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It took biologists about fifteen years to accept Zahavi's handicap principle. Much of that time was spent clarifying what kinds of handicaps could evolve and what kinds could not. Since handicaps are basically fitness indicators, the debate over handicaps helped lay the foundation for the modern theory of fitness indicators.

A handicap cannot usually evolve if it commits all the males to producing a costly signal regardless of their true fitness. This would be like all men buying a five-carat diamond engagement ring regardless of their salaries. Such a fixed-cost strategy is not sensible for anybody—all the poor men would go bankrupt and starve before their wedding day, while the super-rich men would be indistinguishable from the moderately rich men. The same problems explain why we rarely see sexual ornaments in nature that are produced by all males to an equal degree. A handicap gene that committed all low-fitness males to produce a very costly sexual ornament would simply kill them all. The handicap would help females to recognize high-fitness males, but the females could not tell which of the high-fitness males was best. Mathematical models and simulations suggest that this sort of fixed-cost handicap cannot evolve under reasonable conditions.

Handicaps can evolve much more easily if they are a little more sensitive to an animal's fitness level. A gene that says "spend 50 percent of your disposable energy on courtship dancing" could easily spread through a population if females appreciate dancing.

It would be just like the cultural rule invented by the De Beers diamond cartel that insists, "Spend two months of your salary on your engagement ring." Costly signals that take fitness budgets into account evolve much more easily than do costly signals that ignore budgets. Sensitivity to this budget constraint is called "condition-dependence" by most biologists. It could equally be called "fitness-dependence" to reflect the intuition that fitness indicators should be fitness-dependent. Alan Grafen showed that condition-dependent indicators could evolve, giving Zahavi's handicap principle much more credibility.

This sort of condition-dependence seems intuitive when you think of examples. Better-fed animals can afford to grow larger sexual ornaments. Most energetic animals can afford to exert more effort in courtship. Stronger animals can afford to fight other strong animals in ritualized contests. Faster animals can afford to taunt predators from a closer distance. Animals with better memories can afford to learn a large repertoire of courtship songs. Animals with higher social status can afford to act more confident and relaxed around their peers.

Such condition dependence is one of the most important concepts in sexual selection today. It protects low-fitness animals from incurring the costs of sexual ornamentation and courtship if they do not feel up to it. If you are a really unfit peacock, you are not forced to grow a huge tail that will kill you through exhaustion within a week; instead you can grow a drab little tail and hope for the best. Compared to sexual ornamentation that grows on the body, courtship behavior is even more flexible and condition-dependent. If you are a human feeling really ill, you do not have to go to the Ministry of Sound nightclub with your significant other and dance all night after taking lots of drugs. If you are in poor aerobic condition you do not have to run the Olympic marathon and die of heatstroke. If you are not very bright you do not have to go to Stanford Business School and fail. Condition-dependence lets us choose our battles.

Condition-dependence is equally useful at the high end of the fitness scale, for it enables one to tailor the amount one spends on fitness indicators to one's fitness level. This helps the extremely fit to distinguish themselves from the very fit. It spreads out the apparent differences between individuals so that their fitness is easier to judge. Condition-dependence makes mate choice easier because it lets one infer fitness directly from the apparent costliness of a courtship display.

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