Why is Sex Fun?: the evolution of human sexuality

CHAPTER 1. THE ANIMAL WITH THE WEIRDEST SEX LIFE

If your dog had your brain and could speak, and if you asked it what it thought of your sex life, you might be surprised by its response. It would be something like this:

Those disgusting humans have sex any day of the month! Barbara proposes sex even when she knows perfectly well that she isn't fertile-like just after her period. John is eager for sex all the time, without caring whether his efforts could result in a baby or not. But if you want to hear something really gross-Barbara and John kept on having sex while she was pregnant! That's as bad as all the times when John's parents come for a visit, and I can hear them too having sex, although John's mother went through this thing they call menopause years ago. Now she can't have babies anymore, but she still wants sex, and John's father obliges her. What a waste of effort! Here's the weirdest thing of all: Barbara and John, and John's parents, close the bedroom door and have sex in private, instead of doing it in front of their friends like any self-respecting dog!

To understand where your dog is coming from, you need to free yourself from your human-based perspective on what constitutes normal sexual behavior. Increasingly today, we consider it narrow-minded and despicably prejudiced to denigrate those who do not conform to our own standards. Each such form of narrow-mindedness is associated with a despicable “ism”—for instance, racism, sexism, Eurocentrism, and phallocentrism. To that list of modern “ism” sins, defenders of animal rights are now adding the sin of species-ism. Our standards of sexual conduct are especially warped, species-ist, and human-centric because human sexuality is so abnormal by the standards of the world's thirty million other animal species. It's also abnormal by the standards of the world's millions of species of plants, fungi, and microbes, but I'll ignore that broader perspective because I haven't yet worked through my own zoo-centrism. This book confines itself to the insights that we can gain into our sexuality merely by broadening our perspective to encompass other animal species.

As a beginning, let's consider normal sexuality by the standards of the world's approximately 4,300 species of mammals, of which we humans are just one. Most mammals do not live as a nuclear family of a mated adult male and adult female, caring jointly for their offspring. Instead, in many mammal species both adult males and adult females are solitary, at least during the breeding season, and meet only to copulate. Hence, males do not provide paternal care; their sperm is their sole contribution to their offspring and to their temporary mate.

Even most social mammal species, such as lions, wolves, chimpanzees, and many hoofed mammals, are not paired off within the herd/pride/pack/band into male/ female couples. Within such a herd/pride/et cetera, each adult male shows no signs of recognizing specific infants as his offspring by devoting himself to them at the expense of other infants in the herd. Indeed, it is only within the last few years that scientists studying lions, wolves, and chimpanzees have begun to figure out, with the help of DNA testing, which male sired which infant. However, like all generalizations, these admit exceptions. Among the minority of adult male mammals that do offer their offspring paternal care are polygynous male zebras and gorillas with harems of females, male gibbons paired off with females as solitary couples, and saddleback tamarin monkeys, of which two adult males are kept as a harem by one polyan-drous adult female.

Sex in social mammals is generally carried out in public, before the gazes of other members of the troop. For instance, a female Barbary macaque in estrus copulates with every adult male in her troop and makes no effort to conceal each copulation from other males. The best-documented exception to this pattern of public sex is in chimpanzee troops, where an adult male and estrous female may go off by themselves for a few days on what human observers term a “consortship”. However, the same female chimpanzee that has private sex with a consort may also have public sex with other adult male chimpanzees within the same estrus cycle.

Adult females of most mammal species use various means of conspicuously advertising the brief phase of their reproductive cycle when they are ovulating and can be fertilized. The advertisement may be visual (for instance, the area around the vagina turning bright red), olfactory (releasing a distinctive smell), auditory (making noises), or behavioral (crouching in front of an adult male and displaying the vagina). Females solicit sex only during those fertile days, are sexually unattractive or less attractive to males on other days because they lack the arousing signals, and rebuff the advances of any male that is nevertheless interested on other days. Thus, sex is emphatically not just for fun and is rarely divorced from its function of fertilization. This generalization too admits exceptions: sex is flagrantly separated from reproduction in a few species, including bonobos (pygmy chimpanzees) and dolphins.

Finally, the existence of menopause as a regular phenomenon is not well established for most wild mammal populations. By menopause is meant a complete cessation of fertility within a time span that is much briefer than the previous fertile career, and that is followed by an infertile life span of significant length. Instead, wild mammals either are still fertile at the time of death or else exhibit gradually diminishing fertility with advancing age.

Now contrast what I have just said about normal mammalian sexuality with human sexuality. The following human attributes are among those that we take for granted as normal:

1: Most men and women in most human societies end up in a long-term pair relationship (“marriage”) that other members of the society recognize as a contract involving mutual obligations. The couple has sex repeatedly, and mainly or exclusively with each other.

2: In addition to being a sexual union, marriage is a partnership for joint rearing of the resulting babies. In particular, human males as well as females commonly provide parental care.

3: Despite forming a couple (or occasionally a harem), a husband and wife (or wives) do not live (like gibbons) as a solitary couple in an exclusive territory that they defend against other couples, but instead they live embedded in a society of other couples with whom they cooperate economically and share access to communal territory.

4: Marriage partners usually have sex in private, rather than being indifferent to the presence of other humans.

5: Human ovulation is concealed rather than advertised. That is, women's brief period of fertility around the time of ovulation is difficult to detect for their potential sex partners as well as for most women themselves. A woman's sexual receptivity extends beyond the time of fertility to encompass most or all of the menstrual cycle. Hence, most human copulations occur at a time unsuitable for conception. That is, human sex is mostly for fun, not for insemination.

6: All women who live past the age of forty or fifty undergo menopause, a complete shutdown of fertility. Men in general do not undergo menopause: while individual men may develop fertility problems at any age, there is no age-clumping of infertility or universal shutdown.

Norms imply violation of norms: we call something a “norm” merely because it is more frequent than its opposite (the “violation of the norm”). That's as true for human sexual norms as for other norms. Readers of the last two pages will surely have been thinking of exceptions to the supposed generalizations that I have been describing, but they still stand as generalizations. For example, even in societies that recognize monogamy by law or custom there is much extramarital and premarital sex, and much sex that is not part of a long-term relationship. Humans do engage in one-night stands. On the other hand, most humans also engage in many-year or many-decade stands, whereas tigers and orangutans engage in nothing except one-night stands. The genetically based paternity tests developed over the last half-century have shown that the majority of American, British, and Italian babies are indeed sired by the husband (or steady boyfriend) of the baby's mother.

Readers may also bristle at hearing human societies described as monogamous; the term “harem,” which zoologists apply to zebras and gorillas, is taken from the Arabic word for a human institution. Yes, many humans practice sequential monogamy. Yes, polygyny (long-term simultaneous unions between one man and multiple wives) is legal in some countries today, and polyandry (long-term simultaneous unions between one woman and multiple husbands) is legal in a few societies. In fact, polygyny was accepted in the great majority of traditional human societies before the rise of state institutions. However, even in officially polygynous societies most men have only one wife at a time, and only especially wealthy men can acquire and maintain a few wives simultaneously. The large harems that spring to mind at the mention of the word polygamy, such as those of recent Arabian and Indian royalty, are possible only in the state-level societies that arose very late in human evolution and that permitted a few men to concentrate great wealth. Hence the generalization stands: most adults in most human societies are at any given moment involved in a long-term pair bond that is often monogamous in practice as well as legally.

Still another cause for bristling may have been my description of human marriage as a partnership for the joint rearing of the resulting babies. Most children receive more parental care from their mothers than from their fathers. Unwed mothers form a significant proportion of the adult population in some modern societies, though it has been much harder for unwed mothers to rear children successfully in traditional societies. But the generalization again holds: most human children receive some parental care from their father, in the form of child care, teaching, protection, and provision of food, housing, and money.

All these features of human sexuality-long-term sexual pnrtnerships, coparenting, proximity to the sexual partnerships of others, private sex, concealed ovulation, extended female receptivity, sex for fun, and female menopause— constitute what we humans assume is normal sexuality. It titillates, amuses, or disgusts us to read of the sexual habits of elephant seals, marsupial mice, or orangutans, whose lives are so different from ours. Their lives seem to us bizarre. But that proves to be a species-ist interpretation. By the standards of the world's 4,300 other species of mammals, and even by the standards of our own closest relatives, the great apes (the chimpanzee, bonobo, gorilla, and orangutan), we are the ones who are bizarre.

However, I am still being worse than zoo-centric. I am falling into the even narrower trap of mammalo-centrism. Do we become more normal when judged by the standards of nonmammalian animals? Other animals do exhibit a wider range of sexual and social systems than do mammals alone. Whereas the young of most mammal species receive maternal care but no paternal care, the reverse is true for some species of birds, frogs, and fish in which the father is the sole caretaker for his offspring. The male is a parasitic appendage fused to the female's body in some species of deep-sea fish; he is eaten by the female immediately after copulation in some species of spiders and insects. While humans and most other mammal species breed repeatedly, salmon, octopus, and many other animal species practice what is termed big-bang reproduction, or semelparity: a single reproductive effort, followed by preprogrammed death. The mating system of some species of birds, frogs, fish, and insects (as well as some bats and antelope) resembles a singles bar-at a traditional site, termed a “lek,” many males maintain stations and compete for the attention of visiting females, each of which chooses a mate (often the same preferred male chosen by many other females), copulates with him, and then goes off to rear the resulting offspring without his assistance.

Among other animal species, it is possible to point out some whose sexuality resembles ours in particular respects. Most European and North American bird species form pair bonds that last for at least one breeding season (in some cases for life), and the father as well as the mother cares for the young. While most such bird species differ from us in that pairs occupy mutually exclusive territories, most species of sea birds resemble us further in that mated pairs breed colonially in close proximity to each other. However, all these bird species differ from us in that ovula-tion is advertised, female receptivity and the sex act are mostly confined to the fertile period around ovulation, sex is not recreational, and economic cooperation between pairs is slight or nonexistent. Bonobos (pygmy chimpanzees) resemble or approach us in many of these latter respects: female receptivity is extended through several weeks of the estrus cycle, sex is mainly recreational, and there is some economic cooperation between many members of the band. However, bonobos still lack our pair-bonded couples, our well-concealed ovulation, and our paternal recognition of and care for offspring. Most or all of these species differ from us in lacking a well-defined female menopause.

Thus, even a non-mammalo-centric view reinforces our dog's interpretation: we are the ones who are bizarre. We marvel at what seems to us the weird behavior of peacocks and big-bang marsupial mice, but those species actually fall securely within the range of animal variation, and in fact we are the weirdest of them all. Species-ist zoologists theorize about why hammer-headed fruit bats evolved their lek mating system, yet the mating system that cries out for explanation is our own. Why did we evolve to be so different?

This question becomes even more acute when we compare ourselves with our closest relatives among the world's mammal species, the great apes (as distinguished from the gibbons or little apes). Closest of all are Africa's chimpanzee and bonobo, from which we differ in only about 1.6 percent of our nuclear genetic material (DNA). Nearly as close are the gorilla (2.3 percent genetic difference from us) and the orangutan of Southeast Asia (3.6 percent different). Our ancestors diverged “only” about seven million years ago from the ancestors of chimpanzees and bonobos, nine million years ago from the ancestors of gorillas, and fourteen million years ago from the ancestors of orangutans.

That sounds like an enormous amount of time in comparison to an individual human lifetime, but it's a mere eye-blink on the evolutionary time scale. Life has existed on Earth for more than three billion years, and hard-shelled, complex large animals exploded in diversity more than half a billion years ago. Within that relatively short period during which our ancestors and the ancestors of our great ape relatives have been evolving separately, we have diverged in only a few significant respects and to a modest degree, even though some of those modest differences— especially our upright posture and larger brains-have had enormous consequences for our behavioral differences.

Along with posture and brain size, sexuality completes the trinity of the decisive respects in which the ancestors of humans and great apes diverged. Orangutans are often solitary, males and females associate just to copulate, and males provide no paternal care; a gorilla male gathers a harem of a few females, with each of which he has sex at intervals of several years (after the female weans her most recent offspring and resumes menstrual cycling and before she becomes pregnant again); and chimpanzees and bonobos live in troops with no lasting male-female pair bonds or specific father-offspring bonds. It is clear how our large brain and upright posture played a decisive role in what is termed our humanity-in the fact that we now use language, read books, watch TV, buy or grow most of our food, occupy all continents and oceans, keep members of our own and other species in cages, and are exterminating most other animal and plant species, while the great apes still speechlessly gather wild fruit in the jungle, occupy small ranges in the Old World tropics, cage no animal, and threaten the existence of no other species. What role did our weird sexuality play in our achieving these hallmarks of humanity?

Could our sexual distinctiveness be related to our other distinctions from the great apes? In addition to (and probably ultimately as a product of) our upright posture and large brains, those distinctions include our relative hair-lessness, dependence on tools, command of fire, and development of language, art, and writing. If any of these distinctions predisposed us toward evolving our sexual distinctions, the links are certainly unclear. For example, it is not obvious why our loss of body hair should have made recreational sex more appealing, nor why our command of fire should have favored menopause. Instead, I shall argue the reverse: recreational sex and menopause were as important for our development of fire, language, art, and writing as were our upright posture and large brains.

The key to understanding human sexuality is to recognize that it is a problem in evolutionary biology. When Darwin recognized the phenomenon of biological evolution in his great book On the Origin of Species, most of his evidence was drawn from anatomy. He inferred that most plant and animal structures evolve-that is, they tend to change from generation to generation. He also inferred that the major force behind evolutionary change is natural selection. By that term, Darwin meant that plants and animals vary in their anatomical adaptations, that certain adaptations enable individuals bearing them to survive and reproduce more successfully than other individuals, and that those particular adaptations therefore increase in frequency in a population from generation to generation. Later biologists showed that Darwin's reasoning about anatomy also applies to physiology and biochemistry: an animal's or plant's physiological and biochemical characteristics also adapt it to certain lifestyles and evolve in response to environmental conditions.

More recently, evolutionary biologists have shown that animal social systems also evolve and adapt. Even among closely related animal species, some are solitary, others live in small groups, and still others live in large groups. But social behavior has consequences for survival and reproduction. Depending, for example, on whether a species' food supply is clumped or spread out, and on whether a species faces high risk of attack by predators, either solitary living or group living may be better for promoting survival and reproduction.

Similar considerations apply to sexuality. Some sexual characteristics may be more advantageous for survival and reproduction than others, depending on each species' food supply, exposure to predators, and other biological characteristics. At this point I shall mention just one example, a behavior that at first seems diametrically opposed to evolutionary logic: sexual cannibalism. The male of some species of spiders and mantises is routinely eaten by his mate just after or even while he is copulating with her. This cannibalism clearly involves the male's consent, because the male of these species approaches the female, makes no attempt to escape, and may even bend his head and thorax toward the female's mouth so that she may munch her way through most of his body while his abdomen remains to complete the job of injecting sperm into her.

If one thinks of natural selection as the maximization of survival, such cannibalistic suicide makes no sense. Actually, natural selection maximizes the transmission of genes, and survival is in most cases just one strategy that provides repeated opportunities to transmit genes. Suppose that opportunities to transmit genes arise unpre-dictably and infrequently, and that the number of offspring produced by such opportunities increases with the female's nutritional condition. That's the case for some species of spiders and mantises living at low population densities. A male is lucky to encounter a female at all, and such luck is unlikely to strike twice. The male's best strategy is to produce as many offspring bearing his genes as possible out of his lucky find. The larger a female's nutritional reserves, the more calories and protein she has available to transform into eggs. If the male departed after mating, he would probably not find another female and his continued survival would thus be useless. Instead, by encouraging the female to eat him, he enables her to produce more eggs bearing his genes. In addition, a female spider whose mouth is distracted by munching a male's body allows copulation with the male's genitalia to proceed for a longer time, resulting in more sperm transferred and more eggs fertilized. The male spider's evolutionary logic is impeccable and seems bizarre to us only because other aspects of human biology make sexual cannibalism disadvantageous. Most men have more than one lifetime opportunity to copulate; even well-nourished women usually give birth to only a single baby at a time, or at most twins; and a woman could not consume enough of a man's body at one sitting to improve significantly the nutritional basis for her pregnancy.

This example illustrates the dependence of evolved sexual strategies on both ecological parameters and the parameters of a species' biology, both of which vary among species. Sexual cannibalism in spiders and mantises is favored by the ecological variables of low population densities and low encounter rates, and by the biological variables of a female's capacity to digest relatively large meals and to increase her egg output considerably when well nourished. Ecological parameters can change overnight if an individual colonizes a new type of habitat, but the colonizing individual carries with it a baggage of inherited biological attributes that can change only slowly, through natural selection. Hence it is not enough to consider a species' habitat and lifestyle, design on paper a set of sexual characteristics that would be well matched to that habitat and lifestyle, and then be surprised that those supposedly optimal sexual characteristics do not evolve. Instead, sexual evolution is severely constrained by inherited commitments and prior evolutionary history.

For example, in most fish species a female lays eggs and a male fertilizes those eggs outside the female's body, but in all placental mammal species and marsupials a female gives birth to live young rather than to eggs, and all mammal species practice internal fertilization (male sperm injected into the female's body). Live birth and internal fertilization involve so many biological adaptations and so many genes that all placental mammals and marsupials have been firmly committed to those attributes for tens of millions of years. As we shall see, these inherited commitments help explain why there is no mammal species in which parental care is provided solely by the male, even in habitats where mammals live alongside fish and frog species whose males are the sole providers of parental care.

We can thus redefine the problem posed by our strange sexuality. Within the last seven million years, our sexual anatomy diverged somewhat, our sexual physiology further, and our sexual behavior even more, from those of our closest relatives, the chimpanzees. Those divergences must reflect a divergence between humans and chimpanzees in environment and lifestyle. But those divergences were also limited by inherited constraints. What were the lifestyle changes and inherited constraints that molded the evolution of our weird sexuality?