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Abstract

This is a JAMA book review of the 1999 book by Bruce Bagemihl, Biological Exuberance: Animal Homosexuality and Natural Diversity
Sexual Behavior
Biological Exuberance: Animal
Homosexuality and Natural Diversity
William Byne
JAMA. 2000;283(16):2170. doi:10.1001/jama.283.16.2170-JBK0426-3-1
A good thing about science is that, given enough time, it will eventually correct
itself. Biological Exuberance by Bruce Bagemihl illustrates that self-correcting process
by dispelling two prevalent myths: that reproduction is the sole reason for sexual
behavior and that homosexuality is hard to find in the animal kingdom.
The book contains two sections. In the first, "A Polysexual, Polygendered World,"
Bagemihl examines the hidden assumptions behind the way scientists interpret
homosexual behavior in animals. Assumptions that tend to explain animal
homosexuality out of existence are carefully analyzed as are the double standards often
used in characterizing behaviors as sexual when they involve members of the other but
not the same sex. This section concludes with the chapter "A New Paradigm: Biological
Exuberance." Bagemihl writes, "The essence of Biological Exuberance is that natural
systems are driven as much by abundance and excess as they are by limitation and
practicality." This hypothesis is based on the concept of biodiversity—that the vitality of
a biological system is a direct consequence of the diversity it contains. As stated
succinctly by James Lovelock, "as diversity increases, so does stability and resilience."
From this perspective, diverse sexualities, including homosexualities, should be
expected throughout the animal kingdom. Biological Exuberance thus offers a
hypothesis for the maintenance within populations of homosexual behaviors and other
behaviors that are often presumed to be at odds with reproduction.
The second section, "A Wonderful Bestiary," is organized in a field-guide format and
documents homosexuality as well as "nonreproductive and alternative
heterosexualities" in 190 species. In total, this abundantly illustrated book compiles
more than two centuries of observations of homosexual behavior, pair bonding, and
coparenting in more than 400 species. These include observations of species in which
homosexual but not heterosexual pair bonding has been documented and others in
which same-sex courtship and sexuality are so pervasive that "females are said to
`mimic' males in order to mate with them." The sheer scope and thorough
documentation of this book make it an extremely valuable resource for anyone
interested in the diversity of animal behavior and sexuality.
It is often assumed that nature has a prescriptive normative force such that what is
deemed natural is considered to be good, while the virtue of what is not found in nature
is subject to doubt. Ethical analysis shows this reasoning to be flawed. Nevertheless,
Bagemihl's convincing demonstration of pervasive nonprocreative heterosexual and
homosexual behaviors in the animal kingdom undermines one of the more common
arguments in support of the belief that it is wrong (or indicative of psychopathology) for
human beings to engage in such behaviors. "What is remarkable about the entire
debate about the naturalness of homosexuality," according to Bagemihl, "is the frequent
absence of any reference to concrete facts or accurate, comprehensive information
about animal homosexuality." Heretofore, for reasons that are examined in the first
section of the book, much of this information has been virtually inaccessible to
scholars. Biological Exuberance fills that void, and there can no longer be any excuse
for such omissions.
... Spontaneous ejaculation, which is defined as the release of seminal fluids in the absence of apparent sexual stimulation, has been reported in several male land mammals, including Rodentia (rats [1], hamsters [2], guinea pigs [3], mice [4]), Cetartiodactyla (mountain sheep, warthogs (reviewed in [5]), tsessebes [6]), Carnivora (domestic cats [7], spotted hyenas (reviewed in [5])), Perissodactyla (horses [8]), and Primates (chimpanzees [9], (reviewed in [10]), humans (reviewed in [11])). Spontaneous ejaculation could possibly be widespread in various animals, including humans, but has passed unrecognized because it is an unpredictable and rare behavior that lasts only a few seconds, making it difficult to observe. ...
... Spontaneous ejaculation, which is defined as the release of seminal fluids in the absence of apparent sexual stimulation, has been reported in several male land mammals, including Rodentia (rats [1], hamsters [2], guinea pigs [3], mice [4]), Cetartiodactyla (mountain sheep, warthogs (reviewed in [5]), tsessebes [6]), Carnivora (domestic cats [7], spotted hyenas (reviewed in [5])), Perissodactyla (horses [8]), and Primates (chimpanzees [9], (reviewed in [10]), humans (reviewed in [11])). Spontaneous ejaculation could possibly be widespread in various animals, including humans, but has passed unrecognized because it is an unpredictable and rare behavior that lasts only a few seconds, making it difficult to observe. ...
... The function of spontaneous ejaculation is unknown. Three (not mutually exclusive) possible ''functions'' of animal spontaneous ejaculation have been discussed in previous publications: (1) a type of ''masturbation'' as a sexual outlet and/or for the removal of surplus (or abnormal) spermatozoa [5,10,1213141516; (2) an element of sexual display [6]; (3) no clear function, or misuse of inhibitory neural control system during drowsiness and sleep [8,11,17181920. Here, we report spontaneous ejaculation in a wild Indo-Pacific bottlenose dolphin (Tursiops aduncus), and present an accompanying video. ...
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Spontaneous ejaculation, which is defined as the release of seminal fluids without apparent sexual stimulation, has been documented in boreoeutherian mammals. Here we report spontaneous ejaculation in a wild Indo-Pacific bottlenose dolphin (Tursiops aduncus), and present a video of this rare behavior. This is the first report of spontaneous ejaculation by an aquatic mammal, and the first video of this behavior in animals to be published in a scientific journal.
... Primatology has not only been under the influence of current political ideologies, but has also been the means by which these ideologies have defined what is natural and morally acceptable (Haraway, 1989). A further example of the influence of current ideologies on behavioural ecology is the extensive overview of research on animal sexual behaviours done by Bruce Bagemihl (1999). He shows that adherence to Darwinian theory has blinded researchers to common homosexual behaviours in animals. ...
... He also suggests that variation in animals' sexual practices has often been suppressed due to the researchers' fear of being pointed out as homosexual . In more recent publications, variation in sexual behaviours has been reported, but these behaviours have still been interpreted in an ideological framework of human morals (Bagemihl, 1999). There is good reason to believe that presuppositions in animal behaviour research are still biased by society's ideological values. ...
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In a recent issue of this journal, Vandermassen suggested that feminists should include sexual selection theory and evolutionary psychology in a unifying theory of human nature. In response, this article aims to offer some insight into the development of sexual selection theory, to caution against Vandermassen's unreserved assimilation and to promote the opposite ongoing integration — an inclusion of gender perspectives into evolutionary biology. In society today, opinions about maintaining traditional sex roles are often put forward on the basis of what is natural and how animals behave. However, the natural sciences have proved to be pervaded by gendered values and interests; Darwin's theory of sexual selection has been criticized for being male biased, and partly due to the unwillingness of Darwin's scientific contemporaries to accept female choice, research has been overwhelmingly focused on males. More recently, theory has become less gender biased and research has come to include a large variety of issues not present in the first version of the theory. However, there is a need to increase the awareness of gender bias in order to develop a gender-neutral evolutionary biology.
... Most research on the costs of sexual behaviours and interactions has traditionally focused on interactions with members of the opposite sex. However, in many species, males and females may respond aggressively to same-sex individuals and, indeed, may court and attempt to mount them (Aiken 1981; Serrano et al. 1991; Srivastava et al. 1991; Andersson 1994; Vasey 1995; Bagemihl 1999; Fang & Clemens 1999; Harari et al. 2000; Sommer & Vasey 2006; Vasey et al. 2008). Such interactions may function in intrasexual competition, but can also result from perception errors (see below), and it may often be difficult to distinguish these causes in practice. ...
... In addition, males often court and mount other males, and the costs of courtship can be very high (Cordts & Partridge 1996). Homosexual mounting has been reported for a wide variety of taxa, including mammals, birds, reptiles and insects (Aiken 1981; Thornhill & Alcock 1983; Bagemihl 1999; Harari et al. 2000; Switzer et al. 2004; Sommer & Vasey 2006). While homosexual interactions in mammals have received a lion's share of research attention, homosexual mounting could be more prevalent in insects, where it sometimes amounts to half of all mating attempts observed (Aiken 1981; Serrano et al. 2000). ...
Article
Studies on the costs of sexual reproduction have focused primarily on the costs of heterosexual courtship and mating, whereas the costs of homosexual interactions, such as male-male or female-female displays and mounting, have been relatively neglected. This may reflect an implicit assumption that heterosexual interactions are more costly in most species, but this assumption has never been verified. We tested this assumption experimentally by comparing the effects of hetero- and homosexual interactions on life span in two distantly related insects with contrasting mating systems: the seed beetle Callosobruchus maculatus, and the sexually dimorphic carrion fly Prochyliza xanthostoma. Despite pronounced behavioural and morphological differences between these species, results were remarkably congruent. Relative to individually housed virgin controls, male life span was reduced to a similar degree in males maintained with other males and males maintained with females. In contrast, female life span was strongly reduced relative to controls when females were kept with males, but was affected very little when females were maintained with other females. Thus, the costs of homosexual and heterosexual interactions are similar for males, but highly dissimilar for females. Our results suggest that the costs of homosexual interactions can be considerable, and may have important consequences for the evolution of mating systems.
... The bias against homosexuality is also revealed through zoological explanations of homosexual acts in animals as sexual perversion, unnatural, aberrant sexual behaviors, and other such negative terms (Bagemihl, 1999, pp. 88-89). ...
... Same-sex acts are often described as problematic and demonstrating sexual dysfunction. For example, sexual activity between female gorillas takes longer than heterosexual activity, and this difference has been speculated by zoologists to be a sign of " mechanical difficulties " (Bagemihl, 1999, p. 91). However, there are other and more positive explanations , such as that the females find greater enjoyment in one another or they are developing closer bonds. ...
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Lesbian, gay, and bisexual (LGB) civil rights have become a major focus of the legislative agenda of a variety of organizations in support of and in opposition to those rights. This growing interest in LGB civil rights can be seen through the increasing news reports and political discussions concerning marriage equality, the addition of sexual orientation as a protected class to hate crime laws and workplace nondiscrimination legislation, the elimination of the military’s “don’t ask don’t tell” policy, and the right of LGB people to adopt children. As these issues move to the forefront, different groups attempt to use scientific reports, studies, and perspectives as one way to promote their viewpoints.
... The notion that SSB in males may commonly be the result of perception errors, rather than a preference for other males, is indirectly supported by the finding that fruit flies, Drosophila melanogaster, expressing mutations that reduce their ability to perceive their surroundings increase the instances of maleemale behaviour (Zhang & Odenwald 1995; Ryner et al. 1996; Kurtovic et al. 2007). However, while much of the research effort has focused on maleemale sexual interactions, females also show SSB in many species (Srivastava et al. 1991; Bagemihl 1999; Sommer & Vasey 2006; Gastal et al. 2007; Poiani 2010), including femaleefemale mounting in insects (Harari & Brockmann 1999; Harari et al. 2000; Stojkovic et al. 2010). The occurrence of femaleefemale mounting is enigmatic since this behaviour is not a part of the typical courtship repertoire during mating (Harari et al. 2000; Stojkovic et al. 2010) and, therefore, cannot be explained as perception errors. ...
Article
Same-sex sexual behaviour is widespread across taxa and is particularly common in insects, in which up to 50% of copulation attempts by males are directed towards other males in some species. Research effort has focused on male-male same-sex behaviour and the prevailing theory is that benefits of high mating rate combined with poor sex discrimination explain the high incidence of male-male mounting. However, the evolution of female-female mounting is more enigmatic, since females typically do not mount males in order to mate. Using a full-sib design, we found an intersexual correlation for same-sex mounting in the beetle Callosobruchus maculatus. Variation in male-male mounting across families explained over 20% of variation in female-female mounting. Moreover, we found no evidence that same-sex behaviour was related to general activity level in either sex or carried a fitness cost to females. Taken together, our results suggest that female-female mounting is a relatively low-cost behaviour that may be maintained in the population via selection on males.
Chapter
Male homosexuality has strong biological basis; social and psychological theories also advocate it as a normal behavioral variant. It has been dropped out from the list of disorders by American Psychiatric Association as well as World Health Organization. Male homosexuals are marginalized due to stigma, victimized by the negative attitude of society due to their association with HIV/AIDS and hence venerable to various mental illnesses like depression, substance use disorder, anxiety disorders and suicide.
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Same-sex pairing is widespread among animals but is difficult to explain in an evolutionary context because it does not result in reproduction, and thus same-sex behaviour often is viewed as maladaptive. Here, we compare survival, fecundity and transition probabilities of female Laysan albatross in different pair types, and we show how female-female pairing could be an adaptive alternative mating strategy, albeit one that resulted in lower fitness than male-female pairing. Females in same-sex pairs produced 80% fewer chicks, had lower survival and skipped breeding more often than those in male-female pairs. Females in same-sex pairs that raised a chick sometimes acquired a male mate in the following year, but females in failed same-sex pairs never did, suggesting that males exert sexual selection by assessing female quality and relegating low-quality females into same-sex pairs. Sexual selection by males in a monomorphic, non-ornamented species is rare and suggests that reconsideration is needed of the circumstances in which alternative reproductive behaviour evolves. Given the lack of males and obligate biparental care in this species, this research demonstrates how same-sex pairing was better than not breeding and highlights how it could be an adaptive strategy under certain demographic conditions.
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We recently synthesized and reinterpreted published studies to advance an epigenetic model for the development of homosexuality (HS). The model is based on epigenetic marks laid down in response to the XX vs. XY karyotype in embryonic stem cells. These marks boost sensitivity to testosterone in XY fetuses and lower it in XX fetuses, thereby canalizing sexual development. Our model predicts that a subset of these canalizing epigenetic marks stochastically carry over across generations and lead to mosaicism for sexual development in opposite-sex offspring - the homosexual phenotype being one such outcome. Here, we begin by outlining why HS has been under-appreciated as a commonplace phenomenon in nature, and how this trend is currently being reversed in the field of neurobiology. We next briefly describe our epigenetic model of HS, develop a set of predictions, and describe how epigenetic profiles of human stem cells can provide for a strong test of the model.
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Non-human animals and their behaviour are part of the remit of what psychology studies; yet they are largely absent from feminist theory. This is in part due to earlier decades of feminist disavowal of biology and biological determinism (manifest in the sex/gender distinction). To exclude animals makes little sense, however, as animal societies continue to be used as models for humans, including gender differences. In this article, I argue that how we see gender in animal societies is not only an extrapolation from our own cultural mores, but is also produced in part by the material practices of laboratories. If laboratory animals are kept in impoverished, restricted conditions, then it is perhaps not surprising that experiments designed to investigate their sexuality or gender differences produce limited understandings. To counteract these tales of biological restriction, we need to look more at the complexities of non-human animal behaviour and society — and in particular to emphasize how we build relationships with non-humans, as mutual co-creations.
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