Biological Exuberance: Animal Homosexuality and Natural Diversity

extremely common and are further evidence against this hypothesis (since they are examples of bisexuality failing to be “maximized”).

What about species in which the majority of individuals are bisexual, i.e., the examples of maximization of bisexuality mentioned above? In all of the animals in which this is the case (Bonobos, Dolphins, Mountain Sheep, etc.), individuals differ significantly in the degree to which they are bisexual. Some animals participate very little in homosexual and/or heterosexual activity while others account for the majority of (one or both) such activities, and same-sex versus opposite-sex interactions make up varying proportions of each individual’s sexual encounters as well (as we saw in chapter 2). Thus, if bisexuality were related to reproductive success, one would expect animals to differ depending on “how bisexual” they are—successful breeders (i.e., those animals who are the most active heterosexually) should engage in a greater proportion of homosexual activity as well. Again, long-term studies of reproductive output are required to test this, but data on the sexual activity of individual animals in a number of species where bisexuality is widespread do not support this idea. If we take the number of heterosexual copulations that an animal participates in to be a rough measure of its reproductive prowess, then we do not generally find that there is a positive correlation between degree of bisexuality and breeding success.

For example, in Kob antelopes—in which virtually all females engage in both same-sex and opposite-sex mounting—there is generally an inverse relationship between an individual’s heterosexual and homosexual activity. One study revealed that a female who had the most homosexual mounts had the fewest heterosexual ones and vice versa, while individuals who ranked in the upper quarter or third of the population in terms of heterosexual activity often ranked much lower in their homosexual participation. Furthermore, the female whose heterosexual and homosexual activities were most equal—i.e., the most “bisexual” individual—actu—ally participated in the fewest total number of heterosexual matings. Similarly, all Bonobo females interact sexually with both males and females, but differ widely in the extent of their bisexuality. In one troop, three females participated in the most heterosexual copulations—two-thirds of all mating activity—yet these same females accounted for less than one-third of all homosexual activity, and one had among the fewest same-sex encounters of any of the females. Nor were these females necessarily “balanced” in terms of their individual proportions of same-sex and opposite-sex activity. One had fairly equal ratios of homosexual and heterosexual interactions, but the other two were less “proportional” bisexuals, with the majority (two-thirds) of their sexual encounters skewed toward opposite-sex partners. Likewise, those female Japanese Macaques who were the most involved in homosexual activity in each of four mating seasons (the top two in terms of the proportion of time they spent) were rarely as involved in heterosexual interactions and were often among the least heterosexually active members of their troop. Another pattern was revealed in a study of Pig-tailed Macaques. Although all the males in one troop mounted both females and other males, they had roughly the same number of homosexual encounters regardless of their participation in heterosexual activity (which varied enormously). The male who was the most heterosexually active was also the least “bisexual” individual (same-sex mounting made up only 8 percent of his sexual activity, compared to an average of 48 percent for the other males).³²

Of course, heterosexual activity (i.e., number of opposite-sex matings) is not necessarily an accurate measure of reproductive success, and none of these studies tracked individual animals and the number of offspring they produced throughout their entire lives.³³ Nevertheless, there does not appear to be the sort of connection between homosexual and heterosexual activity that would be expected if bisexuality contributed to an animal’s reproductive prowess or success. Moreover, in most of the species where bisexuality seems to be “maximized,” it is usually the case that one sex participates in homosexual activity to a greater extent than the other: females in Kob, Bonobos, and Japanese Macaques, males in Mountain Sheep and Bottlenose Dolphins, for example. Even if bisexuality were somehow an advantageous reproductive strategy, it would remain to be explained why there should be a gender difference in its “efficacy” (and why it should pertain to different genders in different species).

Finally, most of the specific cases mentioned above (e.g., Black Swans, Pukeko, Ruffs) that seem to support some sort of connection between bisexuality and reproductive prowess are not as convincing as they initially appear. In each instance, closer investigation reveals that the connection is doubtful, if not completely spurious. ³⁴ For example, although male pairs in Black Swans tend to be more successful parents, such couples are not necessarily made up of bisexual birds, nor do they always raise their own offspring. Same-sex pairs in this species often “adopt” cygnets by taking over or stealing nests from heterosexual pairs (rather than mating with a female)—thus many successful male pairs need not have been involved in any heterosexual activity at all and may be exclusively homosexual rather than bisexual. Moreover, even if such individuals prove to be bisexual over their entire lives (e.g., by subsequently pairing with females), much of their parenting success involves raising offspring that are not related to them (by virtue of having been “adopted”). This situation is inimical to the rationale behind the bisexual-superiority hypothesis, which depends on bisexual individuals being more successful at passing on their own genes, not other animals’.

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.