Homo Mysterious: Evolutionary Puzzles of Human Nature (20 page)

There are several other hypotheses that speak to the potential of homosexual activity generating a positive social outcome. In fact, from the perspective of “classical ethology”—in the tradition of Konrad Lorenz and Niko Tinbergen—same-sex behavior has long been seen as serving an important social function, quite independent of any sexual motivation.
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Seemingly sexual acts, including genital rubbing, mounting, and even intromission, have thus been interpreted as simply part of a species’ communicative
repertoire, an automatic means of nonerotic signaling, and not necessarily sexual at all.

It has been suggested, accordingly, that homoerotic interactions can contribute to reconciliation after a conflict. It certainly seems to do so among bonobos, at least: Female bonobos engage in significantly more genital–genital rubbing immediately after an aggressive interaction.
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But things are quite different in other species. Among Japanese macaque monkeys, for example, female–female sexual encounters are less frequent, rather than more, following a conflict. In this case at least, aggressive behaviors
inhibit
subsequent homoerotic actions rather than facilitate them.
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And here is an interesting side note, with possible wider implications: When a female Japanese macaque monkey is confronted with a desirable male who is not sexually interested in her, she will often react by mounting him! Suitably stimulated, the male will then frequently reverse positions and copulate with the sexually aggressive female.
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What about the possibility, accordingly, that female–female mounting is a similar tactic, used to inspire otherwise sluggish or distracted males? (One cannot help thinking of the widespread phenomenon whereby men typically find it sexually arousing to see images of lesbian sex.) Sadly for this intriguing hypothesis, the data suggest just the opposite: When male Japanese macaques attempt to mount females who are engaging in female–female mountings, the males are either ignored or sometimes even attacked and driven away!
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Next, some other pro-social roles for homosexuality among certain animals at least and possibly offering models for the initial evolution and/or maintenance of homoerotic behavior among human beings. Just above, we looked briefly at the prospect that same-sex mounting facilitates reconciliation after conflict. In some species, such as acorn woodpeckers, it reduces tension and makes it less likely that conflict will occur in the first place.
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In others, such as American bison, dominant individuals mount subordinates, with essentially no reversals.
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A reasonable interpretation is that in such cases, homosexual behavior functions to diminish the frequency of conflict, just as it does among acorn woodpeckers, but by a more aggressive route: by reinforcing the existing dominance hierarchy, and thereby keeping everyone in line, rather than by directly fostering positive relationships as such.

Here are some more animal examples, also emphasizing competition, but without any discernible human implications. Consider a species of dung fly (doesn’t everyone?). In one particular case, males mount females when they encounter them, and females typically accept the first male to do so. Males also mount other males who resist vigorously, jumping about and kicking while the mounter seeks—usually quite successfully—to remain on their backs, resembling a rodeo cowboy astride a bucking bronco.
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This appears to be an outright male–male competitive strategy, since when a female appears, the male on top—the one who initiated the mounting—has given himself an advantage: He can jump off and immediately mount the female, while the male on the bottom is too encumbered to do so. In this case, although the behavior clearly involves same-sex mounting, it evidently occurs solely in the service of heterosexual mating success.

A similar situation has been described for a species of parasitic acorn worm.
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When engaging in heterosexual copulation, male acorn worms first transfer sperm, followed by a secretion from a specialized cement gland, which seals the female’s vaginal opening and serves as a kind of biological chastity belt that prevents the female from copulating with any other males. Not uncommonly, however, male acorn worms encounter other males, whereupon the aggressor maneuvers so as to transfer his cement gland substance, thereby plugging up the victim’s genital opening and preventing him from copulating with any females. As a result, a possible heterosexual competitor is literally put out of commission. We can be confident, incidentally, that this behavior is not a case of mistaken identity, since in such cases, the aggressor transfers his sexual cement only, and no sperm.

The authors of this particular research report may have been overreaching when they described this phenomenon as “homosexual rape,” since there is no evidence for homoerotic inclination on the part of the aggressor males. But whatever the proximate motivation, it is a behavioral strategy whose evolution can readily be discerned, involving as it does a straightforward competitive strategy that ultimately enhances the “perpetrators’” fitness the old-fashioned way: by making it more likely that such individuals will be able to reproduce heterosexually.

Returning to the general prospect that in at least some cases, enhanced breeding success arrives via competitive aspects of same-sex behavior, here is yet another intriguing animal example. Once again, this one does not offer direct parallels to the human condition but is worth contemplating nonetheless, if only for its “gee whiz” value. I am thinking of reproduction by proxy, as occurs among certain invertebrates, notably flour beetles. Here, males force copulations with other males, who then transfer the “lover’s” sperm when he eventually mates.
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For an example of a more cooperative animal sexual style, consider the following, a case of adjustable sexuality that once again seems unlikely to teach us anything about human homosexuality but is worth pondering nonetheless, perhaps just for its own sake: In the marine snail,
Crepidula fornicata,
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all individuals begin life as male, after which they can change to female depending on the sex of their immediate partner. If a male
C. fornicata
has hooked up with another male, then one or the other will simply switch sexes. It’s a sexual tactic delightfully reminiscent of the science fiction fantasy novel
The Left Hand of Darkness
, by Ursula LeGuin, in which inhabitants of the planet Gethen are neither male nor female, but bipotent. Periodically, they enter a state known as “kemmer,” in which they experience a mating urge along with short-term anatomic differentiation. Depending on the chemistry within each duo, an individual may temporarily transform into either male or female, after which his or her partner develops into the opposite sex. Nothing is preset, however, so in LeGuin’s made-up world, an individual may have been a mother to one child as well as a father to another, depending on how the sexual spirit operated at any given time.

One of the more important recent ideas in evolutionary ecology concerns yet another aspect of social behavior: “reproductive skew” theory, a concept that has possible implications for many aspects of animal and human reproductive behavior, the evolution of homosexuality included.
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The “skew” in reproductive skew
refers to the disparity in reproductive success among members of a social group; typically, of course, dominant individuals are more successful than are subordinates. They are more fit, which is presumably the reason that individuals compete for dominance in the first place. Essentially, subordinates must “decide” whether or not to stay in the group, just as dominants must decide whether or not to let them do so. The currency is breeding success. Subordinates may leave if they are not permitted to breed at all, but this could be disadvantageous to the dominants, if having a group of at least a certain size contributes to their own breeding success (e.g., if it makes the group more successful when deterring predators or competing successfully with other groups). On the other hand, dominants are likely to be unenthusiastic about ceding too much success to the subordinates, that is, to anyone but themselves.
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Reproductive skew is likely to be greater the larger the difference in status between dominant and subordinate individuals, and vice versa: When those on top socially aren’t very dominant over the subordinates, we wouldn’t expect them to experience substantially higher fitness. Also, skew would be higher in proportion as subordinates have less prospect of breeding successfully if they were to set out on their own; this is because as their prospects diminish, subordinates are less able to drive a hard bargain, and dominants are correspondingly more empowered to push them around.

Counterintuitively, perhaps, skew is expected to be greater when dominants and subordinates are closely related, because in such a case, the success of dominant individuals carries within itself a degree of success for subordinates. Hence, the latter are not so greatly disadvantaged if their personal reproductive success is relatively lower, since they succeed genetically, by proxy, so long as the dominants do so. At the same time, dominants need to avoid demanding too much sacrifice from subordinates, who in turn need to restrain themselves so as to keep the dominants from retaliating against them. In short, there’s a need for negotiations.

The relevant point for our purposes is that to some degree, homosexuality might ultimately be found to be imposed upon certain individuals by others within the local community, most likely by stress effects mediated by neurohormones and analogous—in
consequence, if not physiological mechanism—to subordinates being kept from breeding.

It should be clear at this point that when it comes to underwriting gay versus straight sexuality, social interactions may be no less important than direct genetic predispositions. Moreover, it is not obvious whether—and if so, in which cases—animal homosexuality can usefully illuminate the case of
Homo sapiens
. Here is one possibility, suggested to me by the observation that among several different species of nonhuman primates, dominant males accept the homoerotic advances of subordinates, who are often juvenile as well. These subordinates receive physical protection and sometimes status advancement in the social hierarchy. Here is the idea: What if homosexuality among human beings has—at least in the past—served as a means of social advancement, especially on the part of otherwise younger and/or subordinate individuals?

It is known that in classical Greece, for example, boys provided sexual gratification to older and supposedly heterosexual men. If they profited by this, in terms of social advancement and even possibly sexual access to women as well, selection could have favored a degree of bisexuality. This notion, like most of those presented in this chapter, does not exclude any of the many other possible hypotheses already discussed, and it has the added advantage of explaining why homosexuality is more common in men than in women: Insofar as men generally have a more insistent and less discriminating sex drive, they are more likely to desire and appreciate immediate sexual gratification. This would be especially the case in harem-forming societies, in which a comparatively small number of men monopolize a relatively large proportion of the women, thereby leaving many men sexually unsatisfied.

There are other examples of same-sex behavior among animals ultimately serving to convey benefits via competition. Among a number of species—notably fish—males engage in “alternative sexual strategies,” whereby in addition to “traditional” males who are typically large, dark colored, and inclined to vigorously defend mating territories, some males develop into “female mimics,” who are mistaken as such by the traditional males and courted heterosexually. As a result, these female mimics are often able to gain access to females, with whom they attempt to mate. It does not seem likely that cases of this sort carry much direct relevance for human beings,
although they add to our appreciation of the diversity of ways in which seemingly homoerotic behavior may be strictly heterosexual after all, not involving anything approaching the subjective dynamics of what people generally mean by “homosexual.”

Here is another circumstance, well described among animals, that may or may not have any relevance for human beings. I suspect that it does not, although it’s intriguing enough to be worth describing. The phenomenon is known as female mimicry, whereby males increase their (heterosexual) mating success by resembling females. We already considered such tactics among fish. Something similar—known to biologists as “delayed plumage maturation”—also occurs among birds. In many species, male plumage is brighter and more colorful and eye-catching than its female counterpart, so as to attract female attention as well as display the male’s physical qualities. At the same time, such display plumage often invites aggression by other males, so in some cases, not surprisingly, young adult males delay their full-fledged male looks. Since they typically resemble females as a result, such discreet males are often courted by other, traditionally showy males. In such cases, however, there is no reason to think that these recipients of homoerotic attention are actually homosexual in the human sense; rather, they employ female mimicry to buy themselves surcease from male–male competition, as well as increasing the probability that they will be able to obtain sneak copulations from females.
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I don’t know any cases of the inverse, in which females increase their fitness by mimicking males.

Given the high frequency of apparently homosexual play among juvenile mammals in particular, as well as the phenomenon of delayed plumage maturation among birds, another question arises: Is there any sense in which human homosexuality is an example of neoteny, the retention of juvenile characteristics among adults of a species? More specifically, if for whatever reason some individuals retain a more “juvenile” brain into adulthood, couldn’t this predispose toward homosexuality? It is well known that we all lose neurons with age, and so, what if in some people, those neurons associated with
same-sex interactions are simply lost at a lower rate? It has already been proposed that at the subcellular level, modifications in programmed cell death, “apoptosis,” could make male brains more feminine and female brains more masculine.
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