The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (22 page)

No theory of human origins can avoid the fact that evolution depends on reproductive competition, and competition means that some individuals win and some lose. With survival selection, the losers die. With sexual selection, the losers merely get their hearts broken (as their genes die out). If one demands moral guidance from a theory of human evolution, one is free to pick which of these options sounds better. Personally, I think that scientific theories should try to account for facts and inspire new research, rather than trying to conform to contemporary moral values.

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Ornamental Genius

Sexual choice is mediated by the senses. We cannot use telepathy to pick sexual partners. We have to rely on the evidence of our eyes, ears, noses, tongues, and skin. Since the senses are the first filter for sexual choice, sexual ornaments evolved to play upon the senses. Biologists have started to analyze sexual ornaments as sound and light shows designed for sensory appeal.

Yet sexual choice also runs deeper than the senses. It depends on memory, anticipation, judgment, decision-making, and pleasure. Psychological preferences go beyond sensory preferences. For most species these more sophisticated psychological preferences probably do not matter very much. As far as we know, their sexual ornamentation has no way of activating ideas, concepts, narratives, or philosophies in the minds of other members of their species. Stimulating the senses is about as deep as they can go, because they have no communication system capable of conveying rich ideas. But after our ancestors evolved communication systems such as language, art, and music, psychological preferences may have become crucial in sexual selection.

Those preferences could have gone far beyond the eye's love of bright color and the ear's response to rhythm. They could have included mental quirks that make us prefer novelty to boredom, grace to clumsiness, knowledge to ignorance, logic to inconsistency, or kindness to meanness. If these quirks influenced the sexual choices that shaped the mind's evolution, then the mind could be viewed as an entertainment system that appeals to the psychological preferences of other minds. Just as some books become best-sellers for their contents rather than their covers, our

ancestors attracted mates by displaying interesting minds, not just shapely bodies and resonant voices. Our minds may have evolved as sexual ornaments, but ornamentation is not limited to a superficial appeal to the senses. As far as sexual selection is concerned, creativity can be ornamental. Consciousness itself may be ornamental.

As we saw in the previous chapter, many sexual ornaments work as fitness indicators. But almost any trait that varies conspicuously and costs a lot can work as a fitness indicator. One important question is, which fitness indicators will evolve, out of the huge number possible? The runaway process cannot help us here, because it is arbitrary about what kinds of trait it favors.

Sensory preferences might be more help in understanding which indicators evolve, because, by definition, they prefer some styles of

ornamentation over others. This chapter reviews how biologists have been thinking about sensory preferences, and then generalizes their ideas to consider how psychological preferences may have influenced sexual selection among our ancestors. We shall also see how fruitful interactions occur between all three sexual selection processes we have been considering—runaway processes, fitness indicators, and, in this chapter, ornaments that appeal to the senses and the mind. When I go on to analyze specific human capacities such as art and creativity, I shall draw on all three of these ideas. They are not only complementary processes in evolution, but they offer complementary perspectives on the human mind.

The Senses as Gatekeepers

For an individual making a sexual choice, the senses are trusted advisors for making one of life's most important decisions. But for the individual being chosen, the chooser's senses are simply the gateway to the royal treasury of their reproductive system. The gateway may have heavy security. It may be guarded by decisionmaking systems that must be charmed or circumvented. It may respond only to secret passwords or badges of office. But it may be vulnerable to flattery, bribery, or threats. Like burglars learning

about the security systems of banks, animals evolve courtship strategies to sneak through the senses of other animals, through the antechamber of their decision-making systems, into the vault of their reproductive potential. Every security system has weaknesses, and every sensory system used in mate choice can be stimulated by the right ornamentation.

Since the early 1980s, biologists have paid more attention to the role of the senses in sexual selection. This shift in focus was prompted by a radical paper by Richard Dawkins and John Krebs in 1978. They argued that when animals send each other signals, they are selfishly trying to influence each other's behavior. Signals are for the good of the sender, not the receiver. They are sent to manipulate behavior, not to convey helpful information. If the receiver's genetic interests overlap with the sender's interests, they may cooperate. The receiver may evolve greater sensitivity to the signaler's messages, and the messages may evolve to be quieter, simpler, and cheaper. Cells within a body have almost identical interests and strong incentives to cooperate, so intercellular signaling evolves to be very efficient. On the other hand, if the receiver's interests deviate from the sender's, signals will tend to become exploitatively manipulative. Predators may trap prey by evolving lures that resemble the prey's own favorite food. In defense, receivers may become insensitive to the signal. Prey may evolve the ability to discriminate between the lure and the real food. This may be why lures are so rare in nature.

Dawkins and Krebs realized that courtship is especially complicated because it is sometimes exploitative and sometimes cooperative. Typically, males of most species like sex regardless of their fitness and attractiveness to the females, so they tend to treat female senses as security systems to be cracked. This is why male pigeons strut for hours in front of female pigeon eyes, and why male humans buy fake pheromones and booklets on how to seduce women from the ads of certain magazines. On the other hand, females typically want sex only with very attractive, very fit males, so tend to evolve senses that respond only to signals of high attractiveness and high fitness. When a truly fit male courts a

fertile female, they have a shared interest in successful mating. They both benefit. He produces more offspring, and she produces the best offspring she could. But there can also be conflicts of interest. When an unattractive, unfit male courts a female, he would gain a net benefit from copulation (extra offspring at rninimal cost to him), but she would not. Her reproductive system would be monopolized producing his inferior offspring when she could have produced better offspring with a better male. So, the female's senses must remain open to courtship by attractive, fit males; but they must resist seduction by inferior males. She must be discriminating.

Sexual discrimination depends on the senses. But the senses may not be perfectly adapted for mate choice, because they must be used in other tasks of survival and reproduction. Primates have just one pair of eyes, which must serve many functions—finding food, detecting predators, avoiding collisions, caring for infants, and grooming friends, as well as discriminating between sexual partners. Visual systems embody design compromises because they fulfill several functions. Eyes for all trades cannot be masters of mate choice.

For example, primate color vision evolved in part to notice brightly colored fruit. The fruit evolved to spread its seeds by advertising its ripeness with bright coloration, to attract fruit-eaters such as primates and birds. Primates benefit from eating the fruit, so they evolve visual systems attracted to bright colors. The fruit's genes can reproduce only by passing through the digestive tract of a primate, so the ripe fruit's coloration is analogous to a sexual display. The fruit competes with the fruit of other trees to attract the primate's attention. Yet the fruit's sexual display can have side-effects on the sexual displays of the primates themselves, as a result of the primates' attraction to bright colors. (Eve's offer of the apple to Adam symbolizes the overlap between the sexual displays of fruit and those of primates.) If a male primate happens to evolve a bright red face, he might prove more attractive to females. He might catch their eyes, because their survival for millions of years has depended on seeking out ripe red

fruit. Her senses are biased to notice bright colors, and this "sensory bias" may influence the direction that sexual selection takes.

Sensory Bias

The engineering details of sensory systems can influence the direction of sexual selection. Investigating these sensory details became a hot topic in the 1980s, but the research area has as many names as there are biologists. John Endler called it "sensory drive"; William Eberhard and Michael Ryan called it "sensory exploitation"; Amotz Zahavi called it "signal selection"; Tim Guilford and Marian Stamp Dawkins called it "the influence of receiver psychology on the evolution of animal signals." The most common term for the design of sensory systems driving the direction of sexual selection is "sensory bias," so I'll use that.

Sensory bias theory is a rapidly developing set of ideas that deserves much more research. It tries to ground the evolutionary study of animal signaling in the design of animal senses. It recognizes that there are always design compromises in animal sensory systems, and that these compromises sometimes make it possible to predict the direction in which sexual selection will go. It also suggests that there are many possible ways for a perceptual system to evolve a sensitivity to particular patterns of stimulation. The selection pressures on senses do not determine every detail of sensory system design: there are always contingent details about the responsiveness of senses that could not be predicted from their adaptive functions. These contingencies may influence the direction of sexual selection, by leading senses to respond more strongly to some stimuli than to others. Finally, sensory bias theory recognizes that senses evolve interactively with the signals they favor.

Displays Match Senses

The senses used for mate choice in each species tend to be well matched to the sexual ornaments displayed by that species. This is one piece of evidence consistent with sensory bias theory.

Michael Ryan found that in several Central American species of frog, female ears are most sensitive to the auditory frequency of male courtship calls. If female ears of one species hear best at 800 hertz, then the males of that species tend to produce calls at around 800 hertz. This is reasonable, given that females of these species must use the calls to locate suitable males in the forests of Central America. Male frogs calling at the wrong frequency would be harder to hear and harder to find, so would not produce so many offspring, and their genes for off-pitch calls would die with them.

Where there is a mismatch between frog ears and frog calls, Michael Ryan argued, the ears would exert sexual selection on the calls. Often, the female ears were more sensitive to calls slightly lower in pitch than the average male of their species was capable of producing. Females would find it easier to locate males who produced deeper-than-average calls, because they would be more audible. This should favor males who produce deeper calls. Ryan interpreted this as an example of sensory bias. The female senses are biased towards lower-man-average calls, and that bias appears to drive sexual selection.

However, this may just be an example of females favoring males of higher fitness. Larger frogs produce lower-pitched calls, so any female preference for larger frogs could be manifest as greater auditory sensitivity to lower-pitched calls. It may not be a sensory bias at all, but an adaptive way for females to discriminate between large and small males. Any mate choice mechanism that favors fitness indicators will look "biased" because it will not be most sensitive to the commonest sexual display in the current population. Instead, it will be most sensitive to the sexual display associated with the highest fitness. Nonetheless, it was useful for Michael Ryan to focus attention on call frequency as the relevant variable that connects the female senses to the male displays.

Senses as Engineering Compromises

A more significant claim from sensory bias theory is that animal
senses have certain features that evolved just because they

efficiently solve the information-processing problems of perception, and these features can drive sexual selection. Eyes have to perceive objects in general, and there may be general principles relevant to this task, principles which may influence mate choice;

Consider the area at the very back of the brain called the primary visual cortex, or "V1." This is the conduit for almost all information that passes between the eyes and the rest of the brain. Each V1 brain cell covers a tiny area of the visual world, and fires most actively when the local pattern of light in that area corresponds to the edge of an object. V1 seems to be a set of edge-detectors. Vision researchers believe that this is simply an efficient way to process visual information about the world, since vision is about seeing objects, and objects tend to have edges. This edge-detection principle has been used in most successful robot vision systems designed by humans.

Now consider how a male could grab the attention of a female's V1 system. He has to activate her edge-detectors. He could evolve a body that has many more real edges than average, perhaps a sort of fractal design. But the more real edges he has per unit of body volume, the more fragile his body would be and the more heat he would lose. Better to evolve sexual ornaments that display lots of fake edges. Dots would work, but thin parallel stripes would be even better, displaying more edge information per unit area. Perhaps stripes became popular sexual ornaments across many species because stripes are optimal stimuli for activating the visual cortex.