Biological Exuberance: Animal Homosexuality and Natural Diversity

Guianan Cock-of-the-Rock males who participate in the most visits to adult males’ display territories, during which homosexual courtship and mounting often occur, sometimes acquire their own territories at a younger age. With earlier access to heterosexual mating opportunities, this may give them a “head start” on breeding. Likewise, female Oystercatchers in bisexual (as well as heterosexual) trios may have an advantage in acquiring their own breeding territories and heterosexual mates in subsequent years.²²

A number of studies have also shown that animals that are the most active heterosexually are sometimes also the most active homosexually. In specific populations of Sociable Weavers, Bonnet Macaques, and Asiatic Elephants, for example, the top two males in terms of heterosexual mountings and other behaviors also participated in the most homosexual activities. Some of the most complete male homosexual behavior in Japanese Macaques, including full copulations with ejaculation, was exhibited by “one of the most vigorously heterosexual males in the troop,” while in another study the one female in a troop who failed to form any homosexual consortships also did not participate in any heterosexual consortships.²³ And as mentioned in the preceding chapter, in a number of birds such as Common Murres, Laysan Albatrosses, and Swallows, most individuals who participate in homosexual copulations are in fact breeders who have heterosexual mates, rather than nonbreeders who are heterosexually inactive.

In spite of these rather unexpected confirmations, however, the bulk of the evidence does not actually favor this hypothesis and in fact disconfirms many of its predictions. Most of the examples cited above that seem to support the idea of “bisexual superiority” are misleading because they are based on anecdotal, rather than quantitative, information, and because they only look at a few individuals at a single point in time (or, at most, over the span of a few breeding seasons). To assess whether bisexual animals are more successful at reproducing, what is actually needed is a long-term study of large numbers of individuals that tracks them over their entire lifetimes, comparing the total number of offspring produced by bisexual animals to the total number produced by heterosexual individuals. Needless to say, this would be a huge and difficult undertaking, complicated by the logistics of keeping track of hundreds or even thousands of animals over many years and potentially large geographic areas, tabulating not only the reproductive output of each individual but also his or her entire sexual history to determine which animals are bisexual and which are exclusively heterosexual. Not surprisingly, few longitudinal studies of this type have been conducted, and those that have rarely involve species in which homosexual or bisexual activity is prominent (or else they do not take into account such behavior when it is present).

However, one scientist—James A. Mills—has conducted exactly this sort of long-term, comprehensive study on the Silver (Red-billed) Gull in New Zealand, a species in which there is extensive bisexuality and homosexuality. His results show that bisexual individuals are in fact significantly less successful breeders than heterosexual ones. Over more than 30 years, Dr. Mills and his colleagues banded over 80,000 individual gulls, tabulating detailed lifetime reproductive and sexual profiles of more than 5,000 of these. Because of the enormity of this project, special computer programs had to be developed to analyze and keep track of all the data. The Silver Gull is an ideal species in which to test this hypothesis, because the sexual orientation of females (in terms of their pairing behavior) falls into three clear-cut categories: some form only homosexual pairs during their entire lifetimes and hence are exclusively lesbian, while others have both same-sex and opposite-sex partners during their lives and are therefore unequivocally bisexual, while other females only pair with male partners and thus are exclusively heterosexual.²⁴ Moreover, Mills and his team looked not only at how many chicks were hatched and raised by heterosexual versus bisexual (and homosexual) individuals, but also at how many of those chicks survived to adulthood and became breeders themselves—the true measure of whether an individual is actually passing on his or her genes.

Mills’s final results were conclusive: “Females which were bisexual during their life produced 14 percent fewer chicks than females in exclusively male-female pairings.” ²⁵ Furthermore, fewer of those chicks went on to join the breeding population as adults: exclusively heterosexual birds raised chicks who survived to breed at a rate that was more than one and a third times higher than that of bisexual females. Nor was the lower overall reproductive output of bisexual females due to their participation in (potentially less productive) homosexual pairings at some point in their life: such females also “tended to be less successful breeders even with male partners.”²⁶ It would be difficult to find a more definitive or better-documented refutation of the bisexual-superiority hypothesis. Not only do bisexual females hatch and raise fewer chicks than heterosexual females, they also contribute fewer offspring to the pool of breeding individuals in the population, and their decreased reproductive output appears to be independent of whether they happen to be breeding with a male or a female partner.

One criticism that has been leveled at the bisexual-superiority hypothesis is that it is so difficult to test, and a number of scientists have even remarked that they cannot imagine a relevant experiment or study that could possibly verify or falsify its claims.²⁷ Amazingly, although it has all of the elements needed to evaluate the bisexual-superiority hypothesis, Mills’s study was not specifically designed to test this proposal, nor even to focus on the reproductive performance of bisexual animals in particular. Indeed, it is doubtful that Mills was even aware of this hypothesis—it had yet to be formulated at the time he initiated his project in 1958, and it was not widely known or discussed in the scientific community even after it had been published and revised in various forms over the next 30 some years.²⁸ Nevertheless, the procedures and analyses Mills used were almost tailor-made to assess the validity of this hypothesis, and it is a testament to his expertise that his results should prove useful for a line of inquiry so far removed from their original purpose.

Unfortunately, studies of a similar scale and quality have yet to be undertaken for most other relevant species. Nevertheless, although it is possible that different patterns of reproductive performance across sexual orientations may be revealed in other animals, this is unlikely. Most reports of same-sex parenting and/or breeding in other species appear to be in line with the Silver Gull results.²⁹ Notwithstanding the Black Swan case (to which we’ll return shortly), animals in homosexual pairs who also reproduce are generally only as successful or less successful than heterosexual parents in raising offspring, not more successful. Moreover, in a number of instances homosexual activity on the part of breeding animals actually interferes with their reproductive performance: in female Jackdaws, Oystercatchers, Canada Geese, and Calfbirds, for example, homosexual associations may in fact be detrimental to the successful raising of offspring, often by interfering with incubation (these examples will be discussed more fully later in this chapter). Same-sex activity in Buff-breasted Sandpipers often discourages heterosexual mating and breeding opportunities, while male Cheetahs living in bonded pairs or trios often disrupt, compete with, or prevent their companions from mating heterosexually (and thereby reduce their reproductive output).³⁰ Although differential breeding success can be associated with sexual variance in some species, typically transgendered rather than bisexual (or homosexual) individuals are more reproductively successful (as in the examples of Northern Elephant Seals, Red Deer, Black-headed Gulls, and Common Garter Snakes discussed in the preceding chapter).

There are further arguments against the bisexual-superiority hypothesis. If bisexual animals were more successful breeders, one would expect them to make up the majority of the population in any given species, with much smaller proportions being exclusively heterosexual or homosexual—yet the distribution of sexual orientations does not, in fact, typically follow this pattern. In Silver Gulls, heterosexual versus bisexual percentages are in accord with what we have just seen about their relative reproductive proficiencies: 79 percent of all females are exclusively heterosexual, 11 percent are bisexual, and 10 percent are exclusively lesbian. This pattern is characteristic of many other species for which we do not have information about the lifetime reproductive output of a cross-section of individuals: bisexual animals generally make up a much smaller percentage of the population, sometimes even less than the proportion of exclusively homosexual individuals. For example, the heterosexual-bisexual-homosexual proportions for male Black-headed Gulls are 63-15-22 percent, respectively, and for Galahs, 44-11-44 percent.³¹ In many other species the proportion of animals who engage in bisexual activity is even smaller.

Moreover, in some cases there do not appear to be any bisexual individuals at all in a population (i.e., same- sex activity occurs only in nonbreeding animals). For example, female homosexual pairs in Kittiwakes, Red-backed Shrikes, and Mute Swans, among others, appear to consistently lay infertile eggs (indicating that they do not mate with males); in Pied Kingfishers, homosexuality is typical of nonbreeding birds who are not likely to reproduce later in life; while male Ostriches who court other males do not appear to have heterosexual relations. Although longitudinal studies are needed in each case to verify that such individuals are not in fact sequentially bisexual, these patterns do not fit well with a bisexual-superiority hypothesis. More broadly, species in which homosexuality or bisexuality is only found in individuals of one sex—or in which all individuals are exclusively heterosexual—are