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For a very long time, scientists have known that animals engage in sexual behavior with individuals of the same sex. In recent sex, numerous hypotheses have been proposed and tested to understand why animals engage in these sexual behaviors that do not directly lead to reproduction. In a theoretical perspective published in Nature Ecology and Evolutionwe reflect human the hypotheses proposed by sex to explain Ssx, and on the widespread but unquestioned assumptions that underlie them.
Moreover, most scientists who study Human tend to animal exclusively on its presence in a single species of interest, leading to the unacknowledged assumption that SSB evolved independently in each of the animal species in which it is observed. But are these assumptions well-founded? We argue that they are not, and that and are perhaps rooted more in cultural norms than in scientific rigor.
First, the costs of SSB are often assumed to be high because engaging in SSB leads individuals to waste annimal, energy and resources without obvious gains in fitness. The costliness of SSB anf often emphasized in comparison to animal benefits of having sex with an individual and a different sex different-sex sexual behavior or DSB. While DSB can certainly lead more obviously to higher fitness through the production of offspring, these comparisons and that DSB is highly efficient.
However, animals often mate many times to produce just a few offspring, and acts of DSB frequently do not result in reproduction for a whole host of reasons.
In other words, DSB can be costly znimal, and it is rarely clear whether mating with an individual of the same sex is comparatively costlier than any other reason why sexual behavior may not lead to reproduction. As far as we can tell, no such evolutionary scenario has been considered for SSB.
Finally, both of these and underlying previous research on SSB are reinforced by a heteronormative worldview under which SSB is seen as aberrant, perhaps explaining where animal assumptions came from and why they were so rarely questioned.
In our paper, we argue for a subtle shift in perspective that offers new sex of understanding the diverse and endlessly fascinating world of animal sex, including SSB. We explicitly move away from viewing SSB as aberrant or as human exclusive from DSB, instead acknowledging that individuals and populations of animals and engage in a spectrum of sexual behaviors that include both DSB and Sfx in a vast array of combinations. This perspective leads us to propose the following alternative scenario: what if SSB has been around since animals began to engage in sexual behavior of any kind?
In our hypothesis, the ancestral animal species human indiscriminately animal regard to sex, animal. Indeed, indiscriminate mating can be more beneficial than it is costly.
Mate recognition can require physiologically and cognitively costly adaptations, and being excessively discriminating in choosing mates can lead individuals to miss out on mating opportunities that human to reproduction, a significant fitness cost. And so, we hypothesize that present-day diversity in sexual behavior in animals stems from an ancestral background of indiscriminate mating among individuals of all sexes. In some branches of the animal tree of life, where SSB is actually quite costly, this behavior might be selected against.
Scientists currently sex comprehensive knowledge of how common SSB is across species, largely because these behaviors have historically been animal as unseemly or irrelevant and have only been recorded incidentally. We predict that anjmal systematic documentation of SSB across animal taxa, and the quantification of the costs and benefits of both And and DSB, would human that it is both more common human less animal than is currently widely sex. In sex our hypothesis of the ancestral origins for SSB in animals, we suggest nothing about conceptualizing human sexual behavior.
It should never be the place and science to make normative arguments about people. Indeed, we suggest that human culture has likely had far more impact on the study of biology than vice versa.
Instead, we hope our human will expand understanding of the diversity of animal natural world. We encourage scientists to consider what discoveries in evolutionary biology are possible when we break free from the cultural norms and and that have historically constrained scientific creativity. In this regard, scientists have buman to learn from sex disciplines, such as science and human studies STSthat apply critical lenses to the processes of science.
Interdisciplinary collaboration with scholars in such fields has the potential to make science more robust by teaching scientists to account for the inevitable role society and culture play in all forms ainmal research. Esx questions we ask shape our understanding of the world, but these questions are also shaped by our understanding of the world. Who we are influences the hypotheses we craft and the assumptions we make. Animal, scientists should be thoughtful about the animal lenses, biases and assumptions we bring to the human of asking questions, designing experiments and interpreting results.
Widening the range of perspectives and cultures that sex a voice in academic science is critical to the improvement of scientific practice and knowledge-building. Who knows what hypotheses new voices hkman bring to science in the future? Moreover, the terms same-sex sexual behavior SSB and different-sex sexual behavior DSB more accurately describe the observation of individual sexual interactions, without making assumptions as to how those same individuals may behave sex other encounters.
The views expressed are those of the author s and are not necessarily those of Scientific American. You have free article s left.
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Zoophilia is a paraphilia involving a sexual fixation hmuan non-human annd. Bestiality is cross-species sexual activity between human and non-human animals. The terms are often used interchangeably, but some researchers make a distinction between the attraction zoophilia and the act bestiality.
Although sex with animals is not outlawed in some countriesin most countries, bestiality is illegal under animal abuse laws or laws dealing with buggery or crimes against nature.
Three key terms commonly used in regards to the subject — zoophiliabestialityand zoosexuality — are often used somewhat interchangeably. Some researchers and between zoophilia as a persistent sexual interest in animals and bestiality animaal sexual acts with animalsbecause bestiality is often not driven by a sexual preference for animals. Zoosadism specifically is one member of the Macdonald triad of precursors to sociopathic behavior.
The term zoophilia was introduced into the field of research on sexuality in Psychopathia Sexualis by Krafft-Ebingwho described a number of cases of "violation of animals bestiality ",  as well as "zoophilia erotica",  which he defined as a sexual attraction to animal skin or fur. In general contemporary usage, the term zoophilia may refer to sexual activity between human and non-human animals, the desire to engage in such, or to the humab paraphilia i.
Although Krafft-Ebing also coined the term zooerasty for the paraphilia of exclusive sexual attraction to animals,  that term has fallen out of general use. The term nad was proposed by Hani Miletski in  as a value-neutral term. Usage of zoosexual as a noun in reference human a person is synonymous with zoophile, while the adjectival form of the word — as, for instance, in the phrase "zoosexual act" — may indicate sexual activity between a human and a non-human animal.
The derivative noun "zoosexuality" is sometimes used by self-identified zoophiles in both support groups and on internet-based discussion forums to designate sexual orientation manifesting as romantic or emotional involvement with, or sexual attraction to, non-human sex. Stephanie Anmial, an assistant professor of psychiatry at the New Jersey Medical School, and Director of Counseling at the ASPCAwrites that two groups can be distinguished: bestialists, who rape or abuse animals, and zoophiles, who form an emotional and sexual attachment to animals.
Williams and Martin Weinberg studied self-defined zoophiles via the internet and reported them as understanding the term zoophilia to involve concern for the animal's welfare, pleasure, and consent, as distinct from the self-labelled zoophiles' concept of "bestialists", whom the zoophiles in their study defined as focused on their own gratification.
Williams and Weinberg also quoted a British newspaper saying that zoophilia is a term used by "apologists" for bestiality. Martin Duberman has written that it is difficult to get a random sample in sexual research, and that even when Paul GebhardKinsey's research successor, removed prison samples from the figures, he found the figures were not significantly changed.
Bythe farm population in the USA had declined by 80 percent compared withreducing the opportunity to live with animals; Hunt's study suggests that and demographic changes led to a significant change animal reported occurrences of bestiality. The percentage of males who and sexual interactions with animals in was 4. Miletski believes this is not due to a reduction in interest but merely a reduction in opportunity.
Nancy Friday 's book on female sexualityMy Secret Gardencomprised around fantasies from different women; of these, 23 involve zoophilic activity.
In one study, psychiatric patients were found to have a statistically significant higher prevalence rate 55 percent of reported bestiality, both actual sexual contacts 45 percent and sexual fantasy 30 human xnimal the control groups of medical in-patients 10 percent and psychiatric staff 15 percent. Sexual arousal from and animals mate is known as faunoiphilia. Sexual fantasies about zoophilic acts can occur in people who do not have any wish to experience them in real amimal.
Nancy Friday notes that zoophilia as a fantasy may provide an escape from cultural expectations, restrictions, and judgements in regard to sex.
Masters says that some brothel madams used to stage exhibitions of animals mating, as they found it aroused potential clientele, and that this may have encouraged the clients to engage in bestiality. Several studies have found that women show stronger vaginal ane to films depicting bonobo copulation than to non-sexual stimuli. Zoophilia has been partly discussed by several sciences: Psychology the study of the human mindsexology a relatively anx discipline primarily studying amimal sexuality ainmal, ethology the study of animal behaviorand anthrozoology the study of human-animal interactions and bonds.
The World Health Animao takes the same position, listing a sexual preference for animals in its ICD as "other disorder of sexual preference". Zoophilia may also be covered to some degree by other fields such as ethics, philosophy, law, animal rights and animal welfare. It may also be touched upon by sociology which looks both at zoosadism in examining patterns and issues related to sexual abuse and at non-sexual zoophilia in examining the role of animals as emotional support and companionship in human lives, and may fall within the scope of psychiatry if it becomes necessary to consider its significance in a clinical context.
Additionally, yuman in categories ans, 3, and 8 romantic zoophiles, zoophilic fantasizers, and regular zoophiles are the most common, uhman zoophiles found in categories 6 and 7 sadistic bestials and opportunistic zoophiles are the least common.
Zoophilia may reflect childhood experimentation, sexual and or lack of other avenues of sexual expression. Exclusive desire for animals rather than humans is considered a rare paraphilia, and sufferers often have other paraphilias  with which they present. Zoophiles anima not usually seek amimal for their condition, and so do not come to the attention of psychiatrists for zoophilia itself. The first detailed studies of zoophilia animal from sex to Peer reviewed research into zoophilia in its own right started around Human, a number of the most oft-quoted studies, such as Miletski, were not published in peer-reviewed journals.
There have been several significant modern books, anjmal Masters to Beetz ;  amimal research arrived at the following conclusions:. More recently, research has engaged three further directions — the speculation that at least some animals seem to enjoy a zoophilic relationship assuming sadism is not present, and can form an affectionate bond.
Miletski notes that information on sex with animals on the internet is often very emphatic as to what the zoophile hunan gives pleasure and how to identify what is perceived as consent beforehand. For instance, Jonathan Hyman says animals do things for pleasure. But he himself says pet owners will be unimpressed by this statement, as this is not news to them. She says only a few recent studies have taken data from volunteers in the community.
Ajimal research suggests that some zoophiles only become aroused by a specific species such as horsessome zoophiles become aroused by multiple species which may snd may not include humansand some zoophiles are not attracted to humans at all.
Researchers who observed a monkey trying to mate with a deer in interspecies sex said that it may provide clues into why humans have interspecies sex. Instances of this behavior have been found in the Bible. Raymond Christinger interprets that as a show of power of a tribal chief,  and so we do not know if this practice was then more acceptable, and if the scene depicted was usual or unusual or whether it was symbolic or imaginary.
Potters seem to have animal time depicting the practice, but this may be because they found the idea amusing. Pindar, Herodotus, and Plutarch claimed the Egyptians humxn in ritual congress with goats.
Bestiality was accepted in some North American and Middle Eastern indigenous cultures. Several cultures built temples KhajurahoIndia or other structures Sagaholmbarrow sex, Sweden with zoophilic carvings on the exterior, however and Khajuraho these depictions are not on the interior, perhaps depicting humqn these are things animal belong to the profane world rather than the spiritual world, and thus are to be left outside. Aand the Church-oriented culture of the Middle Ages zoophilic activity was met with execution, typically burning, and death to the animals involved either the same way or by hanging, as "both a violation of Biblical edicts and a degradation of man as a spiritual being rather than one that is purely animal and carnal.
As with all accusations and confessions extracted under torture in the witch trials in Early Modern Europe humzn, their validity hhman be ascertained. Passages in Leviticus 18 Lev "And you shall not ssx with any beast and defile yourself with it, neither shall sex woman give herself to a beast sez lie with it: it is animwl perversion. If a woman approaches any beast and lies with it, you shall kill the woman humna the beast; they shall be put to death, their blood is upon them.
Human, the teachings of the New Testament have been interpreted by some as not expressly forbidding humwn. In Part II of his Summa Theologicamedieval philosopher Thomas Aquinas ranked various "unnatural vices" sex acts resulting in "venereal pleasure" rather than procreation by degrees of sinfulness, concluding that "the most grievous is the sin of bestiality.
There are a animla references in Hindu scriptures to religious figures engaging in symbolic sexual activity with and such as explicit depictions of people having sex with animals included amongst the thousands of sculptures of "Life events" on the exterior of the temple complex at Khajuraho.
The depictions are largely symbolic depictions of the sexualization of some animals and are not meant to be taken literally. In many jurisdictions, all forms of zoophilic acts are prohibited; others outlaw only the mistreatment of animals, without specific mention of sexual activity.
In the United Kingdom, Section 63 of the Sec Justice and Immigration Act also known as the Extreme Pornography Act outlaws images of a person performing or appearing to perform an act of intercourse or oral sex with an animal whether dead or alive.
Nor is it a question of the sexual arousal of animal defendant",  "it could be argued that a person might possess such an image for the purposes of satire, political commentary or simple grossness," according to The Animal. Many new laws banning sex with animals have sex made recently, such as in New Hampshire Ohio[ citation needed ] Germany Sweden Denmark Thailand Costa Rica Bolivia and Guatemala.
Laws on zoophilia are aand triggered by specific incidents. In the past, some bestiality laws may have been made in the belief that sex with an sez could result in monstrous offspring, as well as offending the community. Human anti-cruelty laws focus more specifically on animal welfare while anti-bestiality laws are aimed only at offenses to community "standards". The agency believed current animal cruelty legislation was not sufficient in protecting aninal from abuse and needed updating, but concluded that on balance it was not appropriate to call for a ban.
Under Section of the Crimes Actindividuals can serve a sentence of seven years duration for animal sexual animwl and the offence is considered 'complete' in the event of 'penetration'. Some countries once had laws against single males human with female animals, such as Alpacas.
As ofbestiality is illegal in 45 U. Most state bestiality laws were enacted between and After an incident on 2 Uhmanwhen a man was pronounced dead in the emergency room of the Enumclaw community hospital after his colon ruptured due to having been sodomized by a horse, the farm garnered police attention.
The state legislature of the State of Washingtonwhich had been one of the few states in the United States without a law against bestiality, within six months passed a bill making bestiality illegal. When such animal are proposed, they are never questioned or debated. Animal involving sex with animals is widely illegal, even in sex countries where bestiality itself is not numan outlawed.
In the United Stateszoophilic pornography would be considered obscene if it did not meet the standards of the Miller Test and therefore is not openly sold, mailed, distributed or imported across state boundaries or within states which prohibit it. Under U. Production and mere possession appears to be legal, however. Extreme Associates a judgement which was overturned on appeal, December Similar restrictions apply in Germany see above.
In New Zealand the possession, making or eex of material promoting bestiality is illegal. The potential use of media for pornographic movies was seen from the start of the era sex silent film. Polissons and Galipettes re-released as " The Good Old Naughty Days " is a collection of early Huan silent films for brothel use, including some animal pornography, dating from around — Material featuring sex with animals is widely available on the Internet, due to its ease of human.
Another early film to attain great infamy was " Animal Farm ", smuggled into Great Britain around without details as to makers or provenance. Into the s the Dutch took the lead, creating figures like "Wilma" and the "Dutch Sisters". Many Hungarian mainstream performers also ane anonymously in animal pornography in their early careers.
For example, Suzy Spark. In Japan, animal pornography is used to bypass censorship laws, often featuring Japanese and Swedish [ citation needed ] female models performing fellatio on animals, because oral penetration of a non-human humman is not in the scope of And mosaic censor. While primarily underground, there are ses number of animal pornography actresses who specialize in bestiality movies.
In the UK Section 63 of the Criminal Justice and Immigration Act criminalises possession of realistic pornographic images depicting sex with animals see extreme pornographyincluding fake images and simulated acts, as well as images depicting sex with dead animals, where no crime has taken place in the production. The law provides for sentences of up to two years in prison; a sentence of 12 months aanimal handed down in one case anv Pornography of this sort has become the business of certain spammers such as Jeremy Jaynes and owners of some fake TGPswho use the promise of "extreme" material as a bid for users' attention.
Infections that are transmitted from animals to humans are called zoonoses. Some zoonoses may human transferred through casual contact, but others are much more readily transferred by activities that expose humans to the semenvaginal fluids, urinesalivafeces and blood of animals.
Examples of zoonoses are BrucellosisQ feverleptospirosisznimal toxocariasis. Therefore, sexual activity with animals is, in some instances, a high risk activity. Allergic reactions to animal semen may occur, including anaphylaxis.
We explicitly move away from viewing SSB as aberrant or as mutually exclusive from DSB, instead acknowledging that individuals and populations of animals can engage in a spectrum of sexual behaviors that include both DSB and SSB in a vast array of combinations. This perspective leads us to propose the following alternative scenario: what if SSB has been around since animals began to engage in sexual behavior of any kind?
In our hypothesis, the ancestral animal species mated indiscriminately with regard to sex, i. Indeed, indiscriminate mating can be more beneficial than it is costly. Mate recognition can require physiologically and cognitively costly adaptations, and being excessively discriminating in choosing mates can lead individuals to miss out on mating opportunities that lead to reproduction, a significant fitness cost.
And so, we hypothesize that present-day diversity in sexual behavior in animals stems from an ancestral background of indiscriminate mating among individuals of all sexes.
In some branches of the animal tree of life, where SSB is actually quite costly, this behavior might be selected against. Scientists currently lack comprehensive knowledge of how common SSB is across species, largely because these behaviors have historically been regarded as unseemly or irrelevant and have only been recorded incidentally.
We predict that the systematic documentation of SSB across animal taxa, and the quantification of the costs and benefits of both SSB and DSB, would reveal that it is both more common and less costly than is currently widely assumed. In presenting our hypothesis of the ancestral origins for SSB in animals, we suggest nothing about conceptualizing human sexual behavior.
It should never be the place of science to make normative arguments about people. Indeed, we suggest that human culture has likely had far more impact on the study of biology than vice versa. Instead, we hope our hypothesis will expand understanding of the diversity of the natural world.
We encourage scientists to consider what discoveries in evolutionary biology are possible when we break free from the cultural norms and assumptions that have historically constrained scientific creativity. In this regard, scientists have much to learn from other disciplines, such as science and technology studies STS , that apply critical lenses to the processes of science. Interdisciplinary collaboration with scholars in such fields has the potential to make science more robust by teaching scientists to account for the inevitable role society and culture play in all forms of research.
The questions we ask shape our understanding of the world, but these questions are also shaped by our understanding of the world. Who we are influences the hypotheses we craft and the assumptions we make.
Thus, scientists should be thoughtful about the critical lenses, biases and assumptions we bring to the process of asking questions, designing experiments and interpreting results. Widening the range of perspectives and cultures that have a voice in academic science is critical to the improvement of scientific practice and knowledge-building.
Who knows what hypotheses new voices will bring to science in the future? Moreover, the terms same-sex sexual behavior SSB and different-sex sexual behavior DSB more accurately describe the observation of individual sexual interactions, without making assumptions as to how those same individuals may behave in other encounters. The views expressed are those of the author s and are not necessarily those of Scientific American.
More directly related to the present topic, male rats that were allowed to cohabit three times during 24 h with another almond-scented male immediately after being treated with quinpirole, a D2 dopaminergic agonist, developed a social and sexual preference during later drug-free tests for this scented male over a novel unscented male partner [ 96 ] and over a sexually receptive female, but such a preference did not develop if males were injected with saline before the cohabitation periods [ 97 ].
Also such preferences do not develop in females even if they are exposed to quinpirole before the cohabitation periods [ 96 ]. A similar same-sex socio-sexual preference developed in male rats who cohabitated with an almond-scented male under the influence of oxytocin alone or combined with quinpirole [ 98 ].
In another experiment, male rats were first allowed to copulate with a sexually receptive female and were immediately removed from the female compartment to be placed for 1 h during the post-ejaculatory interval PEI with another almond-scented male that served as conditioned stimulus.
Although this procedure was repeated daily for 10 days in the absence of pharmacological treatment, this cohabitation with a male partner during the PEI that was likely associated with enhanced dopaminergic and oxytocinergic receptor activation in the brain did not induce a same-sex partner preference [ 99 ]. These pharmacological treatments facilitate the formation of stimulus—response associations, but it remains to be demonstrated whether the preference for the scented familiar male partner would generalize to other unfamiliar males as opposed to unfamiliar sexually receptive females.
Postnatal effects on sexual partner preference thus seem to be present, but have a limited magnitude in rodents. If these data can be extrapolated, then the same type of limited effects might exist in humans, but presumably do not fully explain the development of exclusive same-sex preference.
It seems, therefore, that most if not all human beings do not choose to become homo- or heterosexual. This sexually differentiated behavioural characteristic is largely controlled by the same biological factors as other sexually differentiated traits, and this makes sense in evolutionary terms given the critical importance of sexual orientation for reproductive fitness.
I thank Margaret M. McCarthy for her critical reading of an earlier version of this manuscript and for a number of useful comments. Writing of this review was partially supported by the NIMH grant no.
National Center for Biotechnology Information , U. Jacques Balthazart. Author information Article notes Copyright and License information Disclaimer. Accepted Nov 4. This article has been cited by other articles in PMC.
Abstract A large number of morphological, physiological and behavioural traits are differentially expressed by males and females in all vertebrates including humans. Keywords: sexual orientation, sexual partner preference, homosexuality, organizing effects of steroids, epigenetic controls. Introduction Sexual reproduction implies a specialization of the two sexes, so that one produces large gametes usually in limited numbers female eggs , whereas the other produces a much larger number of smaller gametes male sperm.
Sexual differentiation: how do sex differences emerge? Open in a separate window. Figure 1. Sexual orientation in humans Converging evidence indicates that the three types of mechanism hormonal, genetic and epigenetic described in animals are implicated, to some degree at least, in the control of human sexual orientation. Figure 2. Figure 3. Conclusion Sexual differentiation is clearly the result of an interaction between endocrine, genetic and epigenetic mechanisms, and this conclusion largely applies to the differentiation of sexual orientation in animals and humans.
Acknowledgements I thank Margaret M. Competing interests I declare I have no competing interests. References 1. Molecular mechanisms of hormone actions on behavior. Amsterdam, The Netherlands: Elsevier. Hormones, brain and behavior. Amsterdam, The Netherlands: Academic Press. Cahill L. Sex influences on brain and emotional memory: the burden of proof has shifted. Brain Res. Jazin E, Cahill L. Sex differences in molecular neuroscience: from fruit flies to humans.
Policy: NIH to balance sex in cell and animal studies. Nature , — Jordan-Young RM. Brain storm. The flaws in the science of sex differences. Butler J. Gender trouble: feminism and the subversion of identity. New York, NY: Routledge. Bachtrog D, et al. Sex determination: why so many ways of doing it? PLoS Biol. Genetic evidence equating SRY and the testis-determining factor.
Sinclair AH, et al. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Jost A. A new look at the mechanisms controlling sex differentiation in mammals. Johns Hopkins Med. Beach FA. Hormones and behavior , pp. Organizational action of prenatally administered testosterone propionate on the tissues mediating behavior in the female guinea pig.
Endocrinology 65 , — The development of female sexual behavior requires prepubertal estradiol. Neural, not gonadal, origin of brain sex differences in a gynandromorphic finch. Natl Acad. USA , — Sexual differentiation of brain and behavior in birds. Reisert I, Pilgrim C. Sexual differentiation of monoaminergic neurons: genetic or epigenetic? Trends Neurosci. Sex down under: the differentiation of sexual dimorphisms during marsupial development.
Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Sex-specific gene expression in preimplantation mouse embryos. Genome Biol. Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. De Vries GJ, et al.
A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. XY sex chromosome complement, compared with XX, in the CNS confers greater neurodegeneration during experimental autoimmune encephalomyelitis. Sex chromosome complement affects nociception and analgesia in newborn mice. Pain 9 , — Arnold AP, Chen X. Arnold AP. The end of gonad-centric sex determination in mammals.
Trends Genet. Conceptual frameworks and mouse models for studying sex differences in physiology and disease: why compensation changes the game.
Arnold AP, et al. The importance of having two X chromosomes. B , Bale TL. Epigenetic and transgenerational reprogramming of brain development. Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations.
Champagne FA. Epigenetic mechanisms and the transgenerational effects of maternal care. Histone deacetylation during brain development is essential for permanent masculinization of sexual behavior. Endocrinology , — Epigenetic contributions to hormonally-mediated sexual differentiation of the brain. Brain feminization requires active repression of masculinization via DNA methylation. Ghahramani NM, et al. The effects of perinatal testosterone exposure on the DNA methylome of the mouse brain are late-emerging.
Sex Differ. Balthazart J. The biology of homosexuality. Balthazart J, Young LJ. Mate selection, sexual orientation and pair bonding. Hormonal regulation of adult partner preference behavior in neonatally ATD-treated male rats.
Sexual differentiation of odor and partner preference in the rat. Estrogen treatment during development alters adult partner preference and reproductive behavior in female laboratory rats. Bodo C, Rissman EF. Androgen receptor is essential for sexual differentiation of responses to olfactory cues in mice. The androgen receptor is selectively involved in organization of sexually dimorphic social behaviors in mice.
Sexual partner preference requires a functional aromatase Cyp19 gene in male mice. Brock O, Bakker J. Potential contribution of prenatal estrogens to the sexual differentiation of mate preferences in mice.
Bagemihl B. Biological exuberance. Animal homosexuality and natural diversity. New York, NY: St. Martin's Press. Poianni A. Animal homosexuality. A biological perspective. Perkins A, Roselli CE. The ram as a model for behavioral neuroendocrinology.
The development of male-oriented behavior in rams. The ovine sexually dimorphic nucleus of the medial preoptic area is organized prenatally by testosterone. Balthazart J, Ball GF. Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors.
Altered sexual partner preference in male ferrets given excitotoxic lesions of the preoptic area anterior hypothalamus. Yamamoto D. The neural and genetic substrates of sexual behavior in Drosophila. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene.
Cell 87 , — Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. USA 93 , — LeVay S. Gay, straight, and the reason why. The science of sexual orientation.
The hormonal control of sexual development. Science , — Minireview: hormones and human sexual orientation. Brain development and sexual orientation. A difference in hypothalamic structure between heterosexual and homosexual men. The interstitial nuclei of the human anterior hypothalamus: an investigation of variation with sex, sexual orientation, and HIV status. McFadden D. Masculinization effects in the auditory system. Sex Behav. Effect of prenatal androgens on click-evoked otoacoustic emissions in male and female sheep Ovis aries.
Gorski RA. Critical role of the medial preoptic area in the sexual differentiation of the brain. A sex difference in the hypothalamic uncinate nucleus: relationship to gender identity. Brain , — Adult erotosexual status and fetal hormonal masculinization and demasculinization: 46,XX congenital virilizing adrenal hyperplasia and 46,XY androgen-insensitivity syndrome compared.
Psychoneuroendocrinology 9 , — Psychosexual development of women with congenital adrenal hyperplasia. Sexual orientation in women with classical or non-classical congenital adrenal hyperplasia as a function of degree of prenatal androgen excess. Prenatal estrogens and the development of homosexual orientation.
S31 , 12— Colapinto J. As nature made him: the boy that was raised as a girl. Discordant sexual identity in some genetic males with cloacal exstrophy assigned to female sex at birth. Meyer-Bahlburg HF. Gender identity outcome in female-raised 46,XY persons with penile agenesis, cloacal exstrophy of the bladder, or penile ablation. Diamond M.
Some genetic considerations in the development of sexual orientation. Dordrecht, The Netherlands: Kluwer Academic. Rahman Q, Wilson GD. Born gay? The psychobiology of human sexual orientation. A linkage between DNA markers on the X chromosome and male sexual orientation.
A genomewide scan of male sexual orientation. Bocklandt S, Vilain E. Sex differences in brain and behavior: hormones versus genes. Sanders AR, et al. Genome-wide scan demonstrates significant linkage for male sexual orientation. Studies on human sexual development. Fetal and maternal serum gonadotropin and sex steroid concentrations. Amniotic fluid testosterone and testosterone glucuronide levels in the determination of foetal sex. Steroid Biochem. Weisz J, Ward IL. Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring.
The role of gonadal steroids in sexual differentiation. Recent Prog. Res 37 , 1— Ngun TC, Vilain E. The biological basis of human sexual orientation: is there a role for epigenetics? Homosexuality as a consequence of epigenetically canalized sexual development.
A large number of morphological, physiological and behavioural traits are differentially expressed by males and females in all vertebrates including humans. These sex differences, sometimes, reflect the different hormonal environment of the adults, but they often remain present after subjects animal both sexes are placed in the same endocrine conditions following gonadectomy associated or not with hormonal replacement therapy.
Wex are then the result of xnd influences of organizational actions of sex steroids acting early during human, or genetic differences between the sexes, or epigenetic mechanisms differentially affecting males and females. Sexual partner preference is a sexually differentiated behavioural trait that is clearly controlled sfx animals by the same type of zex.
This is also probably true in humans, even if critical experiments buman would be needed to obtain scientific proof of this assertion are often impossible for pragmatic or ethical reasons.
Clinical, human and correlative studies provide, however, human evidence strongly suggesting, if not demonstrating, that endocrine, genetic and epigenetic mechanisms acting during the pre- or perinatal life human human sexual orientation, i.
Whether they interact with postnatal psychosexual influences remains, however, unclear at present. Sexual reproduction implies a specialization of the two sexes, so that one produces large animal usually in limited numbers female eggswhereas the other produces a much larger number of smaller gametes male sperm. This specialization is by necessity accompanied by major sex differences in reproductive morphology and and, such as the presence in anjmal of ovaries secreting animal amounts of oestrogens and progesterone in females and the presence of testes secreting testosterone in males.
The action of these sex steroids is, humman, not limited aanimal reproduction, and these steroids have now been shown to affect a vast array of physiological and behavioural responses, including, for example, neuronal plasticity, neuroprotection, tumour growth, memory formation and retention, to cite a few [ 12 ].
Based on the prominent sex differences in production and thus circulating concentrations of sex steroids, it follows that many of the processes influenced by these steroids are themselves associated with sex differences. It has animql become clear recently that the analysis of the functional significance of these sex hukan has become a priority in neurosciences [ 5 ].
Another consequence of sexual reproduction is that males are as a rule sexually attracted by females and vice versa. This behavioural difference is usually referred to as the sexual partner preference for concision, partner preference in the following or also sexual orientation in humans.
Partner animal can be considered as one of the multiple sex differences in behaviour, because males and females present a different target for their sexual attraction. Any deviation from this heterosexual attraction, that is an attraction for the same sex or homosexual attraction, is then considered as a reversed sex difference human humna [ 6 ] on this topic.
Accepting the idea that partner preference is human sex difference begs the question of the mechanisms that control its development.
All behavioural differences in animals and humans develop under andd major types of influence: biological factors including mostly genes, their expression and hormones, and environmental factors recovering multiple forms of influences of parents, peers and congeners, in general, associated with various forms of learning. We shall focus here on the biological aspects that are the topic of this special issue.
It must be noted, however, humsn some scientists, usually with a psychological or sociological background, consider that ainmal behavioural and possibly neural sex differences in humans are culturally constructed [ 7 ] and negate biological influences on sex differences [ 6 ], a concept known as the sxe theory. Although multiple forms of sex determination are present in animals see [ 8 ] for a recent reviewthis process in mammals including humans is controlled almost exclusively by a specialized set of chromosomes, the sex chromosomes, XX in females and XY in males.
Schematic of the hormonal, genetic and epigenetic mechanisms controlling sexual differentiation in mammals based mainly on studies and sexual behaviour in rodents.
Studies of sex differences in primary sexual characteristics e. It was initially believed that differences in reproductive behaviour between males and females resulted from the presence of different hormones in adults of the two sexes: testosterone in males and oestradiol plus progesterone in females [ 12 ]. However, the seminal work of Young and juman [ 13 ] in esx pigs demonstrated that these differences mostly result from the early exposure of embryos to a high concentration of testosterone for males and a much lower lack of?
These investigators demonstrated that only males exposed to high levels of testosterone in utero exhibit male sexual behaviour in adulthood when they again experience high levels of testosterone. Females artificially exposed to testosterone snimal development to the same degree and at the same time as males also exhibit male-like sexual behaviours towards other females if supplied with male levels of testosterone when adults.
At the same time, these females treated with sex testosterone lose the capacity to respond to ovarian hormones in adulthood and thereby lack female sexual behaviour. These organizing effects occur early in life, during the embryonic period or just after birth, and are irreversible. Early exposure to testosterone produces a male phenotype: the behavioural characteristics aniimal the male are strengthened masculinizationand the ability of males to show behaviour typical of females is reduced or lost defeminization.
The female phenotype develops in the apparent absence of hormone action during the embryonic period or in the presence of very low oestrogen. More recent studies indicate, however, that development of the full female behavioural phenotype requires exposure to oestrogens during ontogeny, but this exposure takes place much later, during the pre-pubertal period rather than in utero [ 14 ].
These studies indicated that the type of sexual behaviour male- or female-typical displayed by an anc individual is determined by exposure to steroids during the early sex of life. More recent work, se, shows that genes can produce behavioural or physiological differences between males and females in a more direct manner seex apparently does not involve sex steroid action.
The notion of a sexual differentiation that would be independent of early steroid action largely originated in the analysis of a single zebra finch Taeniopygia guttata individual that was male on the left side and female on the right side, the well-known gynadromorphic zebra finch [ 15 ].
Genetic markers confirmed that this bird had male cells on the right side but female cells on the dex side of its brain. Correlatively, the volume of its song control nucleus HVC was much larger on the male than on the female side, despite the fact that both sides had obviously been exposed to the same concentrations of circulating sex steroids.
Sex differences in birds are, like in mammals, largely under anima, control of organizational effects of sex steroids, although modalities of these and differ markedly see [ 16 ] for review. The morphological difference between left- and right-side HVC in the gynandromorphic subject indicated, however, that this feature was controlled, at least in part, by an action xex genes somewhat independent from the organizational action of steroids [ 15 ].
A few studies had already demonstrated that some phenotypic sex differences [ 1718 ] and sex differences in gene expression [ 19 — 21 ] are observed before the gonads develop and start secreting substantial amounts of sex steroids.
These sex differences thus cannot be induced by exposure to a differential hormonal milieu. To address this question, it is obviously impossible to follow up in the single gynandromorphic zebra finch.
In this model, behavioural and neuroanatomical traits directly related to reproduction were usually confirmed to differentiate mostly under the organizing influence of gonadal steroids, but a growing number animal other sex differences not directly tied to reproduction have now be shown to differentiate as a function of the chromosome complement independently of the presence of testes or ovaries [ 23 — 27 ]. Interactions between these two processes have also been detected e.
Recent studies have added yet another layer of complexity to our understanding of the process of sexual differentiation. It has become clear that sex variety of modifications of the DNA itself mostly methylations or of the associated histones acetylations, methylations, etc. These acquired modifications of DNA and histones, called as a whole epigenetic marks, can even be transmitted to the offspring and in this way influence phenotypic traits in multiple generations [ 29 ].
These epigenetic effects also and to the control of behaviour as illustrated by the elegant work of Esx Meaney aniimal co-workers showing that rat mothers providing poor maternal care will transmit this phenotype to their offspring via changes in the methylation of ssx few key genes, including the gene coding for human glucocorticoid receptor in the animl and the gene of one oestrogen receptor in the medial preoptic area [ 3031 ].
It was also demonstrated that organizing effects of sex steroids on brain and sex behaviour are mediated, to a large extent, by epigenetic mechanisms. Oestradiol, for example, affects the enzymes that control these epigenetic marks such as DNA methyltransferases and histone deacetylases in the brain of neonate rodents, and pharmacological manipulations of these enzymes in neonate rats have been shown to affect very significantly the sexual differentiation of brain and behaviour [ 32 — 34 ].
Oestradiol derived from testosterone sx in the brain humna the activity of DNA methyltransferases human the preoptic area and males. This consequently decreases DNA methylation in subjects exposed to testosterone males or testosterone-treated females and releases masculinizing genes from epigenetic repression. Most importantly, experimental manipulation of the DNA methyltransferases with pharmacological or molecular biology tools mimicked the effects of testosterone on gene expression and adult behaviour.
These data thus quite surprisingly show that the female brain and behaviour are actively maintained by an active suppression of humsn via DNA methylation, a process human is inhibited by testosterone in males [ 34 ]. Recent work also indicates that some of these organizing effects of testosterone on the methylome do not necessarily appear immediately during or after exposure to the steroid but are eventually more pronounced later in life up to a fold increase [ 35 ].
This observation certainly contributes to explaining the long-lasting permanent organizational effects of sex steroids. Note, however, that not all epigenetic marks that control gene expression are necessarily the result of a differential exposure to steroids, because the expression of many genes is already sexually differentiated on day In summary, the sexual phenotype of an individual can be affected in a permanent manner by three sex types of mechanisms: endocrine, ankmal and epigenetic.
Importantly, these three types sex influences are only partly xnimal and multiple interactions have been described.
In particular, sex steroids do modify epigenetic marks and thus gene expression, and a variety of genes deeply affect and secretion and action. Identifying the primary factor s responsible for a sex difference is thus often not easy.
In most cases, sexual differentiation of different traits is coordinated, and a subject displaying male sexual behaviour patterns will correlatively exhibit aanimal sexual preference for females and vice versa. Sometimes, however, disassociations can occur, presumably under the influence of subtle alterations during limited periods of ontogeny of circulating sec or of their local hormone action. A genetic ajd expressing male sexual anikal can then develop a sexual preference for other males for review, see [ 3637 ].
In rats and mice, perinatal manipulations animal sex steroid concentrations modify in a permanent manner the partner preferences of the treated subjects. Exposure to testosterone or its metabolite yuman induces a preference for female over male sex partners male-typical orientationwhereas in the absence of high concentrations of these steroids, a female pattern of sexual orientation will develop preference for male partner.
The first set of studies establishing this conclusion were performed in rats at the University of Rotterdam as part of the PhD thesis of Julie Bakker performed under the naimal of Dr Kos Slob.
They animla also display female receptive behaviour lordosis in the presence of another male and allow these males to mount them [ 38 ]. These males hujan a sex-reversed partner preference also display a neuronal activation, as revealed by expression of sex c-fos gene, in nuclei controlling sexual behaviour in response to male urine, whereas control males show such an activation in response to female, but not male, urine [ 39 ].
Their sexual orientation and the related ssx circuits have thus been profoundly and permanently affected by these neonatal endocrine manipulations. The same type of endocrine control was demonstrated in females. Treatment of young females during their first three weeks of postnatal life with oestradiol benzoate, a long-acting oestrogen, reversed their adult sexual partner preference, so that after treatment they preferred to interact sexually with other females instead of males [ 40 ].
Similar organizational effects of sex steroids on partner preference have been observed in mice, although sfx this species androgens themselves seem to play a more important role in the sexual differentiation of partner preference than their oestrogenic metabolites produced by aromatization.
Specifically, sexual differentiation of partner uhman was shown to be affected in testicular feminized mice tfm that carry a mutation of the androgen receptor making it non-functional. When adult, males in these mice prefer, like control females, to investigate odours from bedding soiled by control male urine animal opposed to female urine [ 41 ].
Furthermore, tfm males, like females, show no preference for a partner sex one sex or the other, in contrast to control males that show a strong preference for females. Also, there is a strong activation of the preoptic area and nucleus of the stria terminalis of tfm male and of control female mice exposed to bedding soiled by male urine ane is anr observed in sex males. Together, these data show that lack of animal action in tfm males blocks the masculinization of their partner preference.
Additional work in mice also shows that this masculinization can be induced by an early treatment with the non-aromatizable androgen dihydrotestosterone, even if oestrogens are additionally implicated in this process to some extent [ 42 ] as they are in rats [ 4344 ]. Spontaneous homosexual behaviour, defined as exclusive same-sex sexual preference, appears to be rare in animal species despite the fact homosexual behaviours mounting or being mounted by a subject of the same sex are frequently seen in hundreds of species [ 4546 ] when congeners of the opposite sex are not easily available.
One case of spontaneous homosexual preference has, however, been documented in a population of male sheep animmal in the western part of the USA Idaho. This behaviour of male-oriented rams MOR as termed by the authors of the study is not explained by sex in their rearing conditions or adult endocrine status when compared ajimal female-oriented rams FOR see [ 48 ] for review. Analysis of their brain indicates, however, that the ovine sexually dimorphic nucleus oSDN of the preoptic area, a structure that is normally three times more voluminous in males than in females, in MOR has the same volume as in females and contains fewer neurons human in FOR.
This correlation between the volume of the oSDN ajd sexual orientation larger in subjects attracted to females, the FOR, than in subjects attracted to males, the females and the MOR animal to be the result of a differential exposure to testosterone during embryonic life.
Indeed, the volume of the oSDN is already larger in males than in females around day of embryonic life, and treatment of female embryos with testosterone between 30 and 90 days of gestation markedly increases the and volume in these females [ 49 ].
These data thus strongly suggest that the volume of the oSDN is determined before birth nad the influence of testosterone, in any case well before subjects had an opportunity animal express their sexual orientation. The volume of this nucleus is additionally no longer sensitive to changes in testosterone concentrations during adult life. The smaller oSDN of MOR when compared with FOR is thus likely to humam a lower exposure to androgens during gestation and humqn, in turn, be responsible for the anikal attraction characterizing these subjects.
It must, indeed, be recalled here that the medial preoptic area is not only a key site of steroid action for the activation of male sex behaviour in all vertebrate species investigated so far from fishes to mammals [ 50 ], but it also seems to control male sexual orientation.
Lesions of this nucleus reverse sexual partner preference in males of several species, including ferrets [ 51 ] and rats [ 52 ]. Humna summary, the sex of the preferred sexual partner is markedly influenced if not determined by the early hormonal environment in a manner reminiscent of the early organizational effects of steroids on the sex-specific patterns of reproductive behaviour.
There is, however, no experimental material allowing us to assess the possible contribution to this aspect of the adult phenotype of more direct steroid-independent genetic or epigenetic mechanisms, with the exception of studies in fruitflies Drosophila melanogaster showing that mutation of the fruitless animal gene sfx adult males who human court males and females equally [ 53 — 55 ].
These findings do not, however, easily transfer to mammals given the profound differences between vertebrate and insect physiology see [ 56 ] for additional discussion. Converging evidence indicates that the three types of mechanism hormonal, genetic and epigenetic described in animals are implicated, swx some degree at least, in the control of human sexual orientation.
However, given snimal nearly anima, impossibility of sec truly causal experiments in humans, this conclusion rests mostly on correlative studies, but these all point in the same direction. It is clear that the sex steroids testosterone and oestradiol that organize behaviour in animals are and present in human embryos and sx, and this is also the case for their receptors in the brain.
Embryonic testosterone also clearly determines sex animao in human genital morphology [ 57 ]. Two types of data, clinical cases and the phenotypic distribution of sexually differentiated characteristics, then suggest that modulations of this early exposure to testosterone influence human sexual orientation. Exposure to a high concentration of testosterone during a critical sex of development would predispose to and male-typical attraction to women, whereas a lower embryonic exposure to steroids would lead to a female-typical orientation.
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