The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (31 page)

contribute the most genes to future generations?

At first glance, it looks as if each pair should contribute the same number of genes, since they have the same number of babies. But we already know that mated pairs differ in their heritable fitness. That is what they were being choosy about when they were sorting themselves into pairs. So, the babies of higher-fitness couples will inherit higher-fitness genes. By definition, higher fitness leads to a better chance of surviving to sexual maturity. The offspring of male number one and female number one may have a very high chance of surviving. The offspring of the lowest-fitness male and the lowest-fitness female may only have a very low chance of surviving. By the time the babies' generation grows up, there will be more surviving offspring of high-fitness parents than of low-fitness parents. In fact, the babies' generation will have a higher average fitness than their parents' generation did.

Evolution just happened. But did sexual selection happen? Things get a little complicated here, because there are two effects at work.

Fitness Spreading

One effect of fitness matching is to increase the variation in fitness in the next generation. In fact, it creates the widest possible fitness differences between babies. Fitness matching by parents leads to fitness spreading among offspring. Consider the extremes of the fitness spread. The only way to produce a baby of the highest possible fitness given the parents available, would have been for the highest-fitness male to mate with the highest-fitness female. That is exactly what happened, through the mating market. And the only way to produce a baby of the lowest possible fitness would have been for the lowest-fitness male to mate with the lowest-fitness female. Again, that is exactly what happened. Fitness matching does not just increase the variation in fitness a little bit. It increases that variation as much as any mate choice process could, with or without monogamy.

The fitness-spreading effect is important because it creates a very tight link between sexual selection and natural selection. The

power of natural selection is proportional to the fitness spread that is available in a population. Bigger fitness differences between babies lead to faster evolution. By creating the largest possible fitness spread, fitness matching gives natural selection the greatest diversity of raw material to work on. Psychologists Aaron and Steven Sloman emphasized the importance of this effect in an important paper they published in 1988.

From a genetic point of view, fitness matching concentrates harmful mutations from low-fitness parents in their low-fitness babies. When those babies die, they take a lot of harmful mutations with them. Fitness matching also concentrates helpful mutations (which are much rarer) in high-fitness babies. When those babies thrive at the expense of lower-fitness competitors, the helpful mutations increase their share of the gene pool. This is a heartlessly unromantic view of sexual selection's effects, but evolution is heartless.

From Fitness Matching to Fitness Indicators

The fitness-spreading effect is interesting, but it doesn't take us very far in understanding the evolution of the human mind. To do that, we have to ask how fitness matching affects the fitness indicators themselves. What follows is admittedly a subtle and speculative argument, but one I think is critical to understanding how sexual selection shaped the human mind.

In the above description of fitness matching, it was assumed that individuals could perceive each other's fitness with perfect accuracy. But it is not that simple. Our hominid ancestors did not have portable DNA sequencing laboratories to measure the mutation load of every potential mate. They had to make do with fitness indicators such as sexual ornaments and courtship displays. By definition, fitness indicators have some correlation with fitness, but it is never a perfect correlation. The handicap principle keeps indicators relatively honest, but it cannot keep them perfectly honest, so there will always be a discrepancy between true fitness and apparent fitness. The evolution of fitness indicators is driven by this discrepancy.

Consider the mating market from female number two's perspective. She is the second-highest-fitness female hominid in the tribe. She would love to get together with male number one and have his higher-fitness babies, who will survive better and attract better mates. But female number one stands in the way, seducing male number one with her high-fitness charms. (For the moment, we are still assuming strict monogamy and no adultery, so female number two cannot just have an affair with male number one.)

What can female number two do? She cannot raise her true heritable fitness, because on the African savanna she has no access to retroviral germ-line genetic engineering. But she could produce an appearance of higher fitness by allocating more energy to her fitness indicators. If she had a mutation that increased the quality of one of her fitness indicators, even at the expense of her other adaptations, she might look better than female number one. In fact, she would become female number one, in terms of apparent fitness. She could attract male number one, and produce high-fitness babies. She might produce the same number of babies she would have had with male number two, but now her babies have higher fitness, and are more likely to survive. Even though, according to our assumption, she has produced no more children than any other woman, she will produce more grandchildren who will carry her mutation. Her granddaughters and grandsons would inherit her propensity to allocate more energy to their sexual ornaments and courtship displays. If those displays included evolutionary novelties such as art, music, and language, sexual selection would improve their performance. This is how fitness matching can push fitness indicators to evolve. This is how sexual choice can drive sexual selection, even under strict monogamy.

Now, step back from female number two's predicament and consider the general point. Here we have a hominid tribe that would make Puritans look sinful. They are perfectly monogamous, they have no adultery, and they all have exactly the same number of children. Yet even here, under the most impossible-looking

conditions, sexual selection still works. It still favors more extreme costlier, more impressive fitness indicators such as sexual ornaments and courtship displays. Sexual selection still works on fitness indicators because fitness still means something: some babies still survive better than others because they have higher fitness. Since fitness matching pays evolutionary dividends to those who have high apparent fitness, there are incentives for displaying the most extreme fitness indicators you can afford. The handicap principle will keep the fitness indicators within reasonably honest limits. It can keep low-fitness pretenders from displaying very high apparent fitness, but it cannot keep high-fitness competitors from escalating their sexual arms race. As long as there is some natural selection going on, fitness matching alone should suffice to drive sexual selection for indicators.

This fitness matching theory may sound speculative, but it is just a variation of Darwin's theory of sexual selection in monogamous birds. Darwin faced the same problem: how to explain sexual ornaments that are equally extreme in both sexes in species that form monogamous pairs. He proposed a fitness matching process that relied on the fittest female birds arriving first at the best nesting sites in each breeding season, mating with the fittest male birds, and producing higher-fitness offspring who are more likely to survive. Sexual selection theorists such as Mark Kirkpatrick have shown that Darwin's model can work as long as fitness remains heritable and sexual choice favors reliable fitness indicators. If fitness matching' can explain ornamentation in monogamous birds, perhaps it can explain courtship abilities in relatively monogamous apes like us.

Sexual Selection Without Sex Differences

The pure fitness matching process would not produce any sex differences. All else being equal, males and females would evolve fitness indicators to precisely the same degree. This is because under strict monogamy they would have equal incentives for displaying their fitness and for selecting mates based on fitness. Fitness matching tends to promote sexual equality in the

indicators it favors. This is one reason why it has the potential to be so important for human evolution. The sexual egalitarianism makes it an attractive model for explaining traits that are ornamental, costly, and sexually attractive, yet do not show the sex differences predicted by traditional models of sexual selection.

How many traits have these features predicted by the fitness matching model? Many traits in many species look ornamental and costly, show minimal sex differences, and probably influence mate choice. However, biologists since the 1930s have usually called such traits "species recognition markers." They assumed, following the tradition of equating sexual selection with a mechanism for producing sex differences, that such traits simply advertise one's species rather than one's fitness. For the last fifty years, whenever a biologist noticed something that exists in both sexes, which would have been called a sexual ornament if it existed only in males, it was called a species recognition marker. If the marker was displayed vigorously by both sexes during mutual courtship, biologists would say that the animals are performing a "pair-bonding ritual." This terminology obscured the fact that one individual would often walk away from the ritual, unimpressed by his or her would-be partner. The evidence for mutual choice was there, but most biologists neglected Darwin's theory of sexual selection in monogamous species.

Birds offer many examples. If, among emus, only males had bright blue bare patches on their cheeks and necks, biologists would probably have called the patches sexual ornaments. But since females have them too, they are usually relegated to the status of species recognition markers. Likewise for the dramatic yellow eyebrow-tufts sprouting from both male and female rockhopper penguins. And the 11-foot wingspans of both male and female wandering albatrosses, which are displayed during mutual courtship by stretching the black tips of the white wings as far apart as possible for the inspection of the opposite sex. All, we are told, for mere species recognition. This viewpoint implies that the hours of mutual conversation during human courtship are likewise nothing more than a way for us to tell that the other

individual is a human rather than a chimpanzee. Amotz Zahavi has mocked the species recognition idea as attributing a very high degree of stupidity and very poor mate choice to animals. I agree with his view. These same animals show good discrimination ability when it comes to food and predators, so why should they need such dramatic markers to tell whether a potential mate is of their own species? Fitness matching, a form of mutual mate choice based on fitness indicators, may be a more sensible explanation for most sexual ornaments that show very small sex differences.

In Search of a Few Good Hominids

The question remains of how our ancestors actually made their sexual choices. Perhaps during large tribal gatherings, they formed huge mixed-sex aggregations like sage grouse, where individuals could weigh up hundreds of prospects. This would have made mutual choice extremely easy. However, such Pleistocene singles bars were probably rare.

Much more likely, individuals would encounter a slow trickle of new sexual possibilities, one at a time. The search for a good sexual partner was sequential and opportunistic. Success would depend on one's ability to manipulate which band one joins, and who joins one's band. (A band is the small group of individuals with whom a hominid would forage and spend most nights; clans and tribes are larger sets.) New individuals might join an existing band. The band may encounter other bands at water sources. Individuals might leave their band, looking for new groups that offer more sexual opportunities.

Contact between bands may have been tense and brief, with the threat of violent confrontation balanced against the possible benefits of trade, gossip, and the exchange of sexual partners. Selection would have favored a capacity for very fast decisions about which individuals were attractive enough to pursue. These snap judgments could have been based on information like physical appearance, bodily ornamentation, apparent social status, and public display behavior (such as sports, music, and story-telling). Our ability to judge the physical attractiveness of a

human face in a seventh of a second is a legacy of selection for such fast decision-making. Since males would usually have been more motivated to pursue sexual prospects, they would have been more active in this initial phase of searching through bands, looking for attractive potential mates, and trying to switch bands to court good possibilities.

Once mutually attracted individuals arranged to be in the same band, they could split off into temporary courting pairs. Their interaction would resemble the consortships formed by chimpanzee pairs who go off into the bush together for several days. During this most intense phase of courtship, hominids could get to know each other much better, bringing into play all of the psychological levels of courtship discussed in this book. Before language evolved, they would have groomed each other, played, canoodled, shared food, and done all the usual primate things to form social relationships. After language, they would have talked endlessly. During these consortships, the male would usually have been trying to copulate because he would have little to lose from a short-term sexual relationship. If he succeeded, he might grow bored and go away, or he might stay around.

Male and female mate choice waxed and waned in importance at different stages of courtship. Basically, males would scan for physically attractive females and pursue them, trying to establish consortships. This would be a major stage of male mate choice, subjecting females to intense sexual selection for immediate physical appeal. Once a male tried to approach a female to form a consortship, the first stage of female mate choice would be triggered. On the basis of his appearance and behavior, she would reject him (usually) or provisionally agree to continue interacting. This would impose sexual selection on males to create a positive impression during the first few minutes of interaction. After several hours or days of consorting, the female would decide whether to have sex. If she agreed, they would probably copulate frequently for several days or weeks. At that stage, male mate choice would once again reassert itself: will he stay with this female, or grow bored and abandon her in search of someone who