The Red Queen: Sex and the Evolution of Human Nature

by Matt Ridley

Sex is about disease. It is used to combat the threat from parasites. Organisms need sex to keep their genes one step ahead of their parasites. Men are not redundant after all; they are woman’s insurance policy against her children being wiped out by influenza and smallpox (if that is a consolation). Women add sperm to their eggs because if they did not, the resulting babies would be identically vulnerable to the first parasite that picked their genetic locks.

Many fungi are sexual, but they do not have males. They have tens of thousands of different sexes, all physically identical, all capable of mating on equal terms, but all incapable of mating with themselves.

To be sexual does not necessarily imply the need for sexes, let alone for just two sexes, let alone for two sexes as different as men and women. Indeed, at first sight, the most foolish system of all is two sexes because it means that fully 50 percent of the people you meet are incompatible as breeding partners. If we were hermaphrodites, everybody would be a potential partner. If we had ten thousand sexes, as does the average toadstool, 99 percent of those we meet would be potential partners. If we had three sexes, two-thirds would be available.

Genes are not conscious and do not choose to cooperate; they are inanimate molecules switched on and off by chemical messages. What causes them to work in the right order and create a human body is some mysterious biochemical program, not a democratic decision. But in the last few years the revolution begun by Williams, Hamilton, and others has caused more and more biologists to think of genes as analogous to active and cunning individuals. Not that genes are conscious or driven by future goals—no serious biologist believes that—but the extraordinary teleological fact is that evolution works by natural selection, and natural selection means the enhanced survival of genes that enhance their own survival. Therefore, a gene is by definition the descendant of a gene that was good at getting into future generations. A gene that does things that enhance its own survival may be said, teleologically, to be doing them because they enhance its survival. Cooperating to build a body is as effective a survival “strategy” for genes as cooperating to run a town is a successful social strategy for human beings.

In some female flour beetles there exists a gene called Medea that kills those offspring that do not inherit it.11 It is as if the gene booby-traps all the female’s young and defuses only those that it itself inhabits.

A male is defined as the gender that produces sperm or pollen: small, mobile, multitudinous 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.21 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 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 th...

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?”

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 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.

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.

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.

Most plants are hermaphrodites. There is a general pattern for mobile creatures to be “dioecious” (with separate genders) and sessile 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.

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.

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, 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 1–2 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.

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.

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.

Therefore, among polygamists the following strategy often appears: If small, be female; if large, be male.

Half-grown male deer spend years in a state of celibacy awaiting the chance to breed, while their sisters produce a fawn a year.

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.

Think of it as a competition to have the most grandchildren. If males are polygamous, a successful son can give you far 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.

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 astonishment 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 1.4 to 1. Well-fed opossums are significantly more likely to have sons than poorly fed ones.

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.

Putting baking soda in the vagina of a rabbit was proved to affect the sex ratio of its babies as early as 1932.

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 them73).

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 1:1, 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.

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 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.

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.

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.

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 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.

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.

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.

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.

Females choose; their choosiness is inherited; they prefer exaggerated ornaments; exaggerated ornaments are a burden to males.

Sir Ronald Fisher had suggested then that females need no better reason for preferring long tails than that other 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.

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.

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.

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.

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

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.

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.

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.

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.

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.

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.

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.

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 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.

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.

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.)