How to Advertise Fitness

Fitness is like money in a secret Swiss bank account. You may know how much you have, but nobody else can find out directly. If they ask the bank, the bank will not tell them. If they ask you, you might lie. If they are willing to mate with you if your capital exceeds a certain figure, you may be especially tempted to lie. This is what makes mate choice difficult. The supposedly low heritability of fitness was one argument against the importance of fitness indicators in sexual selection. The other problem is the potentially low reliability of fitness indicators. An animal trying to find a high-fitness mate is in the position of an attractive gold digger seeking a millionaire. She has incentives to mate only with a male who offers high genetic or financial capital. But every male has incentives to pretend to be richer than he is, to attract more mates. What is a poor girl to do?

Anita Loos's classic 1925 novel Gentlemen Prefer Blondes suggested one good strategy. The blonde protagonist Lorelei Lee forced her suitors to spend vast amounts of money on her, to show how much they really had. Her suitor Gus Eisman may have called himself "the Button King," but who can say whether his business is really profitable? Miss Lee was not the brightest button ever to baffle "Doctor Froyd" in Vienna, but she understood the principle of costly display. If a man can afford to dress as well as a peacock, he is probably not poor. If he gives you a very large diamond, he is likely to be rich. The more they can spend, the more they must have.

Lorelei was not the first to realize this, of course. Thorstein Veblen's Theory of the Leisure Class introduced the idea of "conspicuous consumption" in 1899. Veblen argued that in modern urban societies, where strangers come and go, people increasingly advertise their wealth by ornamenting themselves with costly luxuries. Where nobody knows anyone else's true wealth directly, conspicuous consumption is the only reliable signal of wealth. Sociologists and economists understood this logic immediately. Capitalist consumerism evolved in part as a set of wealth indicators.

It took biologists another three-quarters of a century to apply the same principle to sexual selection for fitness indicators. As we saw earlier, in 1975 Israeli biologist Amotz Zahavi argued that many animal signals—including sexual ornaments—evolved as advertisements of the animal's fitness. He suggested that the only reliable way to advertise one's true fitness is to produce a signal that costs a lot of fitness. This explains why sexual ornaments are so often large, extravagant, costly, and complicated. The peacock's tail is not just a cheap, transient advertisement visible only to peahens. It is heavy, encumbering, hard to grow, hard to preen, and highly visible to predators. Peacocks have to drag it around everywhere they go. Unfit peacocks might be able to grow large tails, but they would not be strong enough to carry them while finding food, or fast enough to escape from predators. Only highly fit peacocks can afford very large tails.

Therefore, if a female sees a male sporting a very large tail, she can be confident that he has high fitness, and that his good genes could be passed on to her offspring. Since very fit peacocks tend to have fit sons and daughters that are more likely to survive and reproduce, peahens benefit by choosing big-tailed peacocks. Their preferences for larger-than-average tails can spread. Conversely, peahens that preferred shorter-than-average tails did not leave many descendants to inherit their misguided preference, because their offspring were less fit than average. Sexual selection favors both the preference for costly sexual displays and the displays themselves.

Zahavi suggested that most sexual ornaments are "handicaps": they advertise true fitness by handicapping an individual with a survival cost. He also argued that handicaps should be the only evolutionarily stable kinds of sexual ornament, because they are the only ones that convey the information about fitness that individuals really want when making sexual choices. His paper unleashed a storm of protest. The handicap idea seemed absurd. Throughout the late 1970s the handicap principle was attacked by almost every eminent evolutionary theorist. Surely sexual selection could not have an intrinsic drive to produce wasteful displays that impair survival?

Apparently, most biologists in the 1970s had not read Thorstein Veblen. They did not make the connection between conspicuous consumption to advertise wealth and costly sexual ornaments to advertise fitness. Without that connection it was hard to see how Zahavi's handicap principle could work (or rather, which of the several possible versions of it might work). How could sexual selection favor fitness indicators that impaired an animal's survival prospects? How could mate choice favor a costly, useless ornament over a cheaper, more beneficial ornament? (Why should a man give a woman a useless diamond engagement ring, when he could buy her a nice big potato, which she could at least eat?)

A clever peahen able to read Veblen might propose that, for the good of the species, peacocks should stop this mad waste. Suppose, for example, that each peacock agreed to wear a little hat showing a number between one and ten that revealed his actual fitness (perhaps a composite score of health, strength, fecundity, intelligence, and screeching ability). The problem with this system of quality-signs is that there would be no effective way to police it. Low-fitness peacocks would lie, because they could attract better mates by lying—they would all proclaim a perfect ten. Zahavi realized that the signaling system has to be self-policing. It has to include a range of sexual signals that differ in cost, and thus differ in affordability by individuals of different fitness, by virtue of which they honestly reveal their fitness.

The handicap principle suggests that prodigious waste is a necessary feature of sexual courtship. Peacocks as a species would be much better off if they didn't have to waste so much energy growing big tails. But as individual males and females, they have irresistible incentives to grow the biggest tails they can afford, or to choose sexual partners with the biggest tails they can attract. In nature, showy waste is the only guarantee of truth in advertising.

The handicap principle was also rejected initially because most biologists did not know about economists' research into costly signaling. During the 1960s, game theorists working in economics departments did a lot of work on what makes signals reliable, given incentives to he. They developed something called signaling theory, which distinguishes two kinds of signal. There are signals that incur a significant cost or commitment, which can therefore be reliable indicators of someone's intentions. And then there are signals that cost nothing, which are called "cheap talk." Economists realized that cheap talk is not to be trusted. It does not commit someone to a course of action. It does not reveal their capabilities. It means nothing, because it costs nothing. If a car company proclaims "We will defend our share of the four-door market at all costs," that is just cheap talk and hot air. But if the company spends a billion dollars building a factory specialized for four-door car production, their proclamation carries some weight.

The factory is not just a capital investment—it is also a strategic signal. It deters competitors from entering the same market niche by reliably revealing the company's financial strength and strategic commitment. In fact, the more (wasteful) excess capacity the factory has, the better a strategic signal it is. Likewise, proclaiming "I have a straight flush" in poker carries less credibility than placing a large bet on one's hand. This costly-signaling principle became so widely accepted among economists in the 1960s that signaling theory withered for lack of controversy.

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