The Handicap Principle Raises the Stakes

The mathematical difficulties with sexual selection were the last barrier to crumble. In 1975, Israeli biologist Amotz Zahavi turned to sexual selection theory and proposed a strange new idea that he called the "handicap principle." It revived Fisher's fitness-indicator idea in a counter-intuitive way. Zahavi suggested that the high costs of many sexual ornaments are what keep the ornaments reliable as indicators of fitness. Peacock tails require a lot of energy to grow, to preen, and to carry around. Unhealthy, unfit peacocks can't afford big, bright tails. The ornament's cost guarantees the ornamented individual's fitness, and this is why costly ornaments evolve.

Zahavi promoted his idea actively and ambitiously, suggesting that the handicap principle applies not only to sexual ornaments, but to warning coloration, threat displays, and many aspects of human culture. Within a year of Zahavi's first paper, Richard Dawkins realized the handicap principle was potentially important, and gave it a remarkably balanced appraisal in his influential 1976 bestseller The Selfish Gene. But to other biologists such as John Maynard Smith, Zahavi's principle seemed so confused that it could not possibly explain sexual ornamentation. Mathematically inclined biologists thought the handicap principle was an easy target, and attacked it vigorously.

The controversy over Zahavi's idea marked the true revival of sexual selection theory. Within ten years of his 1975 paper, more research was published on sexual selection than in the previous hundred years. Fisher's fitness-indicator idea was finally in play, its share value boosted by Zahavi's takeover bid. Soon Fisher's runaway process attracted more intellectual capital as well. In 1980 Peter O'Donald published Genetic Models of Sexual Selection, summarizing twenty years of thinking about the mathematics of sexual selection. This inspired a spate of new mathematical modeling. In the early 1980s Russell Lande and Mark Kirkpatrick showed that Fisher's runaway process could indeed work. The genes underlying female choice really could get swept up in a positive-feedback loop with the genes underlying male sexual ornaments. Species could even split apart into new species entirely as a result of diverging sexual preferences. Critics attacked these runaway models, leading to the kind of rapid revision and rethinking that marks the most productive epochs of science.

Evolutionary controversies attract experimental biologists. For most of the 20th century, the experimental techniques existed for testing Darwin's basic idea that females choose their mates for their ornamentation. Experimental psychology had developed sophisticated methods and statistical tests for investigating how people make choices. These could have easily been applied to animals. But the work was not done, because biologists thought that sexual selection had been dismissed by the leading theorists. Once the theorists revived the ideas of fitness indicators and runaway processes, the experimenters took a fresh look at mate choice. In species after species, females were seen to show preferences for one male over another, for beautiful ornaments over bedraggled ones, for a higher level of fitness over a lower. Female choice was observed by Linda Partridge in fruit flies, by Malte Andersson in widowbirds, and by Michael Ryan in Tungara frogs. David Buss even showed evidence of mate choice in humans. Wherever males had sexual ornaments, females seemed to show sexual choice, just as Darwin predicted.

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