Homosexual behavior in animals

For homosexuality in humans, see homosexuality.

Homosexual behavior in animals refers to the documented evidence of homosexual and bisexual behavior in non-human species. Such behaviors include sex, courtship, affection, pair bonding, and parenting among same sex animals. A 1999 review by researcher Bruce Bagemihl shows that homosexual behavior has been observed in close to 1,500 species, ranging from primates to gut worms, and is well documented for 500 of them.^[1][2] Animal sexual behavior takes many different forms, even within the same species. The motivations for and implications of these behaviors have yet to be fully understood, since most species have yet to be fully studied.^[3] According to Bagemihl, "the animal kingdom [does] it with much greater sexual diversity — including homosexual, bisexual and nonreproductive sex — than the scientific community and society at large have previously been willing to accept."^[4] Current research indicates that various forms of same-sex sexual behavior are found throughout the animal kingdom.^[5] A new review made in 2009 of existing research showed that same-sex behavior is a nearly universal phenomenon in the animal kingdom, common across species.^[6] Homosexual behavior is best known from social species. According to geneticist Simon Levay in 1996, "Although homosexual behavior is very common in the animal world, it seems to be very uncommon that individual animals have a long-lasting predisposition to engage in such behavior to the exclusion of heterosexual activities. Thus, a homosexual orientation, if one can speak of such thing in animals, seems to be a rarity.^[7] One species in which exclusive homosexual orientation occurs, however, is that of domesticated sheep (Ovis aries).^[8][9] "About 10% of rams (males) refuse to mate with ewes (females) but do readily mate with other rams."^[9]

The observation of homosexual behavior in animals can be seen as both an argument for and against the acceptance of homosexuality in humans, and has been used especially against the claim that it is a peccatum contra naturam ('sin against nature').^[1] For instance, homosexuality in animals was cited in the United States Supreme Court's decision in Lawrence v. Texas which struck down the sodomy laws of 14 states.^[10] Whether animal sexuality has logical, ethical, or moral implications in human sexuality is also a source of debate (see appeal to nature).^[11][12][13]

Applying the term "homosexual" to animals

The term homosexual was coined by Karl-Maria Kertbeny in 1868 to describe same-sex sexual attraction and sexual behavior in humans.^[14] Its use in animal studies has been controversial for two main reasons: animal sexuality and motivating factors have been and remain poorly understood, and the term has strong cultural implications in western society that are irrelevant for species other than humans.^[15] Thus homosexual behavior has been given a number of terms over the years. When describing animals, the term "homosexual" is preferred over "gay", "lesbian" and other terms currently in use, as these are seen as even more bound to human homosexuality.^[16]

Animal preference and motivation is always inferred from behavior. In wild animals, researchers will as a rule not be able to map the entire life of an individual, and must infer from frequency of single observations of behavior. The correct usage of the term homosexual is that an animal exhibits homosexual behavior or even same-sex sexual behavior; however, this article conforms to the usage by modern research^{[16][17][18][19][20]} applying the term homosexuality to all sexual behavior (copulation, genital stimulation, mating games and sexual display behavior) between animals of the same sex. In most instances, it is presumed that the homosexual behavior is but part of the animal's overall sexual behavioral repertoire, making the animal "bisexual" rather than "homosexual" as the terms are commonly understood in humans,^[19] but cases of homosexual preference and exclusive homosexual pairs are known.^[21]

Research on homosexual behavior in animals

The presence of same-sex sexual behavior was not 'officially' observed on a large scale until recent times, possibly due to observer bias caused by social attitudes to same-sex sexual behavior,^[22] innocent confusion, or even from a fear of "being ridiculed by their colleagues."^[23] Georgetown University biologist Janet Mann states "Scientists who study the topic are often accused of trying to forward an agenda, and their work can come under greater scrutiny than that of their colleagues who study other topics."^[24] They also noted "Not every sexual act has a reproductive function ... that's true of humans and non-humans."^[24] It appears to be widespread amongst social birds and mammals, particularly the sea mammals and the primates. The true extent of homosexuality in animals is not known. While studies have demonstrated homosexual behavior in a number of species, Petter Bøckman, the scientific advisor of the exhibition Against Nature? in 2007, speculated that the true extent of the phenomenon may be much larger than was then recognized:

No species has been found in which homosexual behaviour has not been shown to exist, with the exception of species that never have sex at all, such as sea urchins and aphis. Moreover, a part of the animal kingdom is hermaphroditic, truly bisexual. For them, homosexuality is not an issue.^[23]

Two male giraffes in Kenya.

An example of overlooking homosexual behavior is noted by Bruce Bagemihl describing mating giraffes where nine out of ten pairings occur between males.

Every male that sniffed a female was reported as sex, while anal intercourse with orgasm between males was only "revolving around" dominance, competition or greetings.^[25]

Some researchers believe this behavior to have its origin in male social organization and social dominance, similar to the dominance traits shown in prison sexuality. Others, particularly Joan Roughgarden, Bruce Bagemihl, Thierry Lodé^[26] and Paul Vasey suggest the social function of sex (both homosexual and heterosexual) is not necessarily connected to dominance, but serves to strengthen alliances and social ties within a flock. Others have argued that social organization theory is inadequate because it cannot account for some homosexual behaviors, for example, penguin species where same-sex individuals mate for life and refuse to pair with females when given the chance.^[27][28] While reports on many such mating scenarios are still only anecdotal, a growing body of scientific work confirms that permanent homosexuality occurs not only in species with permanent pair bonds,^[20] but also in non-monogamous species like sheep.

One report on sheep cited below states:

Approximately 8% of rams exhibit sexual preferences [that is, even when given a choice] for male partners (male-oriented rams) in contrast to most rams, which prefer female partners (female-oriented rams). We identified a cell group within the medial preoptic area/anterior hypothalamus of age-matched adult sheep that was significantly larger in adult rams than in ewes...^[29]

In fact, apparent homosexual individuals are known from all of the traditional domestic species, from sheep, cattle and horses to cats, dogs and budgerigars.^[1]

Genetic and physiological basis for homosexual animal behavior

Researchers found that disabling the (fucose mutarotase) FucM gene in laboratory mice – which influences the levels of estrogen to which the brain is exposed – caused the female mice to behave as if they were male as they grew up. "The mutant female mouse underwent a slightly altered developmental programme in the brain to resemble the male brain in terms of sexual preference" said Professor Chankyu Park of the Korea Advanced Institute of Science and Technology in Daejon, South Korea, who led the research. His most recent findings have been published in the BMC Genetics journal on July 7, 2010.^[30][31]

In March 2011, research shows that serotonin is involved in the mechanism of sexual orientation of mice.^[32][33]

Some selected species and groups

See also: List of animals displaying homosexual behavior

See also: Seabird Same-sex pairing

Birds

Black swans

Black Swans, Cygnus atratus

An estimated one-quarter of all black swans pairings are homosexual and they steal nests, or form temporary threesomes with females to obtain eggs, driving away the female after she lays the eggs.^[34][35] More of their cygnets survive to adulthood than those of different-sex pairs, possibly due to their superior ability to defend large portions of land. The same reasoning has been applied to male flamingo pairs raising chicks.^[36][37]

Gulls

Studies have shown that 10 to 15 percent of female western gulls in some populations in the wild exhibit homosexual behavior.^[38]

Ibises

Research has shown that the environmental pollutant methylmercury can increase the prevalence of homosexual behavior in male American White Ibis. The study involved exposing chicks in varying dosages to the chemical and measuring the degree of homosexual behavior in adulthood. The results discovered was that as the dosage was increased the likelihood of homosexual behavior also increased. The endocrine blocking feature of mercury has been suggested as a possible cause of sexual disruption in other bird species.^[39][40]

Mallards

Two male Mallards, Anas platyrhynchos

Mallards form male-female pairs only until the female lays eggs, at which time the male leaves the female. Mallards have rates of male-male sexual activity that are unusually high for birds, in some cases, as high as 19% of all pairs in a population.^[41]

Penguins

In early February 2004 the New York Times reported that a male pair of chinstrap penguins in the Central Park Zoo in New York City had successfully hatched and fostered a female chick from a fertile egg they had been given to incubate.^[10] Other penguins in New York zoos have also been reported to have formed same-sex pairs.^[42][43]

Zoos in Japan and Germany have also documented homosexual male penguin couples.^[27][28] The couples have been shown to build nests together and use a stone as a substitute for an egg. Researchers at Rikkyo University in Tokyo found 20 homosexual pairs at 16 major aquariums and zoos in Japan.

Bremerhaven Zoo in Germany attempted to encourage reproduction of endangered Humbolt penguins by importing females from Sweden and separating three male pairs, but this was unsuccessful. The zoo's director said that the relationships were "too strong" between the homosexual pairs.^[44] German gay groups protested at this attempt to break up the male-male pairs^[45] but the zoo's director was reported as saying "We don't know whether the three male pairs are really homosexual or whether they have just bonded because of a shortage of females... nobody here wants to forcibly separate homosexual couples."^[46]

A pair of male Magellanic penguins who had shared a burrow for six years at the San Francisco Zoo and raised a surrogate chick, split when the male of a pair in the next burrow died and the female sought a new mate.^[47]

Vultures

In 1998 two male Griffon vultures named Dashik and Yehuda, at the Jerusalem Biblical Zoo, engaged in "open and energetic sex" and built a nest. The keepers provided the couple with an artificial egg, which the two parents took turns incubating; and 45 days later, the zoo replaced the egg with a baby vulture. The two male vultures raised the chick together.^[48] A few years later, however, Yehuda became interested in a female vulture that was brought into the aviary. Dashik became depressed, and was eventually moved to the zoological research garden at Tel Aviv University where he too set up a nest with a female vulture.^[49]

Two homosexual male vultures at the Allwetter Zoo in Muenster built a nest together, although they were picked on and often had their nest materials stolen by other vultures. They were eventually separated to try and promote breeding by placing one of them with female vultures, despite the protests of German homosexual groups.^[50]

Pigeons

Both male and female pigeons sometimes exhibit homosexual behavior. As well as sexual behavior same-sex pigeon pairs will build nests, and hens will lay (infertile) eggs and attempt to incubate them.

Some pigeons also display fetish behavior and attempt to mate with specific inanimate objects.^{[citation needed]}

Mammals

Amazon Dolphin

The Amazon River dolphin or boto has been reported to form up in bands of 3–5 individuals enjoying group sex.^[51] The groups usually comprise young males and sometimes one or two females. Sex is often performed in non-reproductive ways, using snout, flippers and genital rubbing, without regards to gender.^[51] In captivity, they have been observed to sometimes perform homosexual and heterosexual penetration of the blowhole, a hole homologous with the nostril of other mammals, making this the only known example of nasal sex in the animal kingdom.^[52][51] The males will sometimes also perform sex with tucuxi males, a small porpoise.^[51]

American Bison

The American Bison is a bovine mammal which commonly displays homosexual behavior.

Courtship, mounting, and full anal penetration between bulls has been noted to occur among American Bison. The Mandan nation Okipa festival concludes with a ceremonial enactment of this behavior, to "ensure the return of the buffalo in the coming season."^[53] Also, mounting of one female by another is common among cattle.

Bonobo and other apes

Bonobo

The Bonobo, which has a matriarchal society, unusual amongst apes, is a fully bisexual species—both males and females engage in heterosexual and homosexual behavior, being noted for female-female homosexuality in particular. About 60% of all sexual activity in this species is between two or more females. While the homosexual bonding system in Bonobos represents the highest frequency of homosexuality known in any species, homosexuality has been reported for all great apes (a group which includes humans), as well as a number of other primate species.^{[54][55][56][57][58][59][60][61][62]} Dutch primatologist Frans de Waal on observing and filming bonobos noted that there were two reasons to believe sexual activity is the bonobo's answer to avoiding conflict.

Anything that arouses the interest of more than one bonobo at a time, not just food, tends to result in sexual contact. If two bonobos approach a cardboard box thrown into their enclosure, they will briefly mount each other before playing with the box. Such situations lead to squabbles in most other species. But bonobos are quite tolerant, perhaps because they use sex to divert attention and to defuse tension.

Bonobo sex often occurs in aggressive contexts totally unrelated to food. A jealous male might chase another away from a female, after which the two males reunite and engage in scrotal rubbing. Or after a female hits a juvenile, the latter's mother may lunge at the aggressor, an action that is immediately followed by genital rubbing between the two adults.^[63]

Bottlenose dolphins

Dolphins of several species engage in homosexual acts, though it is best studied in the bottlenose dolphins.^[1] Sexual encounters between females take the shape of "beak-genital propulsion", where one female insert her beak in the genital opening of the other while swimming gently forward.^[64] Between males, homosexual behaviour include rubbing of genitals against each other, which sometimes lead to the males swimming belly to belly, inserting the penis in the others genital slit and sometimes anus.^[65]

Janet Mann, Georgetown University professor of biology and psychology, argues that the strong personal behavior among male dolphin calves is about bond formation and benefits the species in an evolutionary context.^[38] She cites studies showing that these dolphins later in life as adults are in a sense bisexual, and the male bonds forged earlier in life work together for protection as well as locating females to reproduce with. Confrontations between flocks of bottlenose dolphins and the related species Atlantic spotted dolphin will sometimes lead to cross-species homosexual behaviour between the males rather than combat.^[66]

Elephants

African and Asian males will engage in same-sex bonding and mounting. Such encounters are often associated with affectionate interactions, such as kissing, trunk intertwining, and placing trunks in each other's mouths. Male elephants, who often live apart from the general herd, often form "companionships", consisting of an older individual and one or sometimes two younger, attendant males with sexual behavior being an important part of the social dynamic. Unlike heterosexual relations, which are always of a fleeting nature, the relationships between males may last for years. The encounters are analogous to heterosexual bouts, one male often extending his trunk along the other's back and pushing forward with his tusks to signify his intention to mount. Same-sex relations are common and frequent in both sexes, with Asiatic elephants in captivity devoting roughly 45% of sexual encounters to same-sex activity.^[67]

Giraffes

Male giraffes have been observed to engage in remarkably high frequencies of homosexual behavior. After aggressive "necking", it is common for two male giraffes to caress and court each other, leading up to mounting and climax. Such interactions between males have been found to be more frequent than heterosexual coupling.^[68] In one study, up to 94% of observed mounting incidents took place between two males. The proportion of same sex activities varied between 30 and 75%, and at any given time one in twenty males were engaged in non-combative necking behavior with another male. Only 1% of same-sex mounting incidents occurred between females.^[69]

Humans

Further information: Homosexuality

Monkeys

Among monkeys, Lionel Tiger and Robin Fox conducted a study on how Depo-Provera contraceptives lead to decreased male attractiveness to females and eventually to male homosexuality.^[70] Janet E. Smith summarizes the findings as follows:

[The] study in the early 70s [...] involved a tribe of monkeys. The alpha monkey of this tribe, named Austin, chose three female monkeys to be his exclusive sexual partners. Austin had a grand time with these three female monkeys. Then the researchers injected Austin's three females with the contraceptive Depo-Provera. Austin stopped having sex with them and chose other female monkeys to be his sexual partners. Then they contracepted all of the females in the tribe. The males stopped have sex with the females and started behaving in a turbulent and confused manner.^[71]

Japanese macaque

With the Japanese macaque, also known as the "snow monkey", same-sex relations are frequent, though rates vary between troops. Females will form "consortships" characterized by affectionate social and sexual activities. In some troops up to one quarter of the females form such bonds, which vary in duration from a few days to a few weeks. Often, strong and lasting friendships result from such pairings. Males also have same-sex relations, typically with multiple partners of the same age. Affectionate and playful activities are associated with such relations.^[72]

Lions

Both male and female lions have been seen to interact homosexually.^[73][74] Male lions pair-bond for a number of days and initiate homosexual activity with affectionate nuzzling and caressing, leading to mounting and thrusting. About 8% of mountings have been observed to occur with other males. Pairings between females are held to be fairly common in captivity but have not been observed in the wild.

Polecat

European polecats Mustela putorius were found to engage homosexually with non-sibling animals. Exclusive homosexuality with mounting and anal penetration in this solitary species serves no apparent adaptive function.^[75]

Sheep

The reason why Ovis aries has attracted so much attention is that some rams seem to have an exclusive homosexual orientation.^[76]

An October 2003 study by Dr. Charles E. Roselli et al. (Oregon Health and Science University) states that homosexuality in male sheep (found in 8% of rams) is associated with a region in the rams' brains which the authors call the "ovine Sexually Dimorphic Nucleus" (oSDN) which is half the size of the corresponding region in heterosexual male sheep.^[29]

Scientists found that, "The oSDN in rams that preferred females was significantly larger and contained more neurons than in male-oriented rams and ewes. In addition, the oSDN of the female-oriented rams expressed higher levels of aromatase, a substance that converts testosterone to estradiol, a form of estrogen which is believed to facilitate typical male sexual behaviors. Aromatase expression was no different between male-oriented rams and ewes."

"The dense cluster of neurons that comprise the oSDN express cytochrome P450 aromatase. Aromatase mRNA levels in the oSDN were significantly greater in female-oriented rams than in ewes, whereas male-oriented rams exhibited intermediate levels of expression." These results suggest that "...naturally occurring variations in sexual partner preferences may be related to differences in brain anatomy and its capacity for estrogen synthesis."^[29] As noted prior, given the potential unagressiveness of the male population in question, the differing aromatase levels may also have been evidence of aggression levels, not sexuality. It should also be noted that the results of this study have not been confirmed by other studies.

The Merck Manual of Veterinary Medicine appears to consider homosexuality among sheep as a routine occurrence and an issue to be dealt with as a problem of animal husbandry.^[77]

Spotted Hyena

The Spotted Hyena is a moderately large, terrestrial carnivore native to Africa.

The family structure of the Spotted Hyena is matriarchal, and dominance relationships with strong sexual elements are routinely observed between related females. Due largely to the female spotted hyena's unique urogenital system, which looks more like a penis rather than a vagina, early naturalists thought hyenas were hermaphroditic males who commonly practiced homosexuality.^[78] Early writings such as Ovid's Metamorphoses and the Physiologus suggested that the hyena continually changed its sex and nature from male to female and back again. In Paedagogus, Clement of Alexandria noted that the hyena (along with the hare) was "quite obsessed with sexual intercourse." Many Europeans associated the hyena with sexual deformity, prostitution, deviant sexual behavior, and even witchcraft.

The reality behind the confusing reports is the sexually aggressive behavior between the females, including mounting between females. Research has shown that "in contrast to most other female mammals, female Crocuta are male-like in appearance, larger than males, and substantially more aggressive,"^[79] and they have "been masculinized without being defeminized.”^[78]

Study of this unique genitalia and aggressive behavior in the female hyena has led to the understanding that more aggressive females are better able to compete for resources, including food and mating partners.^[78][80] Research has shown that "elevated levels of testosterone in utero"^[81] contribute to extra aggressiveness; both males and females mount members of the same sex,^[81][82] who in turn are possibly acting more submissive because of lower levels of testosterone in utero.^[79]

Others

Lizards

Whiptail lizard (Teiidae genus) females have the ability to reproduce through parthenogenesis and as such males are rare and sexual breeding non-standard.^[83] Females engage in sexual behavior to stimulate ovulation, with their behavior following their hormonal cycles; during low levels of estrogen, these (female) lizards engage in "masculine" sexual roles. Those animals with currently high estrogen levels assume "feminine" sexual roles.

Lizards that perform the courtship ritual have greater fertility than those kept in isolation due to an increase in hormones triggered by the sexual behaviors. So, even though asexual whiptail lizards populations lack males, sexual stimuli still increase reproductive success.

From an evolutionary standpoint, these females are passing their full genetic code to all of their offspring (rather than the 50% of genes that would be passed in sexual reproduction). Certain species of gecko also reproduce by parthenogenesis.^[84]

Dragonflies

The head of Darner Dragonfly (Basiaeschna janata).

Male homosexuality has been inferred in several species of dragonflies (the order Odonata). The cloacal pinchers of male damselflies and dragonflies inflict characteristic head damage to females during sex. A survey of 11 species of damsel and dragonflies^[85][86] has revealed such mating damages in 20 to 80 % of the males too, indicating a fairly high occurrence of sexual coupling between males.

Fruit flies

Male Drosophila melanogaster flies bearing two copies of a mutant allele in the fruitless gene court and attempt to mate exclusively with other males.^[21] The genetic basis of animal homosexuality has been studied in the fly Drosophila melanogaster.^[87] Here, multiple genes have been identified that can cause homosexual courtship and mating.^[88] These genes are thought to control behavior through pheromones as well as altering the structure of the animal's brains.^[89][90] These studies have also investigated the influence of environment on the likelihood of flies displaying homosexual behavior.^[91][92]

Bed bugs

Male bed bugs (Cimex lectularius) are sexually attracted to any newly fed individual and this results in homosexual mounting. This occurs in heterosexual mounting by the traumatic insemination in which the male pierces the female abdomen with his needle-like penis. In homosexual mating this risks abdominal injuries as males lack the female counteradaptive spermalege structure. Males produce alarm pheromones to reduce such homosexual matings.^[93]

See also

• Animal sexual behavior
• Xq28
• Against Nature?
• Biology and sexual orientation
• Freemartin
• Homosexuality and psychology
• Hermaphroditism in animals
• Innate bisexuality
• Non-human primate experiments
• Norms of reaction
• Plant sexuality
• Sexual orientation
• Sexual orientation and medicine
• Cross species sex
• List of animals displaying homosexual behavior

References

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2. ^ Harrold, Max (1999-02-16). "Biological Exuberance: Animal Homosexuality and Natural Diversity". The Advocate, reprinted in Highbeam Encyclopedia. http://www.encyclopedia.com/doc/1G1-53877996.html. Retrieved 2007-09-10. 
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External links

• biologists' view
• National Geographic
• Homosexual Behaviour in Animals An Evolutionary Perspective
• Driscoll, E.V. (2008), Bisexual Species, Scientific American Mind, 19(3), p. 68-73.