The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (18 page)

As we shall see, many fitness indicators advertise fitness by revealing an animal's condition. They are "condition-dependent" —very sensitive to an animal's general health and well-being ("condition"), and very good at revealing differences in condition between animals. This sets up a chain of relationships that will prove absolutely central to many arguments in this book: genetic mutations influence fitness, fitness influences condition, condition influences the state of fitness indicators, fitness indicators influence mate choice, and mate choice influences evolution.

From the viewpoint of an animal making sexual choices, fitness indicators are just proxies for good genes. But the sexual selection that results from mate choice does not just influence the genes for fitness. It shapes the fitness indicators themselves. These fitness indicators combine evolutionary fitness with physical fitness and mental fitness. That is the key. By trying to get good genes for their offspring, our ancestors unwittingly endowed us with a whole repertoire of very unusual fitness indicators which have come to form an important component of the human mind.

This theory of fitness indicators suggests that much of human courtship consists of advertising our physical fitness and mental fitness to sexual prospects. Physical fitness may be revealed by

body shape, facial features, skin condition, energy level, athleticism, fighting ability, and dancing ability. Mental fitness may be revealed by creative story-telling, intelligent problem-solving,

skillful socializing, a good sense of humor, empathic kindness, a wide vocabulary, and so forth.

Clearly, many of the traits advertised during courtship also

bring non-genetic benefits to a sexual relationship. As David Buss and others have argued, strong mates offer protection, social intelligence brings social benefits, and kindness signals commitment. Fitness-indicator theory does not deny these other benefits, but points out that they are not the only reasons for mate choice. Good genes are important too—indeed, I shall argue that some human mate preferences have been misunderstood as seeking purely non-genetic benefits, when they have actually been focusing on indicators of genetically heritable fitness.

Ms. Fitness USA

Watch enough American cable television, and sooner or later you will find a pretty good analogy for almost any intellectual revolution in evolutionary biology. For me, the revolution in sexual selection ideas in the last twenty years of the 20th century is nicely symbolized by the eclipse of the "Miss America" beauty pageant by newer, more fitness-oriented contests such as "Ms. Fitness USA." In 1980, before the Ms. Fitness contests were invented, biologists thought that most sexual ornaments were arbitrary. Ornaments supposedly evolved through the runaway process or some other arbitrary process. In this picture, the peacock's tail did not reflect any aspect of a peacock's fitness, so was not a very rational basis for sexual choice. Yet a minority of biologists became skeptical about this view that most beauty is arbitrary. Similarly, feminists protested against Miss America pageants, upset by the apparent arbitrariness of the cultural norms of beauty used by the judges. The ability to totter around in high heels and swimsuit did not seem to reflect any very significant aspect of a woman's being.

In response to such criticisms, a promoter named Wally Boyko turned the tables on the beauty contest industry by inventing the "Ms. Fitness USA' contest in 1985. This contest explicitly favors women with the highest physical fitness, not just the greatest beauty, (Indeed, the Ms. Fitness World contest, founded in 1994, is held in conjunction with the annual Arnold Schwarzenegger Fitness Weekend.) The Ms. Fitness contests include three rounds:

an evening gown round (to judge beauty grooming, poise, and speaking ability), a swimsuit round (to judge muscle tone, body fat, and apparent fitness), and a fitness outfit round (a high-energy, 90 second display of strength, flexibility, endurance, and creativity, set to music). In the third round contestants usually do somersaults, splits, jumps, and one-handed pushups—in such a way as to make the difficult appear effortless. The whole aesthetic shifted from Miss America's soft-bodied, giggly display of femininity to a hard-boiled, active display of health. The judging criteria no longer looked quite so culturally arbitrary. Miss America contestants could improve their chances by dieting, getting silicone breast implants, dyeing their hair, and skillfully applying makeup. But Ms. Fitness contestants, such as the currently top-ranked Monica Brant, can win only by training like professional athletes with aerobics, weightlifting, stretching, sports, and healthy eating. Their physical fitness would be manifest in any culture at any point in history, regardless of minor cultural variations in the norms of beauty.

Some evolutionary biologists responded to the idea of arbitrary sexual ornaments in the same way that Boyko's "International Fitness Sanctioning Body" responded to the Miss America pageant. They rethought the judging criteria. Why should animals choose mates for arbitrary traits, when they can choose mates for traits that reveal their condition and fitness? Certainly, the runaway process can happen in principle, but maybe it is not so important. Maybe it creates transient sexual fashions that come and go, but it does not explain the sexual ornaments that stick around generation after generation. The ornaments that stick around should reveal some information about fitness, about good genes. Most sexual ornaments should be. fitness indicators. The debate over this issue has an illuminating history.

Sexual Choice for Fitness

Sir Ronald Fisher first emphasized that animals could choose their sexual partners for high fitness by favoring certain kinds of sexual display As we saw in Chapter 2, his 1915 paper introduced

this idea of fitness indicators. But his 1930 book barely mentioned them, and devoted more space to the idea of runaway. When runaway sank into the quicksand of scientific skepticism, Fisher's even more obscure fitness-indicator idea sank with it. The idea waited thirty-six years for rescue. George Williams revived it in his influential classic,
Adaptation and Natural Selection.
Several decades on, his description of sexual choice for fitness remains unsurpassed.

It is to the female's advantage to be able to pick the most fit male available for fathering her brood. Unusually fit fathers tend to have unusually fit offspring. One of the functions of courtship would be the advertisement, by a male, of how fit he is. A male whose general health and nutrition enables him to indulge in full development of secondary sexual characters, especially courtship behavior, is likely to be reasonably fit genetically. Other important signs of fitness would be the ability to occupy a choice nesting site and a large territory, and the power to defeat or intimidate other males. In submitting only to a male with such signs of fitness a female would probably be aiding the survival of her own genes.

Since Williams's book became required reading for the new generation of biologists in the 1970s, the indicator idea started to catch on. It received another publicity boost when Richard Dawkins gave it a sympathetic exposition in his 1976 bestseller
The Selfish Gene.

By the mid-1980s, biologists were seriously assessing the fitness indicator idea. The basic intuition seemed sound, but there were two technical problems so difficult that they took another ten years to resolve. One concerned the supposedly low heritability of fitness, and the other concerned the supposedly low reliability of fitness indicators. To understand how the human mind may have evolved as a set of fitness indicators, we have to understand these problems and their solution.

Why Is Fitness Still Heritable?

Fitness indicators are pointless unless individuals vary in their fitness. If we take fitness to mean the possession of good genes that can be inherited by offspring, then it seems hard to understand how evolution can allow any variation in fitness to remain. Selection is supposed to maximize fitness, driving it ever upwards. It is not supposed to permit fitness variation to persist in species just to provide an incentive for sexual choice.

To follow this argument, it is crucial to understand the difference between "inherited" and "heritable." All traits that depend on genes are inherited. But the term "heritable" is much more restrictive: it refers to the proportion of individual differences in a trait that are due to genetic differences between individuals. The concept of heritability applies only to traits that differ between individuals. If a trait exists in precisely the same form across all individuals, it may be inherited, but it cannot be heritable. It should come as no surprise that fitness is inherited, because fitness clearly depends on genes. The surprising thing is that fitness still varies between individuals in most species, and that the variation often seems to depend on genetic differences.

To see why the heritability of fitness is surprising, consider what happens in species that mate in large aggregations called "leks."
Lek

is Swedish for a playful game or party. Some birds like sage grouse congregate in these leks to choose their sexual partners. The males display as vigorously as they can, dancing, strutting, and cooing. The females wander around inspecting them, remembering them, and coming back to copulate with their favorite after they have seen enough. Leks resemble music festivals where mostly male rock bands compete to attract female groupies. In species that lek, the males usually contribute nothing but their genes. The females may never see them again, and raise their offspring as single mothers. Leks create a situation where sexual selection is extremely strong. The most attractive male sage grouse may mate with thirty females in one morning; average males usually mate with none. It is a winner-takes-all contest, and it should spread the most attractive male's genes very quickly through the population.

If the lekking females choose males for good genes generation

after generation, all the males should end up being perfectly fit
and identically attractive. Males of lower apparent fitness will

have died unmated, their mutations having died with them. After

a few generations, all the mutations that show up in fitness
indicators should be gone. Only the good genes should be left. If

every male has the same high fitness, there is no variation for fitness indicators to reveal. If there is no variation in genetic quality and if genes are all that females get, there is no longer any incentive for females to be choosy about their mates. Instead of

spending time and energy wandering around the lek admiring male displays, the females might as well pick randomly. The

reasons for mate choice should disappear as the heritable variation in fitness disappears. According to this evolutionary logic, leks should be temporary phenomena. Yet leks still exist. Presumably, sage grouse have been gathering in leks for thousands of generations. Biologists call this the "lek paradox."

The lek paradox is the most extreme case of a general problem with the heritability of fitness. Any form of sexual selection for fitness indicators should even out genetic variation in fitness. If

female choice in our species favored tall males, all males should be
equally tall. If male choice favored large breasts, all females

should be equally large-breasted. If both sexes favored high intelligence and beautiful faces, all humans should be equally bright and beautiful. Yet we are not. The differences remain, and they are still genetically heritable. So why would selection allow such differences to persist?

Once biologists agreed that the lek paradox was a problem, the hunt was on for evolutionary forces that could maintain variation

in fitness. Two major candidates emerged. One emphasized that fitness is environment-relative; the other emphasized the ubiquity of harmful mutations that erode fitness.

Time, Space, and Fitness

We saw earlier that fitness is relative to a particular environment.
Environment-relative fitness implies that if a population's

environment fluctuates over time or space, then the meaning of fitness will fluctuate too. If the meaning of fitness fluctuates, and the population will not stabilize on any one set of genes that will be good in every environment, then environmental variation could maintain genetic variation.

On evolutionary time-scales, physical environments are changing all the time. The climate gets colder or hotter. Rivers shift course. Mountains rise and fall. Meteorites strike. But such physical changes are usually too slow or rare to maintain variation in fitness. Species adapt fairly quickly to changes in their physical environments, reaching a new equilibrium where all individuals should have optimal traits and high fitness.

More important is the biological environment: the other species that are evolving alongside a given population. Predators may get faster or smarter. New parasites may evolve. Viruses mutate at great speed. In the early 1980s, W. D. Hamilton and John Tooby independently developed the idea that variation in fitness could be maintained over very long periods by populations evolving interactively with their parasites. Every animal large enough for us to see has parasites. Because the parasites are smaller than their hosts, they can grow faster and breed faster—their generation time is shorter. The human generation time is about twenty-five years. For bacteria it can be as little as twenty minutes. For every generation that hosts can evolve to have resistance against parasites, parasites can evolve many generations to exploit their hosts, so parasites can adapt much faster to hosts than vice versa. From a parasite's viewpoint, the host's body is the environment to which it adapts. The host's body determines what counts as fitness for the parasite. But the converse is true as well. From the host's viewpoint, parasites are a major part of the biological environment. The capabilities of