The Red Queen: Sex and the Evolution of Human Nature

by Matt Ridley

A female human being does not have to share her sexual favors with many males to prevent infanticide, but she may have a good reason to share them with one well-chosen male apart from her husband. This is because her husband is, almost by definition, usually not the best male there is—else how would he have ended up married to her? His value is that he is monogamous and will therefore not divide his child-rearing effort among several families. But why accept his genes? Why not have his parental care and some other male’s genes?

First, women most commonly seek monogamous marriage—even in societies that allow polygamy. Rare exceptions notwithstanding, they want to choose carefully and then, as long as he remains worthy, monopolize a man for life, gain his assistance in rearing the children, and perhaps even die with him. Second, women do not seek sexual variety per se. There are exceptions, of course, but fictional and real women regularly deny that nymphomania holds any attraction for them, and there is no reason to disbelieve them. The temptress interested in a one-night stand with a man whose name she does not know is a fantasy fed by male pornography. Lesbians, free of constraints imposed by male nature, do not suddenly indulge in sexual promiscuity; on the contrary, they are remarkably monogamous. None of this is surprising: Female animals gain little from sexual opportunism, for their reproductive ability is limited not by how many males they mate with but how long it takes to bear offspring. In this respect men and women are very different.

Some male damsel flies use their penis to scoop out sperm that was there first; male dogs and Australian hopping mice both “lock” their penis into the female after copulation and cannot free it for some time, thus preventing others from having a go; male human beings seem to produce large numbers of defective “kamikaze” sperm that form a sort of plug that closes the vaginal door to later entrants.)

For example, very little is known about the societies of dolphins and whales, but a good deal is known of their anatomy, thanks to whaling. They all have enormous testicles, even allowing for their size. The testicles of a right whale weigh more than a ton and account for 2 percent of its body weight. So, given the monkey pattern, it is reasonable to predict that female whales and dolphins are mostly not monogamous but will mate with several males.

For an ape, man’s testicles are medium-sized—considerably bigger than a gorilla’s. Like a chimpanzee’s, human testicles are housed in a scrotum that hangs outside the body where it keeps the sperm that have already been produced cool, therefore increasing their shelf life, as it were.16 This is all evidence of sperm competition in man.

In a mammal, by contrast, there is not much he can do to help even if wants to. He can feed his wife while she is pregnant and thereby contribute to the growth of the fetus, and he can carry the baby about when it is born or bring it food when it is weaned, but he cannot carry a fetus in his belly or feed it milk when it is born. The female mammal is left literally holding the baby, and with few opportunities to help her, the male is often better off expending his energy on an attempt to be a polygamist. Only when opportunities for further mating are few and his presence increases the baby’s safety—as in gibbons—will he stay.

A female swallow needs a husband who will help look after her young, but by the time she arrives at the breeding site, she might find all the best husbands taken. Her best tactic is therefore to mate with a mediocre husband or a husband with a good territory and have an affair with a genetically superior neighbor. This theory is supported by the facts: Females always choose more dominant, older, or more “attractive” (that is, ornamented) lovers than their husbands; they do not have affairs with bachelors (presumably rejects) but with other females’ husbands; and they sometimes incite competition between potential lovers and choose the winners.

As expected, he found that high-ranking men were involved most, which is consistent with the idea of having your paternal-genetic cake and eating it. However, unlike in birds, it was not just the wives of low-ranking men who indulged. It is true that Aché adulterers frequently ply their mistresses with gifts of meat, but Hill thinks the most important motive is that Aché women are constantly preparing for the possibility that they will be deserted by their husbands. They are building up alternative relationships and are more likely to be unfaithful if the marriage is going badly. That is, of course, a double-edged sword: The marriage could break up because the affair is discovered.

The other is certain tribes of Australian aborigines, which practice gerontocratic polygamy: Men do not marry until they are forty, and by the age of sixty-five they have usually accumulated up to thirty wives. But this peculiar system is far from what it seems. Each old man has younger assistant men whose help, protection, and economic support he purchases by, among other things, turning a blind eye to their affairs with his wives. The old man looks the other way when the helpful nephew carries on with one of his junior wives.

In the African pygmies Wrangham studied, gossip was rife and a husband’s best chance of deterring his wife’s affairs was to let her know that he kept abreast of the gossip. Wrangham went on to observe that this was impossible without language, so he speculated that the sexual division of labor, the institution of child-rearing marriages, and the invention of language—three of the most fundamental human characteristics shared with no other ape—all depend on another.

Sarah Hrdy proposed that silent ovulation helps prevent infanticide because neither the husband nor the lover knows if he has been cuckolded. Donald Symons thinks women use perpetual sexual availability to seduce philanderers in exchange for gifts. L. Benshoof and Randy Thornhill suggested that concealed ovulation allows a woman to mate with a superior man by stealth without deserting or alerting her husband. If, as seems possible, ovulation is less concealed from her (or her unconscious) than it is from him, then it would help her make each extramarital liaison more rewarding since she is more likely to “know” when to have sex with her lover, whereas her husband does not know when she is fertile. In other words, silent ovulation is a weapon in the adultery game.

Red-winged blackbirds, which nest in marshes in Canada, are polygamous; the males with the best territories each attract several females to nest in them. But the males with the biggest harems are also the most successful adulterers, fathering the most babies in their neighbors’ territories, too.

It is my contention that man is just like an ibis or a swallow or a sparrow in several key respects. He lives in large colonies. Males compete with one another for places in a pecking order. Most males are monogamous. Polygamy is prevented by wives who resent sharing their husbands lest they also share his contributions to child rearing. Even though they could bring up the children unaided, the husband’s paycheck is invaluable. But the ban on polygamous marriage does not prevent the males from seeking polygamous matings. Adultery is common. It is most common between high-ranking males and females of all ranks. To prevent it males try to guard their wives, are extremely violent toward their wives’ lovers, and copulate with their wives frequently, not just when they are fertile.

That is the life of the sparrow anthropomorphized. The life of man sparrowmorphized might read like this: The birds live and breed in colonies called tribes or towns. Cocks compete with one another to amass resources and gain status within the colony; it is known as “business” and “politics.” Cocks eagerly court hens, who resent sharing their males with other hens, but many cocks, especially senior ones, trade in their hens for younger ones or cuckold other cocks by having sex with their (willing) wives in private.

The noble savage, far from living in contented sexual equanimity, was paranoid about becoming, and intent on making his neighbor into, a cuckold. Little wonder that human sex is first and foremost in all societies a private thing to be indulged in only in secret. The same is not true of bonobos, but it is true of many monogamous birds. One reason the high bastard rates of birds came as such a shock was that few naturalists had ever witnessed an adulterous affair between two birds—they do it in private.

Wilson and Daly believe that a study of human society reveals a mindset whose manifestations are diverse in detail but “monotonously alike in the abstract.” They are “socially recognized marriage, the concept of adultery as a property violation, the valuation of female chastity, the equation of ‘protection’ of women with protection from sexual contact, and the special potency of infidelity as a provocation to violence.” In short, in every age and in every place, men behave as if they owned their wives’ vaginas.

As many a modern couple knows, the absence of jealousy, far from calming a relationship, is itself a cause of insecurity. If he or she is not jealous when I pay attention to another man or woman, then he or she no longer cares whether our relationship survives. Psychologists have found that couples who lack moments of jealousy are less likely to stay together than jealous ones.

As Wilson and Daly said: “The major source of conflict in the great majority of spouse killings is the husband’s knowledge or suspicion that his wife is either unfaithful or intending to leave him.” A man who kills his wife in a fit of jealousy can rarely plead insanity in court because of the legal tradition in Anglo-American common law that such an act is “the act of a reasonable man.”

Cuckoldry is an asymmetrical fate. A woman loses no genetic investment if her husband is unfaithful, but a man risks unwittingly raising a bastard. As if to reassure fathers, research shows that people are strangely more apt to say of a baby, “He (or she) looks just like his father,” than to say, “He (or she) looks just like his mother”—and that it is the mother’s relatives who are most likely to say this.44 It is not that a woman need not mind about her husband’s infidelity; it might lead to his leaving her or wasting his time and money on his mistress or picking up a nasty disease. But it does imply that men are likely to mind even more about their wives’ infidelity than vice versa. History and law have long reflected just that. In most societies adultery by a wife was illegal and punished severely, while adultery by a husband was condoned or treated lightly. Until the nineteenth century in Britain, a civil action could be brought against an adulterer by an aggrieved husband for “criminal conversation.”45 Even among the Trobriand islanders, who were celebrated by Bronislaw Malinowski in 1927 as a sexually uninhibited people, females who committed adultery were condemned to die.

When, on their wedding night, Angel Clare confessed to his new wife, Tess, in Thomas Hardy’s Tess of the D’Urbervilles, that he had sown his wild oats before marriage, she replied with relief by telling the story of her own seduction by Alec D’Urberville and the short-lived child she bore him. She thought the transgressions balanced. “Forgive me as you are forgiven! I forgive you, Angel.” “You—yes you do.” “But do you not forgive me?” “O Tess, forgiveness does not apply to the case! You were one person; now you are another. My God—how can forgiveness meet such a grotesque—prestidigitation as that!” Clare left her that night.

Human mating systems are greatly complicated by the fact of inherited wealth. The ability to inherit wealth or status from a parent is not unique to man. There are birds that succeed to the ownership of their parents’ territories by staying to help them rear subsequent broods. Hyenas inherit their dominance rank from their mothers (in hyenas, females are dominant and often larger); so do many monkeys and apes.

Tristan expected to inherit the kingdom of his uncle, King Mark, in Cornwall. While in Ireland he ignored the attentions of the beautiful Isolde until she was summoned by King Mark to be his wife. Panic-struck at the thought of losing his inheritance but determined to save it at least for his son, he suddenly took an enormous interest in Isolde.

The Church’s obsessions with sexual matters were very different from St. Paul’s. It had little to say about polygamy or the begetting of many bastards, although both were commonplace and against doctrine. Instead, it concentrated on three things: first, divorce, remarriage, and adoption; second, wet nursing, and sex during periods when the liturgy demanded abstinence; and third, “incest” between people married to within seven canonical degrees. In all three cases the Church seems to have been trying to prevent lords from siring legitimate heirs. If a man obeyed the doctrines of the Church in the year 1100, he could not divorce a barren wife, he certainly could not remarry while she lived, and he could not adopt an heir. His wife could not give her baby daughter to a wet nurse and be ready to bear another in the hope of its being a son, and he could not make love to his wife “for three weeks at Easter, four weeks at Christmas, and one to seven weeks at Pentecost; plus Sundays, Wednesdays, Fridays, and Saturdays—days for penance or sermons; plus miscellaneous feast days.” He also could not bear a legitimate heir by any woman closer than a seventh cousin—which excluded most noble women within three hundred miles. It all adds up to a sustained attack by the Church on the siring of heirs, and “it was not until the Church started to fill up with the younger brothers of men of state that the struggle over inheritance—over marriage—between them began.” Individuals in the Church (d...

(disinherited younger sons) were manipulating sexual mores to increase the Church’s own wealth or even regain property and titles for themselves.

Among the royal dynasties of Europe, though, in most of which women could inherit thrones (in default of male heirs), eligible marriages were often possible. Eleanor of Aquitaine brought Britain’s kings a large chunk of France. The War of the Spanish Succession was fought solely to prevent a French king from inheriting the throne of Spain as the result of a strategic marriage. Right down to the Edwardian practice of English aristocrats marrying the daughters of American robber barons, the alliances of great families have been a force to concentrate wealth.

Another way, practiced commonly among slave-owning dynasties in the American South, was to keep marriage within the family. Nancy Wilmsen Thornhill of the University of New Mexico has shown how in such families more often than not men married their first cousins. By tracing the genealogies of four southern families, she found that fully half of all marriages involved kin or sister exchange (two brothers marrying two sisters). By contrast, in northern families at the same time, only 6 percent of marriages involved kin. What makes this result especially intriguing is that Thornhill had predicted it before she found it. Wealth concentration works better for land, whose value depends on its scarcity, than for business fortunes, which are made and lost in many families in parallel.

There has been no genetic change since we were hunter-gatherers, but deep in the mind of the modern man is a simple male hunter-gatherer rule: Strive to acquire power and use it to lure women who will bear heirs; strive to acquire wealth and use it to buy other men’s wives who will bear bastards. It began with a man who shared a piece of prized fish or honey with an attractive neighbor’s wife in exchange for a brief affair and continues with a pop star ushering a model into his Mercedes. From fish to Mercedes, the history is unbroken: via skins and beads, plows and cattle, swords and castles. Wealth and power are means to women; women are means to genetic eternity.

Likewise, deep in the mind of a modern woman is the same basic hunter-gatherer calculator, too recently evolved to have changed much: Strive to acquire a provider husband who will invest food and care in your children; strive to find a lover who can give those children first-class genes. Only if she is very lucky will they be the same man. It began with a woman who married the best unmarried hunter in the tribe and had an affair with the best married hunter, thus ensuring her children a rich supply of meat. It continues with a rich tycoon’s wife bearing a baby that grows up to resemble her beefy bodyguard. Men are to be exploited as providers of parental care, wealth, and genes.

Men and women have different bodies. The differences are the direct result of evolution. Women’s bodies evolved to suit the demands of bearing and rearing children and of gathering plant food. Men’s bodies evolved to suit the demands of rising in a male hierarchy, fighting over women, and providing meat to a family.

There are three reasons to expect evolution to have produced different mentalities in men and women. The first is that men and women are mammals, and all mammals show sexual differences in behavior. As Charles Darwin put it, “No one disputes that the bull differs in disposition from the cow, the wild boar from the sow, the stallion from the mare.”3 The second is that men and women are apes, and in all apes there are great rewards for males that show aggression toward other males, for males that seek mating opportunities, and for females that pay close attention to their babies. The third is that men and women are human beings, and human beings are mammals with one highly unusual characteristic: a sexual division of labor. Whereas a male and a female chimp seek the same sources of food, a male and a female human being, in virtually every preagricultural society, set about gathering food in different ways. Men look for sources that are mobile, distant, and unpredictable (usually meat), while women, burdened with children, look for sources that are static, close, and predictable (usually plants).

It is impossible in the end to deny that even a highly conditioned trait can be without some basis in biology—or vice versa. Nurture always reinforces nature; it rarely fights it. (An exception may be aggressiveness, which develops more in boys despite frequent parental discouragement.) I find it very hard to believe that the fact that 83 percent of murderers and 93 percent of drunken drivers in America are male is due to social conditioning alone.

Among birds it is usually only the male that sings. A zebra finch will not sing unless there is sufficient testosterone in its blood. With testosterone, the special song-producing part of its brain grows larger and the bird begins to sing. Even a female zebra finch will sing as long as she has been exposed to testosterone early in life and as an adult. In other words, testosterone primes the young zebra finch’s brain to be responsive later in life to testosterone again and so develop the tendency to sing. Insofar as a zebra finch can be said to have a mind, the hormone is a mind-altering drug.

Women with a condition known as Turner’s syndrome (they are born without ovaries) have even less testosterone in their blood than do women who have ovaries. (Ovaries produce some testosterone, though not as much as testicles do.) They are exaggeratedly feminine in their behavior, with typically a special interest in babies, clothes, housekeeping, and romantic stories. Men with less than usual testosterone in their blood as adults—eunuchs, for example—are noted for their femininity of appearance and attitude. Men exposed to less than usual testosterone as embryos—for example, the sons of diabetic women who took female hormones during pregnancy—are shy, unassertive, and effeminate. Men with too much testosterone are pugnacious. Women whose mothers were injected with progesterone in the 1950s (to avert miscarriage) later described themselves as having been tomboys when young; progesterone is not unlike testosterone in its effects. Girls who were born with an unusual condition called either adrenogenital syndrome or congenital adrenal hyperplasia are equally tomboyish. This disorder causes the adrenal gland, near the kidney, to produce a hormone that acts like testosterone instead of cortisol, its usual product.

The mind is immune to testosterone unless it was exposed to a sufficient concentration (relative to female hormones) in the womb. It would be easy to engineer a society with no sex difference in attitude between men and women. Inject all pregnant women with the right dose of hormones, and the result would be men and women with normal bodies but identical feminine brains. War, rape, boxing, car racing, pornography, and hamburgers and beer would soon be distant memories. A feminist paradise would have arrived.

We are reinforcing the stereotypical obsessions that they already have, but we are not creating them.

The fact that “work” became a male thing and “home” a female one is an accident of history: The domestication of cattle and the invention of the plow made food gathering a task that benefited from male muscle power. In societies where the land is tilled by hand, women do most of the work. The industrial revolution reinforced the trend, but the post industrial revolution—the recent growth of service industries—is reversing it again. Women are going “out to work” again as they did when they sought tubers and berries in the Pleistocene period.

Since the bane of all organizations, whether they are companies, charities, or governments, is that they reward cunning ambition rather than ability (the people who are good at getting to the top are not necessarily the people who are best at doing the job) and since men are more endowed with such ambition than women, it is absolutely right that promotion should be biased in favor of women—not to redress prejudice but to redress human nature.

For a man casual sex with a stranger carried only a small risk—infection, discovery by the wife—and a potentially enormous reward: a cheap addition of an extra child to his genetic legacy. Men who seized such opportunities certainly left behind more descendants than men who did not. Therefore, since we are by definition descended from prolific ancestors rather than barren ones, it is a fair bet that modern men possess a streak of sexual opportunism. Virtually all male mammals and birds do, even those that are mainly monogamous. This is not to say that men are irredeemably promiscuous or that every man is a potential rapist, it is just that men are more likely to be tempted by an opportunity for casual sex than women.

Women are likely to be different. Having sex with a stranger not only encumbered a Pleistocene woman with a possible pregnancy before she had won the man’s commitment to help rear the child, but it also exposed her to probable revenge from her husband if she had one and to possible spinsterhood if she did not. These enormous risks were offset by no great reward. Her chances of conceiving were just as great if she remained faithful to one partner, and her chances of losing the child without a husband’s help were greater. Therefore, women who accepted casual sex left fewer rather than more descendants, and modern women are likely to be equipped with suspicion of casual sex.

A modern woman is exposed to pressure from men to be sexually uninihibited, but she is also exposed to the same pressure from other women. Likewise, men are under constant pressure to be more “responsible,” sensitive, and faithful—from other men as well as from women. Perhaps more out of envy than morality, men are just as censorious of philanderers as they are of women; often more so.

I argued in the last two chapters that men, for whom the reproductive stakes are higher, are likely to be more competitive with one another and therefore are more likely to end up wielding power, controlling wealth, and seeking fame. Consequently, women are more likely to have been rewarded for seeking power, wealth, or fame in a husband than men are in a wife. Women who did so probably left more descendants among modern women, so it follows from evolutionary thinking that women are more likely to value potential mates who are rich and powerful. Another way to look at it is to think of what a woman can most profitably seek in a husband that will increase the number and health of her children. The answer is not more sperm but more money or more cattle or more tribal allies or whatever resource counts.

A man, by contrast, is seeking a mate who will use his sperm and his money to produce babies. Consequently, he has always had an enormous incentive to seek youth and health in his mates. Those men who preferred to marry forty-year-old women rather than twenty-year-olds stood a small chance of begetting any children at all, let alone more than one or two. They also stood a large chance of inheriting a bunch of stepchildren from a previous marriage. They left fewer descendants than the men who always sought out the youngest, postpubertal females on offer. We would expect, therefore, that while women pay attention to cues of wealth and power, men pay attention to cues of health and youth.

To which came this answer: Of course women pay more attention to wealth because men control it. If women controlled wealth, they would not seek it in their spouses. Buss looked again and found that American women who make more money than the average American woman pay more attention than average to the wealth of potential spouses, not less.31 High-earning women value the earning capacity of their husbands more, not less, than low-earning women. Even a survey of fifteen powerful leaders of the feminist movement revealed that they wanted still more powerful men. As Buss’s colleague Bruce Ellis put it, “Women’s sexual tastes become more, rather than less, discriminatory as their wealth, power, and social status increase.”

These results are not alone. Every other study of sexual fantasy has concluded that “male sexual fantasies tend to be more ubiquitous, frequent, visual, specifically sexual, promiscuous, and active. Female sexual fantasies tend to be more contextual, emotive, intimate, and passive.”

Pornography is aimed almost entirely at men. It varies little from a standard formula all over the world. “Soft porn” consists of pictures of naked or seminaked women in provocative positions. Such pictures are arousing to men, whereas pictures of naked (anonymous) men are not especially arousing to women. “A propensity to be aroused merely by the sight of males would promote random matings from which a female would have nothing to gain reproductively and a great deal to lose.”

The romance novel, by contrast, is aimed entirely at a female market. It, too, depicts a fictional world that has changed remarkably little except in adapting to female career ambitions and to a less inhibited attitude toward the description of sex. Authors adhere strictly to a formula provided by the publishers. Sexual acts play a small part in these novels; the bulk of each book is about love, commitment, domesticity, nurturing, and the formation of relationships. There is little promiscuity or sexual variety, and what sex there is, is described mainly through the heroine’s emotional reaction to what is done to her—particularly the tactile things—and not to any detailed description of the man’s body. His character is often discussed in detail but not his body.

So does the repeated failure of magazines that try to repackage the male-porn formula for women (much of Playgirl’s readership is gay men), plus the burgeoning business of selling explicit novels about promiscuous sex at airports—for men. In any bookstore there are magazines for men with pictures of women on the covers, promising more inside, and magazines for women with pictures of women on the covers, promising hints about improving relationships inside. There are romance novels aimed at women with pictures of women on the covers and sexy novels aimed at men with pictures of women on the covers. The publishing industry, living by the market, not the prevailing ideology, has no doubts about the differences between men and women’s attitudes toward sex.

This is a far more enlightened view than the peculiarly uncharitable assumption among the politically correct that the reason women are not more turned on by nudity and pornography is that they are repressed.

A paradox looms. Men are promiscuous opportunists at heart and in their fantasies. Truly promiscuous opportunists would not be too choosy, one would think. And yet men care about women’s looks more than women care about men’s looks. A sports car and an expense account can turn a frog into a prince for women, but even a rich woman cannot afford to be ugly (although in these times of cosmetic surgery, she can sometimes afford the means not to be ugly). Advertisements for “escorts” emphasize looks. A man contemplating an affair should not restrict himself to what he considers a good-looking woman, yet he usually does. This is rather unusual. A male gorilla or sage grouse does not refuse to mate with a female because of her appearance. He takes every opportunity on offer regardless of looks. Polygamous despots of ancient times may have been promiscuous, but they were still choosy; their harems were always recruited from among the young, the virginal, and the beautiful.

The degree to which an animal of either sex is choosy correlates exactly with the degree to which it invests in parental care. A black grouse, investing no more than sperm, is prepared to copulate with anything that even resembles a female: A stuffed bird or a model will do.40 A male albatross, who will put all his best efforts into raising one female’s young, is elaborately suspicious and selective, striving for the best female on offer. So man’s choosiness reflects once more the fact that man does indeed form a pair bond and invest in his young, unlike some of his undiscriminating ape cousins. It is a legacy of his past monogamy: Choose well, for it may be the only chance you will get. Indeed, the overwhelming fascination of men with female youth argues that pair bonds have lasted lifetimes. In this we are quite unlike any other mammal. Chimpanzees find old females just as attractive as young ones as long as both are in estrus. The fact that men do prefer twenty-year-olds adds one piece of evidence to the theory that a Pleistocene man, like a modern man, married for life.

Just as a white man has different skin color from a black man, so it is quite possible that he also has a somewhat different mind. But given what we know of evolution, it is not very likely. The evolutionary pressures that have shaped the human mind—principally competitive relations with kin members, tribal allies, and sexual partners—are and have been the same for white and black men and were at work before the ancestors of whites left Africa 100,000 years ago. While skin color is affected by things such as climate, which differs markedly between Africa and northern Europe, the shape of the mind is affected only very marginally by nonhuman problems such as what kind of game to hunt or how to keep warm or cool. Infinitely more important is how to deal with fellow human beings, and that is the same problem everywhere—