The Myth of Monogamy: Fidelity and Infidelity in Animals and People (3 page)

When asked, men consistently claim to have had more sexual partners than women. As we shall see, it is consistent with evolutionary theory that when it comes to sex, males are comparatively indiscriminate whereas females are likely to be more careful and cautious. But this is only possible if a small number of women make themselves sexually available to a large number of men, because, assuming that every heterosexual encounter involves one man and one woman, the numbers must balance out. There is

10 the myth of monogamy

also strong evidence that men tend to exaggerate their reported number of sexual encounters, while women tend to understate theirs. This discrepancy could result from genuine memory lapses on the part of women and/or unconscious deception (of self and others) by members of both sexes. In addition, social pressures prescribe that having multiple sexual partners (over time, mind you, not necessarily simultaneously) indicates a "real man," whereas being a "real"--that is, virtuous--woman has long been equated with monogamous fidelity. In any event, it is interesting that among many animals, too, females are especially secretive about their extra-pair copulations, whereas males are comparatively brazen... even if they are not inclined to verbal exaggeration.

People (and not just scientists!) have long known that the human species is prone to more than a bit of hypocrisy, saying one thing with regard to fidelity and then--at least on occasion--doing another. But when it comes to the scientific study of animal mating systems, biologists had traditionally assumed that when a species "is" socially monogamous, then it really
is
monogamous; that is, sexually exclusive. No more.

In the movie
Heartburn,
a barely fictionalized account by Nora Ephron of her marriage to the philandering Carl Bernstein, the heroine (played by Meryl Streep) tearfully tells her father about her husband's infidelities, only to be advised, "You want monogamy? Marry a swan." But now, it appears that not even swans are reliably monogamous.

Reports of extra-pair copulations in animals previously thought to be monogamous have come hot and heavy during the last decade or so.' Increasingly, biology journals have featured articles with titles such as "Behavioral, Demographic and Environmental Correlates of Extra-Pair Fertilizations in Eastern Bluebirds," "Multiple Paternity in a Wild Population of Mallards," "Extrapair Copulations in the Mating System of the White Ibis," "DNA Fingerprinting Reveals Multiple Paternity in Families of Great and Blue Tits," "Extrapair Paternity in the Shag, as Determined by DNA Fingerprinting," "Genetic Evidence for Multiple Parentage in Eastern Kingbirds," "Extra-Pair Paternity in the Black-Capped Chickadee," "Density-Dependent Extra-Pair Copulations in the Swallow," "Patterns of Extra-Pair Fertilizations in Bobolinks," and "Extra-Pair Paternity in Monogamous Tree Swallows." We have even had this oxymoronic report: "Promiscuity in Monogamous Colonial Birds."

The situation has reached the point where
failure
to find extra-pair copulations in ostensibly monogamous species--that is, cases in which monogamous species
really
turn out to be monogamous--is itself reportable, leading to the occasional appearance of such reassuring accounts as "DNA Fingerprinting Reveals a Low Incidence of Extra-Pair Fertilizations in the Lesser Kestrel," or "Genetic Evidence for Monogamy in the Cooperatively Breeding Red-Cockaded Woodpecker."

monogamy for beginners 11

Until recently, for a scientific journal to publish a report demonstrating that a "monogamous" species is in fact monogamous would be as silly as for it to publish an account revealing that a particular species of mammal lactates and nurses its young. "Big deal," its readers would say. But now, with the tidal wave of evidence for genetic non-monogamy, any evidence for true monogamy is a big deal indeed, even among those bird species such as eagles and geese that were long seen as paragons of pair-bonding.

The plot thickens: When migrating birds were live-trapped and the cloa-cas of the females rinsed out and examined, at least 25 percent of them were revealed to be already carrying sperm. And this
before
having reached the breeding areas to which they were headed! Evidently, when females--even young ones, in their first reproductive year--arrive at their breeding areas and set up housekeeping with a territorial male, more than a few have already lost their virginity. The likelihood is that such sexual experiences are nonfunctional, or at least nonreproductive, although this remains to be proven, since live sperm can be stored for several days within the genital tract of most birds.

In any event, it is difficult to overstate the conceptual revolution that has followed the discovery that copulations--and, in many cases, fertilizations--often take place outside the social unions that researchers typically identify. After all, reproductive success is the fundamental currency of evolutionary success, and behavioral ecologists and sociobiologists studying red-winged blackbirds, for example, have long been in the habit of evaluating the reproductive success of their male subjects by counting harem size or, better yet, the number of young birds produced by all of a male's "wives." But now comes word that in this polygynous species, too, females don't restrict their mating to the harem-keeper. It turns out that there is no necessary correlation between a male red-winged blackbird's apparent reproductive success (the number of offspring reared on his territory) and his actual reproductive success (the number of offspring he fathered). Similarly, there is no guaranteed correlation between his harem size and his actual reproductive success: A male red-winged blackbird (like a male Turkish sultan) can "have" many wives, which in turn can have many offspring--but those children might not be his.

The pattern is painfully clear: In the animal world generally, and the avian world in particular, there is a whole lot more screwing around than we had thought. (As to the human world, most people have long known that there is a whole lot more of the same than is publicly--or even privately--acknowledged.)

When it comes to mammals, monogamy has long been known as a rarity. Out of 4,000 mammal species, no more than a few dozen form reliable pair-bonds, although in many cases it is hard to characterize them with certainty because the social and sexual lives of mammals tend to be more

12
THE MYTH OF MONOGAMY

furtive than those of birds. Monogamous mammals are most likely to be bats (a few species only), certain canids (especially foxes), a few primates (notably the tiny New World monkeys known as marmosets and tamarins), a handful of mice and rats, several odd-sounding South American rodents (agoutis, pacas, acouchis, maras), the giant otter of South America, the northern beaver, a handful of species of seals, and a couple of small African antelopes (duikers, dik-diks, and klipspringers). A pitiful list.

Even females of seemingly solitary species such as orangutans, gibbons, and black bears have been found to copulate with more than one male; hence, observations of social organization alone clearly can be misleading. Until recently, lacking the appropriate genetic techniques, we had little choice but to define monogamy by the social relationships involved; only with the explosion in DNA fingerprinting technology have we started to examine the genetic connections, those most important to evolution. Thus, according to the highly respected book by David Lack,
Ecological Adaptations for Breeding in Birds,
fully 92 percent of bird species are monogamous. Socially, this figure is still accurate; sexually, it is way off. The highest known frequency of extra-pair copulations are found among the fairy-wrens, lovely tropical creatures technically known as
Malurus spendens
and
Malurus cyaneus.
More than 65 percent of all fairy-wren chicks are fathered by males outside the supposed breeding group. Here is another eye-opener. Warblers and tree swallows are purportedly monogamous, yet when genetic analyses were conducted on six different offspring in each of these species, they were found to have been fathered by five different males!

Although such cases are admittedly extreme, we now know that it is not uncommon for 10 to 40 percent of the offspring in "monogamous" birds to be fathered by an "extra-pair" male; that is, one who isn't the identified social mate of the female in question. (It is much less common for offspring to be "mothered" by an extra-pair female; that is, for an outsider female to slip one of her eggs into the nest of a mated pair. More on this later.)

Given how much we have been learning about non-monogamy and extra-pair matings among animals, and considering the newfound availability of such testing, it is remarkable how rarely genetic paternity tests have been run on human beings. On the other hand, considering the inflammatory potential of the results, as well as, perhaps, a hesitancy to open such a Pandora's box, maybe
Homo sapiens'
reluctance to test themselves for paternity is sapient indeed. Even prior to DNA fingerprinting, blood-group studies in England found the purported father to be the genetic father about 94 percent of the time; this means that for six out of a hundred people, someone other than the man who raised them is the, genetic father. In response to surveys, between 25 percent and 50 percent of U.S. men report having had at least one episode of extramarital sex. The numbers for women

MONOGAMY FOR BEGINNERS
13

are a bit lower--around 30 percent--but still in the same ballpark. Many people already know quite a lot--probably more than they would choose to know--about the painful and disruptive effects of extramarital
sex.
It wouldn't be surprising if a majority would rather not know anything more about its possible genetic consequences, extramarital
fatherhood.
Maybe ignorance is bliss. (If you feel this way, better stop reading here!)

Until quite recently, multiple mating was hidden from biologists. It wasn't so much invisible as unacknowledged, a perfect example of the phenomenon that even in such a seemingly hard-headed pursuit as science, believing is seeing. More to the point, not believing is not seeing. Sexual infidelities among ostensibly monogamous species, when noticed at all by biologists, were generally written off as aberrant, not worth describing, and certainly not suitable for analysis or serious theory. Distasteful as it may have been, Geoffrey Parker's work changed that, along with this important recognition by evolutionary theoretician Robert Trivers. A "mixed strategy" should be favored, as least among males: Maintain a pair-bond with a female, whom you might well assist in rearing offspring, but be ready and available for additional copulations if the opportunity arises. The next step was to ask: What about the female? Is she merely a passive recipient of male attentions, an empty tank to be filled with the sperm of various competing paramours? Or does she choose among the eager male prospects? Might she even actively solicit extra-pair copulations, generating sperm competition among different males? And is it beyond the evolutionary ingenuity of females for them to play hard-to-get
within
their own genital tracts?

| arly work, both empirical research and theorizing, took a decidedly

male-centered perspective on multiple mating, emphasizing how

E
J
males maximize their paternity by being sexually available to more than one female whenever possible, by competing with each other directly (via bluffing, displaying, and fighting) and indirectly (via guarding their mates), and by using an array of anatomical, physiological, and behavioral techniques--such as frequent copulations--to give them an advantage over other males. In his research, David, too, was guilty of this short-sightedness.

More recently, however, biologists have begun to identify how females partake of their own strategies: mating with more than one male, controlling (or, at least, influencing) the outcome of sperm competition, sometimes obtaining direct, personal benefits such as food or protection in return for these extra-pair copulations as well as indirect, genetic benefits that eventually accrue to their offspring. A penchant for non-monogamy among males is no great surprise, but, as we shall see, the most dramatic new findings and revised science brought about by the recent demolition of the myth of monogamy concern the role of
females.
Freud spoke more truth

14 the myth of monogamy

than he knew when he observed that female psychology was essentially a "dark continent." A well-integrated theory of female sexuality in particular still remains to be articulated; perhaps a reader of this book will be suitably inspired.

More on this, too, later. In fact, much more. It is no accident that whereas the male perspective receives one chapter, the female viewpoint gets two. It is something that we are only now beginning to identify and just barely to understand. And as is often the case with new insights, it raises more questions than it answers.

In what follows, we shall try to keep jargon to a minimum. We've already met that deceptively simple term
monogamy,
noting the crucial distinction between social monogamy and sexual monogamy. We've also briefly considered two other mating systems: polygyny (one male mated to many females) and polyandry (one female mated to many males). The derivations of these terms make them easier to remember:
Polygyny
comes from
poly
("many") and
gyny
("female," the same root as "vagina"). So polygyny, the situation of a male harem-keeper, means, in effect, "many vaginas" (or cloacas, in the case of birds). Similarly,
polyandry
comes from
poly
("many") combined with
andry
("male," the same root as "androgen," referring to male sex hormones). So polyandry, which means "many males," is the--much rarer--situation of a female harem-keeper.