The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (19 page)

parasites determine what counts as fitness for the host. Because parasites are constantly evolving against all large-bodied

animals, the biological environment is constantly changing for all such animals. Genes that are good against today's parasites might not be so good tomorrow.

In Hamilton's view, the high-speed evolution of parasites is a

major force in moving the goal posts of fitness. No large-bodied species ever reaches the hypothetical equilibrium where every individual has high fitness, because parasites always evolve faster. Hamilton saw the implications for sexual selection. Mate choice should favor fitness indicators that are especially good at revealing how individuals resist parasites like viruses, bacteria, and intestinal and skin-burrowing worms. A large, bright peacock's tail proclaims, "I have conquered my parasites. If I had not, my tail would be small, drab, and diseased-looking. If you mate with me, your offspring will inherit my resistance." In an influential 1982 paper, W. D. Hamilton and Marlene Zuk proposed that many sexual ornaments evolved as fitness indicators that signal freedom from parasites. For example, an uakari monkey's bright red face may have evolved to reveal that it is not infected by blood parasites that would cause pale-faced anemia. As long as there are parasites in the world, the meaning of fitness will vary from one generation to the next. Large-bodied species are thus chasing an optimal fitness that remains always one
:
step ahead of them. That, in Hamilton's view, explains why fitness remains heritable in most species most of the time. Matt Ridley's book
The Red Queen
lucidly describes how arms races between parasites and hosts could maintain the incentives for mate choice.

Our ancestors had plenty of parasites and germs to worry about too: tapeworms, herpes, crab lice, common colds, malaria, stomach flu. Their communicable diseases were probably not as severe as those that arise in urban civilizations, because their population densities were much lower. They did not have plagues like medieval European cities. But every one of our hominid ancestors was probably exposed to dozens of species of fast-breeding, fast-evolving, energy-sapping organisms, from micro-parasites like viruses and bacteria to macro-parasites like head lice. The variable was not whether they had parasites, but how well they maintained their health and energy despite them. The sexual repulsion we may experience toward someone heavily infected with parasites may reflect more than a fear of contamination. It may be showing that Hamilton is right: that resisting parasites is a major part of

fitness for any large animal, and advertising that resistance is a major function of sexual ornaments.

Environments fluctuate across space as well as time. Our ancestors lived in small groups spread out over wide areas of Africa. The African continent is not one big flat savannah. Each area has slightly different weather, geology, vegetation, competitors, predators, and parasites. There are many micro-habitats. What is optimal in one area may not be optimal in another. Survival pressures vary across space, so each individual's fitness varies across space. As long as some of our ancestors migrated from one area to another in every generation, they would never evolve to the point where every individual in every area has maximum fitness relative to their local environment. Like variation in selection pressures over time, this variation in space helps explain why fitness remains heritable.

Environmental fluctuations across time and space are best at explaining why physical fitness and health remains heritable. But they are not so useful to us if our interest is in mental fitness indicators. Parasites put evolutionary pressure more on immune systems and bodies than on brains. Variations in climate from one part of Africa to another might maintain heritable variation in physical adaptations, but it is not clear why they should maintain variation in mental adaptations. To explain persistent variation in mental fitness, we need something more.

The Black Rain of Mutation

In science-fiction films and comic books, "mutations" are Faustian bargains that confer superhuman powers while damning their possessors to abnormal appearance and impaired sexual attractiveness. Spiderman was bitten by a "mutated" spider, and acquired wall-clinging powers but became alienated from his girlfriend. Monster Island apparently had high levels of mutagenic radiation, which is how Godzilla acquired his "atomic breath" that incinerates his enemies but keeps him single. This comic-book view of mutations is only half right. Mutations do undermine normal appearance and sexual

attractiveness, but they very rarely bring survival or fertility benefits.

Since the late 1980s, many biologists have been coming around to the view that fitness remains heritable mostly because new mutations are constantly arising and causing trouble. As we saw before, mutations almost always lower fitness. The more mutations an individual carries, the lower its expected fitness. To avoid mutational meltdown and extinction, selection had to be potent enough to eliminate those mutations at the same average rate at which they arose. (As we saw, Eyre-Walker and Keightley estimated that at least 1.6 harmful new mutations per individual every generation have been arising in our lineage for the last several million years.)

In most species for most of the time, almost all of the natural selection and sexual selection consists simply of removing harmful new mutations and maintaining the status quo. Selection is mostly conservative and stabilizing. Very rarely does selection favor a new mutant, because only rarely is a mutated gene better than the existing gene at helping an organism survive and reproduce. These rare occasions attract the biologist's attention because they are the times when evolution—genetic change in a species—can occur. But for the rest of the time, there is a tension between selection and mutation. Selection tends to maintain adaptations in their current effective form, while mutation tends to erode them into a chaotic, ineffectual mess.

The Brain as a Target for Mutation

For simple traits that depend on just a few genes, selection is pretty good at eliminating mutations. Each mutation is likely to cause such dramatic change that natural selection rapidly eliminates it But for very complex traits, like human brains, that grow through the interaction of many genes, mutations are harder for selection to eliminate. There are more genes vulnerable to mutation in the first place, and selection's effects get diluted across more genes. This decreases selection's power to eliminate mutations on any one gene. With mutation stronger and selection weaker, complex traits are less likely to be perched on the peak of perfection.

Genetic variation is more likely to be manifest in complex traits. This makes complex traits like the human brain better fitness indicators.

Imagine all the DNA in our 23 pairs of chromosomes laid end to end in a single strip. The DNA from a single human cell would be about six feet long, and contain about 80,000 genes. Imagine that the genes involved in growing a particular trait are lit up in bright green, and that each gene has a tiny chance of having a mutation that turns the green fight red. For a very simple trait like skin color, there might be only half a dozen lights sprinkled along the six-foot length of DNA. It is very unlikely that any of them would be red. For a moderately complex trait like the shape of the human face, there might be several hundred fights. It is likely that a few of them might be red. For a very complex organ like the human brain, there might be tens of thousands of fights. Our DNA would fight up like a Christmas tree. Although the proportion of red lights would still be very low, the absolute number would be much higher. The brain would give much better information about mutation load and fitness, because it gives mate choice a wider window on a larger sample of our DNA. (The larger the sample of genes, the more accurate the estimate of mutation load.) This is what biologists mean by the "mutational target size" of a trait: the proportion of the genome that is involved in a trait's development determines the proportion of all mutations that are visible in the trait.

At the moment, nobody knows exactly how many of our genes are involved in growing our brains. Geneticists sometimes estimate that about half of our genes are involved in brain development, and about a third might be active only in the brain. If this guess is about right (and we shall know within a decade or two whether it is), then the mutational target size of the human brain is about half the human genome. The brain probably has a larger mutational target size than any other organ. Of all the new mutations that mess up something during human development, half of them mess up something in the

human brain.

If mutations maintain most of the variation in fitness that we

see, then the organs with the largest mutational target sizes will make the best fitness indicators. The human brain should make a very good fitness indicator indeed. Its vulnerability to mutation is precisely why sexual choice mechanisms should evolve to pay attention to its performance.

In the rest of this book, I shall take the heritability of fitness for granted. The expectation that fitness should not be heritable was based on theoretical arguments developed in the 1930s. Those arguments are contradicted by the evidence. Wild populations show large amounts of genetic variation. Biologists routinely find individual differences in reproductive success in the wild, differences which are often genetically heritable. Fitness remains heritable in most species for most of the time. It seems likely that a lot of this continuing heritability is due to the continual rain of mutations. Some biologists even wonder how selection can possibly be strong enough to eliminate all these new mutations, and keep the species from falling apart. Fitness-eroding mutations are ubiquitous, and usually stick around for a fairly long time. There is always a tension between mutation and selection. And there are always fluctuations in fitness across time and space which keeps fitness heritable. These are just the facts of life. Mate choice evolves to deal with them.

How to Advertise Fitness

Fitness is like money in a secret Swiss bank account. You may know how much you have, but nobody else can find out directly. If they ask the bank, the bank will not tell them. If they ask you, you might lie. If they are willing to mate with you if your capital exceeds a certain figure, you may be especially tempted to lie. This is what makes mate choice difficult. The supposedly low heritability of fitness was one argument against the importance of fitness indicators in sexual selection. The other problem is the potentially low reliability of fitness indicators. An animal trying to find a high-fitness mate is in the position of an attractive gold digger seeking a millionaire. She has incentives to mate only with a male who offers high genetic or financial capital. But every male

has incentives to pretend to be richer than he is, to attract more mates. What is a poor girl to do?

Anita Loos's classic 1925 novel
Gentlemen Prefer Blondes
suggested one good strategy. The blonde protagonist Lorelei Lee forced her suitors to spend vast amounts of money on her, to show how much they really had. Her suitor Gus Eisman may have called himself "the Button King," but who can say whether his business is really profitable? Miss Lee was not the brightest button ever to baffle "Doctor Froyd" in Vienna, but she understood the principle of costly display. If a man can afford to dress as well as a peacock, he is probably not poor. If he gives you a very large diamond, he is likely to be rich. The more they can spend, the more they must have.

Lorelei was not the first to realize this, of course. Thorstein Veblen's
Theory of the Leisure Class
introduced the idea of "conspicuous consumption" in 1899. Veblen argued that in modern urban societies, where strangers come and go, people increasingly advertise their wealth by ornamenting themselves with costly luxuries. Where nobody knows anyone else's true wealth directly, conspicuous consumption is the only reliable signal of wealth. Sociologists and economists understood this logic immediately. Capitalist consumerism evolved in part as a set of wealth indicators.

It took biologists another three-quarters of a century to apply the same principle to sexual selection for fitness indicators. As we saw earlier, in 1975 Israeli biologist Amotz Zahavi argued that many animal signals—including sexual ornaments—evolved as advertisements of the animal's fitness. He suggested that the only reliable way to advertise one's

true fitness is to produce a signal that costs a lot of fitness. This explains why sexual ornaments are so often large, extravagant,

costly, and complicated. The peacock's tail is not just a cheap,

transient advertisement visible only to peahens. It is heavy, encumbering, hard to grow, hard to preen, and highly visible

to predators. Peacocks have to drag it around everywhere they go. Unfit peacocks might be able to grow large tails, but they would not be strong enough to carry them while finding food,

or fast enough to escape from predators. Only highly fit peacocks can afford very large tails.

Therefore, if a female sees a male sporting a very large tail, she can be confident that he has high fitness, and that his good genes

could be passed on to her offspring. Since very fit peacocks tend to

have fit sons and daughters that are more likely to survive and reproduce, peahens benefit by choosing big-tailed peacocks. Their

preferences for larger-than-average tails can spread. Conversely,

peahens that preferred shorter-than-average tails did not leave many descendants to inherit their misguided preference, because