Evidence for Perinatal Steroid Influence on Human Sexual Orientation and Gendered Behavior

Abstract

In laboratory animals, exposure to gonadal steroid hormones before and immediately after birth can exert permanent effects on many behaviors, particularly reproductive behaviors. The extent to which such effects occur in humans remains an open question, but several lines of evidence indicate that perinatal levels of both androgens and estrogens may affect adult human psychology and behavior, including sexual orientation and gender nonconformity. Some putative indicators of prenatal androgen exposure, including the ratio of the length of the index finger to that of the ring finger (2D:4D), have repeatedly indicated that lesbians, on average, were exposed to more prenatal androgens than straight women, suggesting that sufficient fetal androgen exposure predisposes a fetus to gynephilia (attraction to women) at maturity. The digit ratios of gay men do not differ from those of straight men, suggesting that prenatal androgen levels are not responsible for their androphilia (attraction to men). However, evidence that gay men who prefer an insertive anal sex role (ASR) have more masculine digit ratios than those preferring a receptive ASR suggests that early androgens influence some sexual preferences in men. Furthermore, digit ratios among gay men have been found to correlate with recalled childhood gender nonconformity (CGN). People with isolated gonadotropin-releasing hormone (GnRH) deficiency (IGD) offer further insight into the effects of perinatal gonadal steroid exposure. In people with IGD, gonadal hormone production is low or absent after the first trimester of gestation. However, because placental gonadotropins drive gonadal hormone secretion during the first trimester when genitalia sexually differentiate, individuals with IGD are unambiguously male or female at birth, consistent with their chromosomal and gonadal sex. Men with IGD report greater CGN, again suggesting that perinatal androgen exposure contributes to male-typical behavioral patterns in humans. Interestingly, women with IGD report less androphilia and more bisexuality than control women, suggesting that perinatal ovarian steroids in females typically augment androphilia in adulthood. Taken together, these findings indicate that the perinatal hormonal milieu influences human sexual orientation and gender conformity.

Figure 1.

Sexual orientation and digit ratios. In this sample, a significant sex difference in digit ratios was seen only for the right hand. Women who reported a lesbian orientation had more masculine (smaller) right-hand digit ratios than self-reported straight women. No differences in digit ratios between gay and straight men were seen. (Figure reprinted from Williams et al. 2000 with permission from the authors.)

Figure 2.

Digit ratios in butch and femme lesbians. Lesbians who self-report as being “butch” have more masculine (smaller) digit ratios than self-reported “femme” lesbians, but only on the right hand. (Figure reprinted from Brown et al. 2002a with permission from Springer © 2002.)

Figure 3.

Differences in right-hand digit ratios in gay men based on their anal sex role (ASR) preference. ASR bottoms have more female-typical (higher) digit ratios than ASR tops (P < 0.05; d = 0.62). Versatiles displayed intermediate digit ratios, which were not significantly different from either of the other two groups. (Figure reprinted from Swift-Gallant et al. 2021 under a Creative Commons Attribution 4.0 International License.)

Figure 4.

Right-hand digit ratios correlate with gender nonconformity scores. A more female-typical digit ratio is associated with higher gender nonconformity, in both childhood and adulthood, based on self-reports from gay men. (Figure reprinted from Swift-Gallant et al. 2021 under a Creative Commons Attribution 4.0 International License.)

Figure 5.

Schematic representation of perinatal hormone secretion. Estimated circulating levels of human chorionic gonadotropin (hCG; gray shading) and gonadal sex steroid hormone production in males (top) and females (bottom). In males, androgen production typically begins about the eighth week of gestation with the differentiation of the bipotential gonad (Siiteri and Wilson 1974; Negri-Cesi et al. 2004), persisting until the 24th week (Forest et al. 1973). In females, estrogen levels typically increase across gestation, peaking perinatally and fluctuating through mini-puberty, then ovarian activity ceases until puberty. In people with isolated gonadotropin-releasing hormone (GnRH) deficiency (IGD) (dotted lines), gonadal hormone production declines as hCG levels wane. (Figure from Shirazi et al. 2021a, adapted from Lanciotti et al. 2018, reprinted under the terms of the Creative Commons Attribution License (CC BY).)

Figure 6.

Childhood gender nonconformity (CGN) and isolated gonadotropin-releasing hormone (GnRH) deficiency (IGD). While men with IGD report similar levels of heterosexuality as control men, they do report greater gender nonconformity as children than control men. The differences seen in two samples of men with IGD, one a clinic-based group with diagnoses confirmed by physicians, and the other a web-based group of men self-identifying as having IGD, displayed the same pattern of results. (Figure reprinted from Shirazi et al. 2021b with permission from the authors.)