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  Biologist friends to whom I pose this conundrum usually think of distinctive features of human coitus where they suppose a long penis might somehow be useful: our frequent use of the face-to-face position, our acrobatic variety of coital positions, and the supposedly long duration of our coital bouts. None of these explanations survives close scrutiny. The face-to-face position is also a preferred one for orangutans and pygmy chimps, and is used occasionally by gorillas. Orangutans vary face-to-face copulation with dorso-ventral and sideways positions, and do it while hanging from branches of trees – surely that demands more penile acrobatics than our comfortable boudoir exercises. Our mean duration of coitus (about four minutes for Americans) is much longer than for gorillas (one minute), pygmy chimps (fifteen seconds), or common chimps (seven seconds), but shorter than for orangutans (fifteen minutes) and lightning-fast compared to the twelve-hour-long copulations of marsupial mice. (Are you listening, ghosts of Errol Flynn and Don Juan?)

  Since it thus seems unlikely that special features of human coitus demand a large penis, a popular alternative theory is that the human penis has also become an organ of display, like a peacock’s tail or a lion’s mane. This theory is reasonable but begs the question, what type of display, and to whom?

  Proud male anthropologists unhesitatingly answer, an attractive display, to women, but this represents mere wishful thinking. Many women say that they are turned on by a man’s voice, legs, and shoulders more than by the sight of his penis. A telling point is that the women’s magazine Viva initially published photos of nude men but dropped them after surveys showed lack of female interest. When Viva’s nude men disappeared, the number of female readers increased, and the number of male readers decreased. Evidently, the male readers were the ones buying Viva for its nude photos. While we can agree that the human penis is an organ of display, the display is intended not for women but for fellow men.

  Other facts confirm the role of a large penis as a threat or status display towards other men. Recall all the phallic art created by men for men, and the widespread obsession of men with their penis size. Evolution of the human penis was effectively limited by the length of the female vagina: a man’s penis would damage a woman if it were significantly larger. However, I can guess what the penis would look like if this practical constraint were removed and if men could design it themselves. It would resemble the penis sheaths (phallocarps) used as male attire in some areas of New Guinea where I do field work. Phallocarps vary in length (up to 2 feet), diameter (up to 4 inches), shape (curved or straight), angle made with the wearer’s body, colour (yellow or red), and decoration (such as a tuft of fur at the end). Each man has a wardrobe of several sizes and shapes from which to choose each day, depending on his mood that morning. Embarrassed male anthropologists interpret the phallocarp as something used for modesty or concealment, to which my wife had a succinct answer on seeing a phallocarp: ‘The most immodest display of modesty I’ve ever seen!’

  Thus, astonishing as it seems, important functions of the human penis remain obscure. Here is a rich field for research.

  *

  Passing now from anatomy to physiology, we are immediately confronted by our sexual activity pattern, which must be considered freakish by the standards of other mammal species. Most mammals are sexually inactive most of the time. They copulate only when the female is in oestrus – that is, when she is ovulating and capable of being fertilized. Female mammals apparently ‘know’ when they are ovulating, for they solicit copulation then by presenting their genitals towards males. Lest a male miss the point, many female primates go further; the area around the vagina, plus in some species the buttocks and breasts, swells up and turns red, pink, or blue. This visual advertisement of female availability affects male monkeys in the same way that the sight of a seductively dressed woman affects male humans. In the presence of females with brightly swollen genitals, male monkeys stare much more often at the female’s genitals, develop higher testosterone levels, attempt to copulate more often, and penetrate more quickly and after fewer pelvic thrusts than in the presence of females not displaying their wares.

  Human sexual cycles are quite different. The human female maintains her sexual receptivity more or less constantly, instead of having it sharply confined to a short oestrus phase. Indeed, despite numerous studies aimed at settling whether a woman’s receptivity varies at all through her cycle, there is still no agreement about the answer – nor about the cycle phase when receptivity is maximal if it does vary.

  So well concealed is human ovulation that we did not have accurate scientific information on its timing until around 1930. Before that, many physicians thought that women could conceive at any point in their cycle, or even that conception was most likely at the time of menstruation. In contrast to the male monkey who has only to scan his surroundings for brightly swollen lady monkeys, the unfortunate human male has not the faintest idea which ladies around him are ovulating and capable of being fertilized. A woman herself may learn to recognize sensations associated with ovulation, but it is often tricky, even with the help of thermometers and ratings of vaginal mucus quality. Furthermore, today’s would-be mother, who tries in such ways to sense ovulation in order to achieve (or avoid) fertilization, is responding by cold-blooded calculation to hard-won, modern book knowledge. She has no other choice; she lacks the innate, hot-blooded sense of sexual receptivity that drives other female mammals.

  Our concealed ovulation, constant receptivity, and brief fertile period in each menstrual cycle ensure that most copulations by humans are at the wrong time for conception. To make things worse, menstrual cycle length varies more between women, or from cycle to cycle in a given woman, than for other female mammals. As a result, even young newlyweds who omit contraception and make love at maximum frequency have only a twenty-eight per cent probability of conception in each menstrual cycle. Animal breeders would be in despair if a prize cow had such low fertility, but in fact they can schedule a single artificial insemination so that the cow has a seventy-five per cent chance of being fertilized!

  Whatever the main biological function of human copulation, it is not conception, which is just an occasional by-product. In these days of growing human overpopulation, one of the most ironic tragedies is the Catholic Church’s claim that human copulation has conception as its natural purpose, and that the rhythm method is the only proper means of birth control. The rhythm method would be terrific for gorillas and most other mammal species, but not for us. In no species besides humans has the purpose of copulation become so unrelated to conception, or the rhythm method so unsuited for contraception.

  For animals, copulation is a dangerous luxury. While occupied in acto flagrante, an animal is burning up valuable calories, neglecting opportunities to gather food, vulnerable to predators eager to eat it, and vulnerable to rivals eager to usurp its territory. Copulation is something to be accomplished in the minimum time required to do the job of fertilization. In contrast, human sex, as a device to achieve fertilization, would have to be rated a huge waste of time and energy, an evolutionary failure. Had we retained a proper oestrus cycle like other mammals, the wasted time could have been diverted by our hunter-gatherer ancestors to butchering more mastodons. By this results-oriented view of sex, any hunter-gatherer band whose females advertised their oestrus period could thereby have fed more babies and out-competed neighbouring bands.

  Thus, the most hotly debated problem in the evolution of human reproduction is to explain why we nevertheless ended up with concealed ovulation, and what good all our mistimed copulations do us. For scientists, it is no answer just to say that sex is fun. Sure, it’s fun, but evolution made it that way. If we were not getting big benefits from our mistimed copulations, mutant humans who had evolved not to enjoy sex would have taken over the world.

  Related to this paradox of concealed ovulation is the paradox of concealed copulation. All other group-living animals have sex in public, whether they are promiscuous or monogamous. Paired
seagulls mate in the middle of the colony; an ovulating female chimpanzee may mate consecutively with five males in each other’s presence. Why are we unique in our strong preference for copulating in private?

  Biologists are currently arguing over at least six different theories to explain the origin of concealed ovulation and concealed copulation in humans. Interestingly, the debate proves to be a Rohrschach test for the gender and outlook of the scientists involved. Here are the theories and their proponents:

  1. Theory preferred by many traditional male anthropologists.

  According to this view, concealed ovulation and copulation evolved in order to enhance cooperation and reduce aggression among male hunters. How could cavemen bring off the precise teamwork needed to spear a mammoth, if they had been fighting that morning for the public favours of a cavewoman in oestrus? The implicit message of this theory is that women’s physiology is important chiefly for its effect on bonds between men, the real movers of society. However, one can broaden this theory to make it less blatantly sexist. Visible oestrus and sex would disrupt human society by affecting female/female and male/female as well as male/male bonds.

  To illustrate this broadened version of the prevalent theory, consider the following scene from an imaginary soap opera, showing what life would be like for us modern hunter-gatherers if we did not have concealed ovulation and private copulation. Our soap opera stars Bob and Carol and Ted and Alice and Ralph and Jane. Bob, Alice, Ralph, and Jane work together in an office where the men hunt contracts and the women gather accounts payable. Ralph is married to Jane. Bob’s wife is Carol, and Alice’s husband is Ted. Carol and Ted work elsewhere.

  One morning, Alice and Jane both discover on awakening that they have turned bright red in order to advertise impending ovulation and sexual receptivity. Alice and Ted make love at home before they go off in their separate directions to work. Jane and Ralph go together to work, where they copulate occasionally on the office sofa in the presence of their co-workers.

  Bob cannot help lusting for Alice and Jane when he sees them bright red and sees Jane and Ralph copulating. He is unable to concentrate on his work. He repeatedly propositions Jane and Alice.

  Ralph drives Bob away from Jane.

  Alice is faithful to Ted and rejects Bob, but the hassle also interferes with her work.

  All day, Carol in her office elsewhere is seething with jealousy at the thought of Alice and Jane, because Carol knows that Alice and Jane are bright red and attractive to Bob, while she (Carol) is not.

  As a result, the office succeeds in bagging few contracts and accounts. In the meantime, other offices, where ovulation is concealed and where copulation is private, prosper. Eventually, Bob’s, Alice’s, Ralph’s, and Jane’s office goes extinct. The only offices that survive are those with concealed ovulation and copulation.

  This parable suggests that the traditional theory, by which concealed ovulation and copulation evolved to promote cooperation within human societies, is plausible. Unfortunately, there are other, equally plausible theories that I will now explain more briefly.

  2. Theory preferred by many other traditional male anthropologists.

  Concealed ovulation and copulation cement the bonds between a particular man and woman, thereby laying the foundations of the human family. A woman remains sexually attractive and receptive so that she can satisfy a man sexually all the time, bind him to her, and reward him for his help in rearing her baby. The sexist message: women evolved to make men happy. Left unexplained by this theory is the question of why pairs of gibbons, whose unflinching devotion to monogamy should make them role models for the Moral Majority, remain constantly together despite having sex only every few years.

  3. Theory of a more modern male anthropologist (Donald Symons).

  Symons noted that a male chimpanzee who kills a small animal is more likely to share the meat with an oestrus female than with a non-oestrus female. This suggested to Symons that human females might have evolved a constant state of oestrus, in order to ensure a frequent meat supply from male hunters by rewarding them with sex. As an alternative theory, Symons noted that women in most hunter-gatherer societies have little say in selection of a husband. The societies are male-dominated, and male clans just suit themselves by exchanging daughters in marriage. However, by being constantly attractive, even a woman wed to an inferior male could privately seduce a superior male and secure his genes for her children. Symons’ theories, while still male-orientated, at least represent a step forward in that he views women as cleverly pursuing their own goals.

  4. Theory produced jointly by a male biologist and a female biologist (Richard Alexander and Katherine Noonan).

  If a man could recognize signs of ovulation, he could use that knowledge to fertilize his wife by copulating with her only while she is ovulating. He could then safely neglect her the rest of the time and go off and philander, secure in the knowledge that the wife he left behind was unreceptive, if not already fertilized. Hence women evolved concealed ovulation to force men into a permanent marriage bond, by exploiting male paranoia about fatherhood. Not knowing the time of ovulation, a man must copulate often with his wife to have a chance of fertilizing her, and that leaves him less time to develop dalliances with other women. The wife benefits, but so does the husband. He gains confidence in his paternity of his children, and he need not worry that his wife will suddenly attract many competing men by turning bright red on a particular day. At last, we have a theory seemingly grounded in sexual equality.

  5. Theory of a female sociobiologist (Sarah Hrdy).

  Hrdy was impressed by the frequency with which many primates – including not only monkeys but also baboons, gorillas, and common chimps – kill infants not their own. The bereaved mother is thereby induced to come into oestrus again and often mates with the murderer, thus increasing his output of progeny. (Such violence has been common in human history: male conquerors kill the vanquished men and children but spare the women.) As a counter-measure, Hrdy reasoned, women evolved concealed ovulation in order to manipulate men by confusing the issue of paternity. A woman who distributed her favours widely would thereby enlist many men to help feed (or at least not to kill) her infant, since many men could suppose themselves to be the infant’s father. Whether this theory is right or wrong, we must applaud Hrdy’s overturning of conventional masculine sexism and transferring sexual power to women.

  6. Theory of another female sociobiologist (Nancy Burley).

  The average 7-pound newborn human weighs double a newborn gorilla, but the 200-pound gorilla mother dwarfs the average human mother. Because the newborn human is so much larger in relation to its mother than are newborn apes, birth is exceptionally painful and dangerous in humans. Until the advent of modern medicine, women often died in childbirth, whereas I have never heard of such a fate befalling a female gorilla or chimpanzee. Once humans had evolved enough intelligence to associate conception with copulation, oestrous women could have chosen to avoid copulating at the time of ovulation, and could have thereby spared themselves the pain and peril of childbirth, but such women would have left fewer descendants than women who could not detect their ovulation. Thus, where male anthropologists saw concealed ovulation as something evolved by women for men (Theories 1 and 2), Nancy Burley sees it as a trick that women evolved to deceive themselves.

  *

  Which of these six theories for the evolution of concealed ovulation is correct? Not only are biologists uncertain; it is only in recent years that the question has begun to receive serious attention. This dilemma exemplifies a pervasive problem in establishing causation in evolutionary biology, as well as in history, psychology, and many other fields where one cannot manipulate variables to perform controlled experiments. Such experiments would afford the most convincing way to demonstrate cause or function. If we could remodel one tribe of people so that all women advertised their day of ovulation, we could then see whether cooperation within or between couples broke down, or whether t
he women used their new knowledge to avoid becoming pregnant. In the absence of such experiments, we can never be certain what human society would really be like today without concealed ovulation.

  If it is hard to determine the function of things happening today under our eyes, how much harder must it be to determine functions in the vanished past! We know that human bones and tools were different hundreds of thousands of years ago, when concealed ovulation may have been evolving. Probably human sexuality, including the function of concealed ovulation, may also have been different then, in ways now hard for us to picture. Interpretation of our past runs the constant risk of degenerating into mere ‘paleopoetry’ stories that we spin today, stimulated by a few bits of fossil bone, and expressing like Rohrschach tests our own personal prejudices, but devoid of any claim to validity about the past.

  Nevertheless, having mentioned six plausible theories, I cannot just walk away from the problem without attempting some synthesis. Here again, we come up against another pervasive problem in establishing causation. It is rare for complex phenomena such as concealed ovulation to be influenced by only a single factor. It would be as silly to seek a single cause of concealed ovulation as to claim that there was a single root cause of the First World War. Instead, there were many independent factors in the period 1900–1914 pushing towards war, others pushing towards peace. War finally broke out when the net weight of factors tipped towards war. Yet that does not excuse going to the opposite extreme of ‘explaining’ complex phenomena by an unweighted laundry list encompassing every conceivable factor.