The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (10 page)

In the space of a few pages, Huxley managed to confuse sexual selection with natural selection, and failed to distinguish natural selection due to competition between individuals and natural selection due to competition between species. He argued that sexual ornaments are immoral because they undermine the good of the species, and if they are immoral, they must not really be sexual ornaments after all, but threat displays, or signals to prevent breeding between species, or perhaps something else. More damage was done by Huxley's popular 1942 textbook
Evolution: The Modern Synthesis,
which cast sexual selection

in a marginal, even criminal role in evolution. After mentioning that biologists used to presume that bright colors displayed in courtship were products of sexual selection, Huxley observed that "It was rather the opposite of the presumption of British law that a prisoner is to be regarded as innocent until definite proof of guilt is adduced." Huxley apparently despised sexual selection because he thought it was bad for species, and he thought evolution should be for the good of species. He defined evolutionary progress as "improvement in efficiency of living" and "increased control over and independence of the environment." Since sexual ornaments had high costs that undermined survival chances and did not help an animal cope with the hostile environment, Huxley viewed them as anti-progressive, degenerate indulgences. His contempt for sexual selection combined Puritan prudery and socialist idealism with anxieties about the supposed degeneration of North European races—an ideological cocktail popular among biologists at the time.

After Huxley, the cause of sexual selection foundered again. The years from 1930 to about 1980 saw it exiled to the hinterlands of biology. Unlike the turn-of-the-century exile, this later rejection was not due to a general neglect of evolutionary theory On the contrary, the Modern Synthesis of the 1930s and 1940s revived Darwinian selection ideas by showing how they could be reconciled with Mendelian genetics. In many ways, this was a golden age for evolutionary theory. Biologists now had proofs and mathematical insights, just as physicists did. Theoretical population genetics was thriving. Darwin was every biologist's hero again— but he was now regarded as a fallible hero, prone to endearing blunders like the hypothesis that female animals select their sexual partners by aesthetic criteria.

Science Troubled by Mate Choice

Biologists could have revived sexual selection in the 1930s by building upon Fisher's work. If they had, the benefits to the behavioral sciences would have been enormous. Anthropologists could have studied real mate choice in primitive cultures instead

of concentrating on incest taboos and inter-tribal marriages. Psychotherapists might have rejected Freud's Lamarckian theories about our ancestors inheriting acquired memories of sexually competitive patricide and incest. Psychologists might have overcome the Behaviorist obsession with maze learning by rats, and found a more fruitful way to study human nature. The pioneering sex researchers Alfred Kinsey, William Masters, and Virginia Johnson could have interpreted their questionnaire studies from a richer evolutionary perspective. Archeologists interested in human evolution might not have been so concerned with hunting and warfare, and so baffled by cave paintings and Venus statuettes. Yet none of this happened.

Sexual selection's modern neglect owed more to scientific problems than to ideological biases. One problem is that sexual selection is hard to model mathematically. When a species is adapting to a fixed environment through natural selection, it is possible to predict how a given gene with a given survival effect will spread through a population. With sexual selection, however, the pressures come from other members of the species, which are themselves evolving. It is hard to know where to begin an analysis of sexual selection, because the feedback loops between sexual preferences and sexual ornaments make evolution hard to model and hard to predict. Only in the 1980s did some brilliant mathematical biologists finally start to develop workable models of sexual selection.

Also, the biologists of the Modern Synthesis were consumed by the problem of speciation—how a lineage splits into two distinct species that no longer interbreed. Sexual selection was seen as a possible explanation for speciation, rather than as an explanation for ornamentation. Mate preferences were viewed as nothing more than a way of making sure that individuals mate only with

members of their own species. The boundaries of the species were defined by mate preferences, but these preferences were not

viewed as ranking individual attractiveness within the species. For many biologists, such as Ernst Mayr, this led to the assumption that most sexual ornaments were nothing more than marks

showing what species an animal is. Following Wallace, they were considered to be "species recognition signals."

Sexual selection also suffered at the hands of the early 20th-century doctrines of behaviorism in psychology and reductionism in the sciences generally. These warned against attributing any mental capacities to animals, and this made biologists feel uncomfortable talking about the evolution of female choice mechanisms. Even animal behavior researchers such as Konrad Lorenz and Niko Tinbergen viewed copulation as a stereotyped behavior that is "released" by a few simple stimuli. They did not view mate choice as a complex strategic decision with high stakes. Behaviorist psychologists were not willing to credit even humans with free will or the capacity for choice, so it seemed unscientific to talk about "mate choice" in animals rather than "sexual stimuli." The mid-20th century was the era of B. F. Skinner's manifesto
Science and Human Behavior,
in which people were portrayed as robots driven by conditioned associations. Only with the rise of cognitive psychology in the 1970s did it once again become intellectually respectable in psychology to talk about judgment and decisionmaking in humans or animals. By then, most psychologists had forgotten all about Darwin. When they thought of sex, they thought of Freud and his theories of subconscious drives and neurotic complexes. Human sexuality, with its alleged existential intricacies, had been set apart from animal sexuality, with its supposedly stereotyped copulation reflexes. A science of mate choice applicable to both animals and humans seemed an absurd conceit.

Moreover, many evolutionary biologists before the 1970s had a very limited concept of adaptation. To them, evolution basically solved problems of survival posed by the external environment. Evolution was supposed to be about the survival of the fittest and the good of the species. Sexual selection was neither progressive nor respectable. Certainly, runaway sexual selection was a theoretical possibility, but bizarre ornaments were not considered to be real adaptations. They impaired individual survival and predisposed species to extinction. Mere ornamentation was not a proper role for a genuine adaptation.

This narrow definition of adaptation was perhaps reinforced by 20th-century aesthetics, which held conspicuous, costly ornamentation in low regard. The modernist reaction against Victorian ornamentation may have spilled over into a reaction against Darwin's sexual selection theory. The Modern Synthesis coincided with the peak of an austere, modernist machine aesthetic. In the 1920s Walter Gropius and other theorists of the Bauhaus movement in Germany had argued that, in a socialist Utopia, working people would not waste time and energy hand-decorating objects for purchase by the rich, merely so the rich could show how much wasteful ornamentation they could afford. Form should follow function. Ornament was viewed as morally decadent and politically reactionary, while simplicity and efficiency were considered progressive. This anti-ornament aesthetic seems to have spilled over from culture into nature, leading 1930s biologists to express their contempt for sexual selection's baroque excesses. For example, the socialist biologist J. B. S. Haldane suggested that with sexual selection, "the results may be biologically advantageous for the individual, but ultimately disastrous for the species." In one of his 1938 papers, Julian Huxley declared sexual selection a selfish process because it may "favour the evolution of characters which are useless or even deleterious to the species as a whole." Similar views were held by leading biologists such as Konrad Lorenz, George Simpson, and Ernst Mayr right through to the 1960s. They believed that evolved adaptations, like modernist design, should serve their economic purposes simply, efficiently, and plainly. Sexual ornamentation served no legitimate species-benefiting purpose, so must be ignored or derogated.

Darwin's sexual selection theory was kept in exile by these five factors: mathematical difficulties, an overemphasis on ornaments as species-recognition markers, a mechanistic view of animal psychology, a narrow definition of biological adaptation, and a modernist machine aesthetic. In other words, Darwin's favorite idea was not ignored because there was evidence against it. On the contrary, the mountain of evidence presented in
The Descent of

Man
was never seriously challenged. Sexual selection was ignored because biology was not ready—ideologically, conceptually or methodologically—to deal with it.

A Second Chance

Sometimes an idea needs to be published twice so that a second generation can judge whether it makes sense. In 1958, almost three decades after the first edition, Fisher produced a second edition of
The Genetical Theory of Natural Selection.
This time it took root in the minds of a new, more mathematically skilled generation of young biologists such as John Maynard Smith and Peter O'Donald. They saw what Fisher was getting at: one could think seriously about the evolutionary origins of sexual preferences, and their evolutionary effects. Maynard Smith set about studying the courtship dances of fruit flies. He found that highly inbred, unfit males could not keep up with healthy females, so would be rejected as mates. The females seemed to be choosing for male fitness as evidenced by dancing ability. Maynard Smith also spent the next several decades wondering why sex evolved in the first place. O'Donald explored the mathematics of sexual selection throughout the 1960s and 1970s, trying to develop proofs of Fisher's intuitions.

A rivulet of interest in sexual selection started to flow through the minds of leading biologists. In his widely read
Adaptation and Natural Selection
of 1966, the young theorist George Williams used Fisher's sexual selection ideas to interrogate the concept of an evolved adaptation. Sexual selection was found not guilty of debauching evolution and making species degenerate. Williams put ornaments on an equal footing with other adaptations, giving

sexual selection a status equal to that of selection for survival. In
expanding and clarifying the definition of biological adaptation,

Williams helped to overcome the machine aesthetic of the Modern Synthesis, and its emphasis on ornaments as species-recognition markers.

Finally, the reductionistic behaviorism of previous decades gave way to cognitive psychology in the 1970s, Once again it became

respectable to talk about the mind. Cognition, choice, judgment, decsion-making, and planning became part of psychology once again. This laid the foundation for the modern understanding of mate choice in general.

An increased acceptance of the role of female choice may have also been due to social trends. The sexual revolution of the 1960s and the rise of feminism led to more women studying and contributing to biology, and to a new appreciation of female choice in human social, sexual, and political life. Married male biologists could no longer take for granted the obedient support of their wives. They faced a new world in which women made choices more consciously and took more control of their lives. Although evolutionary theory was still extremely male-dominated, individual males were feeling more pressure from female choice. Female biologists doing field-work also drew more attention to female choice among the animals they studied. This was especially important in primatology, as women such as Jane Goodall, Dian Fossey, Sarah Hrdy, Jeanne Altmann, Alison Jolly, and Barbara Smuts explored female social and sexual strategies. Dismissing the idea that female choice could influence the direction of evolution began to look both sexist and unscientific. By drawing attention to the evolution of social and sexual behavior in animals, the sociobiology of the 1970s did for the study of animal sexuality what feminism did for the study of human sexuality. It empowered thinkers to ask "Why does sex work like this, instead of some other way?"

The Handicap Principle Raises the Stakes

The mathematical difficulties with sexual selection were the last barrier to crumble. In 1975, Israeli biologist Amotz Zahavi turned to sexual selection theory and proposed a strange new idea that he called the "handicap principle." It revived Fisher's fitness-indicator idea in a counter-intuitive way. Zahavi suggested that the high costs of many sexual ornaments are what keep the ornaments reliable as indicators of fitness. Peacock tails require a lot of energy to grow, to preen, and to carry around. Unhealthy, unfit peacocks

can't afford big, bright tails. The ornament's cost guarantees the ornamented individual's fitness, and this is why costly ornaments

evolve.

Zahavi promoted his idea actively and ambitiously, suggesting that the handicap principle applies not only to sexual ornaments, but to warning coloration, threat displays, and many aspects of human culture. Within a year of Zahavi's first paper, Richard Dawkins realized the handicap principle was potentially important, and gave it a remarkably balanced appraisal in his influential 1976 bestseller
The Selfish Gene.
But to other biologists such as John Maynard Smith, Zahavi's principle seemed so confused that it could not possibly explain sexual ornamentation. Mathematically inclined biologists thought the handicap principle was an easy target, and attacked it vigorously.