Biological Exuberance: Animal Homosexuality and Natural Diversity

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.

This certainly does not mean that homosexuality lacks a genetic basis in this (or any other) species. Rather, it demonstrates the importance—the primacy, even—of nongenetic factors in the expression of homosexuality, regardless of whether it has a genetic component. A male Ruff may begin his adult life as a marginal, engaging in no sexual activity whatsoever, then change over to resident status and begin copulating with both males and females, or only females, or only males. He may even revert back to marginal status later in life, becoming asexual once again—or he may never engage in same-sex activity even as a resident or perhaps never become a resident in the first place. Other males live their entire lives as either residents or satellites, with or without homosexual activity—but in all cases, the manifestation of their sexuality is dependent on the social and behavioral contexts in which they find themselves as much as, if not more so than, on their genes. This is not to say that genetic programming or an innate predisposition for homosexuality does not exist or is unimportant—only that many other factors are involved as well.