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Chapter One

Monogamy for Beginners

Anthropologist Margaret Mead once suggested that monogamy is the hardest of all human marital arrangements. It is also one of the rarest. Even long-married, faithful couples are new at monogamy, whether they realize it or not. In attempting to maintain a social and sexual bond consisting exclusively of one man and one woman, aspiring monogamists are going against some of the deepest-seated evolutionary inclinations with which biology has endowed most creatures, Homo sapiens included. As we shall see, there is powerful evidence that human beings are not "naturally" monogamous, as well as proof that many animals, once thought to be monogamous, are not. To be sure, human beings can be monogamous (and it is another question altogether whether we should be ), but make no mistake: It is unusual--and difficult.

    As G. K. Chesterton once observed about Christianity, the ideal of monogamy hasn't so much been tried and found wanting; rather, it has been found difficult and often left untried. Or at least, not tried for very long.

    The fault--if fault there be--lies less in society than in ourselves and our biology. Thus, monogamy has been prescribed for most of us by American society and by Western tradition generally; the rules as officially stated are pretty clear. We are supposed to conduct our romantic and sexual lives one-on-one, within the designated matrimonial playing field. But as in soccer or football, sometimes people go out of bounds. And not uncommonly, there is a penalty assessed if the violation is detected by a referee. For many people, monogamy and morality are synonymous. Marriage is the ultimate sanction and departures from marital monogamy are the ultimate interpersonal sin. In the acerbic words of George Bernard Shaw, "Morality consists of suspecting other people of not being legally married."

    Ironically, however, monogamy itself isn't nearly as uncomfortable as are the consequences of straying from it, even, in many cases, if no one finds out. Religious qualms aside, the anguish of personal transgression can be intense (at least in much of the Western world), and those especially imbued with the myth of monogamy often find themselves beset with guilt, doomed like characters from a Puritan cautionary tale to scrub eternally and without avail at their adultery-stained souls, often believing that their transgression is not only unforgivable, but unnatural. For many others--probably the majority--there is regret and guilt aplenty in simply feeling sexual desire for someone other than one's spouse, even if such feelings are never acted upon. When Jesus famously observed that to lust after another is to commit adultery in one's heart, he echoed and reinforced the myth of monogamy--the often-unspoken assertion that even desire-at-a-distance is not only wrong, but a uniquely human sin.

    Whether such inclinations are wrong is a difficult, and perhaps unanswerable, question. But as we shall see, thanks to recent developments in evolutionary biology combined with the latest in technology, there is simply no question whether sexual desire for multiple partners is "natural." It is. Similarly, there is simply no question of monogamy being "natural." It isn't.

    Social conservatives like to point out what they see as a growing threat to "family values." But they don't have the slightest idea how great that threat really is or where it comes from. The monogamous family is very definitely under siege, and not by government, not by a declining moral fiber, and certainly not by some vast homosexual agenda ... but by the dictates of biology itself. Infants have their infancy. And adults? Adultery.

    If, as Ezra Pound once (somewhat self-servingly) observed, artists are the "antennae of the race," these antennae have long been twitching about extramarital affairs. If literature is any reflection of human concerns, then infidelity has been one of humankind's most compelling, long before biologists had anything to say about it. The first great work of Western literature, Homer's Iliad, recounts the consequences of adultery: Helen's face launched a thousand ships and changed the course of history only after it first launched an affair between Helen, a married woman and Greek queen, and Paris, son of King Priam of Troy. Helen proceeded to leave her husband Menelaus, thereby precipitating the Trojan War. And in the Odyssey, we learn of Ulysses' return from that war, whereupon he slays a virtual army of suitors, each of whom was trying to seduce his faithful wife, Penelope. (By contrast, incidentally, Ulysses himself had dallied with Circe the sorceress, but he was not considered an adulterer as a result. The double standard is ancient and by definition unfair; yet it, too, is rooted in biology.)

    It seems that every great literary tradition, at least in the Western world, finds it especially fascinating to explore monogamy's failures: Tolstoy's Anna Karenina, Flaubert's Madame Bovary, Lawrence's Lady Chatterley's Lover, Hawthorne's The Scarlet Letter, Henry James's The Golden Bowl . More recently, John Updike's marriage novels--not to mention scores of soap operas and movies--describe a succession of suburban, middle-class affairs. The present book, by contrast, is not fiction. And it is not concerned with affairs as such, but rather with the biological underpinnings of affairs, in human beings and other animals as well. More precisely, it is about what the latest research has been revealing about the surprisingly weak biological underpinnings of monogamy.

Our approach will be biological, because whatever else human beings may be, we are biological creatures through and through. We eat, we sleep, we feel emotions, we engage in sex, and although we are unique in some regards, so is every other living thing! Rhinos and cobras are uniquely rhinos and cobras in their evolutionary history, their physiology, their anatomy, their behavior, just as human beings are uniquely human. But are we--can we be-- more unique than other creatures? Moreover, it should quickly become apparent that despite the oxymoronic "shared uniqueness" of all living things, there is also a genuine commonality of pattern, especially--for our purposes--a shared susceptibility to certain basic behavioral tendencies. It is taken for granted that we can learn about human digestion, respiration, or metabolism by studying these processes in other animals, making due allowance, of course, for certain unavoidable differences among different species. The same applies for much, although assuredly not all, behavior.

    In this book, we'll be concerned with a range of living things, in part because each is worth understanding in its own right and also because of the light they can shed on ourselves. Don't misunderstand: There will be no claim that because hairy-nosed wombats show a particular sexual pattern, people do, too. Arguments of this sort are absurdly naive, if only because there is such remarkable variety in the animal world. Among so-called lekking species of birds, for example, males gather at a ceremonial plot of ground, with each male defending a small territory; many different females then mate preferentially with one of these males, typically the one occupying the most central "lek" and whose displays are especially intense. (No pair-bond here.) Then there are the pygmy chimps, also known as bonobos, which engage in what seems to be a nonstop sexual free-for-all. Once again, nothing close to monogamy is found ... and these are our closest animal relatives.

    On the other hand, there are cases of lifelong social and sexual partnership that might give pause even to the most committed advocates of intimate, intense, altogether faithful male-female bonding: Not many living things partake, for example, of the extreme monogamy shown by the parasitic flatworm Diplozoon paradoxum, a fish parasite whose partners meet as virgin adolescent larvae, whereupon they literally fuse at their midsections and subsequently become sexually mature; they then remain "together" (in every sense of the word) till death parts them--in some cases, years later.

    The above examples ranged from birds to mammals to invertebrates. And yet it isn't at all clear which is most "relevant" to human beings. If by relevant we mean which one provides a model or--worse yet--a set of rules or some sort of evolutionary premonition as to our "deeper selves," the answer must be: none. But at the same time, each is relevant in its own way. Not only does every animal species cast its unique light on life's possibilities, but each case also helps illuminate a facet of ourselves.

    For most laypersons, there is an understandable bias toward mammals, especially primates. But although the lives of chimpanzees, gorillas, gibbons, and orangutans are fascinating and colorful (especially the highly sexed bonobos, about whom more later), the truth is that when it comes to similarities between their lives and those of human beings, these great apes just aren't that great. Birds--at least, certain species--are far more informative.

    This is because we're not looking for direct historical antecedents, but rather for similarities based on similar circumstances. Among nearly all mammals, including most primates, monogamy just isn't in the picture. Nor is male care of the young. By contrast, although birds aren't nearly as monogamous as once thought, they are at least inclined in that direction. (The same can be said about human beings.) Not only that, but social monogamy--as opposed to genetic monogamy--is strongly correlated with parental involvement on the part of fathers as well as mothers, a situation that is common in birds and quite unusual among mammals, except for that most birdlike of primates, Homo sapiens .

    In this book, we won't be especially focused on mammals (except for ourselves). When it comes to dispelling the myth of monogamy, most of the really useful discoveries in recent years have come from research by ornithologists, who, interestingly enough, have directed much of their attention to those species that are "polygynous" (where the typical mating arrangement is one male and many females) or "polyandrous" (one female and many males). Only recently have they turned their attention to monogamy, only to discover that it is more myth than reality.

    We'll also spend some time with invertebrates, because they include so many different species, each of which is, in a sense, a distinct zoological experiment, whose results we are only now beginning to decipher.

    Certain insects have had an important historical role in helping us appreciate the rarity of monogamy. Thus, some time ago, environmentalists had great hope for a novel technique that promised to eradicate insect pests. The idea was to release large numbers of sterilized males, which would mate with females, who would therefore fail to reproduce. Eventually, no more pests ... and no more pesticides, to boot. But the success of this procedure never extended beyond one species, the screw-worm fly.

    This is what happened. During the 1930s, E. F. Knipling, a forward-looking entomologist with the U.S. Department of Agriculture, may have sensed that "natural" (that is, noninsecticidal) means of controlling unwanted insects would be superior to the widespread use of poisons. In any event, he began exploring a promising technique: Introduce sterilized male screw-worms into nature, whereupon they would mate with wild female screw-worms, whose offspring would fail to materialize. It worked, becoming for a time one of the great success stories of post-Rachel Carson environmentalism. By the 1960s, male screw-worms were being exposed to radioactive cobalt by the vatful, after which insect eunuchs were airdropped over a vast region along the Mexican-U.S. border. This technique succeeded in eliminating the screw-worm scourge. However, such an outcome has never been replicated. As it turns out, Knipling's choice of a target species was fortunate (or scientifically inspired): Female screw-worms--despite their name--are strictly monogamous. By contrast, we now know that for nearly all insects, one screw is not enough: Females commonly mate with more than one male, so even when they are inundated with a blizzard of sterile males, it only takes a small number of intact ones for reproduction to go merrily along. And so the "sterile-male technique," for all its environmental, nonpesticide appeal, has gone nowhere.

    At the same time, the door was opened to a startling insight--namely, that multiple mating is common in nature. And here is the key point: Multiple mating doesn't refer only to the well-known tendency of males to seek numerous sexual partners, but to females, too. Probably the first modern biologist to call attention to this phenomenon, and to recognize its significance, was British behavioral ecologist Geoffrey A. Parker. In 1970, in what can truly be called a seminal paper, Parker wrote of "Sperm Competition and Its Evolutionary Consequences in the Insects." In one stroke, a new idea was born (or, at least, recognized). It is really a simple concept, a direct result, in fact, of multiple mating: Sperm from more than one male will often compete to fertilize a female's eggs. Sperm competition is in no way limited to insects; examples have been found in virtually every animal group ... including human beings.

    Sperm competition is essentially another way of saying nonmonogamy. If a female mates with only one male, then, by definition, no sperm competition occurs. (Except, of course, for the scramble among individual pollywogs within an ejaculate. Although this may be intense, it is nonetheless different from competition among sperm from different males.) Another way of saying this: If females mate with more than one male, sperm competition will ensue. Of course, this depends on the females in question being nonmonogamous, something we can prove by showing that their offspring were sired by more than one male.

    Sperm competition was actually first documented by none other than Charles Darwin, although he did not identify it as such. Indeed, Darwin seems to have carefully refrained from pursuing the matter, perhaps because the question of females mating with more than one male was more than Darwin's social climate could bear. Thus, in The Descent of Man and Selection in Relation to Sex (1871), Darwin described a female domestic goose who produced a mixed brood consisting of some goslings fathered by a domestic goose who was her social partner as well as others evidently fathered by a Chinese goose ... this second male being not only not her mate, but also not even of the same species!

    Darwin's refusal to pursue the question of extra-pair copulations--those occurring outside the ostensibly monogamous pair-bond--may have been more than simply a quaint Victorian fastidiousness. Even today, in our supposedly liberated sexual climate, many people get a bit queasy over the image of sperm from more than one man competing within the vagina and uterus of a single woman. ("Single," that is, as opposed to plural; such a woman may well be married or otherwise paired with an identified male: That is the point.)

    Here is an account of sperm competition, co-authored by the doughty Geoffrey Parker and intended to present the basic points of a simple physical model, known as "constant random displacement with instant sperm mixing."

    Imagine a tank of sperm, representing the fertilization set, which has an input pipe and an outlet pipe. During copulation, sperm flow at a constant rate into the tank through the inlet and out (by displacement) through the outlet. First imagine that the sperm entering the tank do not mix with the sperm already present, which are pushed towards and out from the outlet. The new sperm displace only the old sperm, so that the proportion of sperm from the last male ... rises linearly at a rate equal to the input rate.... But, now suppose that there is swift random mixing of the oncoming sperm with the previous sperm in the tank. At first the sperm displaced from the outlet will be only the old sperm. As the last male's sperm build up in the tank, some of the displaced sperm will be his own ("self-displacement"). By the time most of the sperm in the tank is new, most of the outflow will represent self-displacement.

    Parker's physical model (accompanied with equations, predictions, and supportive data) is entirely sound and logical. At the same time, the very idea of a tankful of sperm is not one likely to make the heart sing! (Why not? I'm not at all sure, but it wouldn't be surprising if most people's disinclination to think deeply and cheerfully about semen or sperm is related to the general disinclination of biologists to think about non-monogamy among animals and, in turn, to the discomfort most of us feel when considering non-monogamy among human beings as well. Not to mention a likely female disinclination to be designated a "tank"!)

    Geoffrey Parker's initial studies of sperm competition employed the "irradiated-male" technique, much like Knipling's more applied research several decades earlier. In Parker's case, the idea was that after subjecting males to radiation, their sperm was damaged, not enough to prevent them from fertilizing eggs but sufficient to interfere with the normal development of any resulting embryo. So, by mating females to irradiated and nonirradiated males, then counting how many eggs were fertilized but didn't develop in each case, it was possible to assign paternity and thus calculate the success of the different males.

    Other techniques quickly followed, notably direct genetic evidence for multiple paternity using "allozymes." This depends on the existence of distinct genetic differences among individuals. In some cases, these differences are well known and readily seen, as with traits such as eye color or hair color in people, the presence or absence of attached earlobes, or the ability or inability to roll one's tongue. For most allozyme-based studies, however, the genetic differences in question are more subtle, analogous to blood types. Knowing, for example, whether a child's blood type is A, B, AB, or O, it is possible to determine whether a given adult could have been the father. (For example, if a child is type O, a man accused in a paternity suit could not be the father if he is type AB.) But it is one thing to prove or disprove the possibility of parentage--to say that someone could or, alternatively, could not be the father--and quite another to say that he definitely is .

    Such certainty is now available. It required the next and most significant breakthrough to date on the way toward disproving the myth of monogamy: the discovery of "DNA fingerprinting," not only for human beings but also animals. Just as each person has a unique fingerprint, each of us has a unique pattern of DNA, so-called minisatellite regions that are "hypervariable," offering a range of possibility that encompasses more than a hundred million different identifying traits, far more than, for example, blood types A, B, AB, or O. As a result, just as each citizen of the United States can be uniquely identified by a personalized Social Security number (so long as we allow enough digits), DNA fingerprinting provides enough genetic specification to guarantee that only one individual will possess a particular pattern.

    Given tissue samples from offspring and adults, we can now specify, with certainty, whether a particular individual is or is not the parent, just as it is possible to specify, with certainty, the donor of any sample of blood, hair, or semen. After subjecting the tissue to appropriate treatments, research technicians end up with a DNA profile that looks remarkably like a supermarket bar code, and with about this level of unique identification. Armed with this technique, field biologists--studying the behavior of free-living animals in nature--have at long last been able to pinpoint parenthood. As a result, the field of "biomolecular behavioral ecology" has really taken off, and with it, our understanding of a difference that may sound trivial but is actually profound: between "social monogamy" and "sexual monogamy."

    Two individuals are socially monogamous if they live together, nest together, forage together, and copulate together. Seeing all this togetherness, biologists not surprisingly used to assume that the animals they studied were also mixing their genes together, that the offspring they reared (usually together) were theirs and theirs alone. But thanks to DNA fingerprinting, we have been learning that it ain't necessarily so. Animals--not unlike people--sometimes fool around, and much more often than had been thought. When it comes to actual reproduction, even bird species long considered the epitome of social monogamy, and thus previously known for their fidelity, are now being revealed as sexual adventurers. Or at least, as sexually non-monogamous.

    Incidentally, it is not easy to obtain the so-called minisatellite DNA profiles needed to assign accurate parentage to animals--or to human beings, for that matter. The actual laboratory techniques are elaborate and detailed. Here is a sample, taken from the "methodology" section of a recent scientific paper describing this latest wedding of genetic insight to animal sexual behavior. We present it here not to provide a cookbook recipe for do-it-yourself DNA analysts, but as a kind of penance, so that when in this or subsequent chapters you encounter an off-hand mention of "DNA fingerprinting," you will pause--if only briefly--and give credit to the sophisticated labor that made such information possible:

    We added 30 µl of 10% SDS and 30 µl of proteinase K and incubated the [blood] sample at 55 degrees C for 3 h. A further 10 µl of proteinase K were then added and the sample returned to 55 degrees C overnight. An extra Tris-buffered Phenol wash was also performed to remove additional proteins present in the tissue. To 20 µl of genomic DNA, we added 4 µl 10 x Buffer (react 2), 2 µl 2 mg/ml BSA, 1 µl 160 nM Spoermidine, 1µl of the restriction enzyme Hae III and 11 µl milli-Q water. This mixture was incubated overnight at 37 degrees C. Another 1 µl of Hae III was added the following day and the sample was incubated at 37 degrees C for a further 1 h. Digested samples were then stored at -20 degrees C. About 5 µg of digested DNA were loaded in each lane of the gel. DNA fragments were resolved on a 0.8% agarose gel (19 x 27 cm) in 1 x TBE running buffer at 55 C for 72 h. We then denatured the DNA by washing each gel for 15 min in 0.25 M HCl and then for 45 min in 0.5 M NaOH, 1.5 M NaCl. Gels were then neutralized by two 15-min washes in 1.5 M NaCl, 0.5 M Tris-HCl pH 7.2, 1mM EDTA. Southern blot techniques were used to transfer DNA from agarose gels to nulon membranes in 6 x SSC. Membranes were then dried for 10 min at 37 degrees C before being baked at 80 degrees C for 2 h.

    Baked membranes were soaked in prehybridization mix (75 ml 0.5 disodium hydrogen orthophosphate pH 7.2.75 ml milli-Q water, 300 µl 0.5 M EDTA pH 8.0, 10.5 g SDS for 2 h at 65 degrees C. First a Jeffrys 33.15 probe was labelled with [a.sup.-32] PdCtp by random priming with Amersham radprime kit. Unincorporated label was removed using a G50 sephadex column. Hybridization of Jeffreys 33.15 to membranes was at 65 degrees C for a minimum of 18 h. Membranes were then washed twice with 5 x SSC, 0.1% SDS at 65 degrees C. DNA fragments hybridized to the 33.15 probe were exposed on X-ray film at either -80 degrees C with one intensifying screen or at room temperature for 1-6 days. After adequate exposure, membranes were stripped and reprobed with CA probe, which was similarly labelled to [a.sup.-32] PdCTP.

    Had enough?

(Continues...)

Copyright © 2001 W. H. Freeman and Company. All rights reserved.