Bisexual Superiority and the Genetics of Homosexuality

In attempting to argue for the evolutionary value of homosexuality, scientists are confronted with an apparent paradox: if homosexuality is a valuable trait, it should have a genetic basis—yet how can a gene that doesn’t lead directly to reproduction continue to be passed on from one generation to the next? Perhaps, some have suggested, because the putative gene for homosexuality does not operate on its own, but rather is acting in tandem with another gene to promote reproduction. An often-cited analogy involves the genetics of sickle-cell anemia and malaria resistance in humans. People who receive a sickle-cell gene from one parent and a regular hemoglobin gene from the other parent are resistant to malaria; those who receive two sickle-cell genes (one from each parent) succumb to sickle-cell anemia, while those who receive two regular hemoglobin genes are more likely to succumb to malaria. Thus, genes that (on their own) can potentially decrease an individual’s reproductive capacity continue to be passed on because they are beneficial when combined with each other. Scientists have suggested that this might also be the case with homosexuality, as follows: Suppose there were one gene that predisposed an individual to homosexuality, and another that predisposed an individual to heterosexuality. Those individuals who receive two homosexual genes (one from each parent) would be exclusively homosexual; others would receive two heterosexual genes and be exclusively heterosexual; while those receiving one of each would be bisexual. If individuals who have one homosexual and one heterosexual gene were somehow more successful at reproducing, then the gene for homosexuality would confer an advantage and would continue to be passed on, even though it would sometimes result in individuals who do not reproduce (those who receive a homosexual gene from each parent).²⁰

At first glance, this hypothesis seems counterintuitive: regardless of the genetic mechanism involved, why should bisexual individuals be superior at procreating or have a reproductive advantage? On the contrary, one would expect individuals with two heterosexual genes—those who are exclusively or “doubly” heterosexual, as it were—to be more successful breeders than bisexuals. Nevertheless, this hypothesis accords surprisingly well with a number of aspects of animal homosexuality that remain puzzling under other accounts. First of all, as noted previously, bisexuality is widespread in the animal kingdom. Unlike other theories about the evolutionary value of homosexuality, this hypothesis recognizes that many individuals who participate in homosexual activity may also be involved in heterosexual behavior, and therefore capable of reproducing and passing on their genes. Additionally, the incidence of bisexuality within populations is often high: in a number of animals such as Bonobos, Japanese Macaques, Bottlenose Dolphins, Mountain Sheep, Giraffe, and Kob, for instance, virtually all members of the species (or of one sex) participate in both same-sex and opposite-sex interactions (either concurrently or at different points in their life). Again, this hypothesis predicts that such situations should exist, since it argues for the maximization of bisexuality in a population—that is, if bisexual individuals are more successful breeders, they should tend to make up the majority of a population.

Even more startling, in a few species bisexual animals actually do appear to be more successful than exclusively heterosexual individuals at reproduction, heterosexual mating, and/or attracting members of the opposite sex. As we have already discussed, pairs of male Black Swans, who can father cygnets by associating temporarily with a female and then raise the resulting offspring on their own, are generally more successful parents than heterosexual pairs. In part, this is because such same-sex pairs are more aggressive than male-female pairs and are therefore able to acquire larger and better-quality territories, which are essential for successfully raising cygnets. They may also have an advantage because both males contribute to incubating the eggs, whereas in heterosexual pairs males may take part in less of the incubation duties. Over a three-year period, 80 percent of male pairs in one study were found to be successful parents, while only about 30 percent of heterosexual pairs successfully raised offspring (unsuccessful parents either deserted their clutches, lost them to predators or other hazards, or ended up having their cygnets die). Homosexual pairs constituted up to a quarter of all successful parents even though they made up only 13 percent of all breeding pairs or associations in the study population.²¹

Animals who participate in homosexual activity are also sometimes more successful at attracting members of the opposite sex, or participate more often in heterosexual mating. For example, male Ruffs who display with and mount male partners on their courtship territories attract females for mating more often than males who display by themselves. Because of their superior strength and courage, as well as their high rank in the flock, Greylag Geese in gander pairs or other homosexual associations are also sometimes attractive to the opposite sex. Females may associate themselves with a gander pair and eventually form a bisexual trio, mating with one or both of the males and raising their goslings together. In Pukeko, breeding groups in which homosexual interactions take place between males are also the groups in which the most intense heterosexual copulatory activity occurs. Adolescent 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 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. 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.

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.

This is in line with what else we know about the genetics of homosexuality in animals (and people). Direct evidence for a genetic component is accumulating: in several species of insects, for example, scientists have recently isolated genetic markers for homosexuality (and there are parallel findings of genetic links to homosexuality in humans).⁴² Yet it is also clear that social, behavioral, and individual factors are at least as important as genetic ones, especially in “higher animals” such as mammals that have complex forms of social organization and highly flexible behavioral interactions. The expression of homosexuality often varies widely between different social contexts, age groups, activities, individuals, and even populations and geographic areas, in ways that transcend any possible genetic “control.” We also saw in chapter 2 that there are good reasons to consider homosexual (and other sexual) activity to have a “cultural,” social, and/or learned dimension in a number of species, especially primates. Ultimately, then, it is of relatively little importance whether there is an actual homosexual “gene” or whether it is part of a pattern of “superior” bisexual reproduction. Even if homosexuality is shown definitively to have a genetic component (as is likely), it will always remain just that—a component, one part of a much larger picture that includes the totality of an animal’s biology and social environment.