Sex and the Female Agenda

Most female mammals are anything but subtle when it comes to telling males it's time for sex. Not humans. For good evolutionary reasons, women have found it's much better to keep men in the dark.

By Jared Diamond|Wednesday, September 01, 1993
Scene One: A dimly lit bedroom; a handsome man lies in bed. A beautiful young woman, in nightgown, enters. A diamond wedding ring flashes virtuously on her left hand; her right clutches a small blue strip of paper. She bends, kissing the man’s ear.

She: Darling! It’s time!

Scene Two: Same bedroom, same couple, making love; details obscured by dim lighting. Camera shifts to a calendar being flipped by a graceful hand wearing the same diamond wedding ring.

Scene Three: Same couple, blissfully holding smiling baby.

He: Darling! I’m so glad Ovu-stick told us when it was exactly the right time!

Last Frame: Close-up of same graceful hand, clutching same small blue strip of paper. Caption reads: Ovu-stick. Home urine test to detect ovulation.

If baboons could understand our TV ads, they’d find that one especially hilarious. Neither a male nor a female baboon needs a hormonal test kit to detect the female’s ovulation, the sole time when her ovary releases an egg and she can be fertilized. Instead, the skin around the female’s vagina swells and turns bright pink. She gives off a distinctive smell. And in case a dumb male still misses the point, she also crouches in front of him and presents her hindquarters. Most other female animals are similar, advertising ovulation with equally bold visual signals, odors, or behaviors.

We consider female baboons with bright pink hindquarters an oddity. In fact, though, we humans are the odd ones--our scarcely detectable ovulations make us members of a small minority in the mammalian world. Granted, quite a few other primates--the group of mammals that includes monkeys, apes, and us--also conceal their ovulations. However, even among primates, baboon-style advertisement remains the majority practice. Human males, in contrast, have no means of detecting when their partners can be fertilized; nor did the women themselves until modern, scientific times.

We’re also unusual in our continuous practice of sex, which is a direct consequence of our concealed ovulations. Most other animals confine sex to a brief period of estrus around the advertised time of ovulation. At estrus, a female baboon emerges from a month of sexual abstinence to copulate up to 100 times. A female Barbary macaque does it on an average of every 17 minutes, distributing her favors at least once to every adult male in her troop. Monogamous gibbon couples go several years without sex, until the female weans her most recent infant and comes into estrus again. The gibbons relapse into abstinence as soon as the female becomes pregnant.

We humans, though, practice sex on any day of the month. Hence most human copulations involve women who are unable to conceive at that moment. Not only do we have sex at the wrong time of the cycle, but we continue to have sex during pregnancy and after menopause, when we know for sure that fertilization is impossible.

Human sex does seem a monumental waste of effort from a biological point of view. After all, most other animals are sensibly stingy of copulatory effort, and for a simple reason--sex is expensive. Just count the ways: for males, sperm production is metabolically costly, so much so that mutant worms with few sperm live longer than normal sperm- producing worms. Sex takes time that could otherwise be devoted to finding food. During the sex act itself, couples locked in embrace risk being surprised and killed by a predator or enemy. Finally, fights between males competing for a female often result in serious injury to the female as well as to the males.

So why don’t human females behave the way most other animals do and give clear ovulatory signals that would let us restrict sex to moments when it could do us some good?

By now, you may have decided that I’m a prime example of an ivory-tower scientist searching unnecessarily for problems to explain. I can hear several million of you protesting, There’s no problem to explain, except why Jared Diamond is such an idiot. You don’t understand why we have sex all the time? Because it’s fun, of course! Unfortunately, that answer isn’t enough to satisfy scientists. Humans’ concealed ovulations and unceasing receptivity must have evolved for good reasons, and ones that go beyond fun. While engaged in sex, animals, too, look as if they’re having fun, to judge by their intense involvement. And with respect to Homo sapiens, the species unique in its self-consciousness, it’s especially paradoxical that a female as smart and aware as a human should be unconscious of her own ovulation, when female animals as dumb as cows are aware of it.

In speculating about the reasons for our concealed ovulations, scientists tend to focus their attention on another of our unusual features: the helpless condition of our infants, which makes lots of parental care necessary for many years. The young of most mammals start to get their own food as soon as they’re weaned and become fully independent soon afterward. Hence most female mammals can and do rear their young without any assistance from the father, whom the mother never sees again after copulation. For humans, though, most food is acquired by means of complex technologies far beyond the dexterity or mental ability of a toddler. As a result, our children have to have food brought to them for over a decade after weaning, and that job is much easier for two parents than for one. Even today, it’s hard for a single human mother to rear kids unassisted. It was undoubtedly much harder for our prehistoric ancestors.

Consider the dilemma facing an ovulating cavewoman who has just been fertilized. In many other mammal species, the male would promptly go off in search of another ovulating female. For the cavewoman, though, that would seriously jeopardize her child’s survival. She’s much better off if that man sticks around. But what can she do? Her brilliant solution: remain sexually receptive all the time! Keep him satisfied by copulating whenever he wants! In that way, he’ll hang around, have no need to look for new sex partners, and will even share his daily hunting bag of meat.

That in essence is the theory that was formerly popular among anthropologists--among male anthropologists, anyway. Alas for that theory, there are numerous male animals that require no such sexual bribes to induce them to remain with their mate and offspring. I already mentioned that gibbons, seeming paragons of monogamous devotion, go years without sex. Male songbirds cooperate assiduously with their mates in feeding the nestlings, although sex ceases after fertilization. Even male gorillas with a harem of several females get only a few sexual opportunities each year because their mates are usually nursing or out of estrus. Clearly, these females don’t have to offer the sop of constant sex.

But there’s a crucial difference between our human couples and those abstinent couples of other animal species. Gibbons, most songbirds, and gorillas live dispersed over the landscape, with each couple or harem occupying its separate territory. That means few encounters with potential extramarital sex partners. Perhaps the most distinctive feature of traditional human society is that it consists of mated couples living within large groups of other couples, with whom we have to cooperate. A father and mother must work together for years to rear their helpless children, despite being frequently tempted by other fertile adults nearby. The specter of marital disruption by extramarital sex, with its potentially disastrous consequences for parental cooperation in child-rearing, is pervasive in human societies. Somehow we evolved concealed ovulation and constant receptivity to make possible our unique combination of marriage, co-parenting, and adulterous temptation. How does that combination work?

More than a dozen new theories have emerged as possible explanations. From this plethora of possibilities, two--the father-at-home theory and the many-fathers theory--have survived as most plausible. Yet they are virtually opposite.

The father-at-home theory was developed by University of Michigan biologist Richard Alexander and graduate student Katharine Noonan. To understand it, imagine what married life would be like if women did advertise their ovulations, like female baboons with bright pink derrieres. A husband would infallibly recognize the day on which his wife was ovulating. On that day he would stay home and assiduously make love, in order to fertilize her and pass on his genes. On all other days he would realize from his wife’s pallid derriere that lovemaking with her was useless. He would instead wander off in search of other, unguarded pink- hued ladies so he could pass on even more of his genes. He’d feel secure in leaving his wife at home because he’d know she wasn’t sexually receptive to men and couldn’t be fertilized anyway.

The results of those advertised ovulations would be awful. Fathers wouldn’t be at home to help rear the kids, mothers couldn’t do the job unassisted, and babies would die in droves. That would be bad for both mothers and fathers because neither would succeed in propagating their genes.

Now let’s picture the reverse scenario, in which a husband has no clue to his wife’s fertile days. He then has to stay at home and make love with her on as many days of the month as possible if he wants to have much chance of fertilizing her. Another motive for him to stay around is to guard her against other men, since she might prove to be fertile on any day he’s away. Besides, now he has less reason to wander, since he has no way of identifying when other women are fertile. The heartwarming outcome: fathers hang around and share baby care, and babies survive. That’s good for both mothers and fathers, who have now succeeded in transmitting their genes. In effect, both gain: the woman, by recruiting an active co-parent; the man, because he acquires confidence that the kid he is helping to rear really carries his genes.

Competing with the father-at-home theory is the many-fathers theory, developed by anthropologist Sarah Hrdy of the University of California at Davis. Anthropologists have long recognized that infanticide used to be common in many human societies. Until field studies by Hrdy and others, though, zoologists had no appreciation for how often it occurs among other animals as well. Infanticide is especially likely to be committed by males against infants of females with whom they have never copulated--for example, by intruding males that have supplanted resident males and acquired their harem. The usurper knows that the infants killed are not his own. (Of course, animals don’t carry out such subtle reasoning consciously; they evolved to behave that way instinctively.) The species in which infanticide has been documented now include our closest animal relatives, chimpanzees and gorillas, in addition to a wide range of other species from lions to African hunting dogs.

Naturally, infanticide horrifies us. But on reflection, one can see that the murderer gains a grisly genetic advantage. A female is unlikely to ovulate as long as she is nursing an infant. By killing the infant, the murderous intruder terminates the mother’s lactation and stimulates her to resume estrous cycles. In most cases, the murderer proceeds to fertilize the bereaved mother, who then bears an infant carrying the murderer’s own genes.

Infanticide is a serious evolutionary problem for these animal mothers, who lose their genetic investment in their murdered offspring. This problem would appear to be exacerbated if the female has only a brief, conspicuously advertised estrus. A dominant male could easily monopolize her during that time. All other males would consequently know that the resulting infant was sired by their rival, and they’d have no compunctions about killing the infant.

Suppose, though, that the female has concealed ovulations and constant sexual receptivity. She can exploit these advantages to copulate with many males--even if she has to do it sneakily, when her consort isn’t looking. (Hrdy, by the way, argues that the human female’s capacity for repeated orgasms may have evolved to provide her with further motivation to do so.)

According to Hrdy’s scenario, no male can be confident of his paternity, but many males recognize that they might have sired the mother’s infant. If such a male later succeeds in driving out the mother’s consort and taking her over, he avoids killing her infant because it could be his own. He might even help the infant with protection and other forms of paternal care. The mother’s concealed ovulation will also serve to decrease fighting between males within her own troop, because any single copulation is unlikely to result in conception and hence is no longer worth fighting over.

In short, where Alexander and Noonan view concealed ovulation as clarifying paternity and reinforcing monogamy, Hrdy sees it as confusing paternity and effectively undoing monogamy. Which theory is correct?

To find the answer, we turn to the comparative method, a technique often used by evolutionary biologists. By comparing primate species, we can learn which mating habits are shared by those species with concealed ovulation but absent from those with advertised ovulation. As we shall see, the reproductive biology of each species represents the outcome of an experiment, performed by nature, on the benefits and drawbacks of concealing ovulation.

This comparison was recently conducted by Swedish biologists Birgitta Sillén-Tullberg and Anders Møller. First they tabulated the visible signs of ovulation for 68 species of higher primates (monkeys and apes). They found that some species, including baboons and our close relatives the chimpanzees, advertise ovulation conspicuously. Others, including our close relative the gorilla, exhibit slight signs. But nearly half resemble humans in lacking visible signs. Those species include vervets, marmosets, and spider monkeys, as well as one ape, the orangutan. Thus, while concealed ovulation is still exceptional among mammals in general, it nevertheless occurs in a significant minority of higher primates.

Next, the same 68 species were categorized according to their mating system. Some, including marmosets and gibbons, turn out to be monogamous. More, such as gorillas, have harems of females controlled by a single adult male. Humans are represented in both categories, with some societies being routinely monogamous and others having female harems. But most higher primate species, including chimpanzees, have a promiscuous system in which females routinely associate and copulate with multiple males.

Sillén-Tullberg and Møller then examined whether there was any tendency for more or less conspicuous ovulations to be associated with some particular mating system. Based on a naive reading of our two competing theories, concealed ovulation should be a feature of monogamous species if the father-at-home theory is correct, but of promiscuous species if the many-fathers theory holds. In fact, almost all monogamous primate species analyzed prove to have concealed ovulation. Not a single monogamous primate species has boldly advertised ovulations, which instead are mostly confined to promiscuous species. That seems to be strong support for the father-at- home theory.

But the fit of predictions to theory is only a half-fit, because the reverse correlations don’t hold up. Yes, most monogamous species have concealed ovulation, yet perpetually pallid derrieres are in turn no guarantee of monogamy. Out of 32 species that hide their ovulations, 22 aren’t monogamous but promiscuous or live in harems. So regardless of what caused concealed ovulation to evolve in the first place, it can evidently be maintained under varied mating systems.

Similarly, while most species with boldly advertised ovulations are promiscuous, promiscuity doesn’t require flashing a bright pink behind once a month. In fact, most promiscuous primates either have concealed ovulation or only slight signs. Harem-holding species can have any type of ovulatory signal: invisible, slightly visible, or conspicuous.

These complexities warn us that concealed ovulation will prove to serve different functions according to the particular mating system with which it coexists. To identify these changes of function, Sillén-Tullberg and Møller got the bright idea of studying the family tree of living primate species. Their underlying rationale was that some modern species that are very closely related, and thus presumably derived from a recent common ancestor, differ in mating system or in strength of ovulatory signals. This implies recent evolutionary changes, and the two researchers hoped to identify the points where those changes had taken place.

Here’s an example of how the reasoning works. Comparisons of DNA show that humans, chimps, and gorillas are still about 98 percent genetically identical. Measurements of how rapidly such gene changes accumulate, plus discoveries of dated ape and protohuman fossils, show that humans, chimps, and gorillas all stem from an ancestral missing link that lived around 9 million years ago. Yet those three modern descendants now exhibit all three types of ovulatory signal: concealed ovulation in humans, slight signals in gorillas, bold advertisement in chimps. This means that only one of those three descendants can be like the missing link, and the other two must have evolved different signals.

A strong hint of the problem’s resolution is that many living species of primitive primates--creatures like tarsiers and lemurs--have slight signs of ovulation. The simplest interpretation, then, is that the missing link inherited slight signs from a primitive ancestor, and that gorillas in turn inherited their slight signs unchanged from the missing link. Within the last 9 million years, though, humans must have lost even those slight signs to develop our present concealed ovulation, while chimps, in contrast, went on to evolve bolder signs.

Identical reasoning can be applied to other branches of the primate family tree, to infer the ovulatory signals of other now-vanished ancestors and the subsequent changes in their descendants. As it turns out, signal switching has been rampant in primate history. There have been several independent origins of bold advertisement (including the example in chimps); many independent origins of concealed ovulation (including humans and orangutans); and several reappearances of slight signs of ovulation, either from concealed ovulation (as in some howler monkeys) or from bold advertisement (as in many macaques).

All right, so that’s how we can deduce past changes in ovulatory signals. When we now turn our attention to mating systems, we can use exactly the same procedure. Again, we discover that humans and chimps evolved in opposite directions, just as they did in their ovulatory signals. Studies of living primitive primate behavior suggest that ancestral primates of 60 million years ago mated promiscuously, and that our missing link of 9 million years ago had already switched to single-male harems. Yet if we look at humans, chimps, and gorillas as they are today, we find all three types of mating system represented. Thus, while gorillas may just have retained the harems of their missing link ancestor, chimps must have reinvented promiscuity and humans invented monogamy.

Overall, it appears that monogamy has evolved independently many times in higher primates: in us, in gibbons, and in numerous groups of monkeys. Harems also seem to have evolved many times, including in the missing link. Chimps and a few monkeys apparently reinvented promiscuity, after their recent ancestors had given up promiscuity for harems.

Thus Sillén-Tullberg and Møller have reconstructed both the type of mating system and the ovulatory signal that probably coexisted in numerous primates of the remote past. Now, finally, we can put all this information together to examine what the mating system was at each of the points in our family tree when concealed ovulation evolved.

Here’s what one learns. In considering those ancestral species that did have ovulatory signals and that went on to lose those signals and evolve concealed ovulation, only one was monogamous. The rest of them were promiscuous or harem-holding--one species being the human ancestor that arose from the harem-holding missing link. We thus conclude that promiscuity or harems, not monogamy, are the mating systems associated with concealed ovulation. This conclusion is as predicted by Hrdy’s many-fathers theory. It doesn’t agree with the father-at-home theory.

But we can also ask the reverse question: What were the ovulatory signals prevailing at each point in our family tree when monogamy evolved? We find that monogamy never evolved in species with bold advertisement of ovulation. Instead, monogamy has usually arisen in species that already had concealed ovulation, and sometimes in species that had slight ovulatory signals. This conclusion agrees with predictions of Alexander and Noonan’s father-at-home theory.

How can these two apparently opposite conclusions be reconciled? Recall that Sillén-Tullberg and Møller found that almost all monogamous primates today have concealed ovulation. That result must have arisen in two steps. First, concealed ovulation arose, in a promiscuous or harem- holding species. Then, with concealed ovulation already present, the species switched to monogamy.

Perhaps, by now, you’re finding our sexual history confusing. We started out with an apparently simple question deserving a simple answer: Why do we hide our ovulations and have sex on any day of the month? Instead of a simple answer, you’re being told that the answer is more complex and involves two steps.

What it boils down to is that concealed ovulation has repeatedly changed and actually reversed its function during primate evolutionary history. That is, both the father-at-home and the many-fathers explanations are valid, but they operated at different times in our evolutionary history. Concealed ovulation arose at a time when our ancestors were still promiscuous or living in harems. At such times, it let the ancestral woman distribute her sexual favors to many males, none of whom could swear that he was the father of her baby but each of whom knew that he might be. As a result, none of those potentially murderous males wanted to harm the baby, and some may actually have protected or helped feed it. Once the woman had evolved concealed ovulation for that purpose, she then used it to pick a good man, to entice or force him to stay at home with her, and to get him to provide lots of help for her baby.

On reflection, we shouldn’t be surprised at this shift of function. Such shifts are very common in evolutionary biology. Natural selection doesn’t proceed in a straight line toward a distant perceived goal, in the way that an engineer consciously designs a new product. Instead, some feature that serves one function in an animal begins to serve some other function as well, gets modified as a result, and may even lose the original function. The consequence is frequent reinventions of similar adaptations, and frequent losses, shifts, or even reversals of function as living things evolve.

One of the most familiar examples involves vertebrate limbs. The fins of ancestral fishes, used for swimming, evolved into the legs of ancestral reptiles, birds, and mammals, used for running or hopping on land. The front legs of certain ancestral mammals and reptile-birds then evolved into the wings of bats and modern birds respectively, to be used for flying. Bird wings and mammal legs then evolved independently into the flippers of penguins and whales respectively, thereby reverting to a swimming function and effectively reinventing the fins of fish. At least two groups of fish descendants independently lost their limbs, to become snakes and legless lizards. In essentially the same way, features of reproductive biology--such as concealed ovulation, boldly advertised ovulation, monogamy, harems, and promiscuity--have repeatedly changed function and been transmuted, reinvented, or lost.

Think of all this the next time you are having sex for fun. Chances are it will be at a nonfertile time of the ovulatory cycle and while you’re enjoying the security of a lasting monogamous relationship. At such a time, reflect on how your bliss is made paradoxically possible by precisely those features of your physiology that distinguished your remote ancestors, condemned to harems or promiscuity. Ironically, those wretched ancestors had sex only on rare days of ovulation, when they discharged the biological imperative to fertilize, robbed of leisurely pleasure by their desperate need for swift results.
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