The Myth of Monogamy: Fidelity and Infidelity in Animals and People (26 page)

WHY DOES MONOGAMY OCCUR AT ALL?
125

female more in resources, territory quality, and so forth, than she would lose if she forgoes his paltry paternal assistance. And so most mammals are not even socially monogamous.

Human beings are a dramatic exception to this generalization. Baby people are more like baby birds than like baby mammals. To be sure, newborn cats and dogs are helpless, but this helplessness doesn't last for long. By contrast, infant
Homo sapiens
remain helpless for months ... and then they become helpless toddlers! Who in turn graduate to being virtually helpless youngsters. (And then? Clueless adolescents.) So there may be some payoff to women in being mated to a monogamous man after all.

It is an interesting proposition that monogamy may have arisen as a male response to sperm competition; that is, as a way for males to minimize the risk that someone else's sperm will fertilize the eggs of a given female. Male rats, for example, prefer the odor of unmated females to that of females that have recently mated with another male. It seems likely that polygynous males are more liable to being cuckolded than are monogamous males, simply because it is harder for a male to keep track of many wives than of just one. This, in turn, could help tip the balance in favor of monogamy or, at least, ostensible monogamy. The argument may seem contradictory, but it is internally consistent: Females, as we have seen, have many reasons to seek EPCs, and, moreover, they have become quite adroit at hiding such behavior from males. Male animals, unlike the fabled sultans of yore, cannot enlist the assistance of eunuchs to guard their harems. Accordingly, it is quite possible that such males find that in the long run their reproductive success is higher if they have only one mate, and keep close tabs on her extracurricular sex life, than if they accumulate many ... each of whom might be unfaithful to him.

This speculation can be carried further, to the possibility that mate-guarding (by either sex, or both) in turn paved the way for the evolution of paternal care. The idea is that if a male remains closely associated with a female, copulating with her until she is no longer fertile, then he has a high level of confidence as to his own paternity and thus is predisposed to help care for the offspring. Moreover, in the case of birds at least, he is likely to be on the scene when the eggs are laid and is therefore available to do his share of the parenting. This is the case among birds because it is most common for one egg to be laid per day and for that egg to be fertilized shortly before it is laid. If a male bird copulates with a female just before she lays her egg, such an egg will probably be carrying his genes. In birds, therefore, there is a payoff to being the last male to copulate, and since one egg is typically produced per day, there is a further payoff to staying around; hence--#

126
THE MYTH OF MONOGAMY

perhaps--monogamy. Among mammals, on the other hand, the benefit of male attentiveness is generally more limited, since estrus is more restricted in time. It therefore pays male mammals to be sexually attentive to a female when she is in heat, but--unlike in the case of male birds, who are in attendance at eg^-laying because they are likely to be have copulated with the female immediately before--there is no particular reason for male mammals to be present when the female is giving birth.

Unlike birds, mammals experience a long delay between copulation and birth, during which time the female is pregnant. It therefore doesn't seem likely that fatherly behavior among male mammals simply results from the fact that they are nearby when "their" female gives birth, as has been argued for birds. (Remember, daddy birds may be present in the avian delivery room simply because they've recently copulated with their female.) At the same time, it seems that when mammals
are
paternal, it is when they have been in attendance not just at the birth of their young but also throughout their mate's estrous; after all, female mammals, unlike insects and birds, lack obvious sperm storage organs. Paternal mammals are likely to be fathers, not cuckolds ... a correlation unlikely to be coincidental.

Often, mammalian monogamy and paternal care depend on the alternatives available. Earlier, we considered those large ground squirrels known as hoary marmots--western, mountain-dwelling relatives of the woodchuck. They show a range of male parenting behavior, from devoted fatherhood to virtual indifference. Local ecology holds the key. Some marmots occupy large open meadows in which there are numerous adult males, many adult females, and a range of juveniles. Under these conditions, males spend much of the early summer gallivanting about in search of additional mating opportunities and also mate-guarding, attempting to thwart the gallivanting of other males. Males in this busy social situation essentially ignore their offspring; they are too taken up with the press of sexual threats and opportunities. On the other hand, some marmots occupy small isolated meadows that can only support what is essentially a single extended family: one male, one or two females, and their offspring. Here, without the social and sexual distractions of other adults, male marmots settle down and become devoted family men, playing with their offspring, warning them of the approach of predators, and so forth. It may be significant that under these more isolated conditions, males are also more likely to be the fathers of those young toward whom they are so solicitous.

In the case of hoary marmots, as for most mammals, it appears that males are
capable
of paternal behavior; it's just that they can often reap a more substantial payoff by interacting with other adults... especially because their mates are guaranteed to lactate and, thus, to provide at least minimal care. Substantial parental involvement is evidently a lower priority, something that happens only by default: "If there are no other females to

WHY DOES MONOGAMY OCCUR AT ALL?
127

solicit, and no other males to worry about," one can almost hear the males announcing to themselves, "then I may as well help take care of the kids."

In contrast to male parenting, which is generally "facultative"--that is, something that may or may not happen--female parenting (especially among mammals) is likely to be obligatory. Even female birds generally get stuck with most of the child care. Among birds known as lapwings, both monogamy and polygyny occur, and yet neither males nor females behave differently from one social situation to the other. Whether monogamous or polygynous, female lapwings still end up bearing the brunt of parental care. Wlien mated polygynously, females end up doing nearly all the incubation, to the extent that they have little time available for feeding themselves. When mated monogamously--so that, presumably, they had the advantage of male assistance with some of the parenting chores-- things are no better!

(Something distressingly similar seems to happen in at least one other species; namely,
Homo sapiens.
Even in supposedly liberated households, women are often expected to do most of the domestic and child-related chores. Even when women work full time, men typically do very little to pick up the slack at home. For a large number of women, vocational effort is simply added to home effort.)

Ecological circumstances seem to loom large in the "decision" whether a species--or a particular individual--is monogamous, polygamous, promiscuous, or anything else. Examples are as diverse and as fascinating as life itself. Here is a small sampling: The birds of paradise, a group of tropical species in which the males sport spectacular plumage--hence their name-- are nearly all polygynous, with males seeking to mate with a relatively large number of females and providing essentially no parental care. However, in a closely related species, the trumpet manucode, males are faithful mates and devoted fathers. The reason? Manucodes eat figs, which are rich in carbohydrates but comparatively poor in protein and fat. In addition, fig trees are relatively rare (at least in the mountains of New Guinea, where these birds were studied) and, moreover, they fruit unpredictably. Two parents are needed, therefore, to bring enough of the low-quality, semidigested fig glop to the nestlings to assure their survival. The result? Manucode monogamy-- not from manucode morality, but fig-forced. Among the other birds of paradise, incidentally, the preferred food is more energy rich, and so females can generally provide enough by themselves, which in turn emancipates the males to go seeking additional sexual partners ... which they do.

One of the attractive things about monogamy is its egalitarianism: one male, one female, everyone equal. After all, polygamy is inherently unequal, regardless of which sex ends up being the harem-keeper. If one male "has" many females (polygyny), there is the implication

128
THE MYTH OF MONOGAMY

that he is somehow "worth" all of them put together and is more valuable and more important than any one of his wives; similarly, if one female "has" many males (polyandry), it seems that the worth and value of each of her husbands is less than that of the one, dominant female. Not so with monogamy, which--whatever its biological difficulties--feels morally right, if only because it is a perfect tie, a 50-50 compromise in which both male and female enjoy equal weighting.

It is also appealing to think that monogamy is a situation of mutual gratification in which the needs of male and female are equally met. This can in fact be true, but a darker, more cynical view can also be justified, one in which monogamy is not so much the result of a beneficent positive-sum game, with balanced winners all around, as of a prolonged conflict of interest in which both males and females lose equally. (Instead of a glass half full, monogamy may thus be a glass half empty.)

The fundamental conflict here is the interest of each sex in confining its mate to only one sexual partner--itself--while at the same time obtaining additional mates, via either polygamy or EPCs. Mate-guarding would therefore be one of many examples of how such conflicts of interest play themselves out. It is most conspicuous on the part of males, each of whom typically seeks to enhance his fitness by reducing his mate's opportunities to engage in EPCs ... contrary to the female's preference. So, as we have seen, females occasionally circumvent mate-guarding, sneaking away for EPCs when possible. When females mate-guard, their goals are similar: to prevent their male from obtaining those additional mates--or matings-- that he would prefer. In this admittedly glum perspective, monogamy is still a success story of sorts: Each sex is equally successful in thwarting the other's desires!

Close and persistent mate-guarding can be costly in other ways--as demonstrated in animals as distinct as dunnocks (birds) and water striders (insects)--interfering with the females' ability to obtain food or avoid predators. Sometimes, as in the water strider case, there are direct energy costs, since guarding males commonly mount the females, who are then obliged to carry their "guardians" on their backs.

The opportunities for conflict seem endless. For example, there may be conflict over resources provided by the male. Among scorpionflies, males generate a salivary mass rich in calories that is transferred to the female during mating; while the female munches, the male mates. The larger the male's nuptial gift, the longer the duration of copulation (simply because it takes the female longer to consume it); and the longer the duration of copulation, the greater a male's success in fertilizing the female's eggs. Also, the larger the male's salivary mass consumed by the female, the greater the size and success of the eggs that the female is able to produce. Not surprisingly, when a male's salivary mass is too small, females seek to end the copulation ...

WHY DOES MONOGAMY OCCUR AT ALL?
129

prematurely, from the male's perspective. At this point, the male scorpionfly is likely to use a specialized anatomical structure, his notal organ, which clasps the female--evidently against her will--and coerces her to continue mating longer than would be in her interest.

The natural world is filled with similar examples of the male-female conflicts that are inherent in sexual reproduction. Among fruit flies, for example, males benefit from repeated matings. The more copulations, especially with additional females, the more offspring. But for females, the situation is quite different. Although a minimum number of matings is necessary if they are to reproduce, matings are costly. In fact, copulation is dangerous to their health: The more a female fruit fly mates, the shorter her life span. This is because, during insemination, males introduce not only sperm but also a sublethal cocktail of chemicals that enhance their own reproductive success, but at a cost to their female partners. These sexual substances induce females to lay eggs more rapidly, diminish their receptivity to other males, and do battle with any sperm already present in the female's reproductive tract. These latter chemicals in particular appear to damage the female and shorten her life span. All this male-male chemical warfare may also reflect yet another devious male strategy: by producing such a nasty brew, they not only compete with prior (and subsequent) males, they also might restrict the eagerness of females to mate yet again with another male, since any who do so will obtain yet another dose of troublesome chemicals. The result is not quite male-imposed female monogamy, but doubtless a female disinclination to be as sexually adventurous as they would otherwise be.

One notable study, conducted by William Rice of the University of California at Davis, sought to tease apart the likely adaptations and counter-adaptations of male and female
Drosophila
by establishing a system in which one sex was, in effect, unilaterally disarmed. Through complex genetic manipulations, male
Drosophila
in a laboratory population were permitted to evolve, but females were prevented from developing counter-adaptations. After 41 generations, the evolving male line was more successful in sperm competition than males from control populations, whereas the nonevolving female line suffered unusually high mortality due to the toxicity of seminal fluid. Under normal conditions, when natural selection acts on females as well as males, the tug-of-war between male adaptations for sperm competition and female counteradaptations evidently results in a more balanced outcome, with each kept in check by the other.