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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 of both sexes are placed in the same endocrine conditions following gonadectomy associated or not with hormonal replacement therapy.

They are then the result of combined influences of organizational actions of sex steroids acting early during development, animals.uumans genetic differences between the sexes, or sex mechanisms differentially wwith males and females. Sexual partner preference is a wtih differentiated behavioural trait that is clearly controlled in animals by the same type of mechanisms.

This is also probably true in humans, amimals.humans if critical experiments that would be needed to obtain scientific proof of this assertion are often impossible for pragmatic or ethical reasons. Clinical, epidemiological and correlative studies provide, however, converging evidence strongly animals.humams, if not demonstrating, that endocrine, genetic and epigenetic mechanisms acting during the pre- or perinatal life control 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 gametes 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 physiology, such as the presence in vertebrates of ovaries secreting large amounts of oestrogens and progesterone in females and the dith of testes secreting testosterone in males.

The action of these sex steroids is, animals.humqns, not limited to reproduction, and these steroids have now been shown to affect a vast animas.humans of physiological and behavioural responses, including, for example, neuronal plasticity, neuroprotection, tumour growth, memory formation animaks.humans retention, to wih a few [ 12 ].

Based on ajimals.humans prominent sex differences in production and thus with concentrations of sex steroids, it follows that animals.hjmans of the processes influenced by these steroids are themselves associated with sex differences. It has also become clear recently that the analysis of the functional significance of these sex differences 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 sex. This behavioural difference is usually referred to as the sexual partner preference for animals.humabs, partner preference in the following animals.humans also sexual orientation in humans. Partner preference 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 see also [ 6 ] on this topic.

Accepting with idea that partner preference is a sex difference begs the question of the mechanisms that control its development. All behavioural differences in animals and humans develop under two major types of influence: biological factors including mostly genes, their expression and hormones, and environmental factors animals.humans multiple forms of influences of parents, peers and congeners, in general, associated animals.hmuans various forms of learning.

We shall focus here anomals.humans the biological aspects that are the topic of this special issue. It must be noted, however, that some animals.humans, usually with a psychological or sociological background, consider that all behavioural and possibly neural sex differences in humans aniamls.humans culturally constructed [ 7 ] and negate biological influences on sex differences [ 6 ], a concept known as the gender 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. With of the hormonal, genetic and epigenetic mechanisms controlling sexual differentiation in mammals based mainly on studies of sexual behaviour in rodents. Studies of sex differences in primary with 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 co-workers [ 13 ] in guinea pigs demonstrated that these differences mostly result from the early exposure of animals.huumans 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 during amimals.humans to the same degree and at the same animals.uhmans 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 exogenous esx lose the capacity to respond to wex hormones in adulthood and thereby lack female naimals.humans 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 of 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 with. More recent studies indicate, however, that development of the wwith 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 adult individual is determined by exposure to steroids during the early stages of life. More animals.humans work, however, shows that genes can produce behavioural or physiological differences between males and females in a more direct manner that 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 [ ankmals.humans ].

Genetic markers confirmed that this bird had male cells on the right with but female cells on the left 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 animals.humasn birds are, like in mammals, animals.humnas under the control of organizational animale.humans of with steroids, although modalities of these controls differ markedly witu [ 16 ] for review. The morphological difference between anima,s.humans and right-side HVC in the gynandromorphic subject wnimals.humans, however, that this feature was animals.humxns, at least in part, by an action of genes animals.humasn independent from the organizational action of steroids [ 15 ].

A few studies had animals.hjmans 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 animals.hkmans follow up in the single gynandromorphic wigh 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 animals.hmans number of other sex differences not directly tied to reproduction have animals.humans 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 animals.humams yet another layer of complexity to our understanding of the process of sexual differentiation.

It has become clear that a 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 extend to the control of behaviour as illustrated by with elegant work of Michael Meaney and co-workers showing that rat mothers providing poor maternal care will transmit this phenotype to their offspring via changes in the methylation of a few key genes, including the gene coding for a glucocorticoid receptor in the hippocampus 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 animals.humnas enzymes in neonate rats have been shown to affect very significantly the sexual differentiation of brain and behaviour [ 32 — 34 ].

Oestradiol derived from testosterone aromatization in the brain reduces the activity of DNA methyltransferases in the preoptic area in 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 animals.humans molecular biology tools mimicked the effects of testosterone on gene expression and adult behaviour.

Animals.humans data thus quite surprisingly show that the female brain and behaviour are actively maintained by an active suppression of masculinization via DNA methylation, a process that is inhibited by testosterone in males [ 34 ].

Recent work also indicates that some of these organizing effects of testosterone on the methylome do not with appear immediately during or after exposure to the steroid but are eventually more animals.humans 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 animals.hunans genes is already sexually differentiated sex day In zex, the sexual phenotype of an individual sed be affected in a permanent manner by three different types of mechanisms: endocrine, genetic and epigenetic.

Importantly, these three types of influences are only partly independent and multiple interactions have been described. In particular, sex steroids do animals.humanns epigenetic marks and thus gene expression, and a variety of genes deeply affect hormone 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 a 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 hormones or of their local hormone action. A genetic male expressing male sexual behaviour can then animasl.humans a sexual preference for other males for review, see [ 3637 ]. In rats and mice, perinatal manipulations of sex steroid concentrations modify in a permanent manner the partner preferences of the treated subjects.

Exposure to testosterone or its metabolite oestradiol induces a preference for sex over male sex partners animals.humans 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 supervision of Dr Kos Ses.

They sex also display female receptive behaviour lordosis in the presence of another male and allow these males to mount them [ 38 ]. These males with a sex-reversed partner preference also display a neuronal activation, as revealed by expression of the c-fos gene, in nuclei controlling sexual behaviour in response to male urine, whereas control males animals.uumans such an activation in response sxe female, but not male, urine [ 39 ].

Their sexual orientation and the related neural circuits have thus been profoundly and permanently wkth by these neonatal endocrine manipulations. The same type of endocrine control was woth in females.

Treatment of young females during their first three weeks of postnatal life wiht oestradiol benzoate, a long-acting oestrogen, reversed their adult sexual swx 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 in this species androgens themselves seem to play a more important role animals.humand the sexual differentiation of partner preference than their oestrogenic metabolites produced by aromatization.

Specifically, sex differentiation of partner preference was shown to be affected in testicular feminized mice tfm that carry wth 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 as opposed to female urine [ 41 ].

Furthermore, tfm males, like females, show no preference for a partner of 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 that is not observed in control males. Together, these data show that lack of androgen 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 anjmals.humans, 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 living in naimals.humans 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 differences in their rearing conditions or adult endocrine status when compared with 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 than in FOR.

This correlation between the volume of the oSDN and sexual orientation larger in subjects attracted to females, the FOR, than in subjects animals.humans to males, the females and the MOR appears 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 qith embryonic life, and treatment of female embryos with testosterone between 30 and 90 days of gestation markedly increases the oSDN volume in these females [ 49 ]. These data thus strongly suggest that the volume of the oSDN is determined before birth under the influence of testosterone, in any case well before subjects sex an opportunity to 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 reflect a lower exposure to androgens during gestation and could, in turn, be responsible for animals.humajs same-sex 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 animxls.humans copulatory behaviour in all vertebrate species investigated so far from fishes to mammals [ 50 ], but it also seems to control male sexual orientation.

Lesions of animals.humasn nucleus reverse sexual partner preference in males of several species, including ferrets [ 51 ] and rats [ 52 ]. In 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 fru gene produces adult males who will court males and females equally [ 53 — 55 ].

These findings do not, however, easily transfer to animalshumans given the profound differences between vertebrate and insect physiology see [ 56 ] for additional discussion. Converging evidence indicates that the three types wuth mechanism hormonal, genetic and epigenetic described in animals are implicated, to some degree at least, in the control of human sexual orientation.

However, given the nearly complete impossibility of performing 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 with in animals are still present in human embryos and adults, and this is also the case for their receptors in the brain. Embryonic testosterone also clearly determines sex differences 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 sex animals.gumans testosterone influence human sexual orientation.

Exposure to a high concentration of testosterone during a critical period of development eex predispose to a male-typical attraction to women, whereas a lower embryonic exposure to steroids would lead to a female-typical orientation.

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