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 decision-making 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.
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