The Myth of Monogamy: Fidelity and Infidelity in Animals and People (24 page)

Guppy males engage in one of two courtship strategies: attempting to persuade females to mate with them by vibrating and bending their colorful bodies (traditional guppy courtship) or attempting to sneak a copulation. With the first strategy, brightly colored males have a definite advantage, being preferred by the females. This seems doubly beneficial for the females, since they not only increase their chance of producing young that are brightly colored because of inheriting their father's sexy genes, but they also avoid parasitized males, who might infect them or their offspring and whose parasitized state may indicate a genetic weakness when it comes to keeping parasites at bay.

Lopez noted, however, that virtually nothing was known about the effect of being parasitized on the behavior of females. So she established populations of virgin guppies, some of whom were parasite-free, and some, infected. Her findings? They are indicated by the title of her research report: "Parasitized Female Guppies Do Not Prefer Showy Males." Beggars, it seems, can't be choosers ... even among guppies. Maybe parasitized females lack the energy to assess several different males and then choose the best one. Or maybe these females recognize that they are, in a sense, "damaged goods" and lower their sights accordingly. It is even possible that their

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behavior is somehow manipulated by their parasites: Bear in mind that parasites have an interest in getting themselves transmitted to new hosts, and unparasitized males may well be somewhat resistant to them, so the guppy parasites may opt for parasitized males as a more vulnerable target. The biological world has seen other outcomes that are at least as devious.

In any event, the result in this case is that females, no less than males, may be limited in their choice of mating partners by factors related to their own desirability. It probably wouldn't be wise to anticipate a glowingly faithful monogamous future for a healthy female mated to a heavily parasitized male or vice versa. But matched pairs--in which male and female are both healthy or both unhealthy--may be destined for (or doomed to) a lifetime of monogamous bliss.

And in her "General Review of the Sex Situation," Dorothy Parker put it this way:

Woman wants monogamy; Man delights in novelty. Love is woman's moon and sun; Man has other forms of fun. Woman lives but in her lord; Count to ten, and man is bored. With this the gist and sum of it,

We now understand that women (females) are not all that monogamous, and that men (males) aren't always polygamous. But we also know that males--because they are sperm-makers rather than egg-makers--are more likely, in general, to seek multiple mating opportunities than are females. It is also generally true that the biological success of a male is more likely to be diminished by his female's EPCs than her success is by EPCs on his part. (This is because males are liable to being cuckolded--reproductively excluded--by their female's extra-pair matings, whereas a female will continue to be the mother of her offspring even if her male copulates with one

llliam James is said to have composed this ditty, although with insights inspired by opium rather than evolutionary biology:

Higamous hogamous, woman monogamous Hogamous higamous, man is polygamous.

What earthly good can come of it?

why does monogamy occur at all?
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or more additional females.) Nonetheless, a male's EPCs can still have consequences for his social mate, and nearly always these consequences are negative. The male may be injured during his gallivanting and thus less able to help with his domestic responsibilities. He may contract a sexually transmitted disease and then infect his mate. He may elect to leave his mate, having discovered a more desirable partner. And--probably the greatest risk, because the most likely--he might find himself devoting time and effort to his lover's offspring, providing benefits that are deducted from his "official" mate and her offspring.

This risk is greater yet in species that are sometimes monogamous, sometimes polygynous--that is, in which males occasionally succeed in transforming an EPC conquest into an additional, full-time reproductive partner. We can therefore expect that in such cases, females will be strongly motivated to keep their males from engaging in EPCs--and even more strongly inclined to prevent their switching from monogamy to polygyny. The end result? Males may seek multiple mates and even polygyny but end up with monogamy because of the intervention of their females, who won't let them bring their girlfriends home.

In a species of lizards common in the Southwest, females defend small territories from which they exclude other females. Males cannot monopolize more than one female because females are so antagonistic to one another that their territories are dispersed.

In most such cases, it appears that females are moved to keep other females at bay when the males have something of value--usually, parental care--to contribute. But sometimes, even when males provide virtually nothing (besides sperm) to their offspring, monogamy remains the most frequent system; for example, among willow ptarmigans, grouse-like residents of mountain and arctic habitats, it seems likely that females are too dispersed to permit bigamy. These animals may also be too aggressive toward each other to accommodate a second female within their domain ... much as the male might want to.

It isn't clear what the "married" female ptarmigan would lose by permitting her husband to have a second wife, since his contribution is essentially nil; probably it isn't a matter of having to share
him,
but, rather, having to share limited food resources with another female and her brood. Similarly, among eastern bluebirds (normally monogamous), males provide little more than a nesting cavity. WTiat generates social monogamy in the bluebird world is the fact that suitable nest-sites are few and far between, and--acting in their own self-interest--female bluebirds won't share them. (It must be pointed out, however, that polygynous females do not always suffer an obvious cost when their male takes another mate; it is possible, that in such cases, males are able to add one or more additional females to

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the myth of monogamy

their harems precisely because doing so imposes no extra cost to existing females. When this is true, the current wives do not seek to interfere.)

In the world of European starlings, breeding occurs in socially monogamous pairs, or in bigamous trios consisting of one male and two females, or occasionally even trigamous quartets of one male and three females. The latter arrangements benefit males but are disadvantageous to females, since multiple-mated males provide less parental care per nest than do their monogamous counterparts. In an experiment, males were given the opportunity to form bigamous or trigamous relationships, or to remain monoga-mously mated to their current female. Males who remained monogamous when they apparently had the opportunity to attract a second or third female were those mated to unusually aggressive females. (This aggression, incidentally, was directed toward the potentially home-wrecking females, not toward the male.) In starlings, at least, female aggression is a reliable predictor of male mating status. So, if you are a male starling with a yen for multiple mates, better choose them from the mild-mannered end of the female spectrum.

In another bird species whose breeding system is all over the marital map, the European dunnock, it appears that female song serves to deter rival females. Just as males sing to attract females and post a vocal "no trespassing" sign to other males, females evidently can inform other females that "this male is taken" ... and not only that, he is taken by a feisty female.

Such feistiness can become lethal. Spanish biologist Jose Veiga studied house sparrows breeding monogamously, yet close to other mated pairs. He wanted to know why 90 percent of them were monogamous. Veiga could eliminate several possible explanations: House sparrow monogamy was not due to the fact that an attentive male is needed for rearing young (biga-mously mated females reared as many offspring). Nor was it due to female reluctance to mate with already-mated males. And it wasn't because there weren't enough unmated, available females. Why then? Because mated females were aggressive toward other females: Moving nestboxes closer together induced females to attack each other. Earlier, Veiga had found that a female house sparrow will sometimes kill the young of another female who is sharing her male's sexual attentions ... shades of the movie
Fatal Attraction.
Given that female house sparrows are willing to carry their sexual rivalry to such extremes, there is evidently a certain proactive, nonviolent wisdom in a healthy degree of female-female repulsion.

A growing number of studies have in fact confirmed that among animals, females are frequently aggressive toward potential "home-wreckers." In Chapter 4, we examined the peculiar phenomenon of egg dumping, whereby females occasionally deposit eggs in another's nest; female-female aggression among birds may often be motivated by anti-dumping watchful-

why does monogamy occur at all?
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ness on the part of mated females. Thus, when a female bird chases other females away, she might well be less concerned that the intruders will attempt to mate with "her" male than that they have already mated with someone and are now seeking--like Horton's nemesis, the infamous Mayzie bird--to dump the offspring in her lap (or rather, nest).

Whatever its origin, it is likely that such female-female alertness gives a boost to monogamy as well, simply by making it difficult for a male to affiliate with more than one female. One might also recall those animals--birds, in particular--for which EPCs often precede divorce. By extension, therefore, it could pay a female to break up any such liaisons, so as to make it less likely that her mate will desert her and set up housekeeping with a new paramour. (It is pretty much taken for granted that male-male aggressive alertness serves in many species to keep social monogamy from becoming polyandry, insofar as, by mate-guarding, males keep "their" females from affiliating--if not EPC-ing--with other males.)

Among mammals, monogamy also seems to be maintained, on occasion, by female-female aggression: There is some tendency among monogamous mammals for the females to be aggressive, especially toward other females. The feistiness of resident female beavers, for example, seems to keep other females away. If Madame Beavery were less aggressive, perhaps the species would be polygynous.

Female vigilance of this sort is evidently common in nonhuman primates, too. Primatologist Barbara Smuts reports that female baboons behave aggressively toward other females that show sexual interest in their consort partner or in which their partner shows sexual interest. There are also many cases in which female mammals--especially among the social canids, including wolves, jackals, and African wild dogs--prevent subordinate females from breeding. A wolf pack, for example, will typically contain only one breeding female, who also, not surprisingly, is socially dominant over the other females. Only if this alpha female is removed will the others copulate and produce pups. As a result, the dominant male of the pack may be
socially
polygynous (that is, he "has" a harem consisting of more than one female) but be kept
reproductively
monogamous by the breeding female's impact on her female rivals.

We have been discussing cases in which monogamy is maintained by female aggression toward other females, thwarting the polygynous inclinations of their mates. It seems only logical that there should also be species in which females impose monogamy by aggressive behavior toward their males when the latter show a hankering for EPCs or--worse yet, from the female's perspective--one or more additional mates. We are only aware of one such case, the burying beetle
Nicrophorus defodiens.
In this monogamous insect, male and female cooperate in the unseemly task of burying a dead animal--

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commonly a mouse--upon which the female will lay her eggs. Having initiated the burying of a carcass, which the female has duly anointed with her fertilized eggs, male beetles are sometimes moved to emit mate attraction chemicals (pheromones). If successful in this maneuver, the male will have lured a second female, who, after copulating with him, would add her eggs to the appealing lump of moldy mouse meat already occupied by the initial female's developing brood. As a result, the freshly hatched maggots of female number two would compete for food with the offspring of female number one, who, after all, got there first, has already "shot her wad" of eggs, and, moreover, has also expended effort in getting the dead mouse prepped to become grub for her own grubs.

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