The Myth of Monogamy: Fidelity and Infidelity in Animals and People (18 page)

But at the same time, females would be ill advised to carry this too far. Fussy is fine, but those who set the bar so high that no male could succeed in fertilizing their eggs would be strongly selected against, outcompeted by those whose expectations are more modest and realistic. Therefore, even the most well-defended egg-bearers are likely to be penetrated eventually--and when they are, it is likely to be by the most well-endowed males, possibly with a little help from the females themselves.

We might call it the Atalanta solution, after the Greek story of Atalanta and Hippomenes. According to master myth-recounter Thomas Bulfinch, Atalanta was as fleet-footed as she was lovely, and quite a catch in more ways than one:

To all suitors (for she had many) she imposed a condition which was generally effectual in relieving her of their persecutions--"I will be the prize of him who shall conquer me in a race; but death must be the penalty of all who try and fail." In spite of this hard condition some would try. Hippomenes was to be judge of the race. "Can it be possible that any will be so rash as to risk so much for a wife?" said he. But when he saw her lay aside her robe for the race, he changed his mind, and said, "Pardon me, youths, I knew not the prize you were competing for." As he surveyed them he wished them all to be beaten and swelled with envy of any one that seemed at all likely to win. While such were his thoughts, the virgin darted forward. As she ran she looked more beautiful than ever. The breezes seemed to give wings to her feet; her hair flew over her shoulders. ... All her competitors were distanced, and were put to death without mercy. Hippomenes, not daunted by this result, fixing his eyes on the virgin, said, "Why boast of beating those laggards? I offer myself for the contest."

Atalanta looked at him with a pitying countenance, and hardly knew whether she would rather conquer him or not. "What god can tempt one so young and handsome to throw himself away? Ipity him, not for his beauty (yet he is beautiful), but for his youth. I wish he would give up the race, or if he will be so mad, I hope he may outrun me."

Hippomenes could not outrun Atalanta, but he got some help from Venus. The goddess of love obligingly provided Hippomenes with three

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golden apples, which, at strategic points during the race, he threw down. And Atalanta, equally obliging, stopped to pick them up. As a result, Hippomenes won the race--and Atalanta.

n this chapter, we have sampled part of the female perspective on extra-pair copulations, concentrating on the EPC partner's genes. Next, we continue our female focus, turning to some other considerations.

CHAPTER FOUR

Undermining the Myth: Females (Other Considerations)

'/^ eek simplicity," advised Alfred North Whitehead, "and then distrust it." In the previous chapter, we sought to understand why females engage in EPCs by looking simply at female choice of male genes. (In the process, we found that even this "one" explanation is a far cry from simplicity, connected as it is to matters of fertilization, health, diversity, dominance, desirability, "sexy sons," and sperm competition--the latter perhaps engineered by females.) Now we turn to other factors, each of which appears to offer the seductive Siren call of simplicity, although in reality each is complex and subtly entwined with many others. Such understanding is a consummation devoutly to be sought. .. and then, perhaps, distrusted.

Wlien done by males, EPCs are indeed interesting but, in a sense, unremarkable, since they are a logical, "simple" extension of the expected male sexual strategy: Given what it means to be male (i.e., a producer of comparatively cheap, easily replaced sperm), we can expect males, even if already mated, to be "fast and loose," and undeterred even if their extra-pair partner is also already mated. If males are successful in garnering additional copulations, and if these copulations are with fertile females, they generate their own evolutionary reward, because any gene-influenced tendency to engage in EPCs will be promoted into the next generation. In short, an EPC is likely to be a male success or, more precisely, a success for the EPC-inclined genes residing within such males.

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At the same time, from the perspective of the female involved--and assuming said female gains in the process--a departure from monogamy is just as validly a female strategy. Females, no less than males, have much to gain from EPCs. Biologists, too, have much to gain by acknowledging this, and recently they have begun to do so. There has been, in fact, a substantial change in focus on the part of many biologists, and the result has been a more nuanced and accurate sense of how living things go about their lives. Instead of limiting themselves to the male's perspective and identifying animal social systems as polygyny, monogamy, or monogamy plus adultery ("mixed male strategies"), researchers are talking more these days about polyandry: one female mating with many males, regardless of the apparent social system.

In the past, the word
polyandry
was restricted to those exceedingly rare cases in which a single female is simultaneously bonded to more than one male. But, increasingly, we see that a domestic system that is ostensibly monogamous (one male/one female) or even polygynous (one male/many females) may be genetically polyandrous, with the female mating with more than one male, regardless of what the social system appears to be.

At the risk of overdosing on terminology, it is time to employ a new term, increasingly used by biologists:
monandrous
(literally "one male"), to be distinguished from
polyandrous
("many males"). It has the virtue of introducing--finally--a female-centered perspective into the study of mating systems. Using the word
polygynous,
for example, to describe the sexual life of a harem-forming species may be useful in presenting the perspective of the male:
Polygynous
means many females, and a successful polygynous male gets to mate with many females. But what about the females' viewpoint? Calling them
polygynous
implies that they are limited to mating with one male, the harem-keeper. In fact, we used to think that polygyny
meant
multiple mating for the male, single mating for the females. But not any longer. Polygynously mated females can be faithful to the one harem-keeper, in which case they are also
monandrous
("one male"). But now we know that even in harem-dwelling species, females sometimes have additional EPCs with outside males, in which case they are polyandrous as well as polygynously mated.

So, it is useful to employ some new words, reflecting our new understanding.
Monandrous
("one male") means that a female mates with just one male. Thus, a socially monogamous female may also be monandrous, in which case her sexual life matches her social life--she mates only with one male. Or she might combine social monogamy with genetic polyandry, having EPCs with more than one male. Similarly, a polygynous (harem-dwelling) female may be monandrous--mating only with one male, presumably the harem-keeper--or she might be both polygynous and polyan-

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drous--socially part of one male's harem but likely to be involved sexually with one or more additional males, via EPCs.

Note to Lord Whitehead: It is one thing to seek simplicity, quite another to find it. (Distrusting the results is yet another matter!)

Why do females copulate so frequently? After all, it seems clear that females don't have to be inseminated very often just to get their eggs fertilized. Since eggs are much larger than sperm, they are necessarily produced in much smaller numbers. Just a handful of matings should therefore suffice. In a now-classic and much-cited study published in 1948, geneticist A. J. Bateman placed a limited number of male and female fruit flies in small containers and then observed their sexual behavior as well as the reproductive outcome. Obviously, zero copulations resulted in zero reproduction, for either sex. And the breeding payoff of a single copulation was pretty much the same for males and females (although not identical, since a female's breeding success nearly always jumped ahead with her first mating, whereas a male's sometimes didn't, if he copulated with an already-fertilized female).

One of Bateman's most influential findings was that beyond the initial mating, the reproductive success of males increased substantially with additional copulations, whereas that of females did not. Or rather, it increased much more slowly and reached the point of diminishing returns more rapidly. This is because a female's eggs, once successfully fertilized, cannot be fertilized any more, whereas a male can--at least in theory--fertilize additional females each time, until there are no more candidates.

But, in fact, females of many different species copulate many times, more than seems necessary to get their eggs fertilized. Most of the time, this apparent sexual excess takes place with the same male and within the identified social unit; that is, they are IPCs rather than EPCs. But as we shall see, EPCs may nonetheless be implicated.

Kestrels (sparrow hawks) copulate nearly 700 times per clutch. Female lions copulate on average every 15 minutes--day and night--throughout their frenetic, four-day estrous cycle. Generally, when such high mating frequencies are found, it is the female who is the initiator. Indian crested porcupines copulate every day throughout their estrus, pregnancy, and lactation, although in this species females are fertile for only slightly more than 1 percent of their estrus (and not at all when pregnant or lactating).

The traditional explanation for such behavior has long been that nonre-productive sex of this sort helps to maintain or enhance the pair-bond (as in at least one species,
Homo sapiens).
This seems eminently reasonable, but not sufficient. It is simple and, as such, worthy of distrust. Why does a high

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frequency of copulations enhance the pair-bond ... assuming that it does so? On an immediate, "proximate" level, we might conclude that frequent matings generate sexual satisfaction and that this is reason enough. But why should females be wired to be "satisfied" in this way, especially if such behavior is not needed for fertilization?

One possibility--potentially disconnected from the question of EPCs-- is mate assessment. Since it takes time and energy for a male to copulate, a female could assess a male's vigor and health by his sexual ability and inclination. Repeated matings also seem important in pair-formation. Newly-wed kittiwake gulls copulate more often than old married couples, a phenomenon to which nearly all human beings can also attest. Although male sexual inadequacy is occasionally cited by women as the reason for seeking a divorce, there are remarkably few animal parallels, that is, cases in which a female abandons her mate when he reveals himself to be sexually unen-thusiastic, inadequate, or just plain uninspiring. There are also few animal examples of what might be called the "Lady Chatterley option," after D. H. Lawrence's novel in which the wife of the paraplegic Lord Chatter-ley, erotically frustrated by her husband's incapacity, has a series of EPCs with her virile gamekeeper. Lady Chatterley is pictured as aroused and downright awe-struck by her lover's erect penis, although this may tell us more about Lawrence's erotic imaginings than about the realities of female sexual psychology.

On the other hand, something similar may be common in the natural word, motivated not so much by a mate's shortcomings as a lover as by his inadequacy as an inseminator: As we have seen, females of several species have been known to respond to their mate's diminished fertility by engaging in EPCs with other, more reproductively competent males. Sexual performance as such could be used by females as a secondary sexual characteristic analogous to the "sexy son hypothesis": A sexually voracious female kestrel, lion, or Indian porcupine may thus be more a tactician than a nymphomaniac, substituting her mate's sexual enthusiasm and capacity for what in other species is provided by an irresistibly dark throat patch, bright feathers, or impressively forked tail.

In the above cases, EPCs lurk in the background, an option for females if their males should fail their sexual exams. In others, EPCs may be more directly responsible. Females might well copulate repeatedly with a preferred mate so as to swamp sperm already received--for example, via a forced copulation--from a less valued male. Even if not rape victims, females may occasionally acquiesce in EPCs because giving in is less costly than resisting (more on this later). In such cases, a female may then attempt to rectify her situation (i.e., inseminated by a less-desirable male) by repeatedly copulating with a preferred one--who also happens to be her mate.

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Or maybe females seek to ensure fertilization by a preferred male after having recently copulated with one or more other males whose genes they may esteem less but who, in return for being granted EPCs by the female, provide other benefits such as additional courtship feeding, the opportunity to forage on their territory, the promise of parental assistance for any young produced, and so on. High in-pair copulation frequency may also be a female's way of preventing polygyny or of keeping her male from partaking of his own EPCs.