Similar problems or qualifications are apparent in the other cases. Greylag gander pairs do sometimes attract females, it is true, but there is no evidence that they are more attractive to the opposite sex than single, exclusively heterosexual males. While male homosexuality in Pukeko is associated with the most heterosexually active groups, female homosexuality—which is more common, and more highly developed in terms of the courtship behaviors involved—is not. In addition, the greater levels of heterosexuality found in some groups is not necessarily a result of the homosexual or bisexual involvements of their participants. It is just as likely that the increased heterosexuality and homosexuality are both manifestations of a third factor, perhaps something akin to a generally higher sexual “state,” level of activity, or arousal in such groups. This is supported by observations in a number of other species (e.g., Bonobos, Gorillas, Squirrel Monkeys, Wolves, Common Tree Shrews, Bottlenose Dolphins) where homosexual activity actually peaks or increases dramatically along with heterosexual activity (in different age/sex classes or social contexts).35
The matter of causality is also relevant for several of the other species discussed above. For example, although participation in heterosexuality and homosexuality appear to be linked in male Sociable Weavers, Bonnet Macaques, and Asiatic Elephants, this is primarily true for higher-ranking individuals—and such animals tend to have access to more individuals (including sexual partners) of either gender. In other words, greater heterosexual mating opportunities for such individuals are probably not a consequence of their bisexuality, but rather of their status—which also grants them greater homosexual mating opportunities. Similarly for the Guianan Cock-of-the-Rock: although adolescent males who engage in more homosexual encounters seem to have an advantage in their subsequent ability to acquire breeding territories, scientists admit that this may be due to a third factor (such as higher levels of aggression or “initiative” on the part of such males, or even physiological differences between them) rather than being a direct consequence of their same-sex activity. Furthermore, while bisexuality in this species may appear to be related to breeding success for adolescent males, it is definitely not conducive for reproduction in adult males (who nevertheless continue to participate in such activity). Homosexual courtships and sexual activity often interrupt and displace heterosexual activity, and females usually stay away from breeding territories while their owners are having homosexual encounters with adolescents. Likewise, the future reproductive advantages that may accrue to female Oystercatchers in trios are not specifically a function of whether they are bisexual. Compared to nonbreeders, such individuals are more likely to acquire heterosexual mates and breeding territories of their own in subsequent years, but this is regardless of whether their current trio is bisexual (with bonding and sexual activity between the same-sex partners) or strictly heterosexual (with no such same-sex activity). In fact, females in bisexual trios may actually be less likely than females in heterosexual trios to acquire their own mates subsequently, since bisexual trios tend to be more stable and longer-lasting than heterosexual trios. And as in Guianan Cock-of-the-Rock, homosexual activity does not promote reproductive output for such individuals while they remain within bisexual trios.36
Even though some of the most complete sequences of homosexual behavior in Japanese Macaques are seen in some of the most heterosexually active males, this pattern is not universal in either this species or others. In one study of Kob antelopes, for example, a female who exhibited the most fully developed sequence of lesbian courtship also participated in the second-fewest number of heterosexual matings of any of the study animals.37 And while homosexual copulations (as well as promiscuous heterosexual matings) are characteristic of heterosexually paired (breeding) males in a number of bird species (e.g., Swallows, Herons), there is not necessarily a correspondence between specific amounts of same-sex and opposite-sex activity for individual birds. In Cattle Egrets, for example, males often try to mate with birds—male or female—other than their female partner. However, one study revealed that a male who completed the most promiscuous copulations with females—and therefore was probably the most reproductively “successful”—did not engage in any homosexual copulations. Other males had homosexual encounters regardless of whether they also sought nonmonogamous heterosexual activity, indicating no necessary connection between bisexuality and breeding success.38
Paradoxically, some of the strongest evidence against the bisexual-superiority hypothesis, as well as against genetics as the sole determinant of homosexuality, comes from the Ruff—a species in which same-sex activity between males clearly does attract females to breeding territories. To see why, we need to take a closer look at some social and biological patterns in this bird. Male Ruffs fall into four distinct classes—residents, marginals, satellites, and naked-napes—who differ from each other physically, behaviorally, and sexually.39 While it is true that females are drawn to resident males’ display territories by homosexual (and other behavioral) interactions between satellites and residents, satellites actually interfere with heterosexual mating by resident males once females have been attracted. Less than 3 percent of copulations occur when satellite males are on a resident’s territory: not only does their presence inhibit heterosexual interactions, they sometimes directly prevent residents from mating by interposing themselves between the male and the female, or by trying to knock the resident off a female’s back.40 Moreover, not all homosexual activity is associated with attracting females: same-sex mounting and courtship also occur between males who are not involved in breeding (naked-napes), between males when females are not present, and during the nonbreeding season. In addition, not all resident males participate in homosexuality: some display on their own without a satellite “partner.” If same-sex activity were vital for attracting females (and therefore breeding success) in this species, one would expect all males to engage in it. Further geographic and population differences in the occurrence of homosexual activity also argue against its being an essential component of successful reproduction.
Four classes of male Ruffs, which differ in their physical appearance, social and sexual behavior, and genetics. Clockwise from upper left: resident, marginal, naked-nape, and satellite males.
Perhaps the most important piece of evidence concerns genetic differences between the classes of males. Scientists recently discovered that the distinctions between some categories of males are genetically determined—but the genetic differences cut across differences in their homosexual behavior rather than falling in line with their sexual variations. Detailed chromosome and heredity studies revealed that whether a male becomes a resident or a satellite is genetically controlled—a finding corroborated by the fact that these two categories of males are the most physically distinct from one another in their plumage, and also by the fact that category changes between the two types are virtually impossible (satellite males never become residents or vice versa).41 Yet both residents and satellites engage in homosexual behavior—in fact, it is their joint participation in such activity that often attracts females. In stark contrast, residents and marginals are not genetically distinct: the two share many plumage characteristics, and a male may change his class membership from marginal to resident or vice versa. Yet it is precisely these two categories of males who are the most different sexually: resident males are commonly involved in both heterosexual and homosexual encounters, while marginal males are nonbreeders who rarely participate in either same-sex or opposite-sex activity.