The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (20 page)

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Authors: Geoffrey Miller

Tags: #Evolution, #Science, #Life Sciences

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.

Advertising Within One's Budget

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.

An Infinite Variety of Waste

Zahavi's handicap principle and the idea of condition-dependence are different perspectives on the same thing. The handicap idea emphasizes that sexual ornaments and courtship behaviors must be costly in order to be reliable fitness indicators. Their cost can take almost any form. They can increase risk from predators by making an animal more conspicuous with bright colors. They can increase risk from germs by impairing an animal's immune system (which many sex hormones do). They can burn up vast amounts of time and energy, like bird song. They can demand a huge effort to obtain a small gift of meat, as in human tribal hunting.
As with Veblen's conspicuous consumption principle, the form of the cost does not matter much. What matters is the prodigious waste. The waste is what keeps the fitness indicators honest. The wastefulness of courtship is what makes it romantic. The wasteful dancing, the wasteful gift-giving, the wasteful conversation, the wasteful laughter, the wasteful foreplay, the wasteful adventures. From the viewpoint of "survival of the fittest," the waste looks mad and pointless and maladaptive. Human courtship even looks wasteful from the viewpoint of sexual selection for non-genetic benefits, because, as we shall see, the acts of love considered most romantic are often those that cost the giver the most, but that bring the smallest material benefits to the receiver. However, from the viewpoint of fitness indicator theory, this waste is the most efficient and reliable way to discover someone's fitness. Where you see conspicuous waste in nature, sexual choice has often been at work.
Every sexual ornament in every sexually reproducing species
could be viewed as a different style of waste. Male humpback whales waste their energies with half-hour-long, hundred-decibel songs that they repeat all day long during the breeding season. Male weaverbirds waste their time constructing ornamental nests. Male stag beetles waste the matter and energy from their food growing huge mandibles. Male elephant seals waste a thousand pounds of their fat per breeding season fighting other elephant seals. Male lions waste countless calories copulating thirty times a day with female lions before the females will conceive. Male humans waste their time and energy getting graduate degrees, writing books, playing sports, fighting other men, painting pictures, playing jazz, and founding religious cults. These may not be conscious sexual strategies, but the underlying motivations for "achievement" and "status"—even in preference to material sources—were probably shaped by sexual selection. (Of course, the wasteful displays that seemed attractive during courtship may no longer be valued if they persist after offspring arrive—there is a trade-off between parental responsibilities and conspicuous display.)
The handicap principle suggests that in each case, sexual selection cares much more about the prodigious magnitude of the waste than about its precise form. Once the decision-making mechanisms of sexual choice get the necessary information about fitness from a sexual display, everything else about the display is just a matter of taste. This interplay between waste and taste gives evolution a lot of elbow room. In fact, every species with sexual ornaments can be viewed as a different variety of sexually selected waste. Without so many varieties of sexual waste, our planet would not be host to so many species.

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.

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