The Myth of Monogamy: Fidelity and Infidelity in Animals and People (10 page)

What is a penis for? Ask a young boy and you get an unequivocal answer: peeing. (Girls, who manage quite well without one, have good reason to disagree.) So, what is a penis really for? Ask an adult and you'll probably be told that it is for introducing male reproductive products into the female. Once upon a time, long, long ago--when the myth of monogamy still reigned--nearly all biologists would have agreed. But no longer.

Don't misunderstand: The penis
is
for introducing male reproductive products into the female, but that isn't all that it does. Since we now understand that females of many, probably most, species are likely to mate with more than one male, the corresponding likelihood is that these males are not simply adapted to transferring sperm ... even lots of sperm. If you are the second, third, or fourth male to mate with a female, your long-term reproductive interest would be served not only by being able to introduce sperm efficiently and in adequate amounts, but also by being able to remove any rival's previous deposit. In many animals (especially insects), the penis is not merely a pipeline for delivering sperm; it is also variously a scraper, gouger, reamer, corkscrew--a veritable Swiss Army Knife of gadgets and gizmos adapted to removing the sperm of any preceding male.

In the black-winged damselfly, a common streamside insect of the eastern United States, females commonly mate with more than one male. Each male black-winged damselfly sports a specialized penis outfitted with lateral horns and spines, not unlike a scrub brush. Copulating males use their penis

44
THE MYTH OF MONOGAMY

to clean out from 90 to 100 percent of their predecessors' sperm before depositing their own. Some male sharks give their sexual partners a kind of precoital douche, courtesy of a remarkable double-barreled penis. One barrel contains a specialized tube that can act as a high-pressure saltwater hose, sluicing away any sperm deposited by a sexual rival; the other barrel transports sperm into the female. Male pygmy octopuses apparently can detect whether a female with whom they are mating has already copulated, because they spend more time coupling with already-mated lady octopuses: They spend the extra time using a specialized tentacle to scoop out sperm deposited by their predecessors.

We have already described how in most insects, females store transferred sperm in a special organ, a spermatic receptacle, bursa copulatrix, or sper-matheca. Then, as an egg passes along its own conduit, the female contracts special spermathecal musculature, forcing out sperm that fertilize it. Not surprisingly, males of some insect species take advantage of this arrangement: Rather than removing a rival's sperm directly, they induce the female to do it. Prior to mating, they employ specialized genital structures to stimulate the female's sperm-ejection system, so that their spermathecae contract, ejecting previously stored sperm but in the absence of any eggs.

Don't miss the forest for the trees: This is not simply a recitation of Barash's "Believe It or Not" compendium of sexual oddities. These examples all reflect the powerful action of evolution, conveying an advantage to males who are capable of overcoming their rivals' sperm. Males have stumbled onto other techniques for giving their sperm an advantage in the reproductive fray. For example, a small European bird called the dunnock mates occasionally in pairs, and sometimes in threesomes, of both sorts: two males and one female, and two females and one male. (For a drab-looking bird, the unprepossessing dunnock is a bit of a swinger.) When it's two dunnock males and one female, the males typically peck the female's cloaca before copulating with her; in response, she squeezes out a few drops of her other husband's sperm. The more time a female dunnock has spent with one male, the greater the number of precopulatory cloacal pecks delivered by the other one.

Finally, there is traumatic insemination. The best-known examples are found among bedbugs; the males simply pierce the body of their mate/ victim, injecting sperm that then travel through the blood, collecting in the gonads and achieving fertilization. But this is "merely" a way of inseminating females, not sperm competition per se (unless the sperm of two of more males battle it out within a female's bloodstream, something that has not-- yet--been demonstrated). There is, however, at least one bizarre example of males using traumatic insemination against each other; it involves a male

undermining the myth: males 45

hijacking another's reproductive efforts, achieving sperm competition with a vengeance. There exist bugs that live on bats that inhabit caves. Among these aptly named cave bat bugs, males attack other males, injecting sperm as well as seminal fluid directly into the victim's body cavity, which is pierced by the attacker's sharp penis. The male recipients metabolize the seminal fluid, thereby gaining some calories from the transaction. But some surviving sperm also migrate to the recipient's testes. If and when the victim copulates with a female cave bat bug, he will therefore transfer some of the sperm of his attacker, who gets paternity by proxy.

By this point, it should be clear that males work awfully hard to obtain EPCs and, similarly, to prevent rival males from getting any at their expense. For animals, at least, the underlying reason for all this mate-guarding, gallivanting, and sperm competition is the proverbial bottom line: not financial profit, but an evolutionary bonus in the form of reproductive success. A male's reproductive success is gravely threatened if his mate has an EPC or--worse yet--an EPF (extra-pair fertilization). To put it bluntly, there is no payoff to rearing someone else's offspring.

What options are open to a male who has been cuckolded? Not very many, and all carry substantial liabilities. They include:

1. Physical aggression: Punish your mate and/or the interloping male. This makes a certain intuitive sense but is unlikely to convey much evolutionary benefit, except possibly, if it makes either party less likely to transgress again in the future. It also risks physical injury as well as disrupting the current mateship.

2. Force a prompt copulation with your mate, in the interest of sperm competition. This, too, might weaken the pair-bond.

3. Provide less paternal care, possibly even neglecting or abusing any succeeding offspring. This might backfire as well, especially if some of those disadvantaged youngsters include your own.

4. Desert your mate altogether. This only makes sense if alternative mates are available. Not surprisingly, adultery is frequently cited among human beings as the reason for a divorce. It may surprise some readers--although at this point, perhaps not very many!--that divorce also occurs among animals and that here, too, it is closely associated with EPCs, especially on the part of the female.

46 the myth of monogamy

Among the above options, number 3 seems especially prevalent: When males have indications that their mates have been unfaithful, they seem particularly unlikely to act as devoted fathers. We expect that males who follow a "hit-and-run" strategy, contributing sperm but little else to their offspring, would be considerably less troubled if their mates engage in EPCs. Or, at least, since they are not otherwise inclined to be devoted fathers, departures from monogamy on the part of their sexual partners are unlikely to have much effect on the males' behavior. But ostensible monogamy is a different matter. In these cases, males typically give a lot-- parental care, plus typically forgoing large numbers of their own EPCs-- and, not surprisingly, they expect to get a lot, or, at minimum, to "get" to rear their own progeny.

True to expectation, male barn swallows are less attentive in feeding chicks if their mates had previously engaged in EPCs. Among indigo buntings, yearling males are approximately twice as likely as older males to be cuckolded by their mates; significantly, only rarely do these younger males help out in rearing chicks. These findings make perfect biological sense. After all, it is unheard of, and indeed almost unimaginable, for adults to dispense parental care randomly with regard to genetic relationship. Try to imagine a society--animal'or human--in which perfect strangers care for the young, essentially at random. Such an arrangement has never been found for any living things. To be sure, there are many species in which males contribute little or no paternal care, but when they do act paternally, then they, no less than females, direct their attention to particular mates, particular nests, and particular offspring: their own. The next step is to withhold some or all of that attention when there is a good chance that the offspring in question are someone else's. (This doesn't require any special intellectual insight on their part; any genetically mediated tendency to provide care indiscriminately would quickly be replaced by alternative tendencies to direct care to one's own offspring ... which, because they are one's offspring, are likely to possess the genes for such tendencies, which would therefore be given a boost.)

As already noted, monogamy--even social monogamy--is rare among mammals. It is noteworthy, however, that it is essentially only in cases of monogamy that male mammals provide
any
paternal care; after all, even with the danger of EPCs, a monogamous male mammal has much more confidence of his paternity than one whose sexual partner is likely to have been inseminated by one or more other males. And so we find comparatively devoted fathers among foxes, coyotes, beavers, gibbons, and marmosets, species in which the females are by and large sexually faithful to just one male. And we find very little paternal behavior in woodchucks, porcu-

undermining the myth: males 47

pines, squirrels, deer, wildebeests, cougars, or bears. In proportion as fatherhood is in doubt, paternal behavior is likely to be lacking.

At other times, the prospect of parenthood seems capable of generating parent-like behavior, masquerading for a time as disinterested altruism. The emergence of EPCs as a major fact of life has even diluted the impact of another revolution in modern biological theory, known as "kin selection." Numerous perplexing cases have been recorded in which young adults serve as "helpers at the nest," assisting others to reproduce rather than rearing their own offspring. With our recent appreciation of EPCs, a new wrinkle has emerged in interpreting such seemingly altruistic behavior. Even "helper" males may actually be helping themselves... to occasional sex: with the breeding female. So-called cooperative breeding may therefore involve less altruism than had recently been thought, since, in at least some cases, what looks like altruistic baby-sitting is actually full-fledged parental investment, provided to offspring of the helpers themselves, some of whom were conceived via circumspect EPCs.

And yet, confidence of relatedness doesn't explain all aspects of parenting. For example, an experiment looked at the paternal behavior of male common gobies; these are small marine fish, the males of which guard eggs left them by a female. The goal of the experiment was to assess whether male common gobies treat their offspring differently depending on whether they had spawned alone (with a female but no other male) or with a second male present, in which case there was at least a chance that some of the eggs and fry were fathered by the interloper. It turned out that it didn't matter whether a second male had been present.

The gobies are not alone. It is not invariant that paternal care varies with confidence of paternity; there are some notable exceptions, not only among fish but among birds as well. What are we to make of these exceptions? (Make no mistake: Exceptions they are.) If they were the rule, then we'd have to reassess some basic evolutionary and genetic principles. As exceptions, they provide us with the opportunity to fine-tune our predictions.

In the case of occasional paternal care by nonpaternal animals, other factors appear to be at work. For example, if EPCs don't usually occur in a given species, then, lacking the context, there would be little or no evolutionary pressure selecting for a male's ability to detect his likely nonpaternity and to react accordingly. Natural selection can only generate a response if, in the past, situations have arisen that cause individuals responding in one way to be more successful than individuals responding in other ways. By the same token, we lack the ability to hear ultra-high-frequency sounds because such sounds have not been part of the relevant landscape in which our ancestors evolved; the same is not true of certain moths, however, which

48 the myth of monogamy

have evolved the ability to hear and respond to the ultra-high-frequency sounds emitted by a highly relevant part of their environment: hunting bats.

It is also possible that, in some species, males simply lack the ability to detect eggs or offspring not their own, even though it might be to their benefit if they could. Or maybe in certain cases the payoff that comes with discriminating "my genes" from "someone else's" is substantially reduced by certain disadvantages, such as the costs of occasionally erring and discriminating against one's own offspring after all. Nonetheless, there is little doubt that incursions--especially by a male into the territory of a monogamous breeding couple--are not appreciated . . . especially by the resident male.

In the mid-1970s, David conducted this experiment in Mount Rainier National Park: He attached a model of a male mountain bluebird near a female and her nest, so that when the female's actual mate returned, he discovered his female in close association with this apparent stranger. The male behaved aggressively toward the model and also toward his own mate, in one case driving her away; she was eventually replaced with another female, with whom he successfully reared a brood. This little study became somewhat controversial, with researchers debating, among other things, the propriety of biologists acting as Iago and inducing violent sexual jealousy on the part of their subjects! In any event, there have since been numerous studies in which males of different species were removed while their Desde-monas were sexually receptive, in which these males had visual access to their unguarded females, in which the females were removed, in which males witnessed their females in cages with decoy males, and so forth, all looking for possible impact on the males' subsequent behavior, especially his paternal inclinations.