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{168} Chapter 5
Not for Breeding Only: Reproduction on the Periphery of Life

Heterosexual animals that never reproduce, homosexual animals that regularly procreate — breeding and sexual orientation often combine in unexpected and paradoxical ways. In an attempt to understand the origin and function of homosexuality, many scientists have suggested that same-sex activity might actually contribute in some way to reproduction or the perpetuation of the species. In this way, they have tried to carve out a "place" for homosexuality in the scheme of things — but a place on the sidelines, with breeding and heterosexuality decidedly in the center. What many people fail to realize is that reproduction itself often occupies a peripheral position in animal life — either being a "marginal" activity among apparently heterosexual animals, or else a common activity among seemingly "marginal" animals such as those involved in homosexuality. In this chapter we'll explore some of the various attempts to find a "useful" place for homosexuality in the larger patterns of life and consider why these attempts have often been as misguided as efforts to deny such a "purpose" for homosexuality in the first place.

The Evolutionary "Value" of Homosexuality

In 1959 noted evolutionary biologist George Evelyn Hutchinson published a proposal that was radical for its time (and even now remains controversial): he advanced the first theory of the evolutionary value of homosexuality.¹ Hutchinson argued that since homosexuality appears to be a biological constant, appearing in generation after generation (in both humans and animals) at a rate that far exceeds that of biological "mistakes," it must perform some useful function rather than be an aberrant behavior, and moreover, it must have a genetic basis.² Nearly {169} 20 years later, in 1975, renowned biologist Edward O. Wilson published his seminal work Sociobiology, in which he took up the same theme: homosexuality must be beneficial to a species if it keeps reappearing. Since then, many other "positive" explanations have been proposed for animal homosexuality: some provocative, some absurd, but all revolving around the idea that breeding, heterosexuality, or the overall reproductive profile of an individual or species may be enhanced by homosexuality.³

A number of these proposals have been formulated with reference to homosexuality in human beings and have not been rigorously evaluated (in either people or animals), in part because of the difficulty of finding relevant data or situations with which to test them. Many have not been applied to the domain of animal homosexuality at all, in part because of the inaccessibility of information about same-sex activity in nonhumans. In this section we will explore a number of these "explanations," evaluating — in many cases, for the first time — whether they hold true for a variety of different species. While many of these proposals are a welcome change from the view that homosexuality is "abnormal," they still face significant problems. Often such explanations are simply not consistent with the facts about homosexuality across a broad spectrum of animals. In addition, the underlying assumptions of many of these proposals — especially with regard to the participation (or not) of homosexual, bisexual, transgendered, and heterosexual animals in breeding — are frequently incorrect.

For the Good of the Family and the Species?
      Homosexual or transgendered individuals in many human societies perform a special role, acting as shamans, teachers, or caretakers for the benefit of the tribe as a whole, or for particular families. A number of biologists have suggested that homosexuality in animals may work in a similar fashion. One proposal is that homosexual animals, while not reproducing themselves, act as "helpers" in raising the offspring of their relatives, thereby contributing indirectly to the passing on of their own genes. Another idea is that homosexuality, because it is nonreproductive, acts as a self-regulating mechanism to control a species' population growth.⁴ Both of these theories have generated considerable controversy, yet little concrete evidence to either support or refute them has been brought forward. Moreover, neither of these proposals has been evaluated with respect to animals — even though they are directly testable with data from animal species — probably because a comprehensive and detailed survey of nonhuman homosexuality has not been previously available. Once the relevant facets of behavior and social organization are considered, however, it becomes quite clear that neither of these hypotheses can be correct.

Underlying each of these proposals is the assumption that animals who engage in homosexuality do not reproduce (and must therefore "contribute" in some other way) — yet this is patently false. As we saw in earlier chapters, bisexuality is widespread in the animal kingdom: in more than half of the mammal and bird species in which homosexuality occurs, at least some individuals engage in both same-sex and opposite-sex interactions. Moreover, actual breeding by animals who participate in {170} homosexuality has been verified in more than 65 species. This includes animals who are heterosexually paired and raise offspring but have outside homosexual interactions (Greenshanks, Little Egrets, Tree Swallows, Gray-capped Social Weavers); animals who engage in homosexuality as single parents (Japanese Macaques, Hanuman Langurs, Northern Fur Seals); animals who raise offspring in bisexual trios or quartets (Black Swans, Greylag Geese, Oystercatchers, Jackdaws) or in same-sex pairs as a result of outside heterosexual matings (Ring-billed Gulls, Western Gulls); females who participate in homosexual activity while pregnant (Gorillas, Takhi, Vicunas) or even while their infants are clinging to them (Bonobos); animals who breed at some point in their lives prior to or following a period of homosexuality (Orang-utans, Rufous Rat Kangaroos, Emus, Silver Gulls, Bicolored Antbirds); homosexuality among those individuals in a population who monopolize most of the breeding opportunities (Nilgiri Langurs, Mountain Zebras, Bighorn Sheep, Ruffs, Pukeko); and animals that have incestuous homosexual relations with their own offspring (White-handed Gibbons, Red Foxes, Livingstone's Fruit Bats, Ocellated Antbirds). Thus, animals use multiple strategies to combine homosexuality with breeding, and even animals who may "prefer" homosexuality or have more same-sex than opposite-sex interactions can successfully raise offspring.⁵ It is simply not true that animals who participate in homosexuality are unable to reproduce and pass on their genes to future generations. Of course, some animals are exclusively homosexual and never reproduce (as discussed in chapter 2) or else are unsuccessful breeders in either a heterosexual or a homosexual context, but reproduction is most definitely not limited to animals that only have heterosexual contacts.

Setting aside the fact that the initial premise of these two hypotheses is incorrect, is there nevertheless any validity to the substance and implications of each of these proposals? As it turns out, the animal world offers us a ready-made natural "laboratory," as it were, to test the first hypothesis, that homosexual animals act as "helpers" for other members of their own species or families. Numerous animals have developed a variety of "helping systems" in which individuals contribute to the care and upbringing of youngsters that are not their own offspring (although they may be relatives). These arrangements take several different forms: communal or cooperative breeding systems (group-living arrangements in which only some animals breed while the others assist them); "day-care" systems such as creches or nursery groups, in which youngsters from {171} more than one family are pooled together and watched over by one or two caretakers; alloparenting, in which individuals assist parents in duties such as feeding, protecting, carrying, or even "baby-sitting" their offspring; and adoption, involving foster-parenting of orphaned, lost, or abandoned youngsters.⁶ Yet virtually none of these helper systems is preferentially "staffed" by homosexual animals or associated in any particular way with homosexuality. True, some individuals that engage in homosexuality certainly do act as helpers in some of these systems, but there is not a privileged association between homosexuality and helping as has been hypothesized. In fact, in some instances the connection between homosexuality and helping is the exact opposite of what is predicted by this hypothesis.

Consider the example of communal breeding systems: this form of social organization is especially prevalent among birds, where it is found in at least 222 species — yet homosexuality occurs in only 8 (4 percent) of these.⁷ Although caution must always be exercised when drawing conclusions based on the absence of homosexuality in a species, nevertheless this proportion is far less than would be expected if helpers were somehow predisposed to homosexuality, or if individuals that participated in homosexuality were somehow predisposed to helping.⁸ Moreover, in each of these 8 cases the specifics of which birds participate in homosexuality and/or helping do not follow the predicted patterns. In Pukeko and Gray-capped Social Weavers, for example, only breeding birds, not their helpers, engage in homosexuality — directly counter to what is predicted by this hypothesis. In other cases, homosexuality is not limited to helpers, but is also found in breeders: all Acorn Woodpecker communal group members — breeder and helper alike — participate in same-sex mounting, while in Tasmanian Native Hens, Dusky Moorhens, and Mexican and San Blas Jays, homosexuality occurs in both breeders and helpers, but only in a small proportion of each (i.e., many or most helpers do not engage in same-sex relations at all). Finally, homosexuality in Pied Kingfishers is characteristic of neither breeders nor helpers: rather, a subset of the nonbreeding population that does not participate in the helper system is involved in same-sex activity.⁹

Likewise, the other forms of parental help found in animals do not support any connection between helping behavior and homosexuality. Creches, alloparenting, and adoption occur in numerous species without homosexuality. Of those mammals and birds in which at least some individuals do engage in homosexual activity, these types of helping systems are found in less than a third of the species, and they also occur in less than half of the species in which at least some individuals are exclusively homosexual. Moreover, in none of these cases is there a specific association between homosexuality and helping. For example, in many animals helping is performed only by members of the sex in which homosexuality is absent (e.g., Nilgiri Langurs, in which females may help take care of each other's offspring, but only males participate in homosexuality) or else it is characteristic of (heterosexual) breeding animals who assist other heterosexual breeders (for example, parents who take turns watching over a creche, or who help feed and protect other parents' youngsters).¹⁰ In no instance is helping restricted to animals that engage exclusively, primarily, or even sporadically in homosexuality, nor is it even more prevalent in such individuals.¹¹ In some species we find even more confounding {172} situations: among Hanuman Langurs, for instance, "helpers" actually enable breeding animals to participate in homosexual activity. Mothers in this species often engage in same-sex mounting, but only when they have been temporarily "freed" from their parental duties by other individuals who "baby-sit" their young.¹²

What about the idea that homosexuality acts as a mechanism to regulate population growth? Again, little concrete evidence supports this hypothesis, and there are also serious problems with its underlying premises.¹³ Aside from the fact that many animals engaging in homosexual activity continue to reproduce (as already mentioned), it is unlikely that population growth would be seriously affected even if a large proportion of animals were exclusively homosexual. Most animal populations can and do support large numbers of nonbreeding individuals without suffering a decrease in numbers: indeed, in many species a majority of individuals do not reproduce without any adverse effects on the population as a whole. In Damaraland mole-rats, for example, 90-98 percent of all individuals never breed during their lifetime, yet the population sustains itself and even continues to grow. Scientists have also calculated that a stable Killer Whale population can include up to 30 percent nonreproducing females without experiencing any decline. A significant pool of nonbreeding individuals exists in many other species, and up to 90 percent or more of one sex may fail to mate and/or breed.¹⁴ Thus, exclusive homosexuality on a much more massive scale than that seen in any species would have to occur before homosexuality could even begin to impact on population growth and size.

A number of animals experience periodic and often dramatic fluctuations in their numbers, sometimes undergoing regular five- or ten-year cycles of population increase and decrease — for example, snowshoe hares, lemmings, voles, and some species of finches, sandpipers, falcons, and grouse.¹⁵ If homosexuality were correlated with population size, one might expect that it would feature prominently in such species. One might also predict that its occurrence would "shadow" or fluctuate along with the population cycles, becoming more prevalent when population size or growth rate reaches its maximum, and less prevalent or nonexistent when the population is at its ebb. In fact, homosexual behavior has not been reported for most such species, and in the few cases where it has — Scottish Crossbills, Kestrels, and Grouse, for example — it does not appear to be related to either the cyclic or the irregular population increases ("eruptions," as they are sometimes known) that occur in these species.¹⁶

Similarly, if homosexuality actually resulted in a significant decrease in population growth, one might expect it to be disproportionately represented among animals that are suffering a severe decline in numbers, i.e., in endangered species. However, of the 2,203 mammals and birds in the world that are currently classified as threatened (either critically endangered, endangered, or vulnerable), homosexuality has been documented in just over 2 percent of these.¹⁷ Moreover, the distribution of homosexuality across different species clearly has nothing to do with their endangered status: there are examples of two closely related species, such as the Pukeko and the takahe — two birds of New Zealand — in which homosexuality only occurs in the nonendangered one (the Pukeko); or animals in which one subspecies is endangered (e.g., the Asiatic Lion) yet homosexuality is not restricted to this {173} subspecies; or else cases in which one or more subspecies are threatened (e.g., the Baja California and Sonoran Pronghorns), yet homosexual behavior is found in the nonthreatened subspecies of the same animal (the American Pronghorn); or two closely related species, in one of which homosexuality is common yet the species is not endangered (Hanuman Langur), the other in which homosexuality is much less common but the species is threatened (Nilgiri Langur). Conversely, if homosexuality were a form of self-preservation for a species as a whole — a "safety-valve," as it were, activated in times of overpopulation — one would not expect to find it at all in animals suffering severe population declines. Nevertheless, same-sex activity is reported in at least 50 endangered species. Perhaps the most dramatic example is the nearly extinct Black Stilt: less than 50 of these birds are left in the wild, yet some individuals still form lesbian pairs.¹⁸

Animals are perfectly capable of "regulating" their population size with far more efficient and effective strategies than homosexuality. A wide variety of mechanisms for reducing density and/or growth rates have been documented, including emigration, stress-induced hormonal changes that inhibit reproduction, decreased fertility, delayed maturation or slowed development, infanticide, and cannibalism (not to mention "outside" checks on population size such as predators).¹⁹ In summary, then, it appears that homosexuality is neither useful to the species as a way of controlling population growth, nor useful to individual families as a mechanism whereby breeding animals are supplied with nonbreeding "helpers."

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 {174} 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 {175} 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 {176} 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 {177} 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 {178} 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 {179} 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 {180} 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 {181} 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.
{182}
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 {183} "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.

Homosexuality in the Service of Heterosexuality

If homosexuality does not enhance reproductive performance or act as a population regulator or "helper" system, then how else might it be evolutionarily "useful"? A number of scientists have suggested some other ways that homosexual behavior could contribute, directly or indirectly, to heterosexual activity and/or breeding. In this section, we'll look at several of these proposals, including suggestions that homosexuality is a way of practicing heterosexual mating, a method to attract opposite-sex partners, a form of competition to reduce the heterosexual mating opportunities of rivals, and several other more far-fetched "explanations."

Practicing Homosexuals
      Same-sex activity is often claimed to be a way that younger animals practice or "rehearse" heterosexual courtship or mating, or a way for individuals to gain sexual "experience" that will improve their future breeding success.⁴³ While it is possible that homosexuality could provide this "service," it is unlikely that this is its major function. A serious problem with this proposal — as noted by several scientists — is that in most of these species homosexual behavior is not restricted to younger individuals or those who need to acquire sexual experience.⁴⁴ In some cases, it is found in all age groups (Walruses, Northern Elephant Seals, West Indian Manatees), in others it is more prevalent in younger animals but still occurs in older ones (Killer Whales, Giraffes), while in some cases it continues throughout an individual's life (Black-headed Gulls).⁴⁵ Moreover, in these and many other species there are frequently other patterns of homosexual or bisexual orientation that stretch the limits of a "practice" interpretation nearly to absurdity. For instance, are animals who engage primarily or exclusively in same-sex activities "practicing" their whole lives for some never-to-be achieved heterosexual opportunity? Or how about individuals who intermingle or alternate between homosexual and heterosexual activity — do they need to constantly return to same-sex behavior for remedial "practice"? And what about animals who "switch" to homosexuality only after they have been involved in heterosexual activity, or who come to homosexuality late in their lives — are their prior heterosexual involvements then "practice" for their homosexual ones?

When faced with these and other examples of homosexuality "persisting" or (re)appearing in adulthood, advocates of the "practice" interpretation have been forced to adopt exactly such unconvincing scenarios. For example, scientists have actually argued that individuals continue to engage in homosexuality as adults so that they can experience differences in sexual behavior across a wide variety of partners (of both sexes) and thereby continue to improve their heterosexual performance — an ironic reversal of the traditional view, in which homosexuality is {184} considered to detract from, or be incompatible with, heterosexuality.⁴⁶ According to this "practice" interpretation, heterosexual "competence" is apparently so elusive (or difficult to achieve and maintain) that it requires constant, albeit indirect, reinforcement through the help of homosexuality. When we examine the realities of animal behavior we find that in many cases heterosexual mating is far from the automatic or "natural" occurrence that it is commonly assumed to be, and it does require some "practice" (see the next section). However, this "explanation" does a disservice to both heterosexuality and homosexuality in its view of the former as unnecessarily tenuous and the later as necessarily derivative.

Even in species where homosexuality is limited to younger animals or to adult-juvenile interactions, there are often serious discontinuities in participation that challenge a practice interpretation. For example, in the Guianan Cock-of the-Rock, homosexual courtship and mating occur between adolescent and adult males and have been classified as "practice" behavior on the part of the younger males. However, there is a curious gap in the age distribution of participating males: primarily one-year-olds are involved, while two-year-olds almost never participate in such activity. Could it be that once they pass the yearling stage, they no longer need any "practice"? Most definitely not: scientists studying this species report that when males first acquire their own territories, between the ages of three and five, they continue to practice their courtship — but largely without homosexual interactions — thereby gaining valuable experience that they will need before embarking on heterosexual mating.⁴⁷ Why should birds first "practice" using homosexuality as one-year-olds, then cease such practice as two-year-olds, only to resume practice without homosexuality as three-to-five-year-olds, and then once again participate in homosexual "practice" sessions with younger males when they become older? And what exactly is the role of the adult males who willingly participate in all of these "practice" sessions? It seems unlikely that they need to "improve" their skills, too, or that they are simply serving as "mentors" to (probably unrelated) males, altruistically providing them with the opportunity to rehearse their mating skills. Although younger males may gain sexual and courtship experience as an indirect result of homosexual interactions, this appears to be a relatively minor by-product of such activity and is highly problematic as an overall "explanation" for the behavior.⁴⁸

There are other questionable aspects to the notion that homosexual behavior is merely rehearsal for heterosexual behavior. In many species where a "practice" interpretation has been suggested, only a small fraction of the population ever engages in same-sex activity, and often an individual participates only a handful of times. It seems highly unlikely that much sexual experience, or any useful "training," could be gained from such activity.⁴⁹ Moreover, in many species young animals practice heterosexual behavior by participating directly in heterosexuality, either with adults or with each other. In other animals — including ones in which adults engage in homosexuality — heterosexual practice is accomplished without partners or overt same-sex activity. For example, adolescent male Sage Grouse learn the complex courtship display of their species by imitating older males, practicing the "strutting" movements and sounds while they are gathered in their own groups {185} on the periphery of the breeding grounds. Occasionally an older male joins the group so that he can — in the words of one ornithologist — "demonstrate the fine points of strutting to the rapidly maturing novices," but no homosexual courtship or copulation takes place, and in fact homosexual activity in this species is limited to adult females. Among Montagu's harriers and several other species of raptors, young birds are trained in heterosexual courtship displays by parents of both sexes without any homosexual activity.⁵⁰ Even if homosexual behavior were training for heterosexuality, this raises more questions than it answers. Why must some animals "resort" to same-sex practice while others can use opposite-sex interactions (or solo practice)? Why does homosexual "training" in some species involve adults "helping" younger animals, while in other species juveniles only "practice" amongst themselves? And why do some individuals apparently not need to "practice" at all? It is clear from these examples that a "practice" interpretation of homosexuality is at best of limited applicability and explanatory value.⁵¹

Finally, there is a curious gender bias in the application of a "practice" interpretation to homosexuality — in the overwhelming majority of cases, only male animals are said to require such rehearsal.⁵² Where complicated courtship displays are performed only by the male of the species, this is perhaps understandable, but why should it be that no female needs to "practice" sexual activity by engaging in same-sex activity? In many animals, especially primates, females are active participants in heterosexual intercourse, often initiating sexual activity and adopting specific postures, positions, or movements as part of a sexual interaction. In most bird species, heterosexual copulation is impossible without the cooperation and active participation of the female: since most male birds do not have a penis, mating can usually only occur if the female actively facilitates the interaction, for example by positioning herself in such a way as to allow genital contact. Yet in none of these species has it been suggested that females "practice" heterosexual mating via homosexual copulation — not because practice isn't required, or because lesbian activity could not serve this "function," but because many scientists still regard the female as an essentially passive participant in sexual activity.⁵³ This is highly revealing — not only of sexist attitudes in biology, but also of the true "utility" of this explanation. It is not applied systematically and carefully to all potentially relevant cases: more often than not, it is simply introduced when most other "explanations" have failed, a convenient tool with which to discount or dismiss homosexual activity.

Homosexuality as a Breeding Strategy
      Some nonsexual interpretations of homosexual activity discussed in the previous chapters hinge on the indirect contribution of homosexuality to heterosexuality. For example, it has been suggested that homosexuality reinforces group cohesion and social bonds between individuals, thereby improving their well-being and allowing them, ultimately, to reproduce more successfully. It has also been claimed that homosexual "alliances" between animals improve their chances of gaining heterosexual copulations.⁵⁴ Some scientists have been even bolder in their view of the connection between homosexual and heterosexual activity, regarding {186} the two to be directly related or even essentially continuous: same-sex activity is seen as simply an alternative breeding strategy adopted by some animals, or a way to attract or acquire partners of the opposite sex.⁵⁵ It has been proposed, for example, that female Rhesus Macaques sometimes form homosexual consortships to gain access to a male who is himself consorting with their female partner, or that male Bottlenose Dolphins form pairs with each other to seek out female partners.⁵⁶

Another standard "explanation" for homosexual activity among females, especially mammals, is that it attracts males and stimulates them to mate heterosexually. It has also been suggested that female mammals mount each other primarily when one or both partners are in heat, and hence homosexual activity acts as a signal to males of when females are ready to mate. A variation on the notion of homosexuality as a stimulant for heterosexuality is the speculation that males stimulate their own libidos by engaging in same-sex activity (rather than attracting female partners). For example, erotic fighting in African Elephants (during which both participants become sexually aroused) is claimed to stimulate the males so that they can then go out and seek female partners, while male homosexuality in Greenshanks and Golden Plovers is claimed to stimulate and strengthen the birds' heterosexual drive.⁵⁷

Most of these rather fanciful speculations are not based on any systematic evidence, and in fact there are many arguments against such interpretations. To begin with, homosexual activity in many species is not restricted to the breeding season (i.e., the time when it could "stimulate" heterosexual mating) or to females who are in heat. In more than a third of the mammals and birds for which information is available concerning the chronology of homosexual activity, it occurs either year-round (i.e., both in the breeding and nonbreeding seasons or in females regardless of whether they are in heat or fertile), or else only during the nonbreeding season.⁵⁸ In some cases, the majority of homosexual activity occurs when females cannot conceive, e.g., when they are pregnant (some populations of Japanese Macaques) or during nonfertilizable stages of their cycle (Hanuman Langurs),⁵⁹ and therefore it cannot contribute to heterosexual mating.

Furthermore, even when homosexual activity does take place during the breeding season or at times when females can conceive, cases where it attracts members of the opposite sex or stimulates heterosexual mating activity are the exception, not the rule. In most species, other animals are entirely disinterested, nonchalant, or "underwhelmed" by any same-sex activity they may happen to observe (as discussed in chapter 2). Members of the opposite sex are often entirely absent from the vicinity (Hanuman Langurs) or may even stay away or leave when homosexual activity is taking place (Guianan Cock-of-the-Rock) or be chased away or ignored when they attempt to interact with animals engaging in homosexual activity (Japanese Macaques, Hanuman Langurs). Moreover, in many species homosexual alliances do not actually "improve" their participants' chances at gaining opposite-sex partners, and the reproductive advantages of same-sex coalitions are often questionable. Male Calfbird companions who display together, for example, do not attract females, nor are they more successful at acquiring mating territories or overcoming rivals than "single" males. Male Cheetahs living in same-sex bonded coalitions (pairs or trios) {187} are no more likely to encounter females than are single males (even though the standard interpretation of such bonding is that it enhances males' reproductive opportunities and access to opposite-sex partners). They may in fact suffer reduced chances of heterosexual mating (and lowered reproductive output) because of competition or direct interference from their companions. Likewise, although coalitions of male Savanna Baboons sometimes cooperate in obtaining or defending female partners, one researcher points out that this is true for only one-quarter to one-third of all such alliances, concluding that most male partnerships serve many purposes besides obtaining mates and may even lack a recognizable "function."⁶⁰

The case for male pair-bonding being solely a breeding strategy in Bottlenose Dolphins is also far from definitive. Pairing or "coalition" formation between males of this species is often interpreted — and widely cited — as a means whereby the animals obtain heterosexual mates. Although pairs (and trios) of Bottlenose males may cooperatively seek out and herd females for purposes of mating in some populations (e.g., Australia), this is not a uniform aspect of such partnerships, and in many cases it has yet to be documented. Heterosexual matings resulting from such associations have not in fact been observed in the Florida population where the most extensive study of male pairing has been conducted, nor in Ecuador, where it has recently been suggested that paired males may compete for females. In Australia, where herding and mounting of females by paired males have been observed, no "full" copulations involving penetration have actually been documented, so the reproductive status of this behavior is not clear. Moreover, nearly 38 percent of the animals herded by paired males in Australia were not definitvely sexed: researchers simply assumed that they were females. In fact, bonded males in other populations seek out male rather than female sexual partners in at least some contexts. In the Bahamas, pairs or coalitions of adult male Bottlenose Dolphins herd and chase Atlantic Spotted Dolphins; they typically pursue homosexual activities (including full penetrative copulation with other males) during these interspecies encounters. Finally, even if bonded males assist each other in obtaining heterosexual mates, this does not preclude a homosexual dimension to such partnerships — sequential and simultaneous bisexuality are, after all, prominent in this species. Same-sex pairs can form as long as ten to fifteen years before breeding activity commences, and homosexual activity may exist concurrently with heterosexual activity in such pairs once they do reach breeding age.⁶¹

One species in which same-sex activity among males sometimes does attract females is the Ruff. As already noted, however, homosexual behavior in this bird is not limited to contexts in which it might increase opportunities for heterosexual mating. It also occurs among nonbreeding males, when females are not present, and during the nonbreeding season. Similarly, homosexual activity in female Squirrel Monkeys sometimes does arouse the attentions of males. However, it is clear that the participating females engage in such behavior regardless of whether it draws males and even rebuff the advances of males who approach them during such activity. Sometimes heterosexual behavior serves as a stimulant for homosexual activity and not the other way around. Stumptail Macaques, aroused by the sight of heterosexual activity, often initiate same-sex interactions, while in Wolves, Savanna {188} (Yellow) Baboons, and Mountain Sheep, animals watching heterosexual mating often become excited and engage in homosexual activities.⁶²

Even if males of some species are genuinely aroused by sexual activity between females, the evidence clearly shows that females are unconcerned with the effect of their behavior on males and do not structure their participation in homosexuality to maximize its impact on heterosexuality. Yet in spite of all this counterevidence, biologists still claim that a primary "function" of homosexual activity in females is to arouse males: "The sight of one female mounting another is said to excite males sexually in Squirrel monkeys and it may do so to males of other species too, for example men watching pornographic films of lesbian activity."⁶³ By drawing an explicit parallel to human sexuality, the author of this statement hopes to argue for the evolutionary "usefulness" of homosexuality — but the analogy actually highlights the fundamental absurdity of this "explanation," as well as its dependence on cultural rather than biological factors. True, many heterosexual men are aroused by the sight of two women having sex together, and lesbian sexuality is often packaged and trivialized as pornography to be consumed by straight men. But it would be ridiculous to conclude, on the basis of this, that lesbians have sex "in order" to arouse heterosexual men — yet this is exactly the type of reductionist thinking that is routinely applied to homosexual behavior in animals. It is also highly revealing that homosexual behavior among male animals is virtually never described as being stimulating for females.⁶⁴

Perhaps the most widespread version of the idea that homosexuality is really just a form of reproductive behavior concerns same-sex pairing in birds. It is frequently asserted that the "function" of such associations is to allow females to successfully raise young when they are unable to obtain a male mate. Not only is the initial premise of this explanation — that homosexual pairs result from the unavailability of members of the opposite sex — incorrect, but first and foremost, birds do not usually form same-sex pairs specifically to undertake parenting.⁶⁵ Species in which homosexual pairs never attempt to raise young are nearly as common as {189} those in which same-sex parenting does occur. Even in those species where female pairs lay eggs, the proportion of their eggs that are actually fertile is usually low, indicating that the females do not mate with males or "try" to raise a family — fertil — ity rates as low as 0 percent for Kittiwakes, 0-15 percent for Western Gulls, 4-30 percent in Herring Gulls, 33 percent for Silver Gulls, and 8 percent in some populations of Ring-billed Gulls have been documented.⁶⁶ In addition, female pairs whose clutches are entirely infertile have been reported for Mute Swans, Black-winged Stilts, Roseate Terns, Blue Tits, Red-backed Shrikes, King and Gentoo Penguins, and Lovebirds (among others). Female Jackdaws who have lost their male partners sometimes pair up with nonbreeding females. However, these associations develop regardless of whether the widow has young, demonstrating that females do not form same-sex associations solely for the purpose of obtaining help in raising offspring. Moreover, only 10 percent of widowed females are involved in homosexual pairs, so even if such partnerships were "reproductively" motivated, it remains to be explained why only some females take advantage of such alternative parenting arrangements.

Furthermore, there are several different forms of same-sex parenting among birds (and other animals). In some cases, individuals develop full pair-bonds with their coparent, including courtship and sexual activity, and the partnership typically exists prior to and extends beyond the duration of parenting (e.g., Western Gulls, Black-winged Stilts). In other species, partners who already have offspring simply enter into a joint-parenting arrangement with no associated courtship or sexual activity between them, often lasting only until the young have been raised (e.g., Lesser Scaup Ducks). In still other cases, animals develop an intermediate arrangement, with "platonic" coparenting between individuals who may nevertheless continue to associate together even when not breeding (e.g., Acorn Woodpeckers, Squirrel Monkeys). And finally, in many species (e.g., Greylag Geese, Oystercatchers), individuals form bisexual trios that parent their offspring together (often contrasting with heterosexual trios and/or homosexual pairs within the same species).⁶⁷ All four types of arrangement could be interpreted as "strategies" to raise young, yet the differences between them remain unaddressed if homosexual associations are seen strictly as coparenting arrangements.

The putative benefits of same-sex breeding associations are also generally belied by the fact that not many individuals take advantage of them. The proportion of birds who participate in homosexual pairings or joint parenting arrangements is often relatively small — much smaller, in fact, than would be expected if this were simply an efficient or beneficial reproductive strategy. For example, most male Greater Rheas and Emus raise their young as single parents, but occasionally two males join forces, incubating their eggs in tandem and raising their chicks together. Single parenting can be taxing in these species — partnerless males, for instance, may fast during the entire incubation period, and single Greater Rhea fathers often lose eggs because they can't keep large clutches warm — so it has been suggested that two males may be better equipped to handle the difficulties of parenting by helping each other. However, only a small fraction of nests are tended by two males (less than 3 percent in Greater Rheas): if this were truly a useful parenting strategy, why {190} wouldn't all males — or at least a larger proportion — be using it? Clearly something more — or something else — is involved in associations between males than simply the parenting benefits they may accrue. To further confound the picture, in Greater Rheas both same-sex coparenting and same-sex nest helpers occur. While some males jointly parent the same brood of young, a much higher percentage (about a quarter, still a minority of the population) are assisted by an adolescent male who separately parents one of their nests. Once again, this raises the question of why some males opt for joint parenting, others "choose" to have male helpers, while most do neither. And in many species the supposed advantages of coparenting as opposed to single parenting are in fact illusory. Most female Lesser Scaups raise their young with no help from males, but occasionally two or three females coparent. It is usually assumed that this strategy gives such females an advantage in parenting, but detailed studies of parental investment have shown that same-sex coparents are no more and no less successful than single parents. Moreover, each female in such an arrangement generally spends the same amount of time in parenting duties as do single females, i.e., she is not "relieved" of some of her responsibilities by her companion. In other words, there is essentially no reproductive advantage to joining forces with a parenting partner in this species.⁶⁸

Nor is the occurrence of homosexual pairing in other species correlated with the supposed advantages of having an opposite-sex partner to help with parenting. Even in birds where male-female coparenting is typical, there are often significant differences between species in how essential that biparental care is to successful chick-raising. In some birds, females can raise young without the assistance of a male partner, while in other species the male's contribution is indispensable. If homosexual pairing were somehow related to the (in)ability of single birds to raise young on their own, one would expect same-sex associations to occur in species where biparental care is more important, i.e., where single birds cannot raise young on their own — yet the facts do not support this. Consider two parallel examples: Snow Geese and Black-billed Magpies. Homosexual pairing in female Snow Geese is claimed to allow otherwise single birds to raise young. However, biparental care is not essential for successful reproduction in this species: when females in heterosexual pairs have their male partners taken away from them, they are quite capable of raising their young as single parents. On the other hand, biparental care is essential in Black-billed Magpies, since females are unable to raise offspring on their own when they lose (or are deprived of) their male mates. Yet homosexual pairs of Magpies do not raise young together, nor do widowed females form same-sex pairs in this species (unlike the closely related Jackdaws). This is exactly the opposite of what would be expected if mateless birds were forming homosexual associations to enable them to parent.⁶⁹

In fact, most pair-bonding birds do not form same-sex couples when heterosexual mates desert them or are experimentally removed, indicating that homosexual pairing is not a widespread mechanism for achieving two-parent care (regardless of whether the latter is "indispensable" or simply preferred). Moreover, in those polygamous (non-pair-bonding) species such as the Superb Lyrebird where females could benefit significantly from male parental assistance (and appear {191} to suffer detrimental effects in its absence, such as slowed growth of their offspring), female pairing and coparenting is noticeably absent.⁷⁰ Conversely, same-sex pairing and/or coparenting do occur in many species where single parents routinely raise young successfully. This is true for Hooded Warblers and Mallards (where heterosexual parents almost always separate and become single parents before the young are fledged), and Red Squirrels and Grizzlies (where heterosexual coparenting never occurs as part of these species' polygamous mating systems). In none of these animals is a two-parent family (either heterosexual or homosexual) absolutely required for successful parenting.

To take this line of thinking a step further: in a few species homosexual associations may actually be detrimental to parenting. Besides providing no apparent parental benefits to each other, Calfbird female companions may in fact increase their risk of predator attacks by nesting so close to each other (thereby drawing attention to their location). Female Japanese Macaques in homosexual consortships also do not typically assist their partner with parenting and are often notably aggressive toward their consort's offspring. Homosexual bonding is reproductively disadvantageous for both Oystercatchers and Jackdaws in bisexual trios, for slightly different reasons. Oystercatchers in such associations typically do not jointly incubate their supernormal clutches (only one bird sits on the nest at a time); because each incubator is unable to cover all the eggs simultaneously, the outsized clutch is often not kept adequately warm. As a result, bisexual trio parents hatch fewer eggs and produce significantly fewer fledglings than heterosexually paired Oystercatchers. Female Jackdaws in bisexual trios, on the other hand, do jointly incubate their supernormal clutches. However, because the two females are bonded to each other, both leave the nest together when their male partner arrives to relieve them, and he is unable to cover all their eggs and keep them warm. A parallel effect may occur in Lesser Scaup Ducks: although most female coparents exhibit remarkable cooperative defense of their joint broods, some pairs have been observed flying off together at the approach of a predator, temporarily abandoning their young in the face of danger. Finally, female Canada Geese in homosexual pairs sometimes roll eggs between their adjacent nests, breaking many of them in the process.⁷¹ Clearly, then, successful parenting — and, by extension, reproduction or "perpetuation of the species" — cannot be the whole story behind the formation of same-sex pair-bonds.

Sperm-Swapping and Other Flights of Fancy
      Attempts to determine the evolutionary "function" of homosexuality have sometimes led to even more obscure and implausible "explanations," all revolving (predictably) around heterosexual breeding. For example, some scientists have suggested that homosexuality is a form of reproductive "competition": females have sex (or form pair-bonds) with other females to monopolize their partner's time and thereby prevent her from mating heterosexually, while males mount each other to reduce or redirect their rival's sexual drive.⁷² However, in many species homosexual interactions are actively initiated by the animals who are mounted rather than by the mounters, and the participants often have a friendly rather than a competitive {192} relationship with each other.⁷³ Moreover, there is no evidence that participation in homosexual mounting reduces heterosexual activity — indeed, in some species the opposite is true, for the greatest amount of heterosexual mating is accomplished by precisely those individuals who are also the most active homosexually (as discussed previously). And, as already mentioned, in many animals homosexual activity does not even take place during the breeding season or is only exhibited by a small proportion of individuals.

Another version of this competition hypothesis is that homosexuality is a way of directly interfering with the heterosexual activity of a rival. In a number of birds — Pukeko, Guianan Cock-of-the-Rock, Ocher-bellied Flycatchers, and Buff-breasted Sandpipers — homosexual activity is claimed to be a form of "disruption" whereby one male prevents another from mating with a female, while possibly also "usurping" his partner and mating heterosexually himself. The specifics of same-sex courtship and mating in each case, however, do not support this interpretation. In Pukeko, for example, males do sometimes interrupt heterosexual mating attempts by inviting the other male to mount them, but they do not generally take advantage of the situation to mate with the female partner. Moreover, this occurs only infrequently, and males are more likely to ignore heterosexual matings by other males or watch them without interfering than they are to try to prevent them from occurring. In addition, even if a male were trying to use homosexuality as a way to disrupt a heterosexual mating, this strategy would not "work" unless the other male found the prospect of mounting him more appealing than completing his heterosexual copulation. Ironically, then, a "disruption" interpretation of same-sex mounting in this species — typically presented as an example of the primacy of heterosexual relations — actually entails the assumption that male Pukeko would prefer homosexual activity. In Ocher-bellied Flycatchers, the suggestion that males are trying to disrupt heterosexual matings, or to gain access to females, is entirely speculative. Males have never been seen mating with a female as a result of a homosexual interaction in this species, and in fact females are not even present during the majority of courtship pursuits between males. Homosexual activity is also classified as a form of courtship "disruption" in the Guianan Cock-of-the-Rock, yet there is little evidence in favor of this explanation. As much, if not more, homosexual activity takes place when females are not present on the male's display territories, and males who initiate such "disruptions" almost never gain access to members of the opposite sex as a result and have rarely even been observed mating with females. Furthermore, visits by yearling males involving homosexual activity are distinct from true courtship disruptions, which are performed by rival adult males. Yearling visits are directed toward a wide variety of males, all of whom cooperate in the interaction. In contrast, rival males target only the most successful heterosexual breeders and are violently attacked by the males they try to disrupt. In addition, same-sex interactions are sometimes directed toward adult nonbreeders, who do not participate in heterosexual mating at all, so it is difficult to see how this could be a form of "disruption."⁷⁴

One species in which at least some homosexual activity appears to be genuinely associated with disruption of heterosexual mating is the Buff-breasted Sandpiper, {193} in which rival males often interrupt each other's courtship attempts by mounting and pecking them. However, even in this case, the benefits of such activity are not clear-cut, since "disruption" does not always result in more favorable mating opportunities for the "disrupter" or reduced mating for the "disruptee." Although a "disruptive" male is often able to lure females away from his rival, in other cases he may keep returning to mount the rival without trying to mate with any females. In addition, detailed studies have shown that a male's success at copulating with females is not in fact related to his ability to repel disrupting males. Moreover, not all homosexual mounting is directly involved with disruption of heterosexual courtship, while many disruptions occur without any homosexual activity.⁷⁵ This brings up a point that is also relevant for other species. Many animals — including ones that exhibit homosexuality in other contexts — use direct tactics to interrupt or harass heterosexual matings. These include threatening or physically attacking couples during copulation, and trying to pull or dislodge the partners from each other. Even if homosexual behavior were in some instances being used as a form of heterosexual disruption, it would still remain to be explained why some species — or only some individuals in a species — resort to this fairly unusual and indirect strategy, when more effective and efficient measures are available.

Other zoologists have proposed, in all seriousness, that homosexual copulation is a way of transferring or "swapping" sperm between same-sex partners for heterosexual (breeding) purposes. For example, one ornithologist has suggested that a male bird might deposit his sperm in another male's genital tract during a homosexual mating so that the latter would then pass it on to a female during heterosexual copulation, indirectly fertilizing the female with the first male's sperm.⁷⁶ Not only is this explanation highly implausible, it is factually incorrect for many species. Homosexual matings often take place outside of the breeding season or when females are nonfertilizable. In addition, male birds often solicit homosexual mounts from other males or actively facilitate homosexual interactions, which should not occur if they are a form of "insemination rivalry." Finally, male birds frequently defecate when they are stressed (birds use the same orifice for all excretory and sexual functions) — thus, if same-sex activity were not consensual, males could easily empty their genital tract of any sperm that might have been put there by a rival male.⁷⁷

Even more absurdly, this "explanation" has been proposed for lesbian copulations in Pukeko, where no sperm is directly involved. The claim is that female birds mate with each other to transfer ejaculate between them from previous heterosexual matings. And why exactly would they do this? Zoologists have suggested that this is not so they can "fertilize" each other, but so that they can obscure paternity, i.e., confuse several males as to who is the actual father and thereby "trick" more males into caring for their young. This is implausible, however, since a number of other mechanisms already insure that paternity is obscured and parental care is shared in this species. These include multiple copulations by females with all males in the group, variability in timing of ovulation, absence of mate guarding or copulation disruptions, and an independent tendency of males to be "generous" or "indiscriminate" in their parental efforts (i.e., caring for all chicks regardless of whether they {194} fathered them or even mated with any females at all). Another dubious speculation is that female Pukeko copulate with each other so as to "synchronize" their sexual cycles, thereby allowing them to lay their eggs at the same time (which is thought to be a more efficient reproductive strategy). Once again, there is no evidence that lesbian copulations have this effect.⁷⁸

It's hard to imagine more convoluted and conjectural accounts of homosexuality than these. While many of these ideas are highly unlikely and scientifically unsubstantiated, they can actually be traced to misconceptions about human homosexuality that are deeply entrenched in our culture. For example, the belief that lesbian sexual activity serves to transfer semen from heterosexual intercourse can be found in some of the earliest written records concerning same-sex activity in people. A twelfth-century Irish story about Niall Frassach, a king who died in 778 A.D., makes use of this theme:

A woman came to the king carrying a boy child ... "find out for me who the carnal father of this boy is, for ... I have not known guilt with a man for many years now." The king was silent then. "Have you had playful mating with another woman?" said he. "And do not conceal it if you have." "I will not conceal it," said she. "I have." "It is true," said the king. "That woman had mated with a man just before, and the semen which he left with her, she put it into your womb in the tumbling, so that it was begotten in your womb."⁷⁹

In discussing this curious tale, historian John Boswell remarks that it reveals a "preoccupation with women as bearers and conduits of bloodlines rather than as beings with their own erotic lives and needs."⁸⁰ It is an alarming comment on the "progress" of history that, nearly 900 years later, almost identical ideas about female animals should reappear under the guise of scientific theories, with scarcely any improvement in the perceptions of same-sex activity (or females, for that matter).

What Is Valuable?
      Homosexuality is popularly considered to be nonreproductive or even counter(re)productive. In this section we have considered a wide range of proposals about the possible evolutionary value (and genetics) of homosexuality that challenge this "commonsense" view. These proposals concern ways that homosexuality might somehow contribute to the perpetuation of the species, either directly (for example, by improving an animal's reproductive prowess or increasing its heterosexual mating opportunities) or indirectly (for example, by providing breeding animals with "helpers" or acting as a population regulation mechanism). Implausible as some of these ideas may sound, many aspects of animal homosexuality run counter to preconceived ideas, not the least of which is the widespread participation of breeding animals in homosexual activity. A number of other unexpected phenomena in several species led us to consider further whether some of these proposals might actually have some explanatory value. Examination of deeper patterns within a broader range of animals, however, as well as more rigorous investigation {195} of specific cases, showed that they do not. Thus, in the end we have arrived back at our starting point: homosexuality, whether in breeding or nonbreeding individuals, does not generally contribute to the reproduction of the species. This is an obvious point, perhaps, but one whose very obviousness has usually precluded a serious investigation of its validity. And so once again we are confronted with the evolutionary "paradox" of homosexuality: Why does same-sex activity persist — reappearing in species after species, generation after generation, individual after individual — when it is not "useful"?

Part of the problem is that "usefulness" or "value" in most biological theorizing is narrowly defined to refer only to reproduction. A common thread running through each of the proposals considered in this section is that they view homosexuality only in terms of how it could contribute to breeding or facilitate mating relations between males and females, rather than in terms of any intrinsic value it might have. This brings us to the final, and overarching, problem with all such "evolutionarily valuable" explanations. Scientists have often been led to absurd conclusions about the putative "function" of homosexuality precisely because evolutionary theory cannot readily countenance behaviors that are apparently "useless" — and for a behavior to be "useful" it must contribute in some way to mating and reproduction. Perhaps it is the very notion of "utility" or "value" that needs to be reexamined. In the realm of human culture and biology, the idea that life revolves around heterosexuality and that everything in life can be related, ultimately, to reproduction — a view sometimes known as heterocentrism or heterosexism — is currently being challenged on a number of fronts.⁸¹ Yet this view would appear to be a self-evident truth where animals are concerned, since the passing on of genetic material through reproduction is considered to be the very foundation of biology and evolution. In the next section we will see that, on the contrary, this belief is as incomplete a description of animal biology as it is of human society.

Nonreproductive and Alternative Heterosexualities in Animals

The primary reason that animal homosexuality is considered problematic by many scientists and "abnormal" by many nonscientists — and therefore in need of "explanation" — is that it does not lead to reproduction, and reproduction is considered the be-all and end-all of biological existence. However, animal life and sexuality are not organized exclusively around procreation. Just as there is a multiplicity of kinds of homosexuality in the animal world, so, too, there are innumerable ways that males and females interact (sexually and otherwise) with each other, only some of which involve reproduction. In this section we'll explore a wide variety of nonreproductive and alternative heterosexualities: nonbreeding individuals, male-female segregation and hostility, "alternative" parenting and pair-bonding arrangements, and nonprocreative sexual practices. Some form of nonreproductive heterosexuality has been observed in nearly every animal species, far exceeding the incidence of homosexuality. So extensive is this phenomenon that, in the discussion that follows, we will only be able to give the barest indication of its scope and characteristics, {196} as we survey a broad range of behaviors and species. For further details, the reader is referred to the profiles of individual animals in part 2, as well as the references contained in the notes to this section.

Life without Procreation: Nonbreeders, Celibacy, and Reproductive Suppression
      It is apparent that in some cases the bulls withdraw entirely from active participation in sexual competition for the herd.
      — S. K. SIKES, The Natural History of the Elephant⁸²

      Virtually every animal population includes nonbreeding individuals. There is a tendency to regard the urge to procreate among animals as instinctual, all-pervasive, and unstoppable. While heterosexual interactions often do have this quality, there are just as many examples of animals who do not reproduce: individuals who actively remove themselves from the breeding cycle, whose nonparticipation in reproduction is guaranteed by the overall social organization of the species or by physiological constraints, who produce offspring rarely (if ever), or who lead complete lives after (or without) reproducing. Many nonbreeding animals are still sexually active; on the other hand, celibacy, abstinence, and other kinds of asexuality are also prevalent in the animal kingdom. The proportion of nonbreeding individuals varies widely between different species, and between different populations of the same species. In some cases, only a few lone individuals are not actively reproductive; at the other extreme are species where more than half (American Bison, Right Whales), three-quarters (Blackbuck, Giraffe), or even 80-95 percent (New Zealand Sea Lions, Northern Elephant Seals, naked mole-rats, some dragonfly species) of one or both sexes do not reproduce.⁸³ Between these extremes, nonbreeders may constitute a quarter (Long-tailed Hermit Hummingbirds) to a third (Common Murres, Kestrels) of the population.⁸⁴

Many types of nonbreeding are found in the animal world, involving individuals of different ages, social circumstances, and varying lifetime reproductive and sexual histories. In hoofed mammals and seals, for example, males often "delay" reproducing for several years after they reach sexual maturity, frequently living in large "bachelor" herds separated from the breeding animals. Although many such animals eventually go on to reproduce, at any given time nonbreeders constitute a large segment of the population, in part because of a preponderance of younger animals in the demographics. In these species as well as others that have polygamous or promiscuous mating systems (where males typically mate with a large number of females without forming pair-bonds with any of them), there are usually also further "mating skews." Only a portion of the male population establishes breeding territories and courts females; of those who do, moreover, only a fraction ever get to actually mate with females and sire offspring. Among Guianan Cock-of-the-Rock, for example, a fifth of the males, on average, do not have courtship territories, while almost two-thirds of the males who do are unable to mate with females. In {197} species that have a ranked form of social organization, it is typically only the higher-ranking males that participate in the most matings. In Squirrel Monkeys and Grizzly Bears (among others) the opposite sometimes happens: the highest-ranking males may fail to obtain any heterosexual copulations at all, due to their greater aggressiveness.⁸⁵ In many animals with communal breeding systems, only one or two individuals in each group reproduce while the others are nonbreeders; many of the latter help the breeding animals raise their young, but in a few species such as Red Foxes and Gray-capped Social Weavers, some nonbreeders do not even contribute to other group members' reproductive efforts as helpers.

A period of temporary nonbreeding can sometimes involve an entire population. In one troop of gray-cheeked mangabeys, for instance, all the females stopped cycling for a period of four months, while no reproduction took place in a population of Musk-oxen for several years.⁸⁶ In other cases, such as Hanuman Langurs, Northern Fur Seals, Mountain Zebras, Red Deer, Ruffed Grouse, Pied Kingfishers, and red-winged blackbirds,⁸⁷ some individuals live their entire lives without ever reproducing, while in some species of mole-rats as well as in Northern Elephant Seals, 90 percent or more of the population never procreates.⁸⁸ Entire flocks of Flamingos often abandon or "give up" on breeding in the middle of a season, or forgo reproducing for three to four years at a time, while individual female Silver Gulls may go as long as sixteen years without reproducing. Although most animals have yearly breeding cycles (sometimes even reproducing more than once a year), others have nonyearly or "supra-annual" cycles. King Penguins and Australian Sea Lions, for instance, have 16-to-18-month cycles, while large mammals such as Elephants, Manatees, and Whales typically reproduce only once every several years. Among White-handed Gibbons, males and females are thought to interact sexually with each other only every two years or so, while Siamang females often space their pregnancies by a couple of years, turning over parental duties to males while they assume leadership roles.

One particularly interesting form of nonbreeding involves "postreproductive" animals: individuals who have bred previously during their lifetime but are now "retired" from reproducing. Menopause and/or a period of nonbreeding in old age were long thought to be uniquely human traits. It was assumed that all animals continued to reproduce until they died, or alternatively, died shortly after they were no longer able to reproduce. In chapter 2 we saw the pitfalls of asserting human uniqueness in any area of behavior, and indeed postreproductive animals are now known to occur in several primate, hoofed mammal, seal, and whale species, and even in some birds such as Antbirds.⁸⁹ In some cases (e.g., male African Elephants), such animals are loners or peripheral to the social organization of the species. In other instances (e.g., Rhesus Macaques, short-finned pilot whales), they are integrated into the social fabric and may even assume central roles.⁹⁰ Among Killer Whales, for example, pods are often led by older, postreproductive matriarchs. Because males remain with their matriarchal group in this species, some pods eventually "die out" (even though they contain breeding-age males) because all of their females are postreproductive. Many postreproductive individuals remain sexually active until their death. Menopausal or old-aged female short-finned pilot whales, Orcas, Japanese {198} Macaques, and Hanuman Langurs, for example, frequently engage in heterosexual (and in some cases homosexual) activity, sometimes with younger partners.

Sexual activity also occurs in other nonbreeding animals. Among birds that typically form heterosexual pair-bonds, for instance, some individuals remain single yet still court or copulate with members of the opposite sex, often during periods when fertilization is not possible (e.g., Oystercatchers, Humboldt Penguins, Hoary-headed Grebes). In many other cases, birds form heterosexual pairs or trios but do not breed — even though they still continue to be sexually active. Researchers even found that some nonbreeding pairs of Canada Geese had higher copulation rates than breeders.⁹¹ On the other hand, many nonbreeding animals are asexual or "celibate," not courting or interacting with members of the opposite sex at all. An interesting variation of this sort involves Japanese Macaques, who sometimes form "platonic" heterosexual consortships, in which either partner may nevertheless interact sexually with other individuals besides the consort. Similar platonic "friendships" are also found between male and female Savanna Baboons. Paradoxically, the opposite situation to sexually active nonbreeding animals also occurs in a number of animals. In several bird species, pairs that are ostensibly involved in breeding actually stop copulating before the female's fertile period has ended, while males of some marine turtles leave the waters where females are located long before the breeding season is over. Although most such animals do reproduce, it appears that in some ways they are not exploiting their reproductive potential to its fullest.⁹²

Why do animals not reproduce? Biologists have coined the term reproductive suppression to refer to various forms of nonbreeding, implying that all animals would breed if they could, but are somehow "prevented" from doing so. However, the underlying mechanisms involved in nonbreeding are far more complex than this term implies. Numerous social, physiological, environmental, and individual factors are implicated, often interacting in ways that are still poorly understood.⁹³ In some animals, procreation is indeed actively "suppressed." In Wolves, for example, dominant pack members often physically attack lower-ranking individuals who try to mate; female Savanna Baboons sometimes form coalitions to attack cycling or pregnant females and prevent or terminate their reproductive efforts; while in many hoofed mammals, higher-ranking males prevent other males from gaining access to females. However, in other species the term suppression is a misnomer, since no coercion is involved. Young American Bison bulls, for instance, are not "prevented" from mating by older males — they simply do not participate to the same extent (as discussed in chapter 4). In other species — particularly birds with communal breeding systems such as the Pied Kingfisher, as well as primates such as tamarins and marmosets — scientists describe individuals not as "unwillingly" suppressed in their reproductive efforts, but rather as "choosing" to forgo reproduction or exercising "self-restraint" in their reproductive participation.⁹⁴ Further evidence that animals are often "voluntary" nonbreeders involves species such as Ocher-bellied Flycatchers and Ruffed Grouse, where prime breeding territories often go unused even though many nonreproducing individuals are in the population. Sometimes physiological mechanisms are involved in nonbreeding, such as lowered hormonal levels, delay of {199} sexual maturation (sometimes indefinitely), inhibition of ovulation, and even blocking of pregnancy following conception (seen in many rodents).⁹⁵

Finally, reproduction is often a physically demanding and exceedingly dangerous undertaking that some animals may simply "avoid." Nonbreeders are often in better physical condition than breeders, since they do not have to experience the rigors of reproducing and parenting. In fact, breeding could even be considered "suicidal" in some cases, since it may lead to a reduced life expectancy. Male Bighorn Sheep and female Red Deer that breed, for example, have significantly higher mortality rates than nonbreeders. In several species of carnivorous marsupials, most males die after mating while nonbreeders generally survive longer. The life expectancy of nonbreeding male Ruffed Grouse often exceeds that of breeding males. And female Western Gulls that breed more often during their lives have a lower survival rate than individuals that are less reproductively "prolific." Sometimes specific biological factors serve to discourage breeding, such as the astonishing phenomenon of clitoral, as opposed to vaginal, births in the Spotted Hyena. Many females of this species die during their first pregnancy or labor because their genital anatomy requires the baby to be born through the clitoris, which ruptures and often results in many other complications for both mother and fetus.⁹⁶ Finally, the risk of acquiring sexually transmitted diseases (which are found in a surprising number of animals) may also affect reproductive activity. For example, female Razorbills (a kind of bird) avoid reproductive copulations with males when the risk for infection from STDs is greatest (although they continue to have nonprocreative sex, i.e., mounting without direct genital contact). Heterosexual behavior in a number of other species may also be curtailed by the potential danger of STDs.⁹⁷

In the end, then, there is no single "reason" why animals don't reproduce: nonbreeding, like sexuality, is simply a part of the fabric of animals' lives, manifesting itself in many different ways. Heterosexuality constitutes a whole range of behaviors and life histories, not a single, inalterable template that every animal must follow. And nonbreeding is one of the many ways to be "heterosexual." Regardless of the number of nonprocreating animals in a particular population or the "causes" of their nonbreeding, one thing is certain: nonreproducing (heterosexual) animals are a ubiquitous feature of animal life.

Worlds Apart: Sex Segregation, Hostility, and the Dark Side of Heterosexuality
      Adult males and females [of the Sperm Whale] have lifestyles so distinct that they might be separate species. The males leave tropical waters each summer and voyage into the highest latitudes ... but females and young seldom venture more than 40deg from the equator.
      — LYALL WATSON, Sea Guide to Whales of the World⁹⁸

      Heterosexual mating is anything but the "natural," effortless activity that it is often portrayed as. There are many ways that sexual interactions between males and females are avoided, exacerbated, or generally fraught with problems. In numerous {200} animals, for example, it almost seems that the social organization and behaviors of the species have been designed to keep males and females apart and prevent reproduction — or at least make it difficult. Consider sex segregation: partial or total separation of males and females is a surprisingly prevalent form of social organization in the animal world. Various forms of sex segregation occur in mammals and birds of all types, though separation of the sexes is especially prevalent in species such as hoofed mammals that have promiscuous or polygamous mating systems (where individuals mate with more than one partner). Often the only time that the two sexes come together is to mate, sometimes for only a few days or months out of the year — the rest of their time is spent living entirely apart. Even "harems" — in which one male associates with a group of females and often prevents other males from gaining access to them — are not the quintessential example of heterosexual mating opportunity that they are usually thought to be. Scientists studying "harems" in a number of species such as sea lions and some hoofed mammals have found that these groups do not always form as a result of heterosexual attraction or males "controlling" females (and thus the term is somewhat inaccurate). Rather, females prefer to associate with each other and therefore they congregate in relatively autonomous groups of their own; males that participate in breeding then end up associating with such groups out of necessity.⁹⁹ In addition to social and spatial segregation — living in separate groups or habitats — sex segregation can also be seasonal or migratory. It may occur only during the nonbreeding season, for example, or involve separate migratory journeys or latitudinal destinations for males and females (for example, in Northern Elephant Seals and Kestrels). One of the most extreme forms of "sex segregation" occurs in several species of marsupial mice: all the males die a few days after the mating season, so that when females give birth there are no adult males left in the population.¹⁰⁰

Sex segregation during the breeding season is often facilitated by a phenomenon known as sperm storage: most female animals have one or more special organs or sites in their reproductive tract that allow them to store a cache of sperm (from a prior mating) for a long time, using it later to "inseminate" themselves while forgoing heterosexual copulations. Birds and reptiles have special glands that allow them to do this. Female Ruffs, for example, often leave the breeding grounds (after having mated with males) and migrate northward, laying their eggs several weeks later by fertilizing them with stored sperm. In some birds such as the fulmar, sperm may be stored by females for up to eight weeks, while in reptiles (as well as insects) sperm stored in females may remain viable for much longer, up to several months or even years. Female garter snakes, for instance, are able to keep sperm for up to three to six months after mating with a male. In fact, females in this species usually do not ovulate until two to five weeks after their first mating in the spring. They may even become pregnant without mating at all that season, simply by using sperm from a copulation that took place the previous fall before hibernation. The record for sperm storage is held by the female Javan wart snake, who can store sperm for up to seven years! In mammals, sperm is generally "stored" for shorter periods (although some bats can do so for more than six months) and may be kept in "crypts" on the cervix or inside the uterus. Recent work has also shown that {201} females in most species can control, through behavioral, anatomical, and physiological mechanisms, which portion of the sperm (if any) is stored and/or utilized for fertilization.¹⁰¹

A phenomenon known as delayed implantation also enables males and females to spend long periods away from each other. In nearly 50 mammalian species (including seals, bears, other carnivores, marsupials, and some bats) the fertilized egg does not implant right away. It remains in "suspended animation" for several months, after which it implants and begins its regular development. The delay extends the pregnancy by two to five months in seals and up to ten to eleven months in badgers, fishers, stoats, and related small carnivores. In seals, this allows females to spend a longer time out at sea — often completely separate from males — and permits them to optimize the timing of their pregnancies and to take advantage of more favorable times of the year for birthing and pup-raising. Some species of bats also have delayed embryonic development, in which the fertilized egg experiences a temporary cessation of development after implantation.¹⁰²

In fact, delayed implantation as well as sperm storage (among a variety of other factors) effectively result in a separation and reordering of key reproductive events in many vertebrates, and consequently an "uncoupling" of male and female reproductive cycles. We are used to thinking of breeding as an ordered progression, one stage leading inevitably to the next: ovulation followed by mating followed by fertilization followed by pregnancy followed by birth (or egg laying). However, there are often significant gaps and rearrangements of these events: sperm storage can temporally separate mating from fertilization, while delayed implantation separates fertilization from fetal development during pregnancy. As noted above, sperm storage can also result in ovulation taking place after insemination, and in other animals, further rearrangements occur. In birds, for example, "pregnancy" or the development of the egg inside the mother's body actually precedes fertilization: the egg yolks are already quite large (and may cause a noticeable bulge and weight increase in the female) prior to being fertilized. In fact, the eggs can be laid without ever being fertilized — this is what allows females in homosexual pairs to produce (infertile) eggs. In most fishes, "pregnancy" ends, rather than begins, with mating: the eggs develop within the female's body and are then laid or discharged when ready to be fertilized (i.e., fertilization typically takes place outside the female's body).¹⁰³ In addition to these delays and reordering of reproductive events, breeding can also, of course, be interrupted or terminated at any of these stages — this will be discussed in the next section, when we look at naturally occurring forms of birth control.

Another common misconception about animal heterosexuality is that only females experience periodic hormonal fluctuations in their reproductive biology. In fact, many male animals also have sexual cycles, entailing considerable periods in which they are sexually inactive and living separate from females. Occasionally, male and female sexual cycles are poorly synchronized or not optimal for breeding, as sometimes happens in Ostriches and Lovebirds. Male cycles are found in a wide range of animals, including primates, deer, seals, and numerous bird species, and usually entail a yearly, rather than a monthly, periodicity. In some instances, {202} dramatic physical and physiological changes are involved. Male Wattled Starlings, for example, undergo regular periods of "balding" (feather loss) and wattle development, and males of many other bird species develop dramatic nuptial plumages associated with breeding. Male Squirrel Monkeys become "fatted" during the peak of their sexual cycle, while male Elephants experience "musth," involving a whole host of changes such as glandular secretions, increased aggression, and rumbling vocalizations.

The significance of male sexual cycles has often been lost or overlooked under sexist biological theories, which tend to emphasize aspects of animal biology that confirm the unflagging "virility" of male animals, to the exclusion of those things that underscore the similarities between male and female sexuality. In fact, reproductive traits that are usually thought to be exclusively male or female can be found in members of the opposite sex in at least some species. Male pregnancy occurs in sea horses, for example, while lactation — milk production from fully functional mammary glands — was recently discovered in male Dayak fruit bats.¹⁰⁴ Females, for their part, can carry sperm within their bodies and "inseminate" themselves (as discussed above) or may possess elongated, phalluslike clitorides that can undergo erections (this is found in numerous mammals, including Spotted Hyenas, moles, and Squirrel Monkeys, as well as several flightless birds).¹⁰⁵ Some animals (e.g., Seals, Bears, Squirrels) even have a clitoral bone, homologous to the male's baculum or penis bone in these species; in female Walruses, this bone may be over an inch long. Female pipefish and Japanese sea ravens (a kind of fish) even have extendable genital organs used to penetrate or retrieve sperm from their male partners.¹⁰⁶

When males and females do manage to get together, a formidable set of obstacles often stands in the way of achieving sexual contact and, ultimately, reproduction. Refusal or indifference by either the male or female partner is widespread and routine in the animal kingdom, and heterosexual matings are often "incomplete" in the sense that they do not involve erection, genital contact, ejaculation, and/or insemination. In one study of Chaffinch heterosexual copulations, for example, every "complete" and "incomplete" mating attempt was logged: out of 144 attempts, only 75 (52 percent) involved mounting with full genital contact (and therefore could potentially have led to fertilization). Of the remaining "unsuccessful" attempts, 76 percent entailed no mounting at all because one or both partners fled before copulation could take place, 9 percent involved the male mounting without attempting to make genital contact, in 8 percent mounting was terminated when the female refused to continue (in some cases after being pecked by the male), in 5 percent of the mounts the male slipped off the female's back, while in 1 percent of the cases the male mounted in a reversed head-to-tail position and therefore did not make genital contact. In African jacanas, only about one in four sexual solicitations by the female result in the male actually mounting her.¹⁰⁷ In some species, completion of the sexual act is prevented because of interference from other animals, who actively harass males and females while they are copulating. This is typical of many primates, but has also been reported in some birds such as King Penguins, Kittiwakes, and Sage Grouse.¹⁰⁸
{203}
In a number of animals, it appears that male and female anatomy are not ideally suited to heterosexual interactions. The female Elephant's vaginal opening, for example, is much farther forward on her belly than in other mammals. Although the male's penis has a special shape and muscles that allow it to reach the female's genitals, he still often experiences considerable difficulty in achieving penetration and may end up ejaculating on her anus or otherwise outside her body. Moreover, it is not true that male and female genitals always fit together like a "lock and key": in many species the structural "compatibility" of the sex organs is less than perfect. In addition, the female's internal reproductive tract in most animals is — in the words of several zoologists — a tortuous, obstacle-ridden pathway that is "remarkably hostile to sperm." Its structure, chemical composition, and immune response to semen are actually designed to prevent most sperm from ever achieving fertilization, in part to protect the female from possible infection (sperm are, after all, "foreign" bodies) and in part to allow her to control paternity. ¹⁰⁹ Males and females may be anatomically incompatible in other respects as well. Biologists studying Musk-oxen have observed that the male's build — a deep chest with short legs, and most of his considerable weight concentrated in the front half of his body — is decidedly ill-suited to mounting and clasping the female, and studies have shown that males are able to successfully mount females less than a third of the time.¹¹⁰ In many other species of hoofed mammals and seals where there is a significant size difference between the sexes, females often fall or are crushed under the weight of the male during copulation and may suffer serious (even lethal) injuries.

Sometimes outright hostility erupts between males and females, including chasing and harassment, as well as actual aggression, violence, and injury (inflicted by males on females and, less commonly, by females on males). Attacks can be as brutal as they are commonplace. Female Savanna (Olive) Baboons, for instance, are liable to be attacked almost daily by males without provocation, and each female is severely wounded about once a year; injuries are sometimes fatal. Sexual coercion (i.e., punishment or intimidation by males of "uncooperative" females) as well as outright rape also occur in a wide variety of animals, occasionally involving "gangs" of males that attack and forcibly mate with females.¹¹¹ Heterosexual rape is especially prevalent among birds such as ducks and gulls, but also occurs in mammals such as primates (e.g., Orang-utans, Rhesus Macaques), hoofed mammals (e.g., Bighorn Sheep), and marine mammals (Right Whales, and numerous seal species). In birds that form pair-bonds, rape usually involves mating attempts on females other than the male's partner, but forced copulation within the pair-bond is not unknown, occurring, for example, in Silver Gulls, Lesser Scaup Ducks, and several other duck species.

Throughout the animal kingdom, heterosexual mating can be a dangerous and even lethal undertaking for females. Male Sea Otters often bite females on the nose during aquatic copulations, sometimes resulting in drowning or fatal infections; swarms of a dozen or more woodfrogs often try to mate with the same female, occasionally killing her in the process; female sharks of several species are routinely {204} and severely bitten on the back during heterosexual courtship; while male mink may puncture the base of the female's skull and brain with their teeth during mating. ¹¹² These are just a few examples of how heterosexual mating is often a destructive, rather than a procreative, act.

Animal Family Values: Birth Control, Day Care, Divorce, and Infidelity
      Although two young are born [in Pronghorn antelope], four to six embryos are implanted in the uterus, where they fight to the death, so to speak, for the limited space ... . Long projections grow out of the embryonic sheath which puncture other embryos, causing their death. All but two embryos are reabsorbed by the mother's body.
      — VALERIUS GEIST, "Pronghorns"¹¹³

When most people think about animal families, they imagine a mother deer lovingly tending her fawns, or a father bear diligently protecting mother and babies. The realities of animal heterosexuality are a far cry from this romanticized view. More often than not, a mother deer viciously drives her yearlings away from the family group (when she hasn't aborted her fetuses, that is) while father bear rarely has anything to do with his family — and when he does, it is often to kill and eat them. This section examines some of the stark realities of animal "family life," beginning with a look at the many mechanisms that animals use to avoid having families altogether, by limiting reproduction and eliminating offspring.

In addition to infrequent copulation or mating during times when fertilization cannot occur, several other forms of "birth control" — i.e., ways of preventing pregnancy — occur in animals.¹¹⁴ In fact, more than 20 different strategies have been identified whereby females are able to limit, control, or prevent insemination. The widespread occurrence of these phenomena throughout the animal world has led one scientist to conclude that "copulation ... seldom leads directly and inevitably to fertilization."¹¹⁵ Some female birds such as brown boobies defecate during mating rather than performing the customary genital contractions, thereby preventing insemination, while females of a number of insect, bird, and mammal species actively eject semen after copulating.¹¹⁶ Among mammals, vaginal or copulatory plugs (sometimes also known as chastity plugs) are found in a number of species. Gelatinous barriers form (or are deposited) in the female's reproductive tract in several different kinds of rodents, bats, insectivores, and wild pigs, as well as in some primates and dolphins. Although their function is not fully understood, it appears that plugs often serve to prevent insemination. In many species a male leaves a copulatory plug in the female following mating (or the semen simply coagulates to form the plug) so that other males will not be able to fertilize her. In Squirrel Monkeys and some bats, hedgehogs, and opossums, however, the female herself produces the plug (often from sloughed vaginal cells), probably to control or prevent inseminations by males. In addition, female squirrels sometimes entirely remove copulatory plugs — which contain all the semen deposited by a male — thereby effectively preventing insemination from their most recent mating.¹¹⁷ Finally, {205} scientists recently discovered that female Common Chimpanzees employ an extraordinary form of birth control: nipple stimulation. As in a number of other mammals, the regular reproductive cycles of female Chimps are inhibited or interrupted while they are suckling infants (known as lactational amenorrhea). Some females without infants have learned that by stimulating their own nipples they can effectively mimic this physiological effect, thereby preventing themselves from conceiving even though they are not actually lactating. In some cases, Chimps have avoided pregnancy for as long as a decade by employing this ingenious "contraceptive" technique.¹¹⁸

Following conception, pregnancy can be blocked (the fertilized egg does not implant, a phenomenon found in many rodents, where it is known as the Bruce effect). ¹¹⁹ Embryos can also kill each other by puncturing or strangulation (Pronghorns) or by actively devouring one another inside the uterus (sand sharks, some salamanders).¹²⁰ Embryos may also be "eliminated" because the mother has too few nipples to accommodate all of them (some marsupials such as Northern Quolls), while embryos of many hoofed mammals are simply reabsorbed.¹²¹ Actual abortion occurs in many species, including primates (e.g., Hanuman Langurs, Pig-tailed Macaques, Savanna Baboons), marine mammals (Australian Sea Lions, other seals), hoofed mammals (feral Horses, White-tailed Deer), carnivores (Red Foxes), and numerous rodents and insectivores (wood rats, voles, coypus). Abortions may occur either spontaneously, or as a result of stress and harassment from males, or (in primates) possibly also from deliberate ingestion of abortion-inducing plants. Though usually a sporadic or isolated occurrence, abortions may be more commonplace in some species or populations. In California sea lions, for example, large numbers of females routinely abort their fetuses: hundreds of abortions take place each year on some breeding grounds, often as long as four months in advance of the usual birthing period.¹²² Many birds and other species that lay eggs practice the equivalent of "abortion" — that is, the termination of an embryo's development — in the form of egg destruction (also known as ovicide), ejection of eggs from the nest, and/or clutch abandonment.¹²³

Following birth or hatching, many animals employ strategies of direct or indirect killing to "eliminate" offspring. Infanticide or direct killing of young is a widespread phenomenon in the animal kingdom, reported in all major animal groups.¹²⁴ It is also a decidedly heterosexual behavior, often revolving around the creation of new breeding "opportunities." In one common form of infanticide, for instance, a male kills youngsters so that he can mate with their mother and sire his own young.¹²⁵ In another type of infanticide, females kills their own or related offspring — in black-tailed prairie dogs, for example, almost 40 percent of all litters suffer partial or complete loss to infanticide by females.¹²⁶ Cannibalistic infanticide also occurs, in which young animals are not only killed but also eaten.¹²⁷ Offspring are sometimes subjected to neglect and abuse as well, ranging from "absentee" parents who fail to incubate their eggs or properly attend to their youngsters (e.g., storm petrels, Oystercatchers, King Penguins) all the way to abandonment, physical brutality, and/or sexual violence inflicted on youngsters (e.g., Hanuman Langurs, Northern Elephant Seals, Ring-billed Gulls), sometimes resulting in death.¹²⁸ In many bird {206} species, the size of families is regulated through a combination of factors. Parents frequently control the sequence of egg laying and hatching so that some offspring routinely perish (usually the last egg to be laid or hatched). In other cases "surplus" or extra young are produced as a "backup" strategy and usually end up fighting and killing each other (a phenomenon sometimes known as siblicide or cainism).¹²⁹

Once animals establish a family, an enormous number of different parenting arrangements can be employed — only a small fraction of which involve a "nuclear family" configuration with a mother and a father both caring for their offspring. In the majority of animals, single parenting (or no parental investment at all) is the rule. In most mammal species, for example, no long-lasting bonds are formed between the sexes, and females raise their young on their own. Even in birds, where "nuclear" two-parent heterosexual families are typical, single parenting also sometimes occurs. In a number of species, male-female pairs routinely separate and one bird takes over parental duties — often the female, but occasionally the male, as in Common Murres and whimbrels. Sometimes this occurs only a few days after hatching (e.g., whimbrels), or even before hatching (e.g., ducks). In other cases the brood is actually split between the two parents, as in some woodpeckers, Hooded Warblers, and many other perching birds.¹³⁰ The opposite of single parenting is also found: many birds raise their young in communal breeding groups with multiple parents and caretakers of both sexes, and parenting trios occasionally form in species that otherwise have "nuclear families."¹³¹ A phenomenon that could perhaps be called double-parenting also occurs in Golden Plovers, in which two heterosexual couples join forces and raise their youngsters as a quartet of parents. In general, then, a male-female parenting couple is neither a necessary nor a common arrangement among animals.

In addition to the wide range of family constellations in which animals raise their young, nearly 300 species of mammals and birds have developed adoption, parenting-assistance, and "day-care" systems, in which offspring are raised or cared for by animals other than their biological parents. Sometimes a sort of "baby-sitting" arrangement is formed (also known as alloparenting), in which a male or female assists another individual or couple in the care of their young (including "wet nurses" who suckle another female's young). This helper may be a relative or may not be related at all. In other species, groups of youngsters are pooled together into groups — known variously as creches (e.g., Botos, Flamingos, Cliff Swallows, and many other bird species), nursery groups or calf pools (e.g., Giraffes, Wapiti), and pods (e.g., Northern Fur Seals). These groups are usually looked after by one or two adult "guardians" while the parents are out foraging or socializing. Such systems can be viewed both as examples of adults being freed from their parenting duties by a natural "day-care" system and instances of animals forgoing a portion of their reproductive "responsibilities" in order to pursue other activities. Outright adoption and various forms of foster-parenting and stepparenting also occur across a wide spectrum of animals. Many Gull chicks actually desert or "run away" from their families as a result of neglect or violence (and are adopted by other families), and White Stork and lesser kestrel chicks also sometimes abandon their nests and switch to neighboring "foster families." In birds, many other types of "adoption" {207} result from eggs being abandoned by other birds, laid in other families' nests, or even transferred to other nests by being carried or swallowed and regurgitated whole.¹³² In a few species, "kidnapping" of youngsters or stealing of eggs (with subsequent foster-parenting) may also take place.¹³³

Heterosexual mating systems also exhibit a dizzying variety of forms. Pair-bonding between males and females is found in some mammals and most birds, but the majority of animals have polygamous or promiscuous systems, in which animals mate or bond with several different partners. This can take the form of either one male with several females (polygyny, the most common form), one female with several males (polyandry), a combination of both (each sex mating and bonding with several partners, or polygynandry), or mating with multiple partners with no bonding between them (promiscuity).¹³⁴ Even in species that form male-female pairs, however, there are many different arrangements. Heterosexual pair-bonding was long thought to be a simple and straightforward type of mating system, but biologists now recognize that — as in most other aspects of sexuality and social organization — animals exhibit considerable flexibility and diversity in their pairing arrangements.¹³⁵ Many species such as willow warblers, Eleanora's falcons, and sea horses are strictly monogamous. In numerous others, however, "infidelity" or nonmonogamous matings occur, among at least a subset of both males and females.¹³⁶ Often, such copulations take place at times when females cannot be fertilized, so they are not entirely related to reproduction. In spotted sandpipers and Shags, for instance, almost all "unfaithful" copulations occur outside the females' fertilizable periods, while female Razorbills specifically avoid full genital contact during nonmonogamous matings until after fertilization is no longer possible.¹³⁷ Other, more complex arrangements are also found: the mating system of some species, such as Tasmanian Native Hens, is described as "social polygamy with genetic monogamy." These birds live in polygamous groups, often several males mating with one female, but only one male fathers offspring with the female. This is the opposite of birds that form heterosexual pairs ("social monogamy") but mate and produce offspring with other partners ("genetic polygamy"). In many species where individuals typically form pair-bonds, there is also usually a subset of individuals that form heterosexual trios.¹³⁸

Many pairing systems could probably be characterized as "serial monogamy." Even in birds that tend to form lifelong pair-bonds, divorce occasionally happens, and in many species pairs break up much more frequently, individuals usually then remating with other partners.¹³⁹ In Oystercatchers, for instance, divorce and remating is quite common (especially among females), and some individuals have as many as six or seven consecutive mates over their lives. Overall divorce rates vary widely between different individuals and species, from 0 percent in Australian ravens and wandering albatrosses to about a quarter of Kittiwake, a third of natal robin, and two-thirds of Lapland longspur pairs, to nearly 100 percent of all pairs in house martins and Flamingos. Divorce may result from a failure to produce offspring, but in many cases a complex interaction of multiple factors is involved, including general partner incompatibility. Other types of heterosexual family breakup also occur: extended families in Ocellated Antbirds may disintegrate when male-female pairs leave {208} or grandparents isolate themselves; Warthog family units composed of a male and a female with young are generally less stable than female-only families; yearling White-tailed Deer are usually driven away by their own mothers; and Snow Geese family units may break up prematurely when juveniles leave.¹⁴⁰

Heterosexual mating and parenting arrangements come in a staggering variety of forms — it is simply not the case that one type of "family" configuration is utilized by all species, or even by all individuals within the same species, or by the same individual for all of his or her life. Animal heterosexuality (like homosexuality) is a truly multidimensional, polymorphous phenomenon.

Sex without Purpose: Pleasure and Nonreproduction
      Suzie stood with her back to Unk and she leaned her upper torso downward. He proceeded to manipulate her genitalia. That same day, ... Suzie allowed subadult Smitty to lick her clitoris ... . Observations ... indicated that Suzie may experience orgasm ... a shudder coursed through her entire body and then she became rigid.
      — GREYSOLYNNE J. FOX, Social Dynamics in Siamang¹⁴¹

      Even when males and females can overcome the considerable hurdles standing in the way of mating, they often engage in sexual activities that do not lead to reproduction. Several different forms of such "purposeless" sexual behavior can be identified, the most common being heterosexual sex that involves partners or situations where fertilization is impossible. As previously mentioned, many animals routinely mate (or engage in other sexual activities) outside of the breeding season or when the female is not ovulating — including during menstruation and pregnancy (or, in birds, during the incubation period). Not only is this found in a wide variety of animals — in mammals, for example, among various primates, hoofed mammals, carnivores, marsupials, rodents, and so on — but such nonprocreative sexual activity frequently constitutes a significant portion of all sexual behavior. In Common Murres, for instance, about half of all copulations in some populations occur during times when fertilization is not possible, while in Proboscis Monkeys and golden lion tamarins, a peak in sexual activity often occurs during pregnancy. ¹⁴² About half of all pregnant or menstruating Rhesus Macaques are sexually active, and some males mate with pregnant females as often as they do with ovulating females. In fact, sexual activity sometimes occurs during or shortly after birth in this species: males have been observed mounting females who just gave birth, while female attendants occasionally masturbate themselves while watching a female in labor. The birth process itself also stimulates sexual interest (courtship, mounting) in several species of hoofed mammals, including Mountain Goats, addax antelopes, and wildebeest.¹⁴³ In none of these cases can the "function" of such sexual activity be procreation. Heterosexual behavior also occurs among sexually immature animals, between adults and juveniles, between genetically related animals, between members of different species, and sometimes even between live and {209} dead animals — all instances in which reproduction is not optimized (if not altogether impossible).¹⁴⁴

Multiple copulations — in which animals mate far in excess of the amount required for fertilization — are also widespread. Several species of wild cats and birds of prey, for instance, have astonishingly high copulation rates. Lions may mate up to 100 times a day during the breeding season (or as much as 1,500 times for each litter produced), while heterosexual pairs of goshawks and American kestrels mate 500-700 times for each clutch of eggs they produce.¹⁴⁵ Oystercatcher pairs also copulate about 700 times each breeding season, while female Kob antelopes may each experience several hundred heterosexual mounts during a 24-hour visit to the mating grounds.¹⁴⁶ In addition, animals of some species (e.g., Spinner Dolphins, Gray and Bowhead Whales, Herons, Swallows) engage in group sexual activity in which only a small subset of the participants (if any) are actually passing on their genes and reproducing.

Specific nonprocreative heterosexual practices in the animal world are many and varied, and they often parallel homosexual behaviors as well as the wide variety of nonreproductive sexual practices found in humans. To begin with, mounting that does not involve full genital contact — sometimes described as "symbolic," "display," or "noncopulatory" mounting — is widespread. For every "full" copulation in Kob antelopes, for instance, an average of three mounts without erection and six mounts with an erection but no penetration are performed by the male.¹⁴⁷ Reverse mounting — in which the female mounts the male, usually without mutual genital contact — also occurs in a wide variety of species, and sometimes involves "reciprocal" mounting or sequential exchange of positions between the male and the female. ¹⁴⁸ In some species, males occasionally mount females from the side or in other positions that do not involve penetration or genital contact: for example, Japanese Macaques, Waterbuck, Mountain Sheep, Takhi, Collared Peccaries, Warthogs, Koalas, Ruffs, Hammerheads, and Chaffinches. Many other types of nonprocreative sexual acts occur in mammals: various forms of oral sex (including fellatio, genital licking, and beak-genital propulsion); stimulation of a partner's genitals with the hands or other appendages (such as flippers), including vaginal penetration with the fingers (in primates); anal stimulation, including penetration with fingers or oral-anal contact (e.g., Orang-utans), rump rubbing (e.g., in Bonobos and Common Chimpanzees), and even heterosexual anal intercourse (e.g., in Orang-utans).

Masturbation also occurs widely among animals, both male and female. A variety of creative techniques are used, including genital stimulation using the hand or front paw (primates, Lions), foot (Vampire Bats, primates), flipper (Walruses), or tail (Savanna Baboons), sometimes accompanied by stimulation of the nipples (Rhesus Macaques, Bonobos); auto-fellatio, or licking, sucking, and/or nuzzling by a male of his own penis (Common Chimpanzees, Savanna Baboons, Vervet Monkeys, Squirrel Monkeys, Thinhorn Sheep, Bharal, Aoudad, Dwarf Cavies); stimulation of the penis by flipping or rubbing it against the belly or in its own sheath (White-tailed and Mule Deer, Zebras, and Takhi); spontaneous ejaculations {210} (Mountain Sheep, Warthogs, Spotted Hyenas); and stimulation of the genitals using inanimate objects (found in several primates and cetaceans; see chapter 2 for further discussion). Many birds masturbate by mounting and copulating with tufts of grass, leaves, or mounds of earth, and some mammals such as primates and Dolphins also rub their genitals against the ground or other surfaces to stimulate themselves. One fairly unusual form of (indirect) genital stimulation occurs in some hoofed mammals. Among male Red Deer, Moose, Wapiti, and other species of Deer, the antlers are erotic organs that can result in sexual arousal and even ejaculation when they are rubbed. In addition to occasionally stimulating each other this way, males of these species often stimulate themselves by rubbing their antlers in clumps of vegetation.¹⁴⁹

Masturbation in female mammals, as well as heterosexual and homosexual intercourse (especially in primates), often involves direct or indirect stimulation of the clitoris (as in the description at the beginning of this section of oral sex among Siamangs, a primate species). This organ is present in the females of all mammalian species and several other animal groups, yet it has generally elicited a uniform reaction throughout much of scientific history: stunned (and embarrassed) silence. ¹⁵⁰ This is due not only to the general hush surrounding female sexuality, but because the clitoris poses serious challenges to conventional biological theories. Its only "function" appears to be sexual pleasure, and the notion of pleasure in animals, particularly as it relates to the phenomenon of female orgasm, is a difficult one for biologists to come to terms with. Scientists have been remarkably reticent on the subject, refusing even to believe that female animals can experience orgasm until the phenomenon was "proven" with detailed observations and experimental studies on monkeys.¹⁵¹

Even after it was "verified," a debate about the "function" of the female orgasm erupted in the scientific community and continues nearly unabated to this day.¹⁵² When a male animal has an orgasm — i.e., ejaculates — this is typically explained as the "mechanism" that insures sperm is transferred to the female — not as the {211} pursuit of sexual pleasure. But no such mechanistic "explanation" is available for the female orgasm or clitoris. Most current biological discussion of the female orgasmic response attempts to justify its existence in terms of how sexual pleasure might "encourage" or contribute to breeding or social bonding, rather than seeing it as something inherently valuable that requires no further "justification." As always, female sexuality — and sexual pleasure in general — is assumed not to exist until proven otherwise. Once "proven" it requires a "function" or "purpose" rather than having intrinsic worth — a striking echo of the presumption of heterosexuality in biology and the need to find an "explanation" for the occurrence of homosexuality. ¹⁵³

Conclusion: Toward a Biology of the Twenty-First Century
      The phenomena of nonreproductive and alternative heterosexualities have broad implications for how we look at animal behavior and sexuality in general. Animal social organization and biology do not revolve exclusively around reproduction and, in many cases, appear to be designed specifically to prevent procreation. Although heterosexual mating can (and frequently does) lead to reproduction, this is often an incidental consequence rather than an overriding "goal" (or ultimate "purpose"). Sexuality between males and females assumes a wide variety of forms, many of which necessitate recognizing sexual pleasure as a motivating force.¹⁵⁴ Homosexuality is, therefore, not unique in the animal kingdom by virtue of its "failure" to lead to procreation. It is simply one of many animal behaviors that lack the supposed "purpose" of contributing directly to the perpetuation of the species.

Nor is homosexuality unique in being considered a behavioral "anomaly" by scientists. Because they challenge some of biology's most fundamental assumptions about how the natural world is organized — while also reflecting stigmatized human behaviors — nonreproductive and alternative heterosexualities have inspired many of the same negative reactions that homosexuality has. As one ornithologist observes, "Until quite recently, [heterosexual] infidelity among wild birds was written off as aberrant behavior, and males were excused as being 'sick' or having a 'hormone imbalance' or, in one case, being 'dissatisfied at home.'" Likewise, the Brown-headed Cowbird's habit of abdicating parental care (by "parasitizing" other species' nests) was (and in some cases still is) considered particularly "loathsome" by many biologists. As a result, research on this common species has been severely hampered, and information on some basic aspects of its biology and social organization was lacking until fairly recently.¹⁵⁵ Analogously, behaviors such as masturbation, heterosexual trios, interspecies matings, nest desertion, reverse mounting, and forced copulations have all been labeled abnormal, aberrant, unnatural, or anomalous — in some cases as recently as a decade or so ago.¹⁵⁶

Unlike homosexuality and transgender, however, most of these phenomena are no longer pathologized by the majority of contemporary biologists, who now recognize that these behaviors are "normal" — that is, a routine aspect of the social and sexual organization of the species in which they occur. Nevertheless, nonreproductive and alternative heterosexualities continue to evoke profound "puzzlement" {212} regarding their function, which closely parallels the ongoing attempt to find "explanations" for homosexuality. In a recent discussion of alloparenting (helping behavior) in Common Murres, for example, the list of possible "causes" or "functions" of this behavior was virtually identical to those currently invoked to "explain" homosexuality: mistaken identity, heterosexual "practice," coercion or "manipulation," hormonal factors, kinship, and nonadaptiveness.¹⁵⁷ Heated debate about their supposed "purpose" continues to envelop the scientific discussion of most other nonreproductive and alternative heterosexualities: adoption, divorce, nonreproductive copulations, infanticide, nest desertion, reverse mountings, sex segregation, nonmonogamous matings, masturbation, multiple copulations, rape, vaginal plugs, reproductive suppression, postreproductive individuals, and harassment of matings all remain "perplexing" and highly contentious phenomena.¹⁵⁸

Even "kisses" have prompted a barrage of functional "explanations." Unable (or unwilling) to countenance the possibility of pleasure or affection in this "behavior" — much less something more intangible — biologists insist that kisses (even in humans) must be a vestige of ritual food exchange, or olfactory sampling, or have a specific social "function" such as reconciliation or alliance formation,¹⁵⁹ Perhaps this is true — but, as with other social/sexual behaviors, there is so much more to it than this. "The kiss" is a perfect symbol of the limitations of biological reductionism — for even if its origins can ultimately be traced to such functional considerations, something ineffable still remains in the gesture each time it is performed, something that continues to transcend its biological "purpose" and evade "explanation." Poet E. E. Cummings once warned of those who, "given the scalpel," would "dissect a kiss."¹⁶⁰ Considering that biologists now have the analytical tools and theoretical frameworks to "dissect" the function of the kiss — and apparently no qualms about doing so — perhaps his admonitions are more than metaphorical.

In 1923 a biologist "explained" polyandry (females mating with more than one male) in phalaropes (a type of sandpiper) as being caused by the "deranged sex organs" of female birds, whose "wanton" behavior was "forcing polygamy on the race." {213} On discovering this historical "explanation" more than half a century later, one ornithologist conceded that scientific theories often reflect "the passions and prejudices of the time," adding, "Half a century hence, our successors will no doubt find similar amusement in ideas devolving from our present ignorance."¹⁶¹ Much of the "present ignorance" of biology lies precisely in its single-minded attempt to find reproductive (or other) "explanations" for homosexuality, transgender, and nonprocreative and alternative heterosexualities. In the next chapter we'll explore how biology can take a first step into the twenty-first century — by reconciling itself at the most fundamental level to the existence and apparent "purposelessness" of this broad panoply of behaviors, sexualities, and genders in the natural world.
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