29 September 1998
Good Genes Are In The Eye Of The Beholder

We all know a "good-looker" when we see one. But why do some traits, "say, large eyes and broad shoulders" seem attractive, as opposed to nose hair and a paunch? According to University of Texas zoologist Michael J. Ryan, the answer may be that mate choice is colored by perceptual biases hard-wired into an animal's sensory system for reasons other than sexual thrill. Beauty, that is, may be literally in the eye of the beholder.

Ryan's article is part of a special section on the evolution of sex that appears in the 25 September issue of Science. He discusses a growing body of evidence in support of the "preexisting preferences" or "sensory exploitation" theory of sexual selection. This model emphasizes that animals choose mates using sensory systems that primarily have been shaped to meet the daily demands of survival, foraging for food, or example, or avoiding predators. According to this argument, animals looking for potential mates do so with a built-in "receiver bias" toward traits that may not have anything to do with their mate's genetic fitness.

For example, water mites feed on tiny organisms called copepods, which the mites locate by sensing their prey's water-borne vibrations. Males of at least one species of water mite mimic copepod vibrations as part of their mating display. As it turns out, the mites' smooth moves do indeed boost their chances of attracting a mate. Another example can be found among moths that have evolved the ability to detect the ultrasonic echolocation calls of bats, a key predator. A subset of this group, more recently evolved, can also produce calls in the bats' own frequency, essentially jamming their predators' radar. Even further along the family tree are moths that have adapted this sensory channel for communication between the sexes, males and females who woo each other in ultrasonic displays of affection.

To Ryan and others, the theory's main strength is its simple logic. "Any sensory system is going to be more responsive to some stimuli than to others," says Ryan. "If males have a variety of options by which to signal their sexual interest, females will favor those who use signals they are already keyed into." Supporters of the theory have yet to convincingly demonstrate its applicability among humans. But Ryan points to studies that have shown how symmetrical body features, chiefly in the face, tend to be seen as more beautiful than asymmetrical features. "The traditional explanation," says Ryan, "is that if you have a genetic disorder, you may not develop correctly," so the asymmetry sets off a kind of warning signal. "But another possibility is that human perception is simply better at responding to symmetrical cues." Humans learn symmetrical patterns more quickly than asymmetrical ones, for example, and harmonic rather than discordant music strikes us as more pleasing in part, studies suggest, because of the way the inner ear is structured.

Ryan says that the sensory exploitation model challenges, but does not supplant traditional theories of sexual selection of the last 30 years. In general, the theory of natural selection says that if a trait increases an animal's reproductive success, defined in terms of how many viable offspring it produces, then that trait should be favored in the competition for mates. Well-documented male traits favored by females include large size (to better protect her and her offspring) and a bigger territory (to provide more food). But there are confounding exceptions: many females have strong preferences for male traits, red feathers, say, that don't seem to relate to their offspring's number or well-being.

One of the most common explanations for this has been the "good genes" model, in which red feathers, for example, might be coincidentally determined by genes that also confer a trait that natural selection would favor anyway, such as resistance to parasites. In this case, a female's predilection for red feathers is a kind of genetic hitchhiker. A second explanation comes from the "runaway" model of sexual selection, in which (to use the same example) males that sport red feathers mate with females genetically predisposed toward red feathers, thus passing along not only the trait but the preference for the trait, and thus amplifying its frequency in the population.

In both of these models, the female preference genes become genetically correlated with the male trait genes. But in the sensory exploitation model, these two genetic events are uncoupled, evolutionarily speaking, the preference forms before it is ever turned to sexual advantage.

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