The Red Queen: Sex and the Evolution of Human Nature

by Matt Ridley

As every bird-watcher knows, the beauty of a bird’s song is inversely correlated with the colorfulness of its plumage. The operatic 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.

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.

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.

If women didn’t exist, all the money in the world would have no meaning. —Aristotle Onassis

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

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.

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 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.

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. 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 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.

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.

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.

A 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.

The cited study is from 1979. HIV entered the public consciousness in 1985.

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.

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 participate in anonymous orgies in public baths, and to stop off in public restrooms for five minutes of fellatio on the way home from work if women were interested in these activities.

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.

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.

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.

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.

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 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.

Everybody knew or had heard of nearly all the people they were likely to meet in their lives: There were no strangers, a fact that had enormous importance for the history of trade and crime prevention, among other things. The lack of anonymity meant that charlatans and tricksters could rarely get away with their deceptions for long.

Our brains grew so big not to make tools but to psychologize one another. The lesson of socioecology is that our mating system is determined not by ecology but by other people—by members of the same gender and by members of the other gender. It is the need to outwit and dupe and help and teach one another that drove us to be ever more intelligent.

In recent memory there was a preagricultural culture among the salmon-fishing Indians of the Pacific Northwest of America that was highly polygamous. If the local hunter-gathering economy favored it, men were capable of being polygamous and women were capable of joining harems over the protests of the preceding co-wives. If not, then men were capable of being good fathers and women jealous monopolizers. In other words, mankind has many potential mating systems, one for each circumstance.

One of the reasons hunting and gathering cannot support much polygamy is that luck, more than skill, plays a large part in hunters’ success. Even the best hunter would often return empty-handed and would be reliant on his fellow men to share what they had killed. This equitable sharing of hunted food is characteristic of these people (in most other social hunting species there is a free-for-all) and is the clearest example of a habit of “reciprocal altruism” on which the whole of society sometimes appears to be based.

Trading favors in this way was the ancient ancestor of the monetary economy. But because meat could not be stored and because luck did not last, hunter-gatherer societies did not allow the accumulation of wealth.

Pastoral societies are, almost without exception, traditionally polygamous. It is not hard to see why. A herd of cattle or sheep is almost as easy to tend if it contains fifty animals as twenty-five. Such scale economies allow a man to accumulate wealth at an ever-increasing rate. Positive feedback leads to inequalities of wealth, which leads to inequalities of sexual opportunity.

By the time “civilization” had arrived, in six different parts of the globe independently (from Babylon in 1700 B.C. to the Incas in A.D. 1500), emperors had thousands of women in their harems. Hunting and warrior skills had previously earned a man an extra wife or two, then wealth had earned him ten or more.

A man’s livelihood and his allegiance were owed to the same social superior.33 Power is, roughly speaking, the ability to call upon allies to do your bidding, and that depended strictly on wealth (with a little help from violence).

Thanks to the work of Richard Connor, Rachel Smolker, and their colleagues, we now know that groups of male dolphins kidnap single females, bully them and display to them with choreographed acrobatics, then enjoy sexual monopoly over them. Once the female has given birth, the alliances of males lose interest in her, and she is free to return to an all-female group. These male alliances are often temporary and stitched together on a you-help-me-and-I’ll-help-you basis.

In people there is virtually no connection between strength and power, at least not since the invention of action-at-a-distance weapons such as the slingshot, as Goliath learned the hard way. Wealth, cunning, political skill, and experience lead to power among men. From Hannibal to Bill Clinton, men gain power by putting together coalitions of allies. In mankind, wealth became a way of putting together such alliances of power.

For example, in India, high castes practiced more female infanticide than low castes because there were fewer opportunities to export daughters to still higher castes.

There is a cautionary tale that scientists tell one another about a man who cuts the legs off a flea to test his theory that fleas’ ears are on their legs. He then tells the flea to jump and it does not, so he concludes that he was right; fleas’ ears are in their legs.

Looking around the modern world, she was not encouraged; powerful men are often childless. Hitler was so consumed by ambition that he had little time left for philandering.

The six independent “civilizations” of early history—Babylon, Egypt, India, China, Aztec Mexico, and Inca Peru—were remarkable less for their civility than for their concentration of power. They were all ruled by men, one man at a time, whose power was arbitrary and absolute. These men were despots, meaning they could kill their subjects without fear of retribution. Without exception, that vast accumulation of power was always translated into prodigious sexual productivity. The Babylonian king Hammurabi had thousands of slave “wives” at his command. The Egyptian pharaoh Akhenaten procured 317 concubines and “droves” of consorts. The Aztec ruler Montezuma enjoyed 4,000 concubines. The Indian emperor Udayama preserved sixteen thousand consorts in apartments ringed by fire and guarded by eunuchs. The Chinese emperor Fei-ti had ten thousand women in his harem. The Inca Atahualpa, as we have seen, kept virgins on tap throughout the kingdom.

In medieval times the census shows a sex ratio in the countryside that was heavily male-biased because so many women were “employed” in the castles and monasteries. Their jobs were those of serving maids of various kinds, but they formed a loose sort of “harem” whose size depended clearly on the wealth and power of the castle’s owner. In some cases historians and authors were more or less explicit in admitting that castles contained “gynoeciums,” where lived the owner’s harem in secluded luxury.

Meanwhile, many medieval peasant men were lucky to marry before middle age and had few opportunities for fornication.

According to Tacitus, the Germanic tribes that so frustrated several Roman emperors attributed their success partly to the fact that they were a monogamous society and therefore able to direct their aggression outward (though no such explanation applied to the polygamous and successful Romans). No man was allowed more than one wife, so no man had an incentive to kill a fellow tribesman to take his wife.

war have tended to be women rather than men. But echoes

Armies have often been motivated as much by the opportunities that victory would present for rape as they have been by patriotism or fear. Generals, recognizing this, turned blind eyes to the excesses of their troops and were sure to provide camp followers. Even in this century, access to prostitutes has been a more or less recognized purpose of shore leave in navies.

The nature of the human male, then, is to take opportunities, if they are granted him, for polygamous mating and to use wealth, power, and violence as means to sexual ends in the competition with other men—though usually not at the expense of sacrificing a secure monogamous relationship. It is not an especially flattering picture, and it depicts a nature that is very much at odds with modern ethical preferences—for monogamy, fidelity, equality, justice, and freedom from violence. But my task is description, not prescription.

In 1988, political power, far from being a ticket to polygamy, was jeopardized by any suggestion of infidelity. Whereas the Chinese emperor Fei-ti once kept ten thousand women in his harem, Gary Hart, running for the presidency of the most powerful nation on earth, could not even get away with two.

Before “civilization” and since democracy, men have been unable to accumulate the sort of power that enabled the most successful of them to be promiscuous despots. The best they could hope for in the Pleistocene period was one or two faithful wives and a few affairs if their hunting or political skills were especially great. The best they can hope for now is a good-looking younger mistress and a devoted wife who is traded in every decade or so. We’re back to square one.

And it is a curious truth that the monogamous marriage bond survived right through despotic Babylon, lascivious Greece, promiscuous Rome, and adulterous Christendom to emerge as the core of the family in the industrial age. Even in the most despotic and polygamous moment of human history, mankind was faithful to the institution of monogamous marriage, quite unlike any other polygamous animal. Even despots usually had one queen and many concubines. Explaining the human fascination with monogamous marriage requires us to understand the female strategy as closely as we have understood the male one. When we do, an extraordinary insight into human nature will emerge.

SHEPHERD: Echo, I ween, will in the wood reply, And quaintly answer questions: shall I try? ECHO: Try. What must we do our passion to express? Press. How shall I please her who never loved before? Be Fore. What most moves women when we them address? A dress. Say, what can keep her chaste whom I adore? A door. If music softens rocks, love tunes my lyre. Liar. Then teach me, Echo, how shall I come by her? Buy her. —Jonathan Swift, “A Gentle Echo on Woman”

In many ways modern people probably live in social systems that are much closer to those of their hunter-gatherer ancestors than they are to the conditions of early history. No hunter-gatherer society supports more than occasional polygamy, and the institution of marriage is virtually universal. People live in larger bands than they used to, but within those bands the kernel of human life is the nuclear family: husband, wife, and children. Marriage is a child-rearing institution; wherever it occurs, the father takes at least some part in rearing the child even if only by providing food. In most societies men strive to be polygamists but few succeed. Even in the polygamous societies of pastoralists, the great majority of marriages are monogamous ones.

Of the four other apes (gibbons, orangutans, gorillas, and chimpanzees), only the gibbon practices anything like marriage. Gibbons live in faithful pairs in the forests of Southeast Asia, each pair living a solitary life within a territory.

Although men are fickle (“You’re afraid of commitment, aren’t you?” says the stereotypical victim of a seducer), they are also interested in finding wives with whom to rear families and might well be very set on sticking by them despite their own infidelity (“You’re never going to leave your wife for me, are you?” says the stereotypical mistress).

Our sex lives are very different from those of our cousins. If we were like orangutans, women would live alone and apart from one another. Men, too, would live alone but each would visit several women (or none) for occasional sex. If two men ever met, there would be an almighty, violent battle. If we were gibbons, our lives would be unrecognizable. Every couple would live miles apart and fight to the death any intrusion into their home range—which they would never leave. Despite the occasional antisocial neighbor, that is not how we live. Even people who retreat to their sacred suburban homes do not pretend to remain there forever, let alone keep out all strangers. We spend much of our lives on common territory, at work, shopping, or at play. We are gregarious and social. We are not gorillas, either. If we were, we would live in seraglios, each dominated by one giant middle-aged man, twice the weight of a woman, who would monopolize sexual access to all the women in the group and intimidate the other men. Sex would be rarer than saints’ days, even for the great man, who would have sex once a year, and would be all but nonexistent for the other males.9 If we were hairless chimpanzees, our society would still look fairly familiar in some ways. We would live in families, be very social, hierarchical, group-territorial, and aggressive toward other groups than those we belong to. In other words, we would be family-based, urban, class-conscious, nationalist, and belligerent, whi...

which we are. Adult males would spend more time trying to climb the political hierarchy than with their families. But when we turn to sex, things would begin to look very different. For a start, men would take no part at all in rearing the young, not even paying child support; there would be no marriage bonds at all. Most women would mate with most men, though the top male (the president, let us call him) would make sure he had droit du seigneur over the most fertile women. Sex would be an intermittent affair, indulged in to spectacular excess during the woman’s estrus but totally forgotten by her for years at a time when pregnant or rearing a young child. This estrus would be announced to everybody in sight by her pink and swollen rear end, which would prove irresistibly fascinating to every male who saw it. They would try to monopolize such females for weeks at a time, forcing them to go away on a “consortship” with them; they would not always succeed and would quickly lose interest when the swelling went down.

If we were pygmy chimps or bonobos, we would live in groups much like those of chimps, but there would be roving bands of dominant men who visited several groups of women. As a consequence, women would have to share the possibility of paternity still more widely, and female bonobos are positively nymphomaniac in their habits. They have sex at the slightest suggestion and in a great variety of ways (including oral and homosexual) and are sexually attractive to males for long periods. A young female bonobo who arrives at a tree where others of the species are feeding will first mate with each of the males in turn—including the adolescents—and only then get on with eating. Mating is not wholly indiscriminate, but it is very catholic. Whereas a female gorilla will mate about ten times for every baby that is born, a female chimp will mate five hundred to a thousand times and a bonobo up to three thousand times. A female bonobo is rarely harassed by a nearby male for mating with a more junior male, and mating is so frequent that it rarely leads to conception. Indeed, the whole anatomy of male aggression is reduced in bonobos: Males are no larger than females and spend less energy trying to rise in the male hierarchy than ordinary chimps.