understandable: Suppose you find a cow that produces only heifer calves: With whom do you mate those heifers to perpetuate the strain? With ordinary bulls—

diluting the genes in half at once.

Another way of putting it is that the very fact that one segment of the population is having sons makes it rewarding for the other segment to have daughters. Every animal is the child of one male and one female. So if dominant animals are having sons, then it will pay subordinate ones to have daughters. The sex ratio of the population as a whole will always revert to I:I, however biased it becomes in one part of the population, because if it strays from that, it will pay somebody to have more of the rare gender. This insight occurred first to Sir Ronald Fisher, a Cambridge mathematician and biologist, in the 1920s, and Trivers believes it lies at the heart of why the ability to manipulate the sex ratio is never in the genes:

Besides, if social rank is a principal determinant of sex ratio, it would be crazy to put it in the genes, for social rank is GENETIC MUTINY AND GENDER

::: 125 :::

almost by definition something that cannot be in the genes. Breeding for high social rank is a futile exercise in Red Queen running.

Rank is relative. "You can't breed for subordinate cows, " said Trivers as he munched. "You just create a new hierarchy and reset the thermostat. If all your cows are more subordinate, then the least subordinate will be the most dominant and have appropriate levels of hormones: " Instead, rank determines hormones, which determine sex ratio of offspring."

REASON'S CONVERGENT CONCLUSION

Trivers and Willard predict that evolution will build in an unconscious mechanism for altering the sex ratio of an individual 's progeny. But we like to think we are rational, conscious decision makers, and a reasoning person can arrive at the same conclusions as evolution. Some of the strongest data to support Trivers and Willard comes not from animals but from the human cultural rediscovery of the same logic:

Many cultures bias their legacies, parental care, sustenance, and favoritism toward sons at the expense of daughters. Until recently this was seen as just another example of irrational sexism or the cruel fact that sons have more economic value than daughters. But by explicitly using the logic of Trivers-Willard, anthropologists have now begun to notice that male favoritism is far from universal and that female favoritism occurs exactly where you would most expect it.

Contrary to popular belief a preference for boys over girls is not universal. Indeed, there is a close relationship between social status and the degree to which sons are preferred. Laura Betzig of the University of Michigan noticed that, in feudal times, lords favored their sons, but peasants were more likely to leave possessions to daughters. While their feudal superiors killed or neglected daughters or banished them to convents, peasants left them more possessions: Sexism was more a feature of elites than of the unchronicled masses."

As Sarah Blaffer Hrdy of the University of California at

::: 126 :::

Tht Red Quetn

Davis has concluded, wherever you look in the historical record, the elites favored sons more than other classes: farmers in eighteenth-century Germany, castes in nineteenth-century India, genealogies in medieval Portugal, wills in modern Canada, and pastoralists in modern Africa: This favoritism took the form of inheritance of land and wealth, but it also took the form of simple care. In India even today, girls are often given less milk and less medical attention than boys."

Lower down the social scale, daughters are preferred even today: A poor son is often forced to remain single, but a poor daughter can marry a rich man. In modern Kenya, Mukogodo people are more likely to take daughters than sons to clinics for treatment when they are sick, and therefore more daughters than sons survive to the age of four. This is rational of the Mukogodo parents because their daughters can marry into the harems of rich Samburu and Maasai men and thrive, whereas their sons inherit Mukogodo poverty. In the calculus of Trivers-Willard, daughters are better grandchildren-production devices than sons."

Of course, this assumes that societies are stratified: As Mildred Dickemann of California State University has postulated, the channeling of resources to sons represents the best investment rich people can make when society is class-ridden. The clearest patterns come from Dickemann 's own studies of traditional Indian marriage practices: She found that extreme habits of female infanticide, which the British tried and failed to stamp out, coincided with relatively high social rank in the distinctly stratified society of nineteenth-century India. High-caste Indians killed daughters more than low-caste ones. One clan of wealthy Sikhs used to kill all daughters and live off their wives ' dowries:"

There are rival theories to explain these patterns, of which the strongest is that economic, not reproductive, currency determines a sexual preference: Boys can earn a living and marry without a dowry: But this fails to explain the correlation with rank. It predicts, instead, that lower social classes would favor sons, not higher ones, for they can least afford daughters. If instead grandchildren production was the currency that mattered, Indian marriage prac-GENETIC MUTINY AND GENDER

::: 127 :::

tices make more sense. Throughout India it has always been the case that women more than men can "marry up, " into a higher social and economic caste, so daughters of poor people are more likely to do well than sons. In Dickemann 's analysis, dowries are merely a distorted echo of the Trivers-Willard effect in a female-exogamous species: Sons inherit the status necessary for successful breeding; daughters have to buy it. If you have no wealth to pass on, use what you have to buy your daughter a good husband. 79

Trivers and Willard predict that male favoritism in one part of society will be balanced by female favoritism elsewhere if only because it takes one of each to have a baby—the Fisher logic again.

In rodents the division seems to be based on maternal condition. In primates it seems to be based on social rank. But baboons and spider monkeys take for granted the fact that their societies are strictly stratified. Human beings do not. What happens in a modern, relatively egalitarian society?

In that uniform middle-class Eden known as California, Hrdy and her colleague Debra Judge have so far been unable to detect any wealth-related sex bias in the wills people leave when they die. Perhaps the old elite habit of preferring boys to girls has at last been vanquished by the rhetoric of equality. 8o But there is another, more sinister consequence of modern egalitarianism. In some societies the boy-preferring habit seems to have spread from elites to the society at large. China and India are the best examples of this: In China a one-child policy may have led to the deaths of 17 percent of girls. Im one Indian hospital 96 percent of women who were told they were carrying daughters aborted them, while nearly 100 percent of women carrying sons carried them to term. 81 This implies that a cheap technology allowing people to choose the gender of their children would indeed unbalance the population sex ratio.

Choosing the gender of your baby is an individual decision of no consequence to anybody else. Why, then, is the idea inherently unpopular? It is a tragedy of the commons—a collective harm that results from the rational pursuit of self-interest by individuals.

One person choosing to have only sons does nobody else any harm,

::: 128 :::

The Red Queen

but if everybody does it, everybody suffers. The dire predictions range from a male-dominated society in which rape, lawlessness, and a general frontier mentality would hold sway to further increases in male domination of positions of power and influence.

At the very least, sexual frustration would be the lot of many men: Laws are passed to enforce the collective interest at the expense of the individual, just as crossing over was invented to foil outlaw genes. If gender selection were cheap, a fifty-fifty sex ratio would be imposed by parliaments of people as surely as equitable meiosis was imposed by the parliament of the genes.

Chapter 5

THE PEACOCK ' S TALE

Tut, You saw her fair, none else being by, Herself poised with herself in either eye: But in that crystal scales let there be weigh'd Your lady's love against some other maid That I will show you shining at this feast, And she shall scant show well that now seems best:

—William Shakespeare, Romeo and Juliet

The Australian brush turkey builds the best compost heaps in the world. Each male constructs a layered mound of two tons of leaves, twigs, earth, and sand: The mound is just the right size and shape to heat up to the perfect temperature to cook an egg slowly into a chick. Female brush turkeys visit the males ' mounds, lay eggs in them, and depart. When the eggs hatch, the young struggle slowly to the surface of the mound, emerging ready to fend for themselves.

To paraphrase Samuel Butler ( "a hen is just an egg 's way of making another egg "), if the eggs are just the female 's way of making another brush turkey, then the mound is just the male 's way of making another brush turkey. The mound is almost as precisely a product of his genes as the egg is of hers: Unlike the female, though, the male has a residual uncertainty. How does he know that he is the father of the eggs in the mound? The answer, discovered recently by Australian scientists, is that he does not know and, in fact, is often not the father. So why does he build vast mounds to raise other males ' offspring when the whole point of sexual reproduction is for his genes to find a way into the next generation? It turns out that the female is not allowed to lay an egg in the mound until she has agreed to mate with the male; that is his price for the use of the mound. Her price is that he must then accept an egg. It is a fair bargain.

But this puts the mound in an entirely different light. From the male 's point of view the mound is not, after all, his way of making young brush turkeys. It is his way of attracting female

::: 132:::

The Red Queen

brush turkeys to mate with him: Sure enough, the females select the best mounds, and therefore the best mound makers, when deciding where to lay their eggs. The males sometimes usurp one another 's mounds, so the best mound owner may actually be the best mound stealer.

Even if a mediocre mound would do, a female is wise to pick the best so that her sons inherit the mound-building, mound-stealing, and female-attracting qualities of their father. The male brush turkey 's mound is both his contribution to child rearing and a solid expression of his courtship.'

The story of the brush turkey 's mound is a story from the theory of sexual selection, an intricate and surprising collection of insights about the evolution of seduction in animals, which is the subject of this chapter. And, as will become clear in later chapters, much of human nature can be explained by sexual selection.

IS LOVE RATIONAL?

It is sometimes hard even for biologists to remember that sex is merely a genetic joint venture: The process of choosing somebody to have sex with, which used to be known as falling in love, is mysterious, cerebral, and highly selective: We do not regard any and all members of the opposite sex as adequate partners for genetic joint venture. We consciously decide whether to consider people, we fall in love despite ourselves, we entirely fail to fall in love with people who fall in love with us. It is a mightily complicated business.

It is also nonrandom. The urge to have sex is in us because we are all descended from people who had an urge to have sex with each other; those that felt no urge left behind no descendants. A woman who has sex with a man (or vice versa) is running the risk of ending up with a set of genes to partner hers in the next generation: Little wonder that she is prepared to pick those partner genes carefully. Even the most promiscuous woman does not have sex indiscriminately with anyone who comes along: The goal for every female animal is to find a mate with suf-THE PEACOCK ' S TALE

::: 133 :::

ficient genetic quality to make a good husband, a good father, or a good sire. The goal for every male animal is often to find as many wives as possible and sometimes to find good mothers and dams, only rarely to find good wives. In 1972, Robert Trivers noticed the reason for this asymmetry, which runs right through the animal kingdom; the rare exceptions to his rule prove why it generally holds: The sex that invests most in rearing the young—by carrying a fetus for nine months in its belly, for example—is the sex that makes the least profit from an extra mating: The sex that invests the least has time to spare to seek other mates. Therefore, broadly speaking, males invest less and seek quantity of mates, while females invest more and seek quality of mates:'

The result is that males compete for the attention of females, which means that males have a greater opportunity to leave large numbers of offspring than females and a greater risk of not breeding at all: Males act as a kind of genetic sieve: Only the best males get to breed, and the constant reproductive extinction of bad males constantly purges bad genes from the population.' From time to time it has been suggested that this is the "purpose" of males, but that commits the fallacy of assuming evolution designs what is best for the species:

The sieve works better in some species than in others: Elephant seals are so severely sieved that in each generation a handful of males father all the offspring: Male albatrosses are so faithful to their single wives that virtually every male that reaches the right age will breed. Nonetheless, it is fair to state that in the matter of choosing mates, males are usually after quantity and females after quality: In the case of a bird such as a peacock, males will go through their ritual courtship display for any passing female; females will mate with only one male, usually the one with the most elaborately decorated tail: Indeed, according to sexual selection theory, it is the female 's fault that the male has such a ridiculous tail at all: Males evolved long tails to charm females: Females evolved the ability to be charmed to be sure of picking the best males.

This chapter is about a kind of Red Queen contest, one that resulted in the invention of beauty: In human beings, when all

::: 134:::

The Red Queen

practical criteria for choosing a mate—wealth, health, compatibility, fertility—are ignored, what is left is the apparently arbitrary criterion of beauty. It is much the same in other animals. In species where the females get nothing useful from their mates, they seem to choose on aesthetic criteria alone:

ORNAMENTS AND CHOOSINESS

To put it in human terms, we are asking of animals (as we later will of human beings): Are they marrying for money, for breeding, or for beauty? Sexual selection theory suggests that much of the behavior and some of the appearance of an animal is adapted not to help it survive but to help it acquire the best or the most mates.

Sometimes these two—survival and acquiring a mate—are conflict-ing goals: The idea goes back to Charles Darwin, though his thinking on the matter was uncharacteristically fuzzy: He first touched on the subject in On the Origin of Species but later wrote an entire book about it: The Descent of Man and Selection in Relation to Sex:'

Darwin 's aim was to suggest that the reason human races differed from one another was that for many generations the women in each race had preferred to mate with men who looked, say, black or white. In other words, at a loss to explain the useful-ness of black or white skin, he suspected instead that black women preferred black men and white women preferred white men—and posited this as cause rather than effect: Just as pigeon fanciers could develop breeds by allowing only their favorite strains to reproduce, so animals could do the same to one another through selective mate choice.

His racial theory was almost certainly a red herring,' but the notion of selective mate choice was not: Darwin wondered if selective "breeding" by females was the reason that so many male birds and other animals were gaudy, colorful, and ornamented.

Gaudy males seemed a peculiar result of natural selection since it was hard to imagine that gaudiness helped the animal to survive: In fact, it would seem to be quite the reverse: Gaudy males should be more conspicuous to their enemies.

'

THE PEACOCK S TALE

::: 135 :::

Taking the example of the peacock, with its great tail decked with iridescent eyes, Darwin suggested that peacocks have long tails (they are not actually tails but elongated rump feathers that cover the tail) because peahens will mate only with peacocks that have long tails. After all, he observed, peacocks seem to use their tail when courting females. Ever since then the peacock has been the crest, mascot, emblem, and quarry of sexual selection: Why should peahens like long tails? Darwin could only reply: Because I say so. Peahens prefer long trains, he said, because of an innate aesthetic sense—which is no answer at all. And peahens choose peacocks for their tails rather than vice versa because, sperm being active and eggs passive, that is usually the way of the world: Males seduce, females are seduced.

Of all Darwin's ideas, female choice proved the least persuasive: Naturalists were quite happy to accept the notion . that male weapons, such as antlers, could have arisen to help males in the battle for females, but they instinctively recoiled at the frivo-lous idea that a peacock 's tail should be there to seduce peahens.

They wanted, rightly, to know why females would find long tails sexy and what possible value they could bring the hens: For a century after he proposed it, Darwin 's theory of female choice was ignored while biologists tied themselves in furious knots to come up with other explanations. The preference of Darwin 's contempo-rary, Alfred Russel Wallace, was initially that no ornaments, not even the peacock 's tail, required any explanation other than that they served some useful purpose of camouflage. Later he thought they were the simple expression of surplus male vigor. Julian Huxley, who dominated the discussion of the matter for many years, much preferred to believe that almost all ornaments and ritual displays were for intimidating other males: Others believed that the ornaments were aids to females for telling species apart, so that they chose a mate of the right species.' The naturalist Hugh Cott was so impressed by the bright colors of poisonous insects that he suggested all bright colors and gaudy accessories were about warn-ing predators of dangers: Some are. In the Amazon rain forest the butterflies are color-coded: yellow and black means distasteful, blue and green means too quick to catch.' In the 1980s a new version of

::: 136 :::

The Red Queen

this theory was adapted to birds, suggesting that colorful birds are the fastest fliers and are flaunting the fact to hawks and other predators: I 'm fast, so don 't even think of trying to chase me: When a scientist put stuffed male and female pied flycatchers out on perches in a wood, it was the dull females that were attacked first by hawks, not the colorful males.' Any theory, it seemed, was preferred to the idea of female preference for male beauty: Yet it is impossible to watch peacocks displaying and not come away believing that the tail has something to do with the seduction of peahens. After all, that was how Darwin got the idea in the first place; he knew that the gaudiest plumes of male birds were used in courting females and not in other activities: When two peacocks fight or when one runs away from a predator, the tail is kept carefully folded away.'

TO WIN OR TO WOO

It took more than this to establish the fact of female choice. There were plenty of diehards who followed Huxley in thinking courtship was all a matter of competition between males. "Where female choice has been described, it plays an ancillary, and probably less significant, role than competition between males, " wrote British biologist Tim Halliday as late as 1983: 1° Just as a female red deer accepts her harem master, who has fought for the harem, so perhaps a peahen accepts that she will mate with the champion male.

In one sense the distinction does not matter much. Peahens that all pick the same cock and red deer hinds that indifferently submit to the same harem master both end up "choosing " one male from among many. In any case, the peahens ' "choice" may be no more voluntary or conscious than the hinds ': The peahens have merely been seduced rather than won. They may have been seduced by the display of the best male without ever having given the matter a conscious thought—let alone realized that what they were doing was "choosing: " Think of human analogies. Two caricatured cavemen who fought to the death so that the winner could sling the THE PEACOCKS TALE

::: 137 :::

loser's wife over his shoulder and take her away are at one extreme; Cyrano de Bergerac, who hoped to seduce Roxanne with words alone, is at the other. But in between there are thousands of permu-tations: A man can " win" a woman by competing with other men, or he can woo her, or both.

The two techniques—wooing and winning—are equally likely to sieve out the "best" male. The difference is that whereas the first technique will select dandies, the second will select bruis-ers. Thus, bull elephant seals and red deer stags are big, armed, and dangerous. Peacocks and nightingales are aesthetic show-offs.

By the mid-1980s evidence had begun to accumulate that, in many species, females had a large say in the matter of their mating partner: Where males gather on communal display arenas, a male 's success owes more to his ability to dance and strut than to his ability to fight other males."

It took a series of ingenious Scandinavians to establish that female birds really do pay attention to male plumes when choosing a mate. Anders Moller, a Danish scientist whose experiments are famously clever and thorough, found that male swallows with artificially lenghtened tails acquired mates more quickly, reared more young, and had more adulterous affairs than males of normal length. 12 Jakob Hoglund proved that male great snipe, which display by flashing their white tail feathers at passing females, could be made to lure more females by the simple expedient of having white typing-correction fluid painted onto their tails:" The best experiment of all was by Malte Andersson, who studied the widow bird of Africa. Widow birds have thick black tails many times the lengths of their bodies, which they flaunt while flying above the grass.

Andersson caught thirty-six of these males, cut their tails, and either spliced on a longer set of tail feathers or left them shortened. Those with elongated tails won more mates than those with shortened tails or tails of unchanged length:" Tail-lengthening experiments in other species that have unusually long tails have similarly boosted male success:"

So females choose: Definitive evidence that the female preference itself is heritable has so far been hard to come by, but it

::: 138 :::

the Red Queen

would be odd if it were not. A suggestive hint comes from Trinidad where small fish called guppies vary in color according to the stretch of water they inhabit: Two American scientists proved that in those types of guppies in which the males are brightest orange in color, the females show the strongest preference for orange males. 16

This female preference for male ornaments can actually be a threat to the survival of the males: The scarlet-tufted malachite sunbird is an iridescent green bird that lives high on the slopes of Mount Kenya where it feeds on the nectar of flowers and on insects that it catches on the wing. The male has two long tail streamers, and females prefer the males with the longest streamers. By lengthening the tail streamers of some males, shortening those of others, adding weight to those of a third group, and merely adding rings of similar weight to the legs of a fourth, two scientists were able to prove that female-preferred tail streamers are a burden to their bearers. The ones with lengthened or weighted tails were worse at catching insects; the ones with shortened tails were better; the ones with only rings on their legs were as good as normal."

Females choose; their choosiness is inherited; they prefer exaggerated ornaments; exaggerated ornaments are a burden to males. That much is now uncontroversial: Thus far Darwin was right.

DESPOTIC FASHIONS

The question Darwin failed to answer was why: Why on earth should females prefer gaudiness in males? Even if the "preference"

was entirely unconscious and was merely an instinctive response to the superior seduction technique of gaudy males, it was the evolution of the female preference, not the male trait, that was hard to explain.

Sometime during the 1970s it began to dawn on people that a perfectly good answer to the question had been available since 1930. Sir Ronald Fisher had suggested then that females need no better reason for preferring long tails than that other

'

THE PEACOCK S TALE

::: 139 :::

females also prefer long tails. At first such logic sounds suspiciously circular, but that is its beauty. Once most females are choosing to mate with some males rather than others and are using tail length as the criterion—a big once, granted, but we'll return to that—then any female who bucks the trend and chooses a short-tailed male will have short-tailed sons. (This presumes that the sons inherit their father 's short tail.) All the other females are looking for long-tailed males, so those short-tailed sons will not have much success: At this point, choosing long-tailed males need be no more than an arbitrary fashion; it is still despotic. Each peahen is on a treadmill and dare not jump off lest she condemn her sons to celibacy. The result is that the females ' arbitrary preferences have saddled the males of their species with ever more grotesque encumbrances. Even when those encumbrances themselves threaten the life of the male, the process can continue—as long as the threat to his life is smaller than the enhancement of his breeding success: In Fisher 's words: " The two characteristics affected by such a process, namely plumage development in the male and sexual preference in the female, must thus advance together, and so long as the process is unchecked by severe counter-selection, will advance with ever-increasing speed. "i '

Polygamy, incidentally, is not essential to the argument.

Darwin noticed that some monogamous birds have very colorful males: mallards, for example, and blackbirds. He suggested that it would still benefit males to be seductive and so win the first females that are ready to breed, if not the most, and his conjecture has largely been borne out by recent studies. Early-nesting females rear more young than late-nesting ones, and the most vigorous songster or gaudiest dandy tends to catch the early female. In those monogamous species in which both males and females are colorful (such as parrots, puffins, and peewits) there seems to be a sort of mutual sexual selection at work: Males follow a fashion for picking gaudy females and vice versa. 19

Notice, though, that in the monogamous case the male is choosing as well as seducing. A male tern will present his intended with fish, both to feed her and to prove that he can fish well

::: 140 :::

The Red Quern

enough to feed her babies. If he is choosing the earliest female to arrive and she is choosing the best fisherman, they are both employing eminently sensible criteria. It is bizarre even to suggest that choice plays no part in their mating: From terns to peafowl, there is a kind of continuum of different criteria. A hen pheasant, for example, who will get no help from a cock in rearing her young, happily chooses to ignore a nearby cock who is unmated to join the harem of a cock who already has several wives: He runs a sort of protection racket within his territory, guarding his females while they feed in exchange for sexual monopoly over them: The best protector is more use to her than a faithful house-husband: A peahen, on the other hand, does not even get such protection: The peacock provides her with nothing but sperm: 20

Yet there is a paradox here. In the tern 's case, choosing a poor male is a disastrous decision that will leave her chicks liable to starve. In the hen pheasant 's case, choosing the less effective harem defender will apparently leave her inconvenienced. In the peahen 's case, picking the poorest male will leave her hardly affected at all: She gets nothing practical from her mate, so it seems there is nothing to be lost. You would expect, therefore, that the choice would be made most carefully by the tern and least carefully by the peahen.

Appearances suggest the exact opposite. Peahens survey several males and take their time over their decision, allowing each to parade his tail to best advantage. What is more, most of the peahens choose the same male. Terns mate with little fuss. Females are the most choosy where the least seems to be at stake. 21

RUNNING OUT OF GENES

Least at stake? One very important thing is at stake in the peafowl case: a bunch of genes. Genes are the only thing a peahen gets from a peacock, whereas a female tern gets tangible help from the male as well. A tern must demonstrate only paternal proficiency; a peacock must demonstrate that he has the best genes on offer.

Peacocks are among the few birds that run a kind of market

'

THE PEACOCK S TALE

::: 141 :::

in seduction techniques, called a "lek," after the Swedish word for play. Some grouse, several birds of paradise and manakins, plus a number of antelope, deer, bats, fish, moths, butterflies, and other insects also indulge in lekking. A lek is a place where males gather in the breeding season, mark out little territories that are clustered together, and parade their wares for visiting females: The characteristic of the lek is that one or a few males, usually those that display near its center, achieve most of the matings: But the central position of a successful male is not the cause of his success so much as the consequence: Other males gather around him: The sage grouse of the American West has been the best studied of lekking birds: It is an extraordinary experience to drive out to the middle of Wyoming before dawn, stop the car on a fea-tureless plain that looks like every other one, and see it come alive with dancing grouse. Each knows his place; each runs through his routinòf inflating the air sacs in his breast and strutting forward, bouncing the fleshy sacs through his feathers for all the world like a dancer at the Folies Bergere. The females wander through this market, and after several days of contemplating the goods on offer, they mate with one of the males: That they are choosing, not being forced to choose, seems obvious: The male does not mount the female until she squats in front of him. Minutes later his job is done, and her long and lonely parenthood is beginning. She has received only one thing from her mate—genes—and it looks as if she has tried hard to get the best there were to be had.

Yet the problem of greatest choosiness in the species where choice least matters reappears: A single sage grouse cock may perform half of all the matings at one lek; it is not unknown for this top male to mate thirty or more times in a morning. 22 The result is that in the first generation the genetic cream is skimmed from the surface of the population, in the second the cream of the cream, in the third the cream of the cream of the cream, and so on. As any dairy farmer can attest, this is a procedure that quickly becomes pointless. There is just not enough separability in cream to keep taking the thickest layer. It is the same for sage grouse. If 10 percent of the males father the next generation, pretty soon all the

::: 142 :::

The Red Queen

females and all the males will be genetically identical, and there will be no point in selecting one male over another because they are all the same: This is known as the " lek paradox, " and it is the hurdle that all modern theories of sexual selection attempt to leap. How they do so is the subject of the rest of this chapter.

MONTAGUES AND CAPULETS

It is time to introduce the great dichotomy. Sexual selection theory is split into two warring factions. There is no accepted name for each party; most people call them " Fisher " and "Good-genes. "

Helena Cronin, who has written a masterful history of the sexual selection debate, 2' prefers "good-taste " and "good-sense. " They are sometimes also known as the "sexy-son " versus the "healthy-offspring" theories.

The Fisher (sexy-son, good-taste) advocates are those who insist that the reason peahens prefer beautiful males is that they seek heritable beauty itself to pass on to their sons, so that those sons may in turn attract females. The Good-geners (healthy-offspring, good-sense) are those who believe that peahens prefer beautiful males because beauty is a sign of good genetic qualities—

disease resistance, vigor, strength—and that the females seek to pass these qualities on to their offspring: Not all biologists admit to being members of one school or the other: Some insist there can be a reconciliation; others would like to form a third party and cry with Mercutio, "A plague on both your houses. " But nonetheless the distinction is as real as the enduring feud between Capulets and Montagues in Romeo and Juliet: This is biological civil war:

The Fisherians derive their ideas mostly from Sir Ronald Fisher ' s great insight about despotic fashion, and they follow Darwin in thinking the female 's preference for gaudiness is arbitrary and without purpose. Their position is that females choose males according to the gaudiness of their colors, the length of their plumes, the virtuosity of their songs, or whatever, because the

'

THE PEACOCK S TALE

::: 143 :::

species is ruled by an arbitrary fashion for preferring beauty that none dares buck. The Good-gene people follow Alfred Russel Wallace (though they do not know it) in arguing that arbitrary and foolish as it may seem for a female to choose a male because his tail is long or his song loud, there is method in her madness. The tail or the song tells each female exactly how good the genes are of each male. The fact that he can sing loudly or grow and look after a long tail proves that he can father healthy and vigorous daughters and sons just as surely as the fishing ability of a tern tells his mate that he can feed a growing family. Ornaments and displays are designed to reveal the quality of genes.

The split between Fisher and Good-genes began to emerge in the 1970s once the fact of female choice had been established to the satisfaction of most. Those of a theoretical or mathematical bent—the pale, eccentric types umbilically attached to their computers—became Fisherians. Field biologists and naturalists—

bearded, besweatered, and booted—gradually found themselves Good-geners."

1S CHOOSING CHEAP?

The first round went to the Fisherians. Fisher 's intuition was fed into mathematical models and emerged intact. In the early 1980s three scientists programmed their computers to play an imaginary game of females choosing long-tailed males and bearing sons that had the long tails and daughters that shared the preference of their mothers. The longer the male 's tail, the greater his mating success but the smaller his chances of surviving to mate at all: The scientists' key discovery was that there exists a "line of equilibrium " on which the game can stop at any point. On that line the handicap to a female ' s sons of having a long tail is exactly balanced by the advantage those sons have in attracting a mate.''

In other words, the choosier the females, the brighter and more elaborate the male ornaments will be, which is exactly what you find in nature. Sage grouse are elaborately ornamented, and

::: 144 :::

The Red Queen

only a few males get chosen; terns are unornamented, and most males win mates.

The models also showed that the process could run away from the line of equilibrium with Fisher 's "ever-increasing speed "

but only if females vary in their (heritable) preference and if the male 's ornament is not much of an encumbrance to him. These are fairly unlikely conditions except early in the process when a new preference and a new trait have just emerged.

But the mathematicians discovered more. It mattered greatly if the process of choosing was costly to females. If in deciding which male to mate with a female wastes time that could be more profitably spent incubating eggs or she exposes herself to the risk of being caught by an eagle, then the line no longer stands: As soon as the species reaches it, and the advantages of long tails are balanced by their disadvantages, there is no net benefit to being choosy, so the costs of choice will drive females into indifference.

This looked to be fatal to the whole Fisher idea, and there was brief interest in another version of it (which is known as the "sexy-son "

theory) that suggested sexy husbands made bad fathers—a clear cost to being a choosy female:"

Luckily, another mathematical insight came to the rescue.

The genes that cause the elaborate ornament or long tail to appear are subject to random mutation. The more elaborate the ornament, the more likely that a random mutation will make the ornament less elaborate, not more. Why? A mutation is a wrench thrown into the genetic works: Throwing a wrench into a simple device, such as a bucket, may not alter its function much, but throwing a wrench into a more complicated device, such as a bicycle, will almost certainly make it less good as a bicycle: Thus, any change in a gene will tend to make the ornament smaller, less symmetrical, or less colorful: This "mutational bias " is sufficient, according to the mathematicians, to make it worth the female 's while to choose an ornamented male because it means that any defect in the ornament might otherwise be inherited by the sons; by choosing the most elaborate ornament she is choosing the male with the fewest mutations: The mutational bias is also sufficient, perhaps, to defeat the

'

THE PEACOCK S TALE

::: 145 :::

central conundrum that we set the theories earlier—the fact that if the best genetic cream of the cream is taken off each generation, there will soon be no separability left in the cream. Mutational bias keeps turning some,of the cream back into milk."

The result of a decade of mathematical games, then, has been 'to prove that the Fisherians are not wrong. Arbitrary ornaments can grow elaborate for no other reason than that females discriminate between males and end up following arbitrary fashions; and the more they discriminate, the more elaborate the ornaments become: What Fisher said in 1930 was right, but it left a lot of naturalists unconvinced for two reasons: First, Fisher assumed part of what he set out to prove: That females are already choosy is crucial to the theory: Fisher himself had an answer for this, which was that initially females chose long-tailed males for more utilitarian reasons—for example, that it indicated their superior size or vigor: This is not a foolish idea; after all, even the most monogamous species, in which every male wins a female (such as terns), are choosy. But it is an idea borrowed from the enemy camp: And the Good-geners can reply: "If you admit that our idea works initially, why rule it out later on? "

The second reason is more mundane. Proving that Fisher 's runaway selection could happen and the ornament get bigger with ever-increasing speed does not prove that it does happen: Computers are not the real world: Nothing could satisfy the naturalists but an experiment, one demonstrating that the sexiness of sons drove the evolution of an ornament:

Such an experiment has never been devised, but those, like me, with a bias toward the Fisherians find several lines of argument fairly persuasive: Look around the world and what do you see? You see that the ornaments we are discussing are nothing if not arbitrary: Peacocks have eyes in their train; sage grouse have inflatable air sacs and pointed tails; nightingales have melodies of great variety and no particular pattern; birds of paradise grow bizarre feathers like pennants; bower birds collect blue objects. It is a cacophony of caprice and color: Surely if sexually selected ornaments told a tale of their owner's vigor, they would not be so utterly random.

::: 146 :::

The Red Queen

One other piece of evidence seems to weigh in the balance on the side of Fisher—the phenomenon of copying. If you watch a lek carefully, you see that the females often do not make up their own minds individually; they follow one another. Sage grouse hens are more likely to mate with a cock who has just mated with another hen. In black grouse, which also lek, the cocks tend to mate several times in a row if at all. A stuffed female black grouse (known in this species as a greyhen) placed in a male 's territory tends to draw other females to that territory—though not necessarily causing them to mate. De In guppy fish, females that have been allowed to see two males, one of which is already courting a female, subsequently prefer that male to the other even if the female that was being courted is no longer present."

Such copying is just what you would expect if Fisher was right because it is fashion-following for its own sake. It hardly matters whether the male chosen is the "best" male; what counts is that he is the most fashionable, as his sons will be. If the Good-geners are right, females should not be so influenced by each other 's views. There is even a hint that peahens try to prevent one another from copying, which would also make sense to a follower of Fisher.'° If the goal is to have the sexiest son in the next generation, then one way of doing that is to mate with the sexiest male; a second way is to prevent other females from mating with the sexiest male.

ORNAMENTAL HANDICAPS

If females choose males for the sexiness of their future sons, why shouldn 't they go for other genetic qualities, too? The Good-geners think that beauty has a purpose. Peahens choose genetically superior males in order to have sons and daughters who are equipped to survive as well as equipped to attract mates.

The Good-geners can marshal as much experimental support as the Fisherians. Fruit flies given a free choice of mate produce young that prove tougher in competition with the young of THE PEACOCKS TALE

::: 147:::

those not allowed to choose." Female sage grouse, black grouse, great snipe, fallow deer, and widow birds all seem to prefer the males on their leks that display most vigorously. 32 If a stuffed greyhen is put on the boundary between two blackcocks ' dancing grounds, the two males fight over the right to monopolistic necrophilia. The winner is usually the male who is most attractive to females, and he is also more likely to survive the next six months than the other male. This seems to imply that attracting females is not the only thing he is good at; he is also good at surviving." The brighter red a male house finch is, the more popular he is with the females; but he is also a better father—he provides more food for the babies—and will live longer because he is genetically more disease-resistant: By choosing the reddest male on offer, females are therefore getting superior survival genes as well as attractiveness genes.34

It is hardly surprising to find that the males best at seduction tend to be the best at other things as well; it does not prove that females are seeking good genes for their offspring. They might be avoiding feeble males lest they catch a virus from them: Nor do such observations damage the idea that the most important thing a sexy male can pass on to his sons is his sexiness—the Fisher idea.

They merely suggest that he can also pass on other attributes.

Consider, though, the case of Archbold 's bowerbird, which lives in New Guinea. As in other bowerbirds, the male builds an elaborate bower of twigs and ferns and therein tries to seduce females: The female inspects the bower and mates with the male if she likes the workmanship and the decorations, which are usually objects of one unusual color. What is peculiar about Archbold 's bowerbird is that the best decorations consist of feathers from one particular kind of bird of paradise, known as the King of Saxony.

These feathers, which are several times longer than the original owner 's body and stem from just above his eye, are like a car 's antenna sporting dozens of square blue pennants. Because they are molted once a year, do not grow until the bird of paradise is four years old, and are much in demand among local tribesmen, the plumes must be very hard for the bowerbird to acquire: Once

::: 148 :::

The Red Queen

acquired they must be guarded against other jealous male bowerbirds anxious to steal them for their own bowers: So, in the words of Jared Diamond, a female bowerbird who finds a male that has decorated his bower with King of Saxony plumes knows "that she has located a dominant male who is terrific at finding or stealing rare objects and defeating would-be thieves:"

So much for the bowerbird: What about the bird of paradise itself, the rightful owner of the plumes? The fact that he survived long enough to grow plumes, grew longer ones than any other male nearby, and kept them in good condition would be an equally reliable indicator of his genetic quality. But it reminds us of the thing that most puzzled Darwin and got the whole debate started: If the point of the plumes is to indicate his quality, might not the plumes themselves affect his quality? After all, every tribesman in New Guinea is out to get him, and every hawk will find him easier to spot: He may have indicated that he is good at surviving, but his chances of survival are now lower for having the plumes: They are a handicap. How can a system of females choosing males that are good at surviving encumber those males with handicaps to survival?

It is a good question with a paradoxical answer, for which we owe a debt of thanks to Amotz Zahavi, a mercurial Israeli scientist: He saw in 1975 that the more a peacock 's tail or a bird of paradise' s plumes handicapped the male, the more honest the signal was that he sent the female. She could be assured by the very fact of his survival that the long-tailed male in front of her had been through a trial and passed: He had survived despite being handicapped: The more costly the handicap, the better it was as a signal of his genetic quality; therefore, peacocks ' tails would evolve faster if they were handicaps than if they were not. This is the reverse of Fisher ' s prediction that peacocks ' tails should gradually cease evolving once they become severe handicaps:'°

It is an appealing—and familiar—thought: When a Maasai warrior killed a fierce beast to prove himself to a potential mate, he was running the risk of being killed but was also showing that he had the necessary courage to defend a herd of cattle. Zahavi 's

" handicap" was only a version of such initiation rituals, yet it was attacked from all sides, and the consensus was that he was wrong.

THE PEACOCK ' S TALE

::: 149:::

The most telling argument against it was that the sons would inherit the handicap as well as the good genes, so they would be encumbered to the same degree as they were endowed. They would be no better off than if they were unencumbered and unsexy."

In recent years, however, Zahavi has been vindicated. Mathematical models proved that he might be right and his critics wrong." His vindicators have added to his theory two subtleties that lend it special relevance to the Good-gene theory of sexual selection. The first is that handicaps might (perhaps must) not only affect survival and reflect quality but also do so in a graduated way; the weaker the male, the harder it would be to produce or maintain a tail of a given length. And indeed, experiments on swallows have shown that birds promoted above their station, by being given longer tail streamers than they grew naturally, could not the next time grow as long a tail as before; carrying the extra handicap had taken its toll: 39 The second is that the handicapping ornament might be designed so as best to reveal deficiency: After all, life would be a lot easier for swans if they were not white, as anybody who has tried swimming in a lake in a wedding dress would know.

Swans do not become white until they are a few years old and ready to breed; perhaps being whiter than white proves to a skeptical swan that its suitor can spare the time from feeding to clean his plumage.

The vindication of Zahavi played a critical role in reignit-ing the debate between Fishererians and Good-geners. Until that happened, Good-gene theories could work only if the ornaments they resulted in were not encumbrances to the males: Thus, a male might advertise the quality of his genes, but to do so at a high cost to himself would be counterproductive unless there were a sexy-son effect.

LOUSY MALES

The handicap theory now comes face-to-face with the central conundrum of sexual selection: This is the lek paradox: that peahens are constantly skimming off the cream of the genetic cream by

::: 150 :::

The Red Queen

choosing only the very few best males to mate with, and as a result, within a very few generations, no variety is left to choose from: The good-gene assertion that mutations are likely to make ornaments and displays less effective provides a partial answer, but it is not a persuasive one: After all, it argues only for not choosing the worst rather than for choosing the best:

Only the Red Queen can solve our dilemma. What sexual selection theory seems to have concluded is that females are constantly running (by being so selective) but are staying in the same place (having no variety to select from). When we find that, we should be on the lookout for some ever-changing enemy, some arms-race rival. It is here that we meet Bill Hamilton again: We last encountered him when discussing the idea that sex itself is an essential part of the battle against disease. If the main purpose of sex is to grant your descendants immunity from parasites, then it follows directly that it makes sense to seek a mate with parasite-resistance genes: AIDS has reminded us all too forcibly of the value of choosing a healthy sexual partner, but similar logic applies to all diseases and parasites: In 1982, Hamilton and a colleague, Marlene Zuk (now at the University of California at Riverside), suggested that parasites might hold the key to the lek paradox and to gaudy colors and peacocks ' tails, for parasites and their hosts are continually changing their genetic locks and keys to outwit each other. The more common a particular strain of host is in one generation, the more common the strain of parasite is that can overcome its defenses in the next. And vice versa: Whatever strain of host is most resistant to the prevalent strain of parasite will itself be the prevalent strain of host in the next generation. Thus, the most disease resistant male might often turn out to be the descendant of the least resistant one in a previous generation: The lek paradox is thus solved at a stroke: By choosing the healthiest male in each generation, females will be picking a different set of genes each time and never run out of genetic variety to select from.'°

The Hamilton-Zuk parasite theory was bold enough, but

*

the two scientists did not stop there. They looked up the data for 1 09 species of bird and found that the most brightly colored

'

THE PEA0OCK S TALE

::: 151 :::

species were also the ones most troubled by blood parasites. That claim has been challenged and much debated, but it seems to hold up: Zuk found the same in a survey of 526 tropical birds, and others found it to be true of birds of paradise and some species of freshwater fish"—the more parasites, the showier the species. Even among human beings, the more polygamous a society, the greater its parasite burden, though it is not clear if this means anything."Z

And these might be no more than suggestive coincidences; correlation does not imply cause. Three kinds of evidence are needed to turn their conjecture into a fact: first, that there are regular genetic cycles in hosts and parasites; second, that ornaments are especially good at demonstrating freedom from parasites; third, that females choose the most resistant males for that reason rather than the males just happening to be the most resistant.

The evidence has been pouring in since Hamilton and Zuk first published their theory: Some of it supports them, some does not. None quite meets all the criteria set forth above. Just as the theory predicts that the more flamboyant species should be the ones most troubled by parasites, so it predicts that within a species the more flamboyant a male 's ornament, the lower his parasite burden.

This proves to be true in diverse cases; it is also true that females generally favor males with fewer parasites. This holds for sage grouse, bowerbirds, frogs, guppies, even crickets:" In swallows, females prefer males with longer tails; those males have fewer lice, and their offspring inherit louse resistance even when reared by foster swallow parents." Something similar is suspected in pheasants and jungle fowl (the wild species to which domestic chickens belong)." Yet these are deeply unshocking results. It would have been far more surprising to find females being seduced by sick, scrawny males than to find them succumbing to the charms of the healthiest. After all, they might be avoiding a sick male for no better reason than that they do not wish to catch his bug."°

Experiments done on sage grouse have begun to satisfy some of the skeptics. Mark Boyce and his colleagues at the University of Wyoming found that male grouse sick with malaria do poorly, and so do males covered with lice. They noticed, too, that the

::: 152 :::

The Red Queen

lice were easy to notice because they left spots on the males ' inflat-ed air sacs. By painting such spots on a healthy male 's sac, Boyce and his colleagues were able to reduce his mating success." If they could go on to show cycles from one resistance gene to another mediated by female choice, they would have given the Good-gene theory a significant boost.

THE SYMMETRY OF BEAUTY

In 1991, Anders Moller and Andrew Pomiankowski stumbled on a possible way of settling the civil war between Fisher and Good-genes: symmetry. It is a well-known developmental accident that animals ' bodies are more symmetrical if they were in good condition when growing up, and they are less symmetrical if they were stressed while growing: For example, scorpionflies develop more symmetrically when fathered by well-fed fathers that could afford to feed their wives: The reason for this is simply the old wrench-in-the-works argument: Making something symmetrical is not easy. If things go wrong, the chances are it will come out asymmetrical:"

Most body parts, such as wings and beaks, should therefore be most symmetrical when they are just the right size and be the least symmetrical when stress has left them too small or too large: If Good-geners are right, ornaments should be the most symmetrical when they are the largest because large ornaments indicate the best genes and the least stress: If Fisherians are right, you would expect no relationship between ornament size and symmetry; if anything, the largest ornaments should be the least symmetrical because they reflect nothing about the owner other than that he can grow the largest ornament.

Moller noticed that, among the swallows he studied, the longest tails of the males were also the most symmetrical. This was quite unlike the pattern of other feathers, such as wings, which obeyed the usual rule: The most symmetrical were the ones closest to the average length: In other words, whereas most feathers show a U-shaped curve of asymmetry against length, tail streamers show a THE PEACOCK ' S TALE

::: 153 :::

steady upward progression: Since the swallows with the longest tails are the most successful in securing mates, it follows that the most symmetrical tails are also doing better. So Moller cut or elongated the tail feathers of certain males and at the same time enhanced or reduced the symmetry of the tails. Those with longer tails got mates sooner and reared more offspring, but within each class of length, those with enhanced symmetry did better than those with reduced symmetry."

Moller interprets this as unambiguous evidence in favor of Good-genes, for it shows that a condition-dependent trait—symmetry—is sexually selected: He joined forces with Pomiankowski to begin to separate those ornaments that show a correlation between symmetry and size from those that do not—in effect, to separate Good-genes from Fisher: Their initial conclusion was that animals with single ornaments—such as a swallow with a long tail—are Good-geners and show increasing symmetry with increasing size, whereas animals with multiple ornaments—such as a pheasant with its long tail, red facial roses, and colorful feather patterns—are mostly Fisherian, showing no relationship between size and symmetry. Since then, Pomiankowski has returned to the subject from a different angle, arguing that Fisher and many ornaments are likely to predominate when the cost to females of choosing is cheap; Good-genes will predominate when the cost of choosing is high: Again we reach the same conclusion: Peacocks are Fisherian; swallows are Good-geners.'°

HONEST JUNGLE FOWL

So far I have considered the evolution of male ornaments mainly from the female 's point of view because it is her preferences that drive that evolution. But in a species such as a peafowl, where female choice of mate rules, the male is not entirely a passive spectator of his evolutionary fate. He is both an ardent suitor and an eager salesman: He has a product to sell—his genes, perhaps—and information to impart about that product, but he does not simply

::: 154 :::

The Red Queen

hand the information over and await the peahen's decision. He is out to persuade her, to seduce her. And just as she is descended from females who made a careful choice, so he is descended from males who made a hard sell.

The analogy of the sales pitch is revealing, for advertisers do not promote their product merely by providing information about it. They fib, exaggerate, and try to associate it with pleasur-able images: They sell ice cream using sexy pictures, airplane tickets using couples walking hand in hand on beaches, instant coffee using romance, and cigarettes using cowboys.

When a man wants to seduce a woman, he does not send her a copy of his bank statement but a pearl necklace. He does not send her his doctor 's report but lets slip that he runs twenty miles a week and never gets colds. He does not tell her what degree he got but instead dazzles her with wit: He does not display testa-ments to how thoughtful he is but sends her roses on her birthday.

Each gesture has a message: I 'm rich, I'm fit, I'm clever, I 'm nice.

But the information is packaged to be more seductive and more effective, just as the message "Buy my ice cream " catches the eye when it is accompanied by a picture of two good-looking people seducing each other.

In courtship, as in the world of advertising, there is a discrepancy of interests between the buyer and the seller: The female needs to know the truth about the male: his health, wealth, and genes. The male wants to exaggerate the information: The female wants, the truth; the male wants to lie: The very word seduction implies trickery and manipulation."

Seduction therefore becomes a classic Red Queen contest, although this time the two protagonists are male and female, not host and disease: Zahavi 's handicap theory, as explored by Hamilton and Zuk, predicted that honesty would eventually prevail and males who cheat would be revealed: This is because the handicap is the female's criterion of choice for the very reason that it reveals the male 's state of health.

The red jungle fowl is the ancestor of the domestic chicken.

Like a farmyard rooster, the cock is equipped with a good many THE PEACOCK ' S TALE

::: 155 :::

ornaments that his mate does not share: long, curved tail feathers, a bright ruff around the neck, a red comb on the crown of his head, and a loud dawn call, to name the most obvious. Marlene Zuk wanted to find out which of these mattered to female jungle fowl, so she presented sexually receptive hens with two tethered males and examined which they chose. In some of the trials one of the cocks was reared with a roundworm infection in his gut, which affected his plumage, beak, and leg length very little but showed clearly in his comb and eye color, both of which were less colorful than in healthy males. Zuk found that hens preferred cocks with good combs and eyes but paid less attention to plumage. She failed to make hens go for males with fake red elastic combs on their heads, however; they found them too bizarre. Nonetheless, it was clear that hens paid most attention to the most health informative feature of a cock."

Zuk knew that poultry farmers, too, observe the comb and wattles of a cockerel to judge his health. What intrigued her was the idea that the wattles were more "honest " about the state of a cockerel than his feathers. Many birds, especially in the pheasant family, grow fleshy structures about their faces to emphasize during display: Turkeys grow long wattles over their beaks, pheasants have fleshy red "roses " on their faces, sage grouse bare their air sacs, and tragopans have expandable electric blue bibs beneath their chins.

A cockerel's comb is red because of the carotenoid pigments in it. A male guppy fish is rendered orange by carotenoids also, and a housefinch ' s and a flamingo ' s red plumage also depends on carotenoids. The peculiar thing about carotenoids is that birds and fish cannot synthesize them within their own tissues; they extract them from their food—from fruit, shellfish, or other plants and invertebrates. But their ability to extract carotenoids from their food and deliver it to their tissues is greatly affected by certain parasites. A cockerel affected by the bacterial disease coccidiosis, for example, accumulates less carotenoid in his comb than a healthy cockerel—even when both animals have been fed equal quantities of carotenoid: Nobody knows exactly why the parasites have this

::: 156 :::

The Red Queen

specific biochemical effect, but it seems to be unavoidable and is therefore extremely useful to the female: The brightness of carotenoid-filled tissues is a visible sign of the levels of parasite infection. It is not surprising that red and orange are common colors in fleshy ornaments used in display, such as the combs, wattles, and lappets of pheasants and grouse."

The size and brightness of such combs may be affected by parasites, but they are effected by hormones. The higher the level of testosterone in the blood of a cockerel, the bigger and brighter his comb and wattles will be. The problem for the cockerel is that the higher his level of testosterone, the greater his parasite infestation.

The hormone itself seems to lower his resistance to parasites:"

Once again nobody knows why, but cortisol, the " stress" hormone that is released into the bloodstream during times of emotional crisis, also has a marked effect on the immune system. A long study of cortisol levels in children in the West Indies revealed that the children are much more likely to catch an infection shortly after their cortisol levels have been high because of family tension or other stress:" Cortisol and testosterone are both steroid hormones, and they have a remarkably similar molecular structure. Of the five biochemical steps needed to make cholesterol into either cortisol or testosterone, only the last two steps are different: S6 There seems to be something about steroid hormones that unavoidably depresses immune defense. This immune effect of testosterone is the reason that men are more susceptible to infectious diseases than women, a trend that occurs throughout the animal kingdom. Eunuchs live longer than other men, and male creatures generally suffer from higher mortality and strain. In a small Australian creature called the marsupial mouse, all the males contract fatal diseases during the frantic breeding season and die. It is as if male animals have a finite sum of energy that they can spend on testosterone or immunity to disease, but not both at the same time."

The implication for sexual selection is that it does not pay to lie: Having sex-hormone levels that are too high increases the size of your ornaments but makes you more vulnerable to parasites, which are revealed in the state of those ornaments. It is possible

'

THE PEACOCK S TALE

::: 157:::

that it works in the other direction: The immune system suppresses the production of testosterone. In Zuk 's words, "Males are thus necessarily more vulnerable to disease as they acquire the accoutrements of maleness. ""

The best proof of these conjectures comes from a study of roach, which are small fish with reddish fins, in the Lake of Biel in Switzerland. Male roach grow little tubercules all over their bodies during the breeding season, which seem to stimulate females during courtship as the fish rub against each other. The more parasites a male has, the fewer tubercules he grows. It is possible for a zoologist to judge, just from a male 's tubercules, whether he is infested with a roundworm or a flatworm. The implication follows: If a zoologist can deduce which parasite is present, a female roach probably can as well: This pattern results from different kinds of sex hormones; one can be raised in concentration only at the expense of leaving the roach vulnerable to one kind of parasite; the other can be raised only at the expense of lowering defenses against 59

another kind of parasite:

If cockerels ' wattles and roach tubercules are honest signals, so presumably are songs: A nightingale that can sing loud and long must be in vigorous health, and one that has a large repertoire of different melodies must be experienced or ingenious, or both. An energetic display such as the pas de deux of a pair of male manakins may also be an honest signal: A bird that merely shows its feathers, such as a peacock or a bird of paradise, might be a cheat whose strength has been sapped by bad habits since he grew the plumes: After all, peacock feathers still shine brightly when their owner is dead and stuffed. Perhaps it is no surprise, then, that most male birds do not molt just before the breeding season but adopt their spring plumage the autumn before. They have to keep it tidy all winter: The very fact that a male has looked after his plumes for six months tells a female something about his enduring vigor: Bill Hamilton points out that white fluffy feathers around a bird's rear end, which are common in grouse of various kinds, must be especially hard to keep clean if the bird has diarrhea. b°

Zahavi certainly believed that honesty was a prerequisite of

::: 158 :::

The Red Queen

handicaps, and vice versa. To be honest, he thought, an ornament must be costly; otherwise it could be used to cheat. A deer cannot grow large antlers without consuming five times its normal daily intake of calcium; a pupfish cannot be iridescent blue unless it is genuinely in good condition, a fact that will be tested by other male fish in fights. On the assumption that anybody who refuses to play the game and use an honest signal must have something to hide, males are likely to find themselves dragged into honest displays. Therefore, display ornaments are examples of "truth in advertising. "61

All this is very logical, but in about 1990 it started to make one group of biologists uneasy. They had an instinctive aversion to the idea that sexual advertising is about the truth because they knew that television advertising is not about passing on information; it is about manipulating the viewer. In the same way, they argued, all animal communication is about manipulating the receiver.

The first and most eloquent (manipulative?) champions of this view were two Oxford biologists, Richard Dawkins and John Krebs: According to them, a nightingale does not sing to inform potential mates about himself; he sings to seduce them. If that means lying about his true prowess, so be it: 62 Perhaps an ice cream advertisement is honest in a simplistic sense because it gives the name of the brand, but it is not honest in implying that sex is sure to follow after every spoonful. Such a crude lie can surely be perceived by that genius of the animal kingdom, humans. But it is not.

Advertising works. Brand names are better known if they are advertised with sexy or alluring pictures, and better-known brands sell better. Why does it work? Because the price the consumer would have to pay in ignoring the subliminal message is just too high. It is better to be fooled into buying the second-best ice cream than go to the bother of educating yourself to resist the salesmanship.

Any peahens reading this might begin to recognize their dilemma. For they, too, may be fooled by the male's display into buying the second-best male: Remember, the lek paradox argues that there is little to choose between males on a lek anyway because they were all fathered by the same few males in the previous genera-THE PEACOCKS TALE

::: 159:::

tion. So two theories—truth in advertising and dishonest manipulation—seem to come to opposite conclusions. Truth in advertising concludes that females will discover a cheating seducer; dishonest manipulation concludes that males will seduce females against their better judgment.

WHY DO YOUNG WOMEN HAVE NARROW WAISTS?

Marian Dawkins and Tim Guilford of Oxford have recently suggested a resolution to this conundrum. As long as detecting the dishonesty in the signal is costly to the female, it might not be worth her while to do so. In other words, if she has to risk her life seeking out and comparing many males to ensure that she has chosen the best one, then the marginal advantage she gains by picking the best one is outweighed by the risk she has run. It is better to let herself be seduced by a good one than to have the best become the enemy of the good. After all, if she cannot easily distinguish the truthful from the dishonest badge of quality, then other females will not, either, and so her sons will not be punished for any dishonesty they inherit from their father."

A startling example of this sort of logic comes from a controversial theory about human beings that was developed a few years ago by Bobbi Low and her colleagues at dhe University of Michigan: Low was looking to explain why young women have fat on their breasts and buttocks more than on other parts of their bodies. The reason this requires explaining is that young women are different from other human beings in this respect. Older women, young girls, and men of all ages gain fat on their torsos and limbs much more evenly. If a woman of twenty or so gains weight, it largely takes the form of fat on the breasts and buttocks; her waist can remain remarkably nartow.

So much is undisputed fact. What follows is entirely conjecture, and it was a conjecture that caused Low a good deal of sometimes vicious (and mostly foolish) criticism when she published the idea in 1987:

::: 160 :::

The Red Queen

Twenty-year-old women are in their breeding prime; therefore, the unusual pattern of fat distribution might be expected to be connected with getting a mate or bearing children. Standard explanations concern the bearing of children; for example, fat is inconvenient if it competes for space about the waist with a fetus.

Low 's explanation concerns the attraction of mates and takes the form of a Red Queen race between males and females. A man looking for a wife is likely to be descended from men who found two things attractive (among many others): big breasts, for feeding his children, and wide hips, for bearing them. Death during infancy due to a mother 's milk shortage would have been common before modern affluence—and still is in some parts of the world. Death of the mother and infant from a birth canal that was too narrow must also have been common. Birth complications are peculiarly frequent in humans for the obvious reason that the head size of a baby at birth has been increasing quickly in the past 5 million years. The only way birth canals kept pace (before Julius Caesar 's mother was cut open) was through the selective death of narrow-hipped women.

Grant, then, that early men may have preferred women with relatively wide hips and large breasts. That still does not explain the gaining of fat on breasts and hips; fat breasts do not produce more milk than lean ones, and fat hips are no farther apart than lean ones of the same bone structure. Low thinks women who gained fat in those places may have deceived men into thinking they had milkful breasts and wide hip bones: Men fell for it—

because the cost of distinguishing fat from heavy breasts or of distinguishing fat from wide hips was just too great, and the opportunity to do so was lacking. Men have counterattacked, evolutionarily speaking, by "demanding" small waists as proof of the fact that there is little subcutaneous fat, but women have easily overcome this by keeping waists slim even while gaining fat elsewhere."

Low ' s theory might not be right, as she is the first to admit, but it is no less logical or farfetched than any of its rivals, and for our purposes it serves to demonstrate that a Red Queen race between a dishonest advertiser (in this case, unusually, a THE PEACOCKS TALE

::: 161 :::

female) and a receiver who demands honesty may not always be won by the honesty-demanding gender. It is essential, if Low is right, that fat be cheaper to gain than mammary tissue, just as it is essential, for Dawkins and Guilford, that cheating be cheaper than telling the truth."

CHUCKING FROGS

The male 's goal is seduction: He is trying to manipulate the female into falling for his charms, to get inside her head and steer her mind his way: The evolutionary pressure is on him to perfect displays that make her well disposed toward him and sexually aroused so that he can be certain of mating: Male scorpions lull females into the mood for sex at great risk to their lives. One false step in the seduction, and the female 's mood changes so that she looks upon the male as a meal.

The evolutionary pressure on a female—assuming she benefits from choosing the best male—is to invent resistance to all but the most charming displays: To say this is merely to rephrase the whole argument of female choice with a greater emphasis on the how than the why. But such rephrasings can be illuminating, and this one has proved exceptionally so. Michael Ryan of the University of Texas rephrased the question a few years ago, and he did so partly because he studies frogs: It is easy to measure female preferences in frogs because the male sits in one spot and calls, and the female moves toward the sound of the male she likes the most: Ryan replaced the males with loudspeakers and offered each female different recordings of males to test her preference.

The male tungara frog attracts a female by making a long whine followed by a "chuck " noise. All of its close relatives except one make the whine but not the chuck: But at least one of the chuckless relatives turns out to prefer calls with chucks to those without. This was rather like discovering that a New Guinea tribesman found women in white wedding dresses more attractive than women dressed in tribal gear. It seems to indicate that the

::: 162 :::

The Red Queen

preference for the chuck just happens to exist in the fact that the female 's ear (to be precise, the basilar papillae of the inner ear) is tuned to the chuck 's frequency; the male has, in evolutionary terms, discovered and exploited this. In Ryan 's mind this deals a blow to the whole house of female-choice theory: That theory, whether in Fisher 's sexy-son form or the Good-genes form, predicts that the male's ornament and the female 's preference for such an ornament will evolve together: Ryan's result seems to suggest that the preference existed fully formed before the male ever had the ornament: Peahens preferred eyed tails a million years ago when peacocks still looked like big chickens. 66

Lest the tungara frog be thought a fluke, a colleague of Ryan's, Alexandra Basolo, has found exactly the same thing in a fish called the platyfish. Females prefer males who have had long sword-shaped extensions stuck onto their tales: Males of a different species called the swordtail have such swords on their tails, yet none of the platyfish 's other relatives have swords, and it stretches belief to argue that they all got rid of the sword rather than that the swordtail acquired it: The preference for sworded tails was there, latent, in platyfish before there were swords."

In one sense what Ryan is saying is unremarkable. That male displays should be suited to the sensory systems of females is only to be expected: Monkeys and apes are the only mammals with good color vision: Therefore, it is not surprising that they are the only mammals decorated with bright colors such as blue and pink.

Likewise, it is hardly remarkable that snakes, which are deaf, do not sing to each other. (They hiss to scare hearing creatures:) Indeed, one could list a whole panoply of "peacocks ' tails" for each of the five senses and more: the peacock 's tail for vision, the nightingale's song for hearing, the scent of the musk deer for smell;" the pheromones of the moth for taste; the "morphological exuberance "

of some insect "penises " for touch; 69 even the elaborate electrical courtship signals of some electric fish" for a sixth sense. Each species chooses to exploit the senses that its females are best at detecting. This is, in a sense, to return to Darwin 's original idea: that females have aesthetic senses, for whatever reason, and that those senses shape male ornaments."

THE PEACOCK ' S TALE

::: 163 :::

Moreover, you would expect the males to pick the method of display that is least dangerous or costly. Those that did so would last longer and leave more descendants than those that did not. As every bird-watcher knows, the beauty of a bird 's song is inversely correlated with the colorfulness of its plumage. The oper-atic male nightingales, warblers, and larks are brown and usually almost indistinguishable from their females. Birds of paradise and pheasants (in which the males are gorgeous, the females dull) are monotonous, simple songsters given to uninspired squawks.

Intriguingly, the same pattern holds among the bowerbirds of New Guinea and Australia: The duller the bird, the more elaborate and decorated its bower. What this suggests is that nightingales and bowerbirds have transferred their color to their songs and bowers.

There are clear advantages to doing so. A songster can switch his ornament off when danger threatens. A bower builder can leave his behind."

More direct evidence of this pattern comes from fish. John Endler of the University of California at Santa Barbara studies the courtship of guppies and is especially interested in the colors adopted by male guppies: Fish have magnificent color vision; whereas we use three different types of color-detecting cells in the eye (red, blue, and green), fish have four, and birds have up to seven. Compared to the way birds see the world, our lives are mono-chrome. But fish : also have a very different experience from us because their world filters out light of different colors in all sorts of variable ways. The deeper they live, the less red light penetrates compared with blue. The browner the water, the less blue light penetrates. The greener the water, the less red or blue light penetrates.

And so on. Endler 's guppies live in South American rivers; when courting, they are usually in clear water where orange, red, and blue are the colors that show up best. Their enemies, however, are fish that live in water where yellow light penetrates best. Not surprisingly, male guppies are never yellow.

The males use two kinds of color, one red-orange, which is produced by a carotenoid pigment that the guppy must acquire from its food, and the other blue-green, which is caused by guanine crystals in the skin that are laid down when the guppy reaches

::: 164

The Red Queen

maturity. Female guppies that live in tea-colored water, where red-orange is more easily seen, are more sensitive to red-orange light than to blue, which makes sense. The brains of such guppies are tuned to exactly the wavelength of the red-orange carotenoid pigment the male uses in display—and perhaps vice versa."

OF MOZART AND GRACKLE SONG

Down the corridor from Ryan at the University of Texas is Mark Kirkpatrick, who is prepared to upset even more apple carts. Kirkpatrick is acknowledged as one of those who understands sexual selection theory most thoroughly; indeed, he was one of those who made Fisher's idea mathematically respectable in the early 1980s.

But he now refuses to accept that we must choose between Fisher and Zahavi. He does so partly because of what Ryan has discovered: This does not mean Kirkpatrick rejects female choice, as Julian Huxley did. Whereas Huxley thought males did the choosing by fighting among themselves, Kirkpatrick prefers to believe that in many species the females do choose, but their preferences do not evolve. They merely saddle the males with their own idiosyncratic tastes.

Both Good-genes and Fisher theories are obsessed with trying to find a reason for exuberant display that benefits the male.

Kirkpatrick looks at it from the female 's point of view: Suppose, he says, that peahens' preferences have indeed saddled peacocks with their tails. Why must we explain these female preferences only in terms of the effects on their sons and daughters? Might the peahens not have perfectly good direct reasons for choosing as they do? Might their preferences not be determined by something else entirely? He thinks "other evolutionary forces acting on the preferences will overwhelm the Good-genes factor and often establish female preferences for traits that decrease male survival.'

Two recent experiments support the idea that females simply have idiosyncratic tastes that have not evolved. Male grackles—

blackish birds of medium size—sing only one kind of song. Female

'

THE PEACOCK S TALE

::: 165 :::

grackles prefer to mate with males that sing more than one kind of song: William Searcy of the University of Pittsburgh discovered why. He made use of the fact that a female grackle will go up to singing loudspeakers and adopt a soliciting posture as if waiting to be mated. Her tendency to do so declines, however, as she gets bored with the song: Only if the loudspeaker starts singing a new song will her soliciting start afresh. Such " habituation" is just a property of the way brains work; our senses, and those of grackles, notice novelty and change, not steady states: The female preference did not evolve; it just is that way."

Perhaps the most startling discovery in sexual selection theory was Nancy Burley 's work on zebra finches in the early 1980s.

She was studying how these small Australian finches choose their mates, and to make it easier she kept them in aviaries and marked each one with a colored ring on its leg. After a while she noticed something odd: The males with red rings seemed to be preferred by the females. Further experiments proved that the rings were drastically affecting the "attractiveness " of both males and females.

Males with red rings were attractive; those with green rings unattractive; females with black or pink rings were preferred; those with light blue rings disliked: It was not just rings: Little paper hats glued to the birds ' heads also altered their attractiveness: Female zebra finches have a rather simple rule for assessing potential mates: The more red he has on his body (or the less green, which comes to the same thing given that red and green are seen as opposites by the brain), the more attractive he is. 7b If females have an existing aesthetic preference, it is only logical that males will evolve to exploit that preference: For example, it is possible that the "eyes" on a peacock 's tail are seductive to peahens because they resemble huge versions of real eyes. Real eyes are visually arresting—perhaps even hypnotic—to many kinds of animals, and the sudden appearance of many huge staring eyes may induce a state of mild hypnosis in the peahen, which allows the peacock to lunge at her:" This would be consistent with the common discovery that "supernormal stimuli " are often more effective than normal ones. For example, many birds prefer a ridiculous giant

::: 166:::

The Red Queen

egg in their nest to a normal one; a goose will prefer to try to sit on an egg the size of a soccer ball than one of normal size: It is as if their brains have a program that says "like eggs, " and the bigger the egg, the more it likes them. So perhaps the bigger the eye-spot, the more attractive or startling it is for a peahen, and the mile has simply exploited this by evolving lots of giant eyes without any evolutionary change in the female 's preference. 7e HANDICAPPED ADVERTISERS

Andrew Pomiankowski of London accepts much of what Ryan and Kirkpatrick say but parts company with them on the matter of female choice. He says that what they are considering is merely a constraint that channels the male ' s trait into the preferred direction of the female's sensory bias. But that does not mean the exaggeration happens without the female 's preference changing. It is almost impossible to see how females could avoid the Fisher effect as the male 's ornament gets more exaggerated generation by generation. The female who is most discriminating picks the sexiest male and so has the sexiest sons; the one who has the sexiest sons has the most granddaughters. So females get more and more discriminating and more and more difficult to seduce or hypnotize: "The crucial question, " wrote Pomiankowksi, "is not whether sensory exploitation has been involved but why females have allowed themselves to be exploited. " Besides, it is an impoverished view of selection to believe that a frog 's ear can be tuned for detecting predators but not tuned simultaneously and differently to choosing males."

Thus, it is possible to argue with Ryan and Kirkpatrick that male courtship extravagances reflect the innate tastes of females without abandoning the idea that those tastes are of use to the females in that they select the best genes for the next generation. A peacock 's tail is, simultaneously, a testament to naturally selected female preferences for eyelike objects, a runaway product of despotic fashion among peahens, and a handicap that reveals its posses-

'

THE PEACOCK S TALE

::: 167 :::

sor 's condition. Such tolerant pluralism is not to everybody 's taste, but Pomiankowski insists it does not stem from misguided desire to please everybody: On a paper napkin in an Indian restaurant one day he sketched out for me a plausible account of all the sexual selection theories working in concert.

Each male trait begins as a chance mutation: If it happens to hit a sensory bias of the female, it starts to spread. As it spreads, the Fisher effect takes over, and both the trait and the preference are exaggerated: Eventually the point is reached where the trait has spread to all males, and there is no point in females following the fashion anymore. It starts to fade again, under pressure from the fact that there is now a cost to female choice: if nothing else, it is a waste of females ' time and effort to compare different males: The Fisher effect fades more slowly when that cost is small—for example, in lekking species where the males can all be viewed at once.

But some traits do not fade because it so happens that they reflect the underlying health of their possessors—they change color if the male is infected with parasites, for example. And therefore females do not stop choosing the best males at all. They keep picking (or being seduced by) the fanciest male because if they do, they will have disease-resistant offspring: In other words, condition-reflecting traits will not be the only ones brought to an exaggerated state, but they will be the ones that persist the longest: And all the Fisher-exaggerated traits remain in lekking species as well because the cost of choosing is so small: The most promiscuous species end up a collage of different handicaps, ornaments, and gaudy blotches.

Pomiankowski has since begun to confirm his intuition (based on the symmetry idea discussed earlier) that multiple traits on polygamous birds, such as the many adornments of a peacock, are Fisher ornaments, while single features on monogamous birds, such as the swallow 's forked tail, are Good-gene ornaments, or condition-revealing handicaps. 80

The next time you visit a zoo in the spring, try to watch a male Lady Amherst pheasant from China posturing before a hen.

He is a riot of color: His face is pale green, his crest scarlet, his throat iridescent green, his back emerald, his rump orange, and his

::: 168 :::

The Red Queen

belly pristine white: Around his neck is a white ruff trimmed with black, and at the base of his tail are five pairs of vermillion feathers: His tail, white barred with black, is longer than his body: A dull or damaged feather would stand out anywhere on his body: He is one great advertisement for good genes, handicapped by the need to keep clean, healthy, and out of danger, a walking illustration of his mate's evolved sensory biases:

THE HUMAN PEACOCK

The antics of peacocks and guppies are interesting enough in themselves to naturalists; to students of evolution they are intriguing as test cases; but to the rest of us what makes them worth studying is pure self-centeredness: We want to know what lessons they teach us about human affairs: Are some men successful with women because their appearance sends an honest signal of their handicapping good genes and their ability to resist disease?

The idea is ridiculous: Men succeed with women for much more varied and subtle reasons: They are kind or clever or witty or rich or good-looking or just available. Humans are simply not a lekking species. Men do not gather in groups to display for passing women: Most men do not abandon women immediately after copulation: Men are not equipped with gorgeous ornaments or stereotyped courtship rituals, however it may look in the average discotheque. When a woman chooses a man to mate with, she is less concerned with whether he can father sexy sons or disease-resistant daughters than whether he would make a good husband. A man choosing a wife uses equally mundane considerations, though he is perhaps more of a sucker for beauty: Both genders use criteria that bear on parental abilities. They are more like terns, who choose mates that can fish well, than sage grouse hens, who copy one another 's choice of a fast-displaying male. So the Red Queen race between the genders over seduction and sales resistance that follows from pure Good-gene choice does not happen: And yet we cannot be so categorical: There are species of THE PEACOCK ' S TALE

::: 169 :::

mammal in which the effects of sexual selection are few and small.

It is hard to argue that the average rat has been endowed with conspicuous display'ornaments by the preferences of ancestral females: Even our closest relatives, the chimpanzees, are little touched by the effects of female choice: Males look much like females, and courtship is somewhat simple. But we should pause before dismissing the effects of sexual selection on human beings. People, after all, are universally interested in beauty. Lipstick, jewelry, eye shad-ow, perfume, hair dyes, high heels—people are just as willing to exaggerate or lie about their sexually alluring traits as any peacock or bowerbird: And as the list above makes clear, it seems as if men seek female beauty rather more than women seek male beauty. The human being, in other words, may be the victim of generations of male choice even more than female choice: If we are to apply sexual selection theory to man, it is male choice for female genes that we should examine. But it makes little difference: When one gender is being choosy, all the consequences of sexual selection theory inevitably flow: It is quite possible, even likely, as the next few chapters will reveal, that some parts of the human body and psyche have been sexually selected.

Chapter 6

POLYGAMY AND THE

NATURE OF MEN

If women didn't exist, all the money in the world would have no

meaning:

—Aristotle Onassis

Power is a great aphrodisiac:

—Henry Kissinger

In the ancient empire of the Incas, sex was a heavily regulated industry: The sun-king Atahualpa kept fifteen hundred women in each of many "houses of virgins" throughout his kingdom. They were selected for their beauty and were rarely chosen after the age of eight—to ensure their virginity. But they did not all remain virgins for long: They were the emperor 's concubines: Beneath him, each rank of society afforded a harem of a particular legal size: Great lords had harems of more than seven hundred women. "Principal persons " were allowed fifty women; leaders of vassal nations, thirty; heads of provinces of 1 00,000 people, twenty; leaders of I,000 people, fifteen; administrators of 500 people, twelve; gover-nors of 100 people, eight; petty chiefs over 50 men, seven; chiefs of 10 men, five; chiefs of 5 men, three. That left precious few for the average male Indian whose enforced near-celibacy must have driven him to desperate acts, a fact attested to by the severity of the penalties that followed any cuckolding of his seniors. If a man violated one of Atahualpa 's women, he, his wife, his children, his relatives, his servants, his fellow villagers, and all his lamas would be put to death, the village would be destroyed, and the site strewn with stones.

As a result, Atahualpa and his nobles had, shall we say, a majority holding in the paternity of the next generation. They systematically dispossessed less privileged men of their genetic share of posterity. Many of the Inca people were the children of powerful men:

In the kingdom of Dahomey in West Africa, all women were

::: 174:::

The Red Queen

at the pleasure of the king. Thousands of them were kept in the royal harem for his use, and the remainder he suffered to " marry "

the more favored of his subjects: The result was that Dahomean kings were very fecund, while ordinary Dahomean men were often celibate and barren: In the city of Abomey, according to one nineteenth-century visitor, "it would be difficult to find Dahomeans who were not descended from royalty: "

The connection between sex and power is a long one.'

MANKIND, AN ANIMAL

So far this book has taken only a few, sideways glances at human beings. This is deliberate: The principles I have been trying to establish are better illustrated by aphids, dandelions, slime molds, fruit flies, peacocks, and elephant seals than they are by one peculiar ape. But the peculiar ape is not immune to those principles.

Human beings are a product of evolution as much as any slime mold, and the revolution of the last two decades in the way scientists now think about evolution has immense implications for mankind as well. To summarize the argument so far, evolution is more about reproduction of the fittest than survival of the fittest; every creature on earth is the product of a series of historical battles between parasites and hosts, between genes and other genes, between members of the same species, between members of one gender in competition for members of the other gender. Those battles include psychological ones, to manipulate and exploit other members of the species; they are never won, for success in one generation only ensures that the foes of the next generation are fitter to fight harder: Life is a Sisyphean race, run ever faster toward a finish line that is merely the start of the next race: This chapter begins to follow the logic of these arguments into the heart of human behavior: Those who think this unjustified on the grounds that human beings are unique usually advance one of two arguments: that in humans everything about behavior is learned, and nothing is inherited; or inherited behavior is inflexible POLYGAMY AND THE NATURE OF MEN

::: 175 :::

behavior, and human beings are clearly flexible. The first argument is an exaggeration, the second false: A man does not experience lust because he learned it at his father 's knee; a person does not feel hunger or anger because she was taught it. They are human nature: We are born with the potential to develop lust, hunger, and anger.

We learn to direct hunger at hamburgers, anger at delayed trains, and lust at the object of our affection—when appropriate: So we have "changed " our " nature. " Inherited tendencies permeate everything we do, and they are flexible. There is no nature that exists devoid of nurture; there is no nurture that develops without nature: To say otherwise is like saying that the area of a field is determined by its length but not its width. Every behavior is the product of an instinct trained by experience:

The study of human beings remained resolutely unre-formed by these ideas until a few years ago: Even now, most anthropologists and social scientists are firmly committed to the view that evolution has nothing to tell them: Human bodies are products of natural selection; but human minds and human behavior are products of "culture, " and human culture does not reflect human nature, but the reverse. This restricts social scientists to investigating only differences between cultures and between individuals—and to exaggerating them. Yet what is most interesting to me about human beings is the things that are the same, not what is different—things like grammatical language, hierarchy, romantic love, sexual jealousy, long-term bonds between the genders ( "marriage," in a sense). These are trainable instincts peculiar to our species and are just as surely the products of evolution as eyes and thumbs.'

THE POINT OF MARRIAGE

For a man, women are vehicles that can carry his genes into the next generation. For a woman, men are sources of a vital substance (sperm) that can turn their eggs into embryos. For each gender the other is a sought-after resource to be exploited: The question is,

::: 176 :::

The Red Queen

how? One way to exploit the other gender is to round up as many as possible of them and persuade them to mate with you, then desert them, as bull elephant seals do: The opposite extreme is to find one individual and share all the duties of parenthood equally, as albatrosses do: Every species falls somewhere on that spectrum, with its own characteristic "mating system. " Where does humanity fall?

There are five ways to find out. One is to study modern people directly and describe what they do as the human mating system: The answer is usually monogamous marriage. A second way is to look at human history and divine from our past what sexual arrange-ments are typical of our species: But history teaches a dismal lesson: A common arrangement from our past was that rich and powerful men enslaved concubines in large harems: A third way is to look at people living in simple societies with Stone Age technologies and conjecture that they live much as our ancestors lived ten millennia ago. They tend to fall between the extremes: less polygamous than early civilizations, less monogamous than modern society: The fourth technique is to look at our closest relatives, the apes, and compare our behavior and anatomy with theirs: The answer that emerges is that men 's testicles are not large enough for a system of promiscuity like the chimpanzee 's, men's bodies are not big enough for a system of harem polygamy like the gorilla ' s (there is an iron link between harem polygamy in a species and a large size differential between male and female), and men are not as antisocial and adjusted to fidelity as the monogamous gibbon. We are somewhere in between. The fifth method is to compare humans with other animals that share our highly social habits: with colonial birds, monkeys, and dolphins: As we shall see, the lesson they teach is that we are designed for a system of monogamy plagued by adultery: It is at least possible to rule out some options. There are characteristically human things that we do, such as form lasting bonds between sexual partners, even when polygamous: We are not like sage grouse whose marriages last for minutes. Nor are we polyandrous, like the jacana or lily-trotter, a tropical water bird that has big fierce females that control harems of small domesticated males. There is only one truly polyandrous society on Earth; it is in POLYGAMY AND THE NATURE OF MEN

::: 177:::

Tibet and consists of women who marry two or more brothers simultaneously in an attempt to put together a family unit that is economically viable in a harsh land where men herd yaks to support women. The junior brother 's ambition is to leave and obtain his own wife, so polyandry is plainly a second-best outcome for him.'

Nor are we like the robin or the gibbon, which are strictly territorial, each pair monopolizing and defending a home range sufficient to live their whole lives within. We build garden fences, but even our homes are often shared with lodgers or fellow apartment dwellers, and most of our lives are spent on some form of common ground, at work, shopping, traveling, entertaining ourselves: People live in groups.

None of this is much help, then: Most people live in monogamous societies, but this may only tell us what democracy usually prescribes, not what human nature seeks: Relax the antipolygamy laws and it flourishes. Utah has a tradition of theo-logically sanctioned polygamy and in recent years has been less forceful about prosecuting polygamists, so the habit has reemerged.

Although the most populous societies are monogamous, about three-quarters of all tribal cultures are polygamous, and even the ostensibly monogamous ones are monogamous in name only.

Throughout history powerful men have usually had more than one mate each, even if they have had only one legitimate wife: However, that is for the powerful: For the rest, even in openly polygamous societies, most men have only one wife and virtually all women have only one husband: That leaves us precisely nowhere. Mankind is a polygamist and a monogamist, depending on the circumstances.

Indeed, perhaps it is foolish even to talk of humans having a mating system at all: They do what they want, adapting their behavior to the prevailing opportunity.'

WHEN MALES POUNCE AND FEMALES FLIRT

Until recently, evolutionists had a fairly simple view of mating systems based on the essential differences between males and females:

::: I78 :::

The Red Queen

If powerful men had their way, women would probably live in harems like seals; that is certainly the lesson of history. If most women had their way, men would be as faithful as albatrosses.

Although research has modified this supposition, it is nonetheless true that males are generally seducers and females the seduced: Humanity shares this profile of ardent, polygamist males and coy, faithful females with about 99 percent of all animal species, including our closest relatives, the apes.

Consider, for example, the question of marriage proposals: In no society on earth do they usually come from the woman or her family. Even among the most liberated of Westerners, men are expected to ask and women to answer: The tradition of women asking men on Leap Year ' s Day reinforces the very paucity of their opportunities: They get one day to pop the question for every 1,460 that men can do so. It is true that many modern men do not go down on one knee but "discuss " the matter with their girl-friends as equals: Yet even so, the subject is usually first raised by the man. And in the matter of seduction itself, once more it is the male who is expected to make the first move. Women may flirt, but men pounce:

Why should this be? Sociologists will blame it on conditioning, and they are partly right. But that is not a sufficient answer because in the great human experiment called the 1960s much conditioning was rejected yet the pattern survives: Besides, conditioning usually reinforces instinct rather than overrides it.

Since an insight of Robert Trivers 's in 1972,' biologists have had a satisfying explanation for why male animals are usually more ardent suitors than females and why there are exceptions to the rule.

There seems to be no reason why it should not also apply to people. The gender that invests the most in creating and rearing the offspring, and so forgoes most opportunities for creating and rearing other offspring, is the gender that has the least to gain from each extra mating. A peacock grants a peahen one tiny favor: a batch of sperm and nothing else. He will not guard her from other peacocks, feed her, protect a food supply for her, help her incubate her eggs, or help her bring up the chicks. She will do all the work.

POLYGAMY AND THE NATURE OF MEN

::: 179:::

Therefore, when she mates with him, it is an unequal bargain. She brings him the promise of a gigantic single-handed effort to make his sperm into new peacocks; he brings just the tiniest—though seminal—contribution: She could choose any peacock she likes and has no need to choose more than one. At the margin, he loses nothing and gains much by mating with every female who comes along; she loses time and energy for a futile gain. Every time he seduces a fresh female, he wins the jackpot of her investment in his sons and daughters. Every time she seduces a fresh peacock, she wins a little extra sperm that she probably does not need. No wonder he is keen on quantity of mates, and she on quality.

In more human terms, men can father another child just about every time they copulate with a different woman, whereas women can bear the child of only one man at a time: It is a fair bet that Casanova left more descendants than the Whore of Babylon.

This basic asymmetry between the genders goes right back to the difference in size of a sperm and an egg. In 1948 a British scientist named A. J. Bateman allowed fruit flies to mate with one another at will. He found that the most successful females were not much more prolific than the least successful, but the most prolific males were far more successful than the least prolific males.'

The asymmetry has been greatly enhanced by the evolution of female parental care, which reaches its zenith in mammals. A female mammal gives birth to a gigantic baby that has been nurtured inside her for a long time; a male can become a father in seconds.

Women cannot increase their fecundity by taking more mates; men can. And the fruit fly rule holds. Even in modern monogamous societies, men are far more likely to have lots of children than women are. For instance, men who marry twice are more likely to sire children by two wives than women who marry twice are to have children by both husbands.'

Infidelity and prostitution are special cases of polygamy in which no marriage bond forms between the partners. This puts a man's wife and his mistresses in different categories with respect to the investment that he is likely to make in his children: The man who can sufficiently arrange his business affairs to make time,

::: 180 :::

The Red Queen

opportunity, and money available for supporting two families is as rich as he is rare.

FEMINISM AND PHALAROPES

The rule that parental investment dictates which gender will attempt polygamy can be tested by looking at its exceptions. In sea horses the female has a sort of penis that she uses to inject eggs into the male's body, neatly reversing the usual method of mating.

The eggs develop there, and as the theory predicts, it is the female sea horse who courts the male. There are about thirty species of birds, of which the phalaropes and jacanas are the best-known examples, in which the small dowdy male is courted by the large, aggressive female, and it is the male that broods the eggs and rears the chicks.'

Phalaropes and other seducer-female species are the exceptions that prove the rule. I remember watching a whole flock of female phalaropes badgering a poor male so intensely he almost drowned. And why? Because their mates , were quietly sitting on their eggs for them, so these females had nothing better to do than look for second mates. Where males invest more time or energy in the care of the young, females take the initiative in courtship, and vice versa:'

In humans, the asymmetry is clear enough: nine months of pregnancy set against five minutes of fun: (I exaggerate:) If the balance of such investment determines sex roles in seduction, then it comes as no surprise that men seduce women rather than vice versa.

This fact suggests that a highly polygamous human society represents a victory for men, whereas a monogamous one suggests a victory for women. But this is misleading. A polygamous society primarily represents a victory for one or a few men over all other men. Most men in highly polygamous societies are condemned to celibacy.

In any case, no moral conclusions of any kind can be drawn from evolution. The asymmetry in prenatal sexual investment between the genders is a fact of life, not a moral outrage: It is "nat-POLYGAMY AND THE NATURE OF MEN

::: 181 :::

ural: " It is terribly tempting, as human beings, to embrace such an evolutionary scenario because it "justifies " a prejudice in favor of male philandering, or to reject it because it "undermines " the pressure for sexual equality: But it does neither: It says absolutely nothing about what is right and wrong: I am trying to describe the nature of humans, not prescribe their morality. That something is natural does not make it right: Murder is "natural " in the sense that our ape relatives commit it regularly, as apparently did our human ancestors: Prejudice, hate, violence, cruelty—all are more or less part of our nature, and all can be effectively countered by the right kind of nurture: Nature is not inflexible but malleable: Moreover, the most natural thing of all about evolution is that some natures will be pitted against others: Evolution does not lead to Utopia: It leads to a land in which what is best for one man may be the worst for another man, or what is best for a woman may be the worst for a man. One or the other will be condemned to an "unnatural" fate: That is the essence of the Red Queen 's message: In the pages that follow I will again and again be trying to guess what is " natural" for humanity: Perhaps my own moral prejudices will occasionally intrude as wishful thinking, but they will do so unconsciously. And even where I am wrong about human nature, I am not wrong that there is such a nature to be sought: THE MEANING OF HOMOSEXUAL PROMISCUITY

Most prostitutes are female for the simple reason that the demand for female prostitutes is greater than for male ones: If the existence of female prostitutes reveals the male sexual appetite in its naked-ness, then so, too, does the phenomenon of male homosexuality.

Before the advent of AIDS, practicing male homosexuals were far more promiscuous than heterosexual men: Many gay bars were, and are, recognized places for picking up partners for one-night stands.

The bathhouses of San Francisco catered to orgies and feats of repeated sex, assisted by stimulants, that boggled the mind when publicly discussed during the early years of the AIDS epidemic: A

::: 182 :::

The Red Queen

Kinsey Institute study of gay men in the San Francisco Bay area found that 75 percent had had more than one hundred partners; 25

percent had had more than one thousand:'°

This is not to deny that there are many homosexuals who were and are less promiscuous than many heterosexuals: But even homosexual activists admit that, before AIDS arrived, homosexuals were generally more promiscuous than heterosexuals: There is no single convincing explanation of this. Activists would say that homosexual promiscuity is caused largely by society ' s disapproval: Illegitimate, "shameful" activities tend to be indulged to excess when indulged at all: The legal and social difficulty of forming gay

" marriages " mitigates against stable relationships.

But this is not persuasive: Promiscuity is not confined to those who indulge in gay sex clandestinely. Infidelity is acknowledged to be a greater problem in male gay "marriages" than in heterosexual ones, and society 's disapproval is far greater of casual than of stable homosexual relations. Many of the same arguments apply to lesbians, who show a striking contrast: Lesbians rarely tend to indulge in sex with strangers but instead form partnerships that persist for many years with little risk of infidelity. Most lesbians have fewer than ten partners in their lifetimes."

Donald Symons of the University of California at Santa Barbara has argued that the reason male homosexuals on average have more sexual partners than male heterosexuals, and many more than female homosexuals, is that male homosexuals are acting out male tendencies or instincts unfettered by those of women.

Although homosexual men, like most people, usually want to have intimate relationships, such relationships are difficult to maintain, largely owing to the male desire for sexual variety; the unprecedented opportunity to satisfy this desire in a world of men; and the male tendency toward sexual jealousy: : : : I am suggesting that heterosexual men would be as likely as homosexual men to have sex most often with strangers, to partici-pate in anonymous orgies in public baths, and to stop POLYGAMY AND THE NATURE OF MEN

::: 183 :::

off in public restrooms for five minutes of fellatio on the way home from work if women were interested in these activities:"

That is not to say that homosexuals do not long for stable intimacy or even that many are morally repelled by anonymous sex.

But Symons 's point is that the desire for monogamous intimacy with a life companion and the desire for casual sex with strangers are not mutually incompatible instincts: Indeed, they are characteristic of heterosexual men, as proven by the existence of a thriving call girl or "escort" industry that, at a price, supplies happily married businessmen with sexual diversions while they are traveling.

Symons is commenting not on homosexual men but on men—average men: As he says, homosexual men behave like men, only more so; homosexual women behave like women, only more so."

HAREMS AND WEALTH

In the chess game of sex, each gender must respond to the other' s moves: The resulting pattern, whether polygamous or monogamous, is a stalemate rather than a draw or a victory: In elephant seals and sage grouse, the game reaches the point where males care only about the quantity of mates and females only about the quality. Each pays a heavy price, the males battling and exhausting themselves and dying in the often vain attempt to be the senior bull or master cock, the females entirely forgoing any practical help from the fathers in rearing their children.

The chess game reaches a very different stalemate in the case of the albatross. Every female gets her model husband; courtship is a mutual affair, and they share equally the chores of raising the chick: Neither gender seeks quantity of mates, but both are after quality: the hatching and rearing of one solitary chick that is pampered and fed for many months. Given that male albatrosses have the same genetic incentives as male elephant seals, why do they behave so differently?

::: 184 :::

The Red Quern

The answer, as John Maynard Smith was the first to see, can be supplied by game theory, a technique borrowed from economics: Game theory is different from other forms of theorizing because it recognizes that the outcome of a transaction often depends on what other people are doing. Maynard Smith tried pitting different genetic strategies against each other in the same way that economists do with different economic strategies: Among the problems that were suddenly rendered soluble by this technique was the question of why different animals have such different mating systems:"

Imagine a population of ancestral albatrosses in which the males were highly polygamous and spared no time to help rear the young: Imagine that you were a junior male with no prospect of becoming a harem master: Suppose that instead of striving to be a polygamist, you married one female and helped rear her offspring: You would not have hit the jackpot, but at least you would have done better than most of your more ambitious brothers: Suppose, too, that by helping your wife to feed the baby, you greatly increased the chance that the baby survived: Suddenly, females in the population have two options: to seek a faithful mate like yourself or to seek a polygamist: Those that seek a faithful mate leave behind more young, so in each generation the number willing to join harems declines, and the rewards of becoming a polygamist fall with it: The species is "taken over" by monogamy:"

It works in reverse as well: The male lark bunting of Canada sets up a territory in a field and tries to attract several females to breed with him: By joining a male that already has a mate, a female forfeits the chance to make use of his skills as a father. But if his territory is sufficiently richer in food than his neighbor 's, it still pays her to choose him: When the advantage of choosing a bigamist for his territory or genes exceeds the advantage of choosing a monogamist for his parental care, polygamy ensues: This so-called polygyny threshold model seems to explain how so many marshland birds in North America became polygamous: 16

Both of these models could apply easily to humans: We became monogamous because the advantage that a junior father POLYGAMY AND THE NATURE OF MEN

::: 185 :::

could supply in feeding the family outweighed the disadvantage in not being mated to the chief. Or we became polygamous because of the discrepancies in wealth between males. "Which woman would not rather be John Kennedy 's third wife than Bozo the Clown's first?" said one (female) evolutionist:"

There is some evidence that the polygyny threshold does apply to human beings: Among the Kipsigis of Kenya, rich men have more cattle and more wives: Each wife of a rich man is at least as well off as the single wife of a poor man, and she knows it.

According to Monique Borgehoff Mulder of the University of California at Davis, who has studied the Kipsigis, polygamy is willingly chosen by the women: A Kipsigis woman is consulted by her father when her marriage is arranged, and she is only too aware that being the second wife of a man with plenty of cattle is a better fate than being the first wife of a poor man. There is companionship and a sharing of the burden between co-wives. The polygyny threshold model holds for Kipsigis fairly well. 1e

There are two difficulties with this theory, however. The first is that it says nothing about the first wife ' s views: There is little advantage to a first wife in sharing her husband and his wealth with others: Among the Mormons of Utah it is well known that first wives resent the arrival of second wives: The Mormon church officially abandoned polygamy more than a century ago, but in recent years a few fundamentalists have resumed the practice and have even begun to campaign openly for its acceptance. In Big Water, Utah, the mayor, Alex Joseph, had nine wives and twenty children in 1991. Most of the wives were career women who were happy with their lot, but they do not all see eye to eye. " The first wife does not like it when the second wife comes along, " said the third Mrs: Joseph, "and the second wife doesn 't care for the wife who came first: So you can get some fighting and bad feeling. "19

Supposing that first wives usually object to sharing their husbands, what can the husband do about it? He can force her to accept the arrangement, as presumably many despots did in times past, or he can bribe her to accept it: The legitimacy a first wife 's children usually has compared with those from a second wife is a

::: 186 :::

The Red Queen

bonus that must go some way toward mollifying the former. In parts of Africa it is written into the law that the first wife inherits 70 percent of the husband 's wealth.

Incidentally, the polygyny threshold leads me to ask the question In whose interest is it that polygamy be outlawed in our society? We automatically assume it is in the interest of women.

But consider; it would presumably be illegal, as it is now, for people to be forced to marry against their will, so second wives would be choosing their lot voluntarily. A woman who wants a career would surely find a menage a trois more, not less, convenient; she would have two partners to'help share the chores of child care. As a Mormon lawyer put it recently, there are "compelling social reasons "

that make polygamy "attractive to the modern career woman. "20 But think of the effect on men: If many women chose to be second wives of rich men rather than first wives of poor men, there would be a shortage of unmarried women, and many men would be: forced to remain unhappily celibate. Far from being laws to protect women, antipolygamy statutes may really do more to protect men.'

Let us erect the four commandments of mating system theory. First, if females do better by choosing monogamous and faithful males, monogamy will result—unless, second, men can coerce them. Third, if females do no worse by choosing already-mated males, polygamy will result—unless fourth already-mated females can prevent their males from mating again, in which case monogamy will result: The surprising conclusion of game theory is therefore that males, despite their active role in seduction, may be largely passive spectators at their marital fate.

WHY PLAY SEXUAL MONOPOLY?

But the polygamy threshold is a bird-centric view. Those who study mammals take a rather different view, for virtually all mammals lie so far above the polygamy. threshold that the four commandments are irrelevant: Male mammals can be of so little use to their mates during pregnancy that it need not concern the females whether the POLYGAMY AND THE NATURE OF MEN

::: 187:::

males have already married. Humanity is a startling exception to this rule. Because children are fed by their parents for so long, they are more like baby birds than baby mammals. The female can do a great deal better by choosing an unmarried wimp of a husband who will stay around to help rear the young than by marrying a philandering chief if she has to do all the work herself. That is a point to which I shall return in the next chapter. For the moment, forget people and think about deer.

A female deer has little need of a monopolized male. He cannot produce milk or bring grass to the young. So the mating system of a deer is determined by the battle among males, which in turn is determined by how females decide to distribute themselves.

Where females live in herds (for example, elk), males can be harem masters. Where females live alone (white-tailed deer), males are territorial and mostly monogamous: Each species has its own pattern, depending on the behavior of the females: In the 1970s zoologists began to investigate these patterns to try to find out what determined a species ' mating system. They coined a new term, "socioecology," in the process. Its most successful forays were into antelope and monkey society: Two studies concluded that the mating system of an antelope or a primate could be safely predicted from its ecology. Small forest antelopes are selective feeders and, as a consequence, are solitary and monogamous: Middle-sized, open-woodland ones live in small groups and form harems. Big plains antelopes, such as the eland and African buffalo, live in great herds and are promiscuous: At first a very similar system seemed to apply to monkeys and apes. Small nocturnal bush babies are solitary and monogamous; leaf-eating indris live in harems; forest-fringe-dwelling gorillas live in small harems; tree-savanna chimps live in large promiscuous groups; grassland 22

baboons live in large harems or multimale troops.

It began to look as if such ecological determinism was on to something: The logic behind it was that female mammals set out to distribute themselves without regard to sex, living alone or in small groups or in large groups according to the dictates of food and safety. Males then set out to monopolize as many females as

::: 188 :::

Thr Red Queen

possible either by guarding groups of females directly or by defending a territory in which females lived. Solitary, widely dispersed females gave a male only one option: to monopolize a single female 's home range and be her faithful husband (for instance, the gibbon). Females that were solitary but less far apart gave him the chance to monopolize the home ranges of two or more separate females (for instance, the orangutan): Small groups of females gave him the chance to monopolize the whole group and call it his harem (for instance, the gorilla). He would have to share large groups with other males (for instance, the chimp).

That picture has been complicated by one factor: A species '

recent history can influence what mating system it ends up with: Or, to put it more simply, the same ecology can produce two different mating systems depending on the route taken to get there. On Northumbrian moors the red grouse and the black grouse live in virtually identical habitats. The black grouse prefers bushy areas and places that are not too heavily grazed by sheep, but apart from that, they are ecological brothers: Yet the black grouse gather in spring at spectacular leks where all the females mate with just one or two males, those that have most impressed them with their displays. They then rear their young without any help from the males.

The nearby red grouse are territorial and monogamous; the cock is almost as attentive to the chicks as the hens: The two species share the same food, habitat, and enemies, yet have entirely different mating systems. Why? My preferred explanation, and that of most biologists who have studied them, is that they have different histories. Black grouse are the descendants of forest dwellers, and it was in the forest that their maternal ancestors developed the habit of choosing males according to genetic quality rather than territory:"

HUNTERS OR GATHERERS

The lesson for humanity is obvious: To determine our mating system we need to know our natural habitat and our past: We have lived mostly in cities for less than one thousand years. We have POLYGAMY AND THE NATURE OF MEN

::: 189 :::

been agricultural for less than ten thousand: These are mere eye blinks. For more than a million years before that we were recognizably human and living, mostly in Africa, probably as hunter-gatherers, or foragers, as anthropologists now prefer to say. So inside the skull of a modern city dweller there resides a brain designed for hunting and gathering in small groups on the African savanna.

Whatever humanity 's mating system was then is what is " natural "

for him now.

Robert Foley is an anthropologist at Cambridge University who has tried to piece together the history of our social system: He starts with the fact that all apes share the habit of females leaving their natal group, whereas all baboons share the habit of males leaving their natal group: It seems to be fairly hard for a species to switch from female exogamy to male exogamy, or vice versa. On average, human beings are typical apes in this respect even today. In most societies women travel to live with their husbands, whereas men tend to remain close to their relatives: There are many exceptions, though: In some but not most traditional human societies, men move to women.

Female exogamy means that apes are largely devoid of mechanisms for females to build coalitions of relatives. A young•

female chimpanzee generally must leave her mother 's group and join a strange group dominated by unfamiliar males: To do so, she must gain favor with the females that already live in her new tribe.

A male, by contrast, stays with his group and allies himself with powerful relatives in the hope of inheriting their status later: So much for the ape ' s legacy to mankind: What about the habitat in which he lived? Toward the end of the Miocene era, some 25 million years ago, Africa 's forests began to contract. Drier, more seasonal habitats—grasslands, scrublands, savannas—began to spread. About 7 million years ago the ancestors of mankind began to diverge from the ancestors of modern chimpanzees. Even more than 'chimps and much more than gorillas, mankind 's ancestors moved into these new dry habitats and gradually adapted to them: We know this because the earliest fossils of manlike apes (the australopithecines) were living in places that at the time were not cov-