The Myth of Monogamy: Fidelity and Infidelity in Animals and People (20 page)

Such a policy is not cheap. If purchased by chimpanzee females, it is at the cost of substantial risks. For example, females are at risk of predation, especially by leopards, while in transit between groups. Since male chimps are larger than females and physically dominant over them, females can be injured, even killed, when approaching a strange troop. In addition, there is potential risk if home-group members (especially males) discover that a female has been mating outside the social unit, although it isn't clear exactly how they would find out, nor has such a discovery ever been documented.

Bear in mind that in addition to their occasional trysts, female chimps also typically immigrate, as adolescents or occasionally as adults, into a troop different from the one in which they were born. It may be that, at such times, their prominent sexual swellings buy chimpanzee females a crucial degree of social acceptance. (It is an interesting fact that newly immigrant females often keep their sexual swellings for an unusually long time, and

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when they have recently changed troops, even pregnant females often produce swellings . . . something that does not normally happen when they are less at risk.) It seems likely that estrous swellings are important "safe-conduct passes" when an adult female encounters strange males.

It'would seem that males from the home troop would be especially sensitive to the absence of females, particularly if such absence correlated with subsequent pregnancy. But at least in the Tai forest, females that mated with neighboring-group males were not absent from their home group any more than were those that mated exclusively within the troop, who occasionally depart for other reasons, including "legitimate" consortships with in-group males. So a female's absence from the group does not yield reliable cues as to whether she has been inseminated by outsiders. This may be quite important, since it is evident that, in other circumstances, chimps are capable of infanticide directed toward offspring obviously sired by outside males.

Hrdy's original suggestion was that females may engage in multiple mating so as to dupe males as to their paternity and thus obtain protection from infanticide. She has since expanded that notion, suggesting that females may also be inclined to mate with the male(s) best able and most likely to
protect their
young. From here, it is not much of a stretch to envision males displaying a degree of benevolent behavior toward a female's existing offspring as a part of their courtship tactics. It is well documented that among many primates living in multi-male troops, females have a mating preference for one particular male, or sometimes two.

University of Michigan primatologist Barbara Smuts has argued that female baboons mate preferentially with males with whom they have already established close "friendships" and that, in return, the females gain protection from aggression by other males toward themselves and their offspring. She reports that 91 percent of the time when a male defended a female or her young children from other baboons, he was the female's friend. Among the tiny rain-forest primates known as cotton-top tamarins, males carry their benevolence toward their sexual partner's existing offspring to great lengths: They often mate while literally holding the adult females' children.

Given that, among primates in particular, adult males are so often a threat to a female's offspring by a different male, it is not surprising that a male is more likely to win his lady-love's heart by showing that he is benevolently disposed toward her present offspring ... or, at least, is unlikely to kill them.

This idea can be expanded further. It appears that females may often choose their EPC partners with an eye toward finding lovers who will not merely refrain from killing their offspring and will defend

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them from other bloody-minded males, but who will also contribute other forms of direct paternal care.

Female barn swallows, for instance, have an opportunity to assess the quality of a male's future parenting: by the type of nest he has built. In this species, nest-building occurs after mating. It appears that effort expended in nest-building serves as a "post-mating male sexual display," whereby males indicate to their females that they are ready and willing to invest in reproduction. It turns out that female barn swallows actually invest more in reproduction when their mates have constructed a large nest. Female barn swallows, you may recall, prefer males with long, deeply forked tails, even though such males provide less paternal care than do their less forked-tail counterparts. So, if you are a male barn swallow, genetically bequeathed a relatively short tail, all is not lost: To some extent, you can make up for it by demonstrating by your assiduous nest-building that you are still worth a female's attention. This is precisely what barn swallows do: Short-tailed males spend more time and effort nest-building than do long-tailed males.

Female appreciation of males that are potentially good parents is not limited, incidentally, to the comparatively brainy birds and mammals: Among fish known as the sand goby, females are known to reject dominant males in favor of those that are good fathers. Male sand gobies do all the parenting. On the other hand, in species with biparental care, a female who succeeds in deceiving her social mate about an EPC with an especially "paternal" male might receive a double dose of child-rearing assistance: from her social mate as well as from her sexual partner--that is, from her deceived "husband" as well as the actual father of her offspring.

We have already seen how in a small European songbird, the dunnock, males provide paternal assistance in proportion as they have copulated with the breeding female. Switching now to the female's perspective, it is entirely possible that a female dunnock doles out copulations to the males in her entourage, thereby leading each to believe that he is the likely father and to respond by behaving parentally--in particular, by providing food for her nestlings and, if need be, by defending them from predators. (This is reminiscent of the fabled grandmother who hugs her many grandchildren, whispering to each, in turn,
"You
are my favorite!")

It might therefore be in the interest of female dunnocks to mate with a large number of different males, so long as each can be similarly deceived. For their part, males, especially if socially dominant, attempt to monopolize the sexual attention of females, thereby maximizing their own reproductive success. As a result, female dunnocks engage in vast amounts of copulatory solicitation--sometimes more than 1,000 copulations per clutch. Not coin-cidentally, male dunnocks also have huge testes.

Another intriguing bit of dunnock lore: As part of precopulatory behavior, the male pecks at the female's cloaca; she responds by ejecting a small

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drop of semen, the remains of her most recent copulation (likely with a different male). Probably she does this to convince her current mating prospect that with his rival's sperm unceremoniously extruded, he has at least a chance of fertilizing some of her eggs.

Such deception is an option especially available to females that are fertilized internally, such as birds and mammals. In these cases, a male can never be certain that he has fathered a female's offspring: "Mommy's babies; Daddy's maybes." So, by permitting or even soliciting copulations, female birds or mammals may essentially dangle the prospect of paternity before gullible males. There are also many species that partake of external fertilization, as in numerous fishes and salamanders. In such cases, eggs and sperm are extruded into the surrounding water, which--despite the greater vulnerability of gametes to that water--at least gives males greater confidence of their paternity.

It is one thing for human fathers to be in the delivery room--and thus, perhaps, more bonded to their children as a result of this innovation--quite another for a male frog or fish to be literally present at the moment of conception, which happens in "public" instead of in the private confines of his mate's reproductive tract. At the same time, external fertilization can challenge females to ensure that their eggs get fertilized at all, especially when there is a strong water current that threatens to dilute their partner's sperm. One species of catfish has evolved a remarkable solution to this problem: Female
Cory dor as aenus
practice a unique form of oral sex: sperm drinking, in which they place their mouth around the lower abdomen of the male. His sperm pass with extraordinary speed as well as digestive immunity through the female's stomach and intestines to emerge from her anus, whereupon they fertilize her eggs in a protected space created when the female curls her body and her pelvic fins.

Among fish and amphibians--in strong contrast to mammals--it is quite common for males to provide parental care. This makes sense when we consider that, in cases of external fertilization, male fish and amphibians commonly guard the eggs from the moment they are extruded from the female's body; thus, they are able to ensure that they are the fathers. Male birds, too, despite being internal fertilizers, often act paternally, although one especially revealing experiment showed how such tendencies are vulnerable to being exploited by savvy females, especially when such females are in need of help. Male pied flycatchers (another species of small songbird) were removed from the nest shortly after their females had laid eggs. These females--suddenly finding themselves potential single mothers--began soliciting copulations from other males, at least some of whom then helped the females rear broods, even though they were not the genetic fathers. Most likely, the males were duped; certainly, they are never observed to assist in the rearing of brpods when they have
not
copulated

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with the mother. The pattern is reminiscent of those female langur monkeys, suddenly presented with a new and potentially infanticidal male, who respond with a seductive pseudo-estrus. Although female pied flycatchers do not have to worry about infanticide, they nonetheless respond to the loss of their "husbands" in a langur-like way: soliciting copulations from other males, some of whom are thereby recruited to assist with the child-rearing.

The sad truth is that sometimes sex can be a chore... especially, it seems, for females, who must cope with males who are not only more ardent but often physically dangerous as well as demanding. It seems reasonable, therefore, that females may occasionally engage in EPCs not. because doing so is in their interest, but because it is simply easier for them to go along than to resist. Such cases fall short of rape but are nonetheless examples of sexual coercion.

For example, if a female bird is sexually accosted while incubating, it is possible that resistance on her part might damage her eggs. Since most male birds lack a penis, they are probably unable to physically force a copulation. But they might nonetheless coerce an EPC by, in effect, threatening to destroy the victim's existing eggs unless she complies. Thus, among some species--including mallard ducks and indigo buntings--when females engage in EPCs but typically do not solicit them, extra-pair copulations may occur simply because the cost of just saying "no" is too great.

There may even be a physical cost to saying "yes." Among white ibis, marsh-dwelling birds with unusually graceful down-curved bills, EPCs are common--and so is theft. Male ibis never contribute nesting material to their extra-pair mates; instead, they often steal such material from them! A researcher of ibis mating behavior observed 164 cases of nesting-material theft. Of these, 82.5 percent occurred immediately after an EPC attempt, with the male intruder--evidently not content with trying to steal a copulation--also stealing from the nest.

Adding to the burden of EPC-ing females is violence, even when the female does not resist: 16 percent of all EPC attempts in this species involve males attacking females, jabbing and battering them with the tips of their bills, sometimes removing feathers and drawing blood. The researcher reports:

Females that were chronically attacked, usually by particular males, would become wary and leave their nests at the approach of any males other than their mates. As a result, their nests were potentially more prone to predation ... and nesting material theft than the nests of unabused females.

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Interestingly, this behavior was not characteristic of EPC-obtaining males generally, but only of certain individuals: Fewer than one-quarter of all males accounted for more than one-half of all such attacks, suggesting that certain males were especially prone to "rough sex" as part of their EPC tactics; it is also noteworthy that females tended to avoid such males. At the same time, it is possible that if these males were not such aggressive brutes, they wouldn't obtain any EPCs at all.

Here is another example of females acquiescing to multiple matings, if not EPCs as such, in order to avoid the hassle of
not
mating with their importunate suitors. Courting male Sierra dome spiders come and squat in the web of nubile females, where they proceed to steal substantial numbers of prey. Only after females finally break down and mate with them do the freeloading males depart! Virtue may be its own reward, but for a beleaguered female Sierra dome spider, an even greater reward comes from giving the importunate males what they want... so they'll get out of her hair or, at least, her web.