Evolving Better Indicators

The late 1990s have brought an ever-deeper understanding of fitness indicators in sexual selection theory. Biologists such as Alan Grafen, Andrew Pomiankowski, Anders Moller, Rufus Johnstone, Locke Rowe, and David Houle have pushed the idea of condition-dependence deeper into the heart of sexual selection, relating it to the heritability of fitness arguments and the idea of mutation selection balance. Indicator theory is still developing very quickly, and no one has yet had the final word. However, I am especially intrigued by some ideas that Rowe and Houle developed about condition-dependence in a 1996 paper, because they seem most relevant to the human mind's evolution.

In Rowe and Houle's model all fitness indicators start out as ordinary traits. Each trait has certain costs. Higher-fitness individuals have larger energy budgets, so are better able to bear these costs. Initially, a trait may be favored by sexual choice because of some random runaway effect. But once it is favored, individuals with more extreme, costlier versions of the trait will spread their genes more successfully. This sexual selection increases average fitness in the population, because the trait acts as a weak fitness indicator. But here is the crucial point: the sexual selection also puts pressure on the trait to recruit a larger share of the individual's energy budget for itself. Individuals who allocate a low proportion of their fitness to the sexually favored trait will lose out to those who allocate a lot. As the sexually favored trait grabs a larger share of an organism's resources for itself, it becomes ever more dependent on the organism's total fitness budget. The trait turns from a cheap ordinary trait into a true handicap with large costs—in other words, its condition-dependence increases. And the increasing condition-dependence becomes an ever more valuable source of information about fitness. In this way, sexual selection has turned an ordinary trait into a really good fitness indicator.

The fitness indicator does not just recruit an increased share of an organism's energy: it also makes itself dependent on an increased proportion of an organism's genes. Rowe and Houle call this process "genic capture." The indicator captures a larger amount of information about an individual's genetic quality. Typically, this might work by a trait evolving a little bit more complexity, recruiting some of the genes that influence growth and development processes already evolved for other adaptations. This genic capture process makes the fitness indicator a window on an animal's genome. As the window grows wider through genie capture, the indicator lets an observer see a larger amount of all the genetic variation in fitness with the population, making it easier to choose mates for their good genes. Good fitness indicators give sexual choice a panoramic view of a potential mate's genetic quality.

It is not clear yet exactly how genic capture works, and this feature of Rowe and Houle's model needs further research. If it does work, and if the human brain's complexity evolved in part through genic capture, then there is an interesting implication. It would explain why so many unique human mental abilities look to some biologists like "spandrels," mere side-effects of other adaptations. Stephen Jay Gould has argued that most of our uniquely human capacities did not evolve for specific adaptive functions, but emerged as side-effects of already-existing brain circuits and learning abilities. Like most evolutionary psychologists, I find that argument weak for many reasons—for example, it fails to explain why other large-brained species such as dolphins, whales, and elephants did not invent paleontology or socialism.

However, Gould's argument may have this grain of truth: the human brain's distinctive power is its ability to advertise a lot of the computational abilities that were already latent in the brains of other great apes. This does not mean that music, art, and language came for free just because an ape brain tripled in size. But it might mean that when sexual selection seized upon the ape brain as a set of possible fitness indicators, the genic capture process recruited a lot of pre-existing brain circuitry into human courtship behavior. It made that brain circuitry more manifest in courtship behavior, more condition-dependent, and more subject to sexual choice. Our brains may look like a set of spandrels, but they look that way only because our mental fitness indicators are so efficient at advertising the brain's many abilities. (Of course, fitness indicators are different from spandrels because they evolved through sexual selection to have a specific courtship function, whereas spandrels, by definition, do not have any specific evolved function.)

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