Sexual partner preference in animals and humans

Abstract

Sex differences in brain and behavior of animals including humans result from an interaction between biological and environmental influences. This is also true for the differences between men and women concerning sexual orientation. Sexual differentiation is mediated by three groups of biological mechanisms: early actions of sex steroids, more direct actions of sex-specific genes not mediated by gonadal sex steroids and epigenetic mechanisms. Differential interactions with parents and conspecifics have additionally long-term influences on behavior. This presentation reviews available evidence indicating that these different mechanisms play a significant role in the control of sexual partner preference in animals and humans, in other words the homosexual versus heterosexual orientation. Clinical and epidemiological studies of phenotypically selected populations indicate that early actions of hormones and genetic factors clearly contribute to the determination of sexual orientation. The maternal embryonic environment also modifies the incidence of male homosexuality via immunological mechanisms. The relative contribution of each of these mechanisms remains however to be determined.

Keywords: Biological mechanisms; Fraternal birth order effect; Genome-wide associations; Homosexuality; Older brother effect; Organizing effects of steroids; Sexual differentiation; Testosterone; Twin concordance.

Figure 1.

Schematic presentation of the mechanisms that mediate the development of sex differences in mammals including humans. The SRY gene on the Y chromosome induces the formation of testes that will secrete testosterone (T) that will be acting by itself or via aromatization (Arom) into estradiol (E2) to masculinize the genital structures and the brain. Activational effects of steroids will then complete the differentiation of the adult male and female phenotype. Genes can additionally induce sex differences in a more direct manner that is not mediated via the action of sex steroids. Environmental and social influences will additionally modulate this sexual phenotype to determine the gender of an individual including his/her sexual orientation and gender identity.

Figure 2.

Sexual orientation of women affected by congenital adrenal hyperplasia (CAH) as a function of the severity of the disease. The figure shows the individual Kinsey scores on a scale from 0 (completely heterosexual) to 6 (completely homosexual) evaluated for the entire lifetime as well as the means and SD of these scores in each group. The severity of CAH (increased prenatal exposure to androgens) increases from the non classical to the simple virilizing to the salt wasting form. When multiple subjects have the same Kinsey score in one group, the number of subjects is indicated next to the cluster of points. Redrawn from data in (Meyer-Bahlburg et al., 2008)

Figure 3.

Amplitude of click-evoked otoacoustic emissions (CEOAE) observed in male and female humans (A), rhesus monkeys (B) and sheep (C). Data refer to the left ear except in monkeys where the mean responses in both ears are shown. In humans CEOAE have a larger amplitude in heterosexual women than in heterosexual men but they are more masculine in lesbian women. The same sex difference is observed in both monkeys and sheep (females>males) and prenatal treatment with testosterone decrease CEOAE amplitude in females to male levels or below. This suggests that the sex difference observed in control (Ctrl) subjects is due to the early exposure of males to testosterone and that lesbians were similarly exposed to an excess of testosterone during fetal life. Redrawn from data in (McFadden and Pasanen, 1998; McFadden et al., 2006; McFadden et al., 2009).

Figure 4.

Percentage of concordance in sexual orientation of monozygotic or dizygotic homosexual twins with results separated according to whether subjects were recruited by the targeted or registry method (see text). Studies were dedicated to males or females or to mixed-sex populations. The medians of all results are displayed in the rightmost columns. Redrawn from data compiled in (Bailey et al., 2016).

Figure 5.

Mechanisms potentially modulating in a sex-specific manner testosterone action during fetal development in mammals. Large panels of (autosomal) genes are expressed in a sexually differentiated manner, presumably via epigenetic control mechanisms, even before the gonads develop. Testosterone action is modulated by a variety of mechanisms at multiple levels in the circulation and at the level of target cells. The effects of marginally different concentrations of testosterone in males and females can therefore be canalized to produce sexually differentiated phenotypes. Drawn form information in (Rice et al., 2012)

Figure 6.

Mean rank of concentration (from 1= lowest to 142= highest) of antibodies against neuroligin 4Y-linked (NLGN4Y) in different groups of women who either had no son, or only had heterosexual son(s), or had at least one gay son who had no older brother or who had one or several older brothers. The concentration of these antibodies in the mother’s blood significantly increases across these 4 categories. Numbers indicate the sequence of birth from a same mother and parentheses indicate the presence one or more sons of a given category. Heterosexual (straight) sons are illustrated in blue and gay sons with the rainbow flag associated with homosexuality. Redrawn from data in (Bogaert et al., 2018).