鈥淚 WAS young and naive,鈥 recalls Linda Wolfe. 鈥淚 thought everyone would be happy that I had found something new.鈥 But she was in for a big shock. 鈥淧eople started to ask me, do you have some kinky interest we don鈥檛 know about?鈥 And when she came to publish her results, the referees accused her of doctoring the photographs and making up data. What could an innocent young graduate student have found to create such a stir?
In the mid-1970s Wolfe was in the wilds of Japan studying macaques. As she grew to know her troop of monkeys, it soon became apparent that the females were having sex with one another. And these encounters weren鈥檛 mere flings. Females paired off for days or weeks at a time, forming exclusive couples. They moved around together, and spent ages grooming one another between bouts of sexual activity that typically culminated in orgasm for both partners. Wolfe was convinced she was witnessing homosexual behaviour, but most researchers were sceptical. 鈥淭hey said that females were mounting each other by mistake 鈥 they didn鈥檛 know what they were doing,鈥 she recalls. 鈥淧eople wanted to believe that only weirdo humans engaged in this behaviour.鈥
Even today, many researchers are reluctant to admit that same-sex encounters are 鈥渘ormal鈥 鈥 that is, 鈥減art of what primates do, part of their total sexual repertoire鈥 says Wolfe, now chair of anthropology at East Carolina University in Greenville, North Carolina. And not just primates, according to a compendium of animal homosexuality, just published in Britain by Bruce Bagemihl, an independent scholar and author based in Seattle. For 10 years Bagemihl scoured the scientific literature, unearthing documented cases of same-sex encounters with apparent sexual significance. He also contacted scores of researchers to add details not included in published papers. The result is a species-by-species profile of more than 470 species. 鈥淢ost are mammals and birds,鈥 says Bagemihl, 鈥渂ut perhaps only because I didn鈥檛 have time to go further.鈥
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When the book came out in the US earlier this year, it caused quite a stir. The Chicago Tribune called the 750-pager 鈥渁 landmark in the literature of science鈥, while Publishers Weekly declared it to be 鈥渁 brilliant and important exercise in exposing the limitations of received opinion鈥. But it has also provoked criticism, not only from social conservatives. Most scientific readers take exception to one controversial chapter in which Bagemihl presents his own highly speculative alternatives to Darwinian evolutionary theory. He draws on a heady mix of chaos theory and anthropology in an attempt to explain how 鈥渆xuberant鈥 diversity of sexual behaviours could emerge.
That aside, however, a growing band of researchers are welcoming his efforts. 鈥淏agemihl鈥檚 bestiary of homosexual behaviour really impressed me,鈥 says Paul Harvey, an evolutionary biologist at the University of Oxford. 鈥淚t is very clear that animals do it very regularly right across the animal kingdom. The beauty of the book is all that data 鈥 how much that guy鈥檚 read,鈥 Harvey adds. 鈥淭his book should not be ignored.鈥
Describing behaviours as diverse as 鈥渓esbian鈥 gulls that share a nest and rear chicks together or the homosexual 鈥渙rgies鈥 of male manatees, Bagemihl stresses that animal homosexuality is not a single, uniform phenomenon. His mission is to document its sheer diversity: 鈥渟ame-sex behaviour in animals exhibits every conceivable variation鈥. What he deplores is the prevailing 鈥淣oah鈥檚 ark鈥 view of animal sexuality. Sometimes, preliminaries to homosexual encounters closely resemble heterosexual courtship, as in the 鈥渕utual ecstatic鈥 displays of male humboldt penguins and the castanet-like teeth chattering of male walruses. But sometimes homosexual encounters elicit novel displays: male ostriches court other males with a unique 鈥減irouette dance鈥, for instance, while female rhesus monkeys engage in 鈥渉ide-and-seek鈥 games played only during female-female interactions.
In about a quarter of the cases he documents, Bagemihl also finds signs of 鈥渁ffectionate鈥 behaviours. These activities do not involve direct genital contact but 鈥渘evertheless have clear sexual or erotic overtones鈥. Male lions 鈥渉ead-rub鈥 and roll around with each other, while vampire bats develop erections during erotic same-sex grooming and licking. Whales and dolphins rub their bodies together and stroke each other with their flippers or tail flukes. Male giraffes indulge in prolonged bouts of affectionate 鈥渘ecking鈥, often followed by mounting and culminating in apparent orgasm. Novel sexual postures and oral sex of various kinds are also commonplace, says Bagemihl, who notes that female long-eared hedgehogs are known to engage in mutual genital licking, while male orang-utans practice fellatio.
鈥淣early every type of same-sex activity found among humans has its counterpart in the animal kingdom,鈥 he concludes. His take-home message is simple: homosexual behaviour is as 鈥渘atural鈥 as heterosexual behaviour.
Yet despite its apparent ubiquity, homosexuality among animals is far from common knowledge, even among biologists. 鈥淎lthough the first reports of homosexual behaviour among primates were published more than 75 years ago,鈥 says primatologist Paul Vasey of Concordia University in Montreal, 鈥渧irtually every major introductory text in primatology fails to even mention its existence.鈥
Personal prejudice
The neglect reflects an uneasy mix of personal prejudice and intellectual anxiety among professional zoologists, Bagemihl suspects. One time-honoured solution has been to avoid acknowledging that same-sex interactions have anything sexual about them. Most researchers are not as candid as field biologist Valerius Geist, well known for his long-term studies of mountain sheep in the North American Rockies. Some 20 years ago, he bravely confessed: 鈥淚 still cringe at the memory of seeing old D-ram mount S-ram repeatedly. To conceive of those magnificent beasts as `queers鈥. Oh God!鈥 For two years, Geist recounts, he tried to convince himself that the mounting was essentially an aggressive, dominance behaviour. 鈥淚 never published that drivel and am glad of it. Eventually I called the spade a spade and admitted that the rams lived in essentially a homosexual society.鈥
Intellectual worries run even deeper, perhaps. After all, homosexuality seems to be a clear non-starter from a Darwinian perspective. Why waste time in same-sex relationships when you could be making babies? Evolutionary theory measures success in the currency of genes: animals are supposed to be machines intent on spreading theirs around. 鈥淩esearchers find male-male or female-female sexual interactions theoretically difficult to deal with,鈥 says Wolfe. 鈥淥n the face of it, sociobiological theory says it can鈥檛 happen.鈥
No wonder then that putative gay sex among animals is typically explained away as examples of play, mistaken identity or an exercise in power. Indeed, some researchers, notably Tim Clutton-Brock of the University of Cambridge, would say that 鈥渢rue鈥 homosexuality 鈥 if strictly defined as male anal penetration by males who show no interest in females 鈥 is virtually unknown among wild mammals. They argue that animals who mount same-sex partners and the like are behaving aggressively or merely practising for heterosexual encounters. Or they may be advertising their availability, or trying to make a heterosexual partner jealous.
But Bagemihl painstakingly provides counter-arguments for such explanations. He says zoologists should acknowledge that the animal behaviours he describes remain (homo)sexual in nature, whatever their evolutionary origins or social function. Vasey, for one, doesn鈥檛 need to be convinced. 鈥淛ust because a behaviour which is sexual in form serves some social role or function doesn鈥檛 mean it cannot be simultaneously sexual,鈥 he says.
Perhaps we risk overtheorising these behaviours, says Wolfe, who reckons that biologists may never come up with a grand theory to account for the diversity of same-sex interactions. Her explanation of the female macaques鈥 behaviour is refreshingly straightforward: given food and leisure time, 鈥渋t is just part of what they do, socially and to derive sexual pleasure. It is probably mostly just for sexual pleasure.鈥
Such ideas can provoke outrage, however. 鈥淪ome primatologists want to deny that homosexual behaviour has anything to do with pleasure. There is a streak of puritanism running thorough American primatology that says a behaviour can鈥檛 exist just for sexual pleasure,鈥 she says. 鈥淎t a conference in Madison some three years ago, I raised this idea and got drummed out of the room.鈥 Her scandalised colleagues rubbished the idea with remarks such as: 鈥淲ell, if that was the case we鈥檇 all be in the aisle now having sex,鈥 she recalls.
There is one species, however, in which pleasure and homosexual activity seem undeniably linked. Even the sceptical Clutton-Brock, when asked about this species, the bonobos or pygmy chimpanzees, agrees laughingly, 鈥淥h them, well, they鈥檇 probably do anything鈥.
鈥淚f you鈥檙e looking for homosexual sex in vast quantities, forget humans, it鈥檚 bonobos you want,鈥 says primatologist Robin Dunbar. 鈥淚t鈥檚 scandalous,鈥 he chuckles. 鈥淭hey鈥檒l have sex with anyone, never mind the sex or age.鈥 An observer doesn鈥檛 have to wait long to notice females locked into a face-to-face embrace all the better to indulge in mutual genital rubbing, or spy males glued together via open-mouthed kisses with plentiful mutual tongue stimulation. 鈥淥ne plausible explanation is that all this is principally a bonding device,鈥 says Dunbar of the University of Liverpool. 鈥淭he idea is that the relaxing, rewarding qualities of sex have been captured for social purposes, to reduce conflict and hold the group together.鈥
But why should bonobos need post-coital calm more than the next primate? One difference could lie in their feeding strategies. Bonobos forage in much larger social groups than common chimps 鈥 20 or more compared to less than five individuals. So one possible explanation for bonobos鈥 extraordinary sexual proclivities, Dunbar suggests, is this: forced to congregate in large social groups, bonobos must have a mechanism for minimising the disruptive effects of competition. 鈥淭hey鈥檒l be always bumping into one another, treading on each other鈥檚 toes, and noticing that Jemima over there鈥檚 got a temptingly nice fig; they need something that will diffuse conventional stresses and rebuild relationships after squabbles.鈥 For bonobos, sex fits the bill. 鈥淲here we bring chocolates and flowers, they groom and kiss instead.鈥 And it seems to work. Bonobo society is noticeably more harmonious than that of their closest kin, the common chimps.
But while bonobos may remain the most spectacular example of animal homosexuality, Bagemihl is convinced that the case studies in his book represent only the tip of the iceberg that is homosexual life on Earth. After all, even in long-term field studies of many species, sexual behaviour is rarely observed. Heterosexual mating between cheetahs, for instance, has been recorded only five times in the wild. 鈥淭he fact that homosexuality has not been seen in many animals does not necessarily mean that it is absent in those species: only that it has yet to be observed,鈥 says Bagemihl.
Cross-dressing?
To compound the difficulties, in many species, males and females look alike, at least to the human eye 鈥 with embarrassing results on occasion. King penguins in Edinburgh Zoo in the early decades of this century went through a number of name changes as their keepers realised that sexual behaviour was no foolproof clue to biological sex. Two penguins that had initially been seen engaging in what was thought to be 鈥渉eterosexual鈥 activity 鈥 鈥淓ric鈥 and Dora 鈥 later turned out to be both female. (Eric was renamed Erica.) Another pair, initially called 鈥淏ertha鈥 and 鈥淐aroline鈥, eventually escaped from accusations of lesbianism only to be confirmed as the gay males Bertrand and Charles.
DNA testing is now exposing unconventional social set-ups among other identical-looking birds. In an on-going study of rare roseate terns on Bird Island off Massachusetts, researchers are monitoring female-female pairs confirmed by molecular sexing techniques. Ian Nisbet and Jeremy Hatch of the University of Massachusetts in Boston find that 12 per cent of the nests are tended by lesbian terns, who share in the incubation of three or four eggs 鈥 two is the norm for heterosexual couples. The females fertilise their eggs through a quick fling with paired and breeding males, but many have remained faithful to another female over the five years of the study.
Nisbet and Hatch interpret this strategy as a 鈥渟econd-best option鈥 for females keen to reproduce when males are in short supply 鈥 the sex ratio is apparently strongly skewed towards females at birth. They come to this conclusion because it looks as if the lesbians are being penalised from a genetic point of view: a pair usually manage to raise only one chick, so each year one partner would seem to have zero success in genetic terms. But what if the lesbians are genetically related? Then both would have a genetic stake in the solitary chick, regardless of whose it was.
The researchers are now using DNA fingerprinting to discover whether the partners in female pairs are sometimes mothers and daughters, aunts and nieces or sisters. Could it be that the lesbian strategy isn鈥檛 second-best after all? 鈥淭here is certainly a lot more going on here than has been recognised,鈥 says Nisbet cautiously.
But in any case, homosexuality doesn鈥檛 have to be adaptive in a strict genetic sense to be a real phenomenon, argues Bagemihl. 鈥淩esearchers have been blinded by the prevailing preoccupation to find adaptive explanations for every behaviour,鈥 agrees Vasey. He spent his doctoral years hunting in vain for evidence to support such explanations for the sexual proclivities of female Japanese macaques. For instance, the females do not use sex to test or establish dominance ranks or to form social bonds; they form a liaison, and when it is over, they act as though it never happened.
Even the favourite explanation 鈥 a shortage of male attention 鈥 fails to stand up to scrutiny. In one group Vasey observed, lots of females lived with just one male. 鈥淓ven in that skewed situation, that one male was not very busy. By and large the females were more interested in other females 鈥 they鈥檙e bisexual, not preferentially heterosexual,鈥 he says.
It will take a long time before such ideas reach the mainstream. But Vasey sees Bagemihl鈥檚 鈥渆xhaustively and meticulously researched鈥 book as a watershed. 鈥淗is work will make it increasingly difficult for anyone to write off the whole idea of homosexuality in animals.鈥
- Further reading: Biological Exuberance: Animal Homosexuality and Natural Diversity by Bruce Bagemihl, St Martin鈥檚 Press, New York (1999)