The Myth of Monogamy: Fidelity and Infidelity in Animals and People (25 page)

So what does the "outraged" female beetle do? As soon as she detects that her mate is beginning to feel frisky and inclined to broadcast his pheromones, she rushes over to him, pushes him off the perch from which he is attempting to broadcast his love potion, and often bites him as well! Not surprisingly, this interferes with his ability to fulfill his polygynous hopes. To demonstrate this, researchers tried tethering number-one females so that they could not reach their pheromone-secreting mates. Thus liberated from their jealous wives, male burying beetles joyously broadcast their sexy scents for prolonged periods--and were rewarded with additional girlfriends.

These more or less direct examples of female-female competition should not blind us to the existence of subtler forms of female-female sexual maneuvering, all of which are also potentially implicated in the maintenance of monogamy.

Thus, jealous females are not limited to outright aggression in their quest to keep their male partners monogamous. Happily married starlings were experimentally presented with an extra nest-site at different distances from their current nest. Among these birds, as among many others, nest-sites are in short supply, so the prospect of two nest-sites is pretty much equivalent to the prospect of exchanging monogamy for bigamy. But when such additional mating opportunities were close to their existing domicile, very few male starlings became polygamous; the farther the new potential love-nests, the more likely that they were employed. In fact, most males became polygynous when there was enough distance between their new lovers and their preexisting mates--but only then. This suggests that what constrains mated males to monogamy is the existence of their present mates, but, by itself, it doesn't explain how a starling wife interferes with her mate's polygynous designs.

There are several ways for a female to get in the way of her mate's efforts at acquiring additional females. One of the most interesting involves her own

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sexuality: A female starling is especially likely to solicit copulations from her mate when he is actively courting other females! There is nothing as likely to make a female starling feel friendly and sexy than the prospect that her mate is showing interest in another female. Equally interesting: A large proportion of these solicitations are refused by her partner, but they nonetheless succeed in causing any prospecting females to depart.

Not surprisingly, however, the male is often less than entranced at such a show of sexual solicitude from his mate. Belgian biologists Marcel Eens and Rianne Pinxten observed 14 instances of male starlings attacking or chasing their females after the ladies had solicited a copulation. Some of these chases were quite vigorous, lasting more than a full minute. In most of them, males had previously landed on another nestbox and were singing, evidently attempting to attract an additional female. By contrast, of ten males who were monogamous and showed every sign of remaining that way, not one was ever observed to attack his female when she solicited a copulation. Why do would-be polygynous males often refuse to copulate? Two likely reasons: First, by doing so, they give away to any potential new mate the fact that they are already mated. Secondly, by copulating with an existing mate, they might so deplete their sperm resources that they would be less likely to fertilize any newcomer.

(It would be interesting to know if anything comparable were true of harems in that peculiar species
Homo sapiens.
It is widely acknowledged that women in human harems competed with one another for resources and benefits, especially those potentially useful to their children. But did they also compete sexually for the erotic attentions of the harem-keeper? If so, then perhaps we should pity the poor, sexually beleaguered sultans, who were likely to have been doubly exhausted, not only because of the simple, numerical demands mandated by their various wives and concubines, but also because of the extra pressure generated if each female--because of her competitive relationship with her co-wives--was especially desirous of his sexual attention.)

Why don't female starlings simply attack would-be rivals? Probably for the same reason that human harem-members are unlikely to do so: It is bad politics, likely to evoke the wrath of the male. In such cases, subtle, seductive tactics are probably more successful. Thus, mate-guarding--of the sort we saw in Chapter 2--is not a males-only tactic. Females sometimes go out of their way to "keep company" with their males, especially when those males are particularly attractive. Among blue tits, for example, attractive males are followed more by their mates than are unattractive males, with "attractive" defined as "those males that receive many visits from neighboring fertile females." Presumably, female blue tits whose mates are unattractive are confident that their males will not be "hit upon" by other

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females; in addition, such females may well be spending some of their free time prospecting for their own EPCs from other, more attractive males!

There is another reason why females occasionally interfere with their mates' EPC endeavors. To some extent, natural selection is a zero-sum game: Success for you means less success for me and vice versa. This is especially true if certain key resources are in short supply: If, for example, an environment can only support a restricted number of youngsters of a given species, then the offspring of female A will do less well in competing with the offspring of female B if B has been inseminated by a high-quality male. Thus, a female mated to such a male could be more successful if his good genes weren't spread around. This is because her own offspring would not have to compete with others who share their high-quality genetic endowment. By mating repeatedly with an especially desirable male, a female could enhance the competitiveness of her own offspring by keeping the high-quality stud functionally depleted of sperm--and thus unlikely to fertilize other females.

It is notable that female mate-guarding--whether it leads to female-female aggression or enhanced sexual solicitation of the male---has been observed among polygynous species but only rarely among socially monogamous ones. This is counterintuitive. It would seem that possible loss of the male's assistance would be a greater blow to a socially monogamous female (who is more likely to rely on her mate's assistance) than to a polygynous one, who presumably is already resigned to sharing her male with others in his harem. Apparently, it is rare for socially monogamous males to follow up an EPC with other behavior that is costly to their mates; by contrast, among polygynous species, males are more likely to help secondary or tertiary females, or even to invite them into the harem.

In any event, the use of sex as a mate-guarding strategy is not limited to birds (or possibly humans). It may occur in lions, where females in heat are known to solicit--and obtain--upwards of 100 copulations per day during a stretch of four or five days! When it comes to copulations, the lion's share is truly impressive. But one must ask "Why bother?" After all, in the case of lions, there is no question of females enforcing monogamy on the males, since lions typically live in prides consisting of many females, sometimes six or more, and it seems unlikely that her reproductive physiology is so inefficient that a healthy lioness must copulate every 10 or 15 minutes for days on end just to get fertilized.

The answer seems to be that the king of the jungle and his descendants must often endure periods when prey is scarce, and at such times, cubs in particular are at great risk of starvation; accordingly, it is at least possible that by making extraordinary sexual demands on the dominant male, a lovelorn lioness makes it unlikely that another female will be fertilized at the

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same time. The likely outcome is that when her cubs are born, they will not have to compete with another litter, born to another female. If so, then natural selection would reward lionesses who are the most sexually demanding, resulting in a kind of serial reproduction: not monogamy, but a system in which even polygynously mated females reproduce one at a time rather than all at once.

The suggestion has been made that multiple mating by females may be tactic of nonhuman primates as well, designed to deprive other females of sperm from their sexual partner. After all, even though sperm are cheap, they are not infinitely replaceable, and even the "studliest" of males may have difficulty producing a constant and undiminished supply. It is even possible that something akin to female-female competition for male sexual attention explains an interesting womanly mystery: menstrual synchrony. It is a well-known fact that when women live together--in dormitories, sororities, rooming houses--their menstrual cycles tend to become synchronized. Young women typically begin the academic year with their periods randomly distributed throughout the calendar, but by finals in May or June, nearly everyone in the same domicile is reaching for tampons on the same days.

It is, as Yul Brynner famously put it in
The King and I,
"a puzzlement." But not an impossible puzzlement. Maybe by "agreeing" to ovulate at the same time, women are revealing an ancient, prehistoric, and adaptive response to primate polygyny, whereby they reduce the ability of one male to monopolize the fertility of many different women. One problem here is that it is difficult to see how this strategy would benefit subordinate females; they would seem to be better off if they refused to play along and didn't synchronize with the cycles of dominant females. But perhaps they have little choice--perhaps their physiology is simply manipulated by the latter. Moreover, even this could ultimately be in their interest, if the offspring of less-dominant females would be subjected to damaging competition when resources were limited and if their birth coincided with that of infants conceived by dominant females.

If such strategizing seems far-fetched, bear in mind once more that it needn't be conscious at all and is no more sophisticated than the astounding "strategies" by which liver cells deactivate toxins or nerve cells conduct impulses. And, in fact, it isn't only among the "higher" vertebrates that females are known to compete by sexually monopolizing a male. Consider the so-called poison-arrow frogs, named because lethal chemicals contained in the skin of brightly colored individuals are used by indigenous rain-forest peoples to envenom their arrows and darts. Among many of these amphibians, males provide most of the parental care, so it is in a female's interest to restrict his sexual attention to herself. In such cases, females often remain

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near their mates, engaging in repetitive courtship behavior, probably to prevent them from mating with other females.

^"""^aring for offspring emerges time after time as a key issue in the main-

tenance of monogamy. Most biologists' ideas about the evolution of

^^/monogamy have long centered around the presumed necessity of male parental care. The idea was that females nearly always prefer monogamy because it gives them--and their offspring--the undivided attention of a caring male. According to this reasoning, polygyny becomes possible when males can be "emancipated" from parenting duties; that is, when females are capable of carrying the whole burden by themselves. (Also, of course, when females aren't too aggressive toward each other... most likely when they don't need their male's help in rearing offspring.)

There is probably more than a grain of truth in this assumption. Thus, even though monogamy is largely a myth, even among birds, it remains true that the avian world is more prone to monogamy than is any other group of animals. Not coincidentally, birds have very rapid metabolisms and nestlings typically must be fed immense quantities of food, sometimes an insect every 15 seconds or so! Given such extraordinary demands, there is an obvious payoff in having two committed adults caring for a brood, so it is understandable that social monogamy is something of an avian specialty.

For the same reason, it is understandable that monogamy is especially rare among mammals, since female mammals are uniquely qualified to nourish their offspring. Male mammals--although not altogether irrelevant--have comparatively little to contribute. When males do provide for their offspring, they must--not surprisingly--be assured of fatherhood; that is, males are likely to behave paternally only when females do not engage in many EPCs. Hence, we find remarkable paternal solicitude in ostensibly monogamous species such as foxes, beavers, and certain nonhuman primates such as the tiny New World marmosets. In some marmoset species, males carry the juveniles almost as much as females do, and they even act as "midwives," assisting at the birth of their offspring, who--not coincidentally--are likely to be really theirs.

The predominant theoretical explanation for polygyny, the "polygyny threshold model," proposes that females elect polygyny when, by doing so, they obtain sufficient additional benefits (food, good nest-sites, protection) to make up for the undiluted parental assistance they would otherwise receive from a monogamous mate. On the other hand, this model was developed with birds in mind, and it remains ornithocentric. When it comes to direct paternal care, male mammals generally have less to contribute than their avian counterparts; a would-be polygynist can frequently offer a