Two friends of mine, whom I’ll call Art and Judy Smith, had gone through a difficult time in their marriage, and after both had had extramarital affairs, they separated. Recently, however, they had come back together, in part because the separation had been hard on their children. Now Art and Judy were working to repair their damaged relationship, and both had promised not to resume their infidelities. Still, the legacy of suspicion remained.
Art phoned home one morning while he was out of town on a business trip. A man’s deep voice answered the phone. Art’s throat choked instantly as his mind groped for an explanation. (Did I dial the wrong number? What is a man doing there?) Not knowing what to say, Art blurted out, Is Mrs. Smith at home? The man answered matter-of-factly, She’s upstairs getting dressed.
In a flash, rage swept over Art. He screamed inwardly to himself, She’s back to her affairs! Now some bastard stays overnight in my bed! He even answers the phone! Art had visions of rushing home, killing his wife’s lover, and smashing Judy’s head into the wall. Still hardly able to believe his ears, he stammered into the phone, Who -- is -- this?
The voice at the other end cracked, rose from the baritone range to a soprano, and answered, Daddy, don’t you recognize me? It was Art’s 14-year-old son, whose voice was changing. Art gasped again, in a mixture of hysterical relief and sobbing.
Art’s account of that phone call reminded me of how even we humans, the only rational animal species, still live in the irrational thrall of animal-like behavioral programs. A mere one-octave change in pitch of a voice uttering half-a-dozen banal syllables converted the speaker’s image in Art’s mind from threatening rival to unthreatening child, and Art’s mood from murderous rage to paternal love. Other equally trivial cues spell the difference between our images of young and old, ugly and attractive, intimidating and weak. Art’s story illustrates the power of what zoologists term a signal: a cue that can be recognized quickly, and that may itself be insignificant, but that has come to denote an important biological attribute, such as sex, age, aggression, or relationship. Signals are essential to animal communication, the process by which one animal alters the probability of another animal’s behaving in a way that may benefit one or both. Small signals, which in themselves require little energy (like pronouncing a few syllables), may release behaviors requiring a lot of energy (risking one’s own life in an attempt to kill another).
Animals signal to one another via many channels of communication. Among the most familiar to us are auditory signals, such as the territorial songs by which birds attract mates and warn off rivals, or olfactory signals, such as the urine-carried odors used by many mammals to mark off territory. Equally familiar are behavioral signals: dog lovers know that a dog with its ears, tail, and neck hair raised is aggressive, but a dog with its ears and tail lowered and neck hair flat is submissive or conciliatory. There are other means less familiar and accessible to us: the chemical signals with which ants mark a trail to a food source, for example, or the electric signals exchanged by electric fish.
Not all the signals animals employ, though, can be so easily turned on and off. Some are longer lasting, or even a more or less permanent part of an animal’s anatomy. Females of many primate species, for instance, advertise their time of ovulation with swollen, brightly colored skin on the buttocks or around the vagina. Many bird species use their plumage to indicate sex, while gorillas do so through differences in the size and the shape of their heads. Many birds also show their age with their plumage: herring gulls, as a prime example, have distinct plumages as juveniles and at one, two, three, and four or more years of age.
Unlike most human signals, animal signals like these can be studied experimentally, in the lab. For instance, appeal to the opposite sex may depend on specific parts of the body. One group of researchers demonstrated this point for Africa’s long-tailed widowbird, in which the male’s 16-inch-long tail was suspected of playing a role in attracting females. The researchers tested this assumption quite simply by lengthening or shortening the males’ tails. Males whose tails were cut down to 6 inches attracted few mates, while fortunate fellows who had an extra piece of tail glued on, extending their tails to 26 inches, attracted extra mates. Other researchers studied a European bird called the great tit, which has a black stripe on its breast that serves as a signal of social status. Experiments with radio-controlled models placed at bird feeders showed that live tits coming to the feeder retreat if and only if the model’s stripe is wider than the intruder’s stripe.
How on earth did such apparently arbitrary signals evolve? Why should a perfectly good bird back off just because it sees a bird with a slightly wider stripe? One would think that an otherwise inferior bird with a gene for a wide stripe could thereby gain undeserved social status. Why doesn’t such cheating become rampant and destroy the meaning of the signal?
Zoologists still debate these questions, in part because the answers may differ for different signals or different animal species. But three theories that have been proposed do shed some light on the evolution of body sexual signals--that is, on structures, such as peacocks’ tails or women’s breasts, that distinguish the sexes and attract opposite-sex mates or threaten same-sex rivals.
The first theory, put forward by British geneticist Sir Ronald Fisher, is termed Fisher’s runaway selection model. It starts with the observation that all female animals, including humans, do best to mate with males bearing good genes to pass on to their offspring; however, females have no direct way to assess the quality of a male’s genes. But suppose that a female somehow became genetically programmed to be sexually attracted to males with a certain structure that gives those males some advantage at surviving--a slightly longer tail, say, that made the male a better flier. Males with the preferred tail would thereby gain an additional advantage, because they would now transmit their genes to more offspring. Females preferring males with the longer tail would in turn gain an advantage because they would transmit the genes for that elongated structure to their sons, who would in turn survive better and also be chosen by females with such a preference.
A runaway process of selection would then ensue, favoring those males with genes for an exaggerated tail, and favoring those females with genes for an exaggerated preference for the tail. From generation to generation the structure would grow in size or conspicuousness until it lost its original beneficial effect on survival. For instance, a slightly longer tail might be useful for flying, but a peacock’s gigantic tail surely is not. The evolutionary runaway process would halt only when further exaggeration of the trait threatened survival.
A second theory, proposed by Israeli zoologist Amotz Zahavi, emphasizes the fact that many structures functioning as body sexual signals are so big or conspicuous that they must indeed constitute a hazard to their owner. For instance, a huge tail not only doesn’t help a bird survive but actually makes life more difficult by making it hard to slip through dense vegetation, take flight, and escape predators. Many sexual signals, Zahavi notes, like a bowerbird’s golden crest, are big, bright, conspicuous structures that tend to attract a predator’s attention. In addition, such structures cost a lot of biosynthetic energy just to grow. As a result, he argues, any male that manages to survive despite such a handicap is, in effect, boasting to females that he must have terrific genes in other respects. When a female sees a male with that handicap, she is guaranteed that he is not cheating by carrying the gene for a big tail and being otherwise inferior. He would not have been able to afford to make the structure, and would not still be alive, unless he was truly superior.
One can think of many human behaviors that surely conform to Zahavi’s handicap theory of honest signals. Any man can tell a woman that he is rich and that therefore she should go to bed with him in the hope of enticing him into marriage--but he might be lying. Only when she sees him throwing away money on useless expensive jewelry and sports cars can she believe his claims of wealth. Again, some college students make a show of partying on the night before a big examination. In effect, they are saying: Any jerk can get an A by studying, but I’m so smart that I can get an A despite the handicap of not studying.
The remaining theory, as formulated by American zoologists Astrid Kodric-Brown and James Brown, is known as truth in advertising. Like Zahavi, and unlike Fisher, the Browns emphasize that costly body structures surely represent honest advertisements of quality because an inferior animal could not afford the cost. But while Zahavi sees the costly structures as a handicap to survival, in the Browns’ model they favor survival. The costly structure is thus a doubly honest ad: only a superior animal can afford its cost, and it makes the animal even more superior.
For instance, the antlers of male deer represent a big investment of calcium, phosphate, and calories, yet they are grown and discarded each year. Only the best-nourished males, those that are mature, socially dominant, and free of parasites, can afford that investment. Hence a female deer can regard big antlers as an honest ad for male quality, just as a woman whose boyfriend buys and discards a Porsche each year can believe his claim of being wealthy. But antlers carry a second message not shared with sports cars. Whereas a Porsche does not generate more wealth, big antlers bring their owner access to the best pastures by enabling him to defeat rival males and fight off predators.
It’s natural to wonder whether any of these three theories, devised to explain the evolution of animal signals, also explain features of human bodies. First, do our bodies even possess any features requiring such explanation? After all, we have more reasoning ability than other animals, and our unique capacity for speech allows us to transmit far more detailed information than any animal. Why should we need long tails and black stripes when we routinely determine each other’s age and status just by talking? No other animal can tell a potential mate that it is 27 years old, is second assistant vice president at the country’s third largest bank, and earns $200,000 a year. In selecting our sex partners and mates, don’t we go through a dating phase, in effect a long series of tests by which we accurately assess a prospective partner’s relationship skills, parenting skills, and genes?
Well, yes and no. Dates or no dates, we too still rely on signals as arbitrary as a widowbird’s tail and a bowerbird’s crest. Our signals include faces, smells, hair color, beards on men, and breasts on women, structures surely no less ludicrous for selecting a spouse than a long tail. If we think that we have a signaling system immune to cheating, why do so many people resort to makeup, hair dyes, and breast augmentation? As for our supposedly wise and leisurely selection process, all of us know that when we walk into a room full of unfamiliar people, we quickly sense who attracts us physically and who doesn’t. That quick sense is based on sex appeal, which just means the sum of the body signals to which we respond, largely unconsciously.
In fact, like other animal species, we humans evolved many body traits signaling age, sex, reproductive status, and individual quality, as well as programmed responses to such traits. Both human sexes show that they’ve reached reproductive maturity by growing pubic and armpit hair. Men grow a beard and body hair as well, and their voices drop in pitch, as my friend Art was dramatically reminded. Human females additionally signal reproductive maturity by expansion of the breasts. Later in life, we signal that our fertility is on the wane and (in traditional societies) that we’ve attained wise-elder status by the whitening of our hair. We tend to respond to the sight of body muscles, in appropriate amounts and places, as a signal of male physical condition, and to the sight of body fat, also in appropriate amounts and places, as a signal of female physical condition. We use all those same signals of reproductive maturity and physical condition to select our mates and sex partners, but the signals differ from population to population. For instance, the average luxuriance of men’s beards and body hair varies around the world, as do the size and shape of women’s breasts, and the color and size of their nipples.
At least three sets of human signals seem to me to conform to the truth-in-advertising model: men’s muscles, facial beauty in both sexes, and women’s body fat. Men’s muscles tend to impress women as well as other men. While extreme bodybuilders may strike you as grotesque, many or perhaps even most women find a shapely, well-toned hunk more attractive than a scrawny fellow. Men also read the muscular development of other men as a signal that helps them assess quickly whether to get into a fight or to retreat.
At least in traditional societies, muscles, like a deer’s antlers, are a truthful signal of male quality. Muscles enable men to gather food, build houses, and defeat rivals. Moreover, men with other good qualities are better able to acquire all the protein they need to grow and maintain big muscles. One can fake one’s age by dyeing one’s hair, but one cannot fake big muscles. Naturally, men did not evolve muscles solely to impress other men and women, as male bowerbirds evolved a golden crest solely to impress other bowerbirds. Instead, muscles evolved to perform functions, and men and women then learned to respond to muscles as a truthful signal.
A beautiful face may be another truthful signal, although the underlying reason is not as transparent as in the case of muscles. After all, doesn’t it seem absurd that our sexual and social attractiveness depends on facial beauty to such an inordinate degree? It isn’t obvious that someone with a pretty face would have particularly good genes, parenting qualities, or food-gathering skills. However, the face is the part of the body most sensitive to the ravages of age, disease, and injury. Especially in traditional societies, someone with a scarred or misshapen face may be advertising his proneness to disfiguring infections, inability to take care of himself, and his burden of parasitic worms. Before sophisticated cosmetics and surgery, a beautiful face was a signal of good health that could not be faked.
Women’s body fat is a similarly unfakable sign of fitness. Lactation, a big energy drain, tends to fail in an undernourished mother. Before the advent of infant formulas, and before the domestication of milk- producing hoofed animals, a mother’s lactational failure would have been fatal to her infant. Naturally, men should prefer the correct amount of fat: a woman with too little might not be able to nourish his child, but one with too much might have trouble walking and gathering food, and could die early from diabetes.
Perhaps because fat would be difficult to discern if it were spread uniformly over the body, women have evolved to concentrate it in readily visible parts. The anatomic location of these areas varies somewhat among human populations: while women of all populations tend to accumulate more or less fat in the breasts and hips, women of the San population native to southern Africa and women of the Andaman Islands in the Bay of Bengal add extra fat in the buttocks, producing the condition known as steatopygia.
Men throughout the world, of course, tend to be interested in women’s breasts, hips, and buttocks. These areas actually make a lot of sense. Suppose you were designing a woman--you wouldn’t want to put extra fat on her arms and legs, because she would have a harder time walking and using her arms. That leaves many parts of the torso where fat could be safely concentrated without impeding movement, including the three signaling areas emphasized above (and in the Victoria’s Secret catalog). Still, was the evolutionary choice of areas completely arbitrary? Why aren’t there populations of women with other signaling locations, such as the belly or the middle of the back? Paired fat deposits on the back would seem to create no more difficulties for locomotion than do our actual paired deposits in the breasts and buttocks.
Remarkably, though, women of all populations evolved fat accumulation in the breasts, the organs whose lactational performance men may be attempting to assess by looking for fat. Hence some scientists have suggested that large fatty breasts are not only an honest general signal of good nutrition but also a deceptive specific signal of high milk-producing ability (milk is actually secreted by breast glandular tissue rather than by breast fat). Similarly, some scientists believe that fat deposition in the hips of women is also both an honest overall signal and a deceptive specific signal of a wide birth canal that will minimize the risk of birth traumas.
There are three objections raised to these interpretations. First, in traditional societies at least 95 percent of women marry. This seems to suggest that virtually any woman can get a husband and that women have no need to compete for men and thus evolve bodily ornaments for that purpose. But that interpretation is belied by all the effort and pain that women consciously put into decorating and modifying their bodies to make them attractive. In fact, men vary greatly in their genes, in the resources that they control, and in their devotion to their wives and children. Although virtually any woman can get some jerk to marry her, only a few women succeed in getting one of the few high-quality men, for whom women must compete intensely.
A second objection notes that men in traditional societies did not choose their spouse, whether on the basis of sexual ornamentation or any other quality. Instead, marriages were arranged by clan relatives, often with the motive of cementing political alliances. In reality, though, bride prices in traditional societies vary depending on the woman’s desirability, with visible signs of her health and likely mothering qualities being important considerations. That is, although a bridegroom’s views about his bride’s sex appeal are ignored, his relatives who select the bride do not ignore their own views. In addition, when selecting partners for extramarital sex, men surely consider a woman’s sex appeal. And extramarital sex probably accounts for a higher proportion of babies in traditional societies (in which husbands don’t get to follow their sexual preferences in selecting their wives) than in modern societies.
The remaining objection notes that culturally influenced standards of beauty vary with time, and that individual men within the same society differ in their tastes. Skinny women may be out this year but in next year, and some men prefer skinny women every year. However, that merely constitutes noise slightly complicating but not invalidating the main conclusion: that men at all places and times have on the average preferred well-nourished women with beautiful faces.
Apparently, then, human sexual signals such as facial beauty, men’s muscles, and women’s breasts fit the truth-in-advertising explanation. But other signals may have other explanations, as they do in nonhuman animals. For example, the pubic and armpit hair grown by both men and women in adolescence is a reliable but wholly arbitrary signal that we have attained reproductive maturity. Pubic and underarm hair are well placed to trap any pheromones we might secrete into our sweat and urine, which may signal our sex and (if we’re women) the phase of our ovulatory cycle to those with discriminating noses. But hair in those locations differs from muscles, beautiful faces, and body fat in that it carries no deeper message. It costs little to grow, and it makes no direct contribution to survival or to nursing babies. Poor nutrition may leave you with a scrawny body and disfigured face, but it rarely causes your pubic hair to fall out. Even weak, ugly men and skinny, ugly women sport armpit hair. Men’s beards, body hair, and low-pitched voices signaling adolescence, and men’s and women’s hair whitening signaling age, seem equally devoid of inner meaning.
For example, because my voice is deep (I’m a second bass), I feel intuitively that a deep voice should somehow be an honest signal of a man’s superiority over scrawny tenors. But I haven’t been able to think of any direct connection between a bass voice and male prowess sufficiently compelling to convince any of my tenor friends, let alone Placido Domingo. If you were to ask me why adolescent girls weren’t the ones to develop a drop in voice pitch to the bass range, I couldn’t give you a good answer. Like the black stripe on a great tit’s breast and many other animal signals, these human signals are cheap and wholly arbitrary.
Does any human signal exemplify Fisher’s runaway selection model or Zahavi’s handicap principle? At first, we seem devoid of exaggerated signaling structures comparable to a widowbird’s 16-inch tail. On reflection, though, I wonder whether the human male’s penis is such a structure. One might object that it serves a nonsignaling function and is nothing more than well-designed reproductive machinery. However, that’s no obstacle to my speculation: we already saw that women’s breasts simultaneously constitute signals and reproductive machinery. Comparisons with our ape relatives hint that the size of the human penis greatly exceeds bare functional requirements. The length of the erect penis is a mere 1 to 1.5 inches in gorillas and orangutans, but 5 inches in humans, even though males of the two apes have much bigger bodies than men do.
Are those extra several inches of the human penis a useless extravagance? One counterinterpretation is that a large penis might somehow be useful in our wide variety (compared with many other mammals) of copulatory positions. However, the 1.5-inch penis of the male orangutan permits it to perform in a variety of positions rivaling ours, and to outperform us by executing all those positions while hanging from a tree. As for the possible use of a large penis in sustaining prolonged intercourse, orangutans top us in that regard too (mean duration 15 minutes versus a mere 4 minutes for the average American man).
A hint that the large human penis serves as some sort of signal comes from considering what happens when men take the opportunity to design their own penises, rather than remaining content with their evolutionary legacy. Men in the highlands of New Guinea do that by enclosing the penis in a decorative sheath called a phallocarp. The sheath is up to two feet long and four inches in diameter, often bright red or yellow, and variously decorated at the tip with fur, leaves, or a forked ornament. When I first encountered New Guinea men with phallocarps, among the Ketengban tribe in the Star Mountains a few years ago, I had already heard a lot about them and was curious to see how people actually used and explained them. At least whenever I encountered them, the men wore their phallocarps constantly. Each man owned several models to put on according to his mood that day, varying in size and ornaments and angle of erection. When I asked why they wore phallocarps, the Ketengbans told me they felt naked and immodest without them. That answer surprised me from my Western perspective, because the Ketengbans were otherwise completely naked and left even their testes exposed.
In effect, the phallocarp is a conspicuous, erect pseudopenis representing what a man would like to be endowed with. The size of the penis that we evolved was unfortunately limited by the length of a woman’s vagina. A phallocarp shows us what the human penis would resemble if it were not subject to that practical constraint. The actual penis, while more modest than a phallocarp, is immodestly large by the standards of our ape ancestors, although the chimpanzee penis has also become enlarged over the inferred ancestral state to a size rivaling ours. Penis evolution evidently illustrates the operation of runaway selection, just as Fisher postulated. Starting from a 1-inch ancestral ape penis similar to the penis of a modern gorilla, the human penis increased in length by a runaway process, conveying an advantage to its owner as a signal of virility, until its length became limited by counterselection as difficulties with its fit to women’s vaginas became imminent.
What remains debatable is the intended audience at whom the penis’s proclamation of virility is directed. Most men would assume that the ones who are impressed are women. On the other hand, women tend to report that they are more turned on by other features of a man and that the sight of a penis is, if anything, unattractive. Instead, the ones really fascinated by the penis and its dimensions are men, who routinely stare at others’ endowment in the showers of any locker room.
But even if some women are also impressed, our discussion need not degenerate into an either-or argument that assumes the signal to be directed at only one sex. Zoologists studying animals regularly discover that sexual ornaments serve a dual function: to attract mates of the opposite sex and to establish dominance over rivals of the same sex. In that respect, as in many others, we humans still carry the legacy of hundreds of millions of years of vertebrate evolution engraved deeply into our sexuality. Over that legacy, our art, language, and culture have added only a recent veneer.