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 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 macroparasites 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.

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