Carving the Biodevelopment of Same-Sex Sexual Orientation at Its Joints

Abstract

Sexual orientation is a core aspect of human experience and understanding its development is fundamental to psychology as a scientific discipline. Biological perspectives have played an important role in helping to uncover the processes that contribute to sexual orientation development. Research in this field has relied on a variety of populations, including community, clinical, and cross-cultural samples, and has commonly focused on female gynephilia (i.e., female sexual attraction to adult females) and male androphilia (i.e., male sexual attraction to adult males). Genetic, hormonal, and immunological processes all appear to influence sexual orientation. Consistent with biological perspectives, there are sexual orientation differences in brain development and evidence indicates that similar biological influences apply across cultures. An outstanding question in the field is whether the hypothesized biological influences are all part of the same process or represent different developmental pathways leading to same-sex sexual orientation. Some studies indicate that same-sex sexually oriented people can be divided into subgroups who likely experienced different biological influences. Consideration of gender expression in addition to sexual orientation might help delineate such subgroups. Thus, future research on the possible existence of such subgroups could prove to be valuable for uncovering the biological development of sexual orientation. Recommendations for such future research are discussed.

Appendices

Spotlight Feature: Born to Bottom?

• David A. Moskowitz 

1. Institute for Sexual and Gender Minority Health and Wellbeing, Northwestern University, Chicago, IL, USA

   David A. Moskowitz

Questions surrounding the origins and mutability of the sexual self-identities of gay, bisexual, and other men who have sex with men have always played understudy to those surrounding the origins and mutability of sexual orientation and gender identity. Few scholars will argue that sexual orientation and gender identity are “nurtured,” or are strictly developed from childhood and adolescent socialization. It is almost unanimously recognized that both sexual orientation and gender identity are influenced, at least in part, by a confluence of prenatal biological factors (O’Hanlan et al., 2018). However, where sexual self-identities come from is still a mystery, and the debate continues into whether men who identity as tops, bottoms, or versatiles are born that way, or made that way. Since early work by Joseph Carrier 50 years ago (Carrier, 1971, 1977), researchers have recognized the existence of anal sex roles. Initially, the theoretical framework (up until the early 2000s) was that, given men have the same genitals, an implicit or explicit decision is made as to who would be receptive versus insertive during anal sex; and that decision could be predicted largely by “active, activo, dominant” or “passive, passivo, submissive” personas adopted by partners (Hickson et al., 1993; Ho & Tsang, 2000; Wegesin & Meyer-Bahlburg, 2000; Weinrich et al., 1992). These were to a reliable degree, transmitted to, and perceived by, sex partners prior to the sexual encounter and thus, facilitated the anal sex.

Over the past 15 years, scientific inquiries have focused on the contributing factors to men’s orientations towards bottoming or topping, and the degree to which it permeates into other sexual realms (Hart et al., 2003). Many studies, including my own, began exploring the social influencers of sexual self-identity adoption, the most consistent being gender typicality (i.e., outward gender presentation as masculine or feminine) and self-reported penis size (Brennan, 2018; Grov et al., 2010, 2015; Moskowitz & Hart, 2011). My more recent study, exploring a larger model predicting preferences for topping or bottoming, found far more nuanced and indirect relationships at play (Moskowitz & Roloff, 2017). For example, smaller penis size was actually a predictor of sexual anxiety when topping, which led to more bottoming; gender typicality was actually a partner-oriented trait that acted to signal sexual self-identity to other men. These findings pointed to sexual self-identity being learned. Moreover, the same study found men self-reported adopting sexual self-identities, on average, about 2.6 years after beginning to have anal sex, or around 24.6 years old, further suggesting that having sex socialized men into their identities (see Fig. 17.2).

Fig. 17.2

From Moskowitz and Roloff (2017), men’s average growth of sexual milestone recognition and behavioral enactment by their ages. The data represent the mean ages at specific milestones from 282 men, ages 18–76

At the same time as the above findings were published, researchers were reporting compelling results to suggest that biological markers were correlated with different sexual self-identities (Swift-Gallant et al., 2017, 2018). This forced the question: If biological markers were differentially exhibited, could that indicate an underlying biological mechanism that made men more or less likely to adopt a top, bottom, or versatile identity? In response, we conducted a study with 15- to 18-year-olds, both sexually experienced and inexperienced, to see whether they were already developing a sexual self-identity (see Moskowitz et al., 2022). After all, if there was a biological predisposition at play, pubescent teenagers, regardless of sexual experience, should report some gravitation to a sexual self-identity. Of the over 300 teenagers surveyed, only nine did not yet identify with a sexual self-identity. Moreover, of the 56 teenagers who reported never having anal sex in their lives, 48 (85.7%) reported already having a sexual self-identity. Besides testing for degree of early adoption of a sexual self-identity, this study also retested the previous findings about penis size and gender typicality as socialized signaling tools reported by Moskowitz and Roloff (2017). Specifically, in that sample of sexually active adult men, penis size, and gender typicality impacted anal sex role because of sociosexual reactions (i.e., by causing role anxiety and by causing partner selectivity to increase anal sex compatibility). Yet, when comparing sexually active (i.e., having had anal sex) and sexually inactive (i.e., never having anal sex) teenagers, the relationships between having a larger penis and topping, and being more masculine and topping, were significant for both groups. These new findings suggested that penis size and gender typicality may not be activated by the experience of having sex to create a top or a bottom and may instead be influenced by biological influences on sexual self-identity formation.

Origins aside, there remains the question of sexual self-label mutability, which is far less controversial. Research has shown that one’s ideal sexual self-label and their actual enacted sexual behaviors, while generally reliable, can deviate (Dangerfield et al., 2018; Johns et al., 2012; Moskowitz & Hart, 2011; Pachankis et al., 2013). These deviations are usually a function of their partners and not necessarily the men themselves. My own study into sexual self-identities among men in relationships highlights this fact (Moskowitz & Garcia, 2019). In our sample, an overwhelming majority (63%) of the men in romantic partnerships reported acting as a sexual self-identity different than their ideal one. In a different sample of men, many of whom were single, the number reporting different (but current) ideal and enacted sexual self-identities was 35% (Moskowitz & Hart, 2011). Finally, unpublished data from the sample of men described by Moskowitz and Roloff (2017) showed that, when asked whether their sexual self-label had changed over time, 69% reported some degree of movement; however, the majority (55%) reported only one degree of movement (e.g., from being an exclusive top to a versatile top, from being an exclusive versatile to a versatile bottom).

There is the temptation to want to categorize sexual self-identity mutability as evidence of labels being socialized. For if individuals migrate, even one degree, perhaps that means they have decided to move identities for themselves, in reaction to their environment. Yet, humans routinely behave in ways that may be counterintuitive, self-sacrificing, and unexpected, especially regarding sex. Even as I have found some evidence to suggest being a top or bottom may be learned over time, I have found equally compelling data to suggest it is nested in a biological basis for sexual orientation and gender development. In all likelihood, if sexual self-identity is nested in biology, it will only be through more complete scientific understanding of the relationships between sexual orientation, gender identity and gender role progression, and all of their biological correlates that we will be able to identify who is born to top and who is born to bottom.

Spotlight references

• Brennan, J. (2018). Size matters: Penis size and sexual position in gay porn profiles. Journal of Homosexuality, 65(7), 912–933.

• Carrier, J. M. (1971). Participants in urban Mexican male homosexual encounters. Archives of Sexual Behavior, 1(4), 279–291.

• Carrier, J. M. (1977). “Sex-role preference” as an explanatory variable in homosexual behavior. Archives of Sexual Behavior, 6(1), 53–65.

• Dangerfield, D. T., Smith, L. R., Anderson, J. N., Bruce, O. J., Farley, J., & Bluthenthal, R. (2018). Sexual positioning practices and sexual risk among black gay and bisexual men: A life course perspective. AIDS and Behavior, 22(6), 1919–1931.

• Grov, C., Parsons, J. T., & Bimbi, D. S. (2010). The association between penis size and sexual health among men who have sex with men. Archives of Sexual Behavior, 39(3), 788–797.

• Grov, C., Saleh, L. D., Lassiter, J. M., & Parsons, J. T. (2015). Challenging race-based stereotypes about gay and bisexual men’s sexual behavior and perceived penis size and size satisfaction. Sexuality Research and Social Policy, 12(3), 224–235.

• Hart, T. A., Wolitski, R. J., Purcell, D. W., Gómez, C., Halkitis, P., & Seropositive Urban Men’s Study Team (2003). Sexual behavior among HIV‐positive men who have sex with men: What’s in a label? The Journal of Sex Research, 40(2), 179–188.

• Hickson, F., Davies, P. M., & McManus, T. J. (1993). Sex role separation in sexual diaries of homosexual men. Aids, 7(6), 877–882.

• Ho, P. S. Y., & Tsang, A. K. T. (2000). Negotiating anal intercourse in inter-racial gay relationships in Hong Kong. Sexualities, 3(3), 299–323.

• Johns, M. M., Pingel, E., Eisenberg, A., Santana, M. L., & Bauermeister, J. (2012). Butch tops and femme bottoms? Sexual positioning, sexual decision making, and gender roles among young gay men. American Journal of Men’s Health, 6(6), 505–518.

• Moskowitz, D. A., Avila, A. A., Kraus, A. Birnholtz, J., & Macapagal, K. (2022). Top, bottom, and versatile orientations among male androphilic teenagers. Journal of Sex Research, 59(5), 643–651.

• Moskowitz, D. A., & Garcia, C. P. (2019). Top, bottom, and versatile anal sex roles in same-sex male relationships: Implications for relationship and sexual satisfaction. Archives of Sexual Behavior, 48(4), 1217–1225.

• Moskowitz, D. A., & Hart, T. (2011). The influence of physical body traits and masculinity on anal sex roles in gay and bisexual men. Archives of Sexual Behavior, 40(4), 835–841.

• Moskowitz, D. A., & Roloff, M. E. (2017). Recognition and construction of top, bottom, and versatile orientations in gay/bisexual men. Archives of Sexual Behavior, 46(1), 273–285.

• O’Hanlan, K. A., Gordon, J. C., & Sullivan, M. W. (2018). Biological origins of sexual orientation and gender identity: Impact on health. Gynecologic Oncology, 149(1), 33–42.

• Pachankis, J. E., Buttenwieser, I. G., Bernstein, L. B., & Bayles, D. O. (2013). A longitudinal, mixed methods study of sexual position identity, behavior, and fantasies among young sexual minority men. Archives of Sexual Behavior, 42(7), 1241–1253.

• Swift-Gallant, A., Coome, L. A., Monks, D. A., & VanderLaan, D. P. (2017). Handedness is a biomarker of variation in anal sex role behavior and recalled childhood gender nonconformity among gay men. PLoS One, 12(2), e0170241. doi: 10.1371/journal.pone.0170241

• Swift-Gallant, A., Coome, L. A., Monks, D. A., & VanderLaan, D. P. (2018). Gender nonconformity and birth order in relation to anal sex role among gay men. Archives of Sexual Behavior, 47(4), 1041–1052.

• Wegesin, D. J., & Meyer-Bahlburg, H. F. (2000). Top/bottom self-label, anal sex practices, HIV risk and gender role identity in gay men in New York City. Journal of Psychology & Human Sexuality, 12(3), 43–62.

• Weinrich, J. D., Grant, I., Jacobson, D. L., Robinson, S. R., McCutchan, J. A., & Group, H. (1992). Effects of recalled childhood gender nonconformity on adult genitoerotic role and AIDS exposure. Archives of Sexual Behavior, 21(6), 559–585.

Spotlight Feature: Evidence for a Curvilinear Androgen Dose Response in Sexual Differentiation of Brain and Behavior

• Ashlyn Swift-Gallant &
• D. Ashley Monks 

1. Department of Psychology, Memorial University of Newfoundland, St. John’s, NL, Canada

   Ashlyn Swift-Gallant

2. Department of Psychology, University of Toronto Mississauga, Mississauga, ON, Canada

   D. Ashley Monks

3. Cell and Systems Biology, University of Toronto, Toronto, ON, Canada

   D. Ashley Monks

For over 60 years, we have known that gonadal testosterone is a primary endocrine factor shaping sex differences in brain and behavior (Phoenix et al., 1959; reviewed in Swift-Gallant & Monks, 2017). Testosterone does so both as an androgen that acts directly on androgen receptors (AR) or indirectly via estrogen receptors (ER α or β) after conversion to estradiol in the brain. Providing androgens to females during early critical periods in development increases male-typical behaviors, including sexual preference for female cues and copulatory behavior (i.e., mounting and thrusting) towards receptive females. Conversely, taking androgens away from males during early critical periods, or in adulthood prior to sexual experience, or knocking-out AR or ERs, are all manipulations that lead to dramatic decreases in preferences for female cues and male-typical copulatory behaviors.

These findings support the long-standing traditional theory of sexual differentiation, which holds that androgens act to masculinize and defeminize the brain and behavior; however, this theory is vague on the significance of androgen dose, beyond the assumption that male-typical and female-typical androgen doses are essentially discontinuous and androgen dosing in the male range is required for masculinizing and defeminizing actions. This question is important for understanding variation within both male and female populations. Here, we present converging lines of evidence suggesting that the relationship between androgens and masculine phenotype is not always linear. Instead, the evidence supports a nonlinear relationship such that both low and high androgen levels lead to a reduction in male-typical phenotype, and there is an optimal level of androgen that is required for the display of full male-typed behaviors (Swift-Gallant & Monks, 2017; see Fig. 17.3).

Fig. 17.3

Androgens act in a time- and dose-dependent manner to affect the development of male-typical brain and behavior. In rodent development, androgens spike around embryonic day 18 (E18) in males, followed by a smaller peak around the day of birth/postnatal day 1 (PND1). Androgens then subside and remain low until puberty, at which time androgens increase to adulthood levels and remain relatively high until the aging process leads to gradual declines in androgen production. The evidence presented herein indicates that androgens can have dissociable effects on components of sexual behavior, such that in some cases the dose response is linear whereas for other behaviors the relationship is curvilinear. Thus, androgen dose effects can be both linear and nonlinear; further work is needed to understand whether there are timing by androgen dose effects on male-typical phenotype

A plethora of studies have evaluated the consequences of reducing androgen signaling in males, overwhelmingly finding that reducing androgens reduces male-typical behaviors. Far fewer studies have asked what happens when you increase androgens above the typical range (Cruz & Pereira, 2012; Diamond et al., 1973; Henley et al., 2010; Zadina et al., 1979). These studies have found that high levels of androgen exposure during early development leads to a paradoxical decrease in male-typical copulatory behaviors and/or preferences. We recently took the approach of increasing androgen signaling by overexpressing AR in male mice to levels 3–4× higher than in their wildtype counterparts. With this approach, we found that male-typical copulatory behaviors were increased in males with AR overexpression, suggestive of a linear relationship, while sexual preferences were altered such that these males show increased androphilic preferences (Swift-Gallant et al., 2016a, 2016b), suggestive of an inverted-U shape relationship. Specifically, male mice with ubiquitous overexpression of AR exhibited an increase in number of thrusts per mount in response to a receptive female but displayed an increased preference for anogenital investigation of a male partner and an increased preference for same-sex odor stimuli compared to wildtype littermates (Swift-Gallant et al., 2016a, 2016b). This behavioral change was accompanied by a decrease in neural activity in response to female odors along the accessory olfactory pathway (Swift-Gallant et al., 2016b). These results together with the findings from studies of systemic administration of supraphysiological androgen doses suggest that increases in androgenic signaling can lead to a decrease in male-typical behaviors. Notably, some male-typical behaviors remained unchanged or exhibited an increase in the male-typical direction (i.e., copulatory behaviors), while other behaviors exhibited a decrease in male-typical behavior (preference for opposite-sex stimuli), providing further evidence that androgens can have dissociable effects on components of sexual behavior and furthermore suggesting that the relationship between androgen dose and masculine phenotype can be both linear and curvilinear.

Future studies examining the timing of supraphysiological doses of androgen or enhanced androgen signaling may delineate distinct critical periods for copulatory behaviors vs. sexual preferences. Such research might help explain the discrepancy between studies suggesting that high androgen signaling decreases male-typical copulatory behaviors and preferences while others only report declines in male-typical preferences but not copulatory behaviors. Indeed, studies that enhanced androgen levels after birth report decreases in male-typical copulatory behavior (Diamond et al., 1973; Henley et al., 2010; Zadina et al., 1979), whereas supraphysiological doses of androgens administered during embryonic development (Cruz & Pereira, 2012) or lifelong increases in androgen sensitivity (Swift-Gallant et al., 2016b) altered sexual preferences in male rodents.

Based on work in non-human animals, the neuroendocrine hypothesis was the first proposed explanation for the development of same-sex sexual orientation among humans (reviewed in Swift-Gallant et al., 2020). Briefly, it was hypothesized that high prenatal androgens in females would increase same-sex sexual orientations, whereas low prenatal androgens in males would result in increased same-sex sexual orientations. While measuring prenatal androgens (i.e., during brain sexual differentiation) in humans is not practical (i.e., amniotic fluid may be available in some cases, but would only tell us about androgens at a single time point, and subjecting pregnant women to multiple amniotic tests is unethical), there have been attempts to capture the prenatal androgen environment via retrospective markers such as the second-to-fourth digit ratio (2D:4D, i.e., length of the index relative to ring finger). The evidence in women has been fairly consistent—lesbians have a more male-typical finger digit ratio suggesting they were exposed to higher androgens in the womb compared to heterosexual women. Conversely, numerous reviews and meta-analyses have concluded that there is no link between prenatal androgens (as measured via 2D:4D) and sexual orientation in men. However, given the emerging evidence in non-human animals, it is possible that there is a nonlinear relationship, such that both low and high androgens contribute to sexual orientation in men (Swift-Gallant, 2019), which could be masked by unaccounted for diversity within the populations of gay men studied. Indeed, we have recently found evidence for multiple distinct biodevelopmental pathways of same-sex sexual orientation among men, supporting this idea that there may be multiple factors that promote same-sex orientations in men (e.g., both low and high prenatal androgen exposure, immunological mechanisms, genetic; Swift-Gallant et al. 2019).

Androgens shape the brain and behavior in a time- and dose-dependent manner. We are also beginning to see that there can be dissociations in the presentation of sex-typed behaviors such that one can be more male-typical in some behaviors and more female-typical in others. Still, many questions remain unanswered about the relationship of androgen dose and timing on the development of male-typed behaviors. At this time, the emerging evidence suggests that more androgens do not always produce a more masculine phenotype.

Funding

This work was supported by NSERC Discovery Grants to ASG (RGPIN-2019-04999) and to DAM (RGPIN-2016-06302).

Spotlight references

• Cruz, C. D., & Pereira, O. C. (2012). Prenatal testosterone supplementation alters puberty onset, aggressive behavior, and partner preference in adult male rats. The Journal of Physiological Sciences, 62(2), 123–131.

• Diamond, M., Llacuna, A., & Wong, C. L. (1973). Sex behavior after neonatal progesterone, testosterone, estrogen, or antiandrogens. Hormones and Behavior, 4(1–2), 73–88.

• Henley, C. L., Nunez, A. A., & Clemens, L. G. (2010). Exogenous androgen during development alters adult partner preference and mating behavior in gonadally intact male rats. Hormones and Behavior, 57(4–5), 488–495.

• Phoenix, C. H., Goy, R. W., Gerall, A. A., & Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology, 65(3), 369–382.

• Swift-Gallant, A. (2019). Individual differences in the biological basis of androphilia in mice and men. Hormones and Behavior, 111, 23–30.

• Swift-Gallant, A., Coome, L. A., Aitken, M., Monks, D. A., & VanderLaan, D. P. (2019). Evidence for distinct biodevelopmental influences on male sexual orientation. Proceedings of the National Academy of Sciences, 116(26), 12787–12792.

• Swift-Gallant, A., Coome, L. A., Ramzan, F., & Monks, D. A. (2016a). Nonneural androgen receptors affect sexual differentiation of brain and behavior. Endocrinology, 157(2), 788–798.

• Swift-Gallant, A., Coome, L., Srinivasan, S., & Monks, D. A. (2016b). Non-neural androgen receptor promotes androphilic odor preference in mice. Hormones and Behavior, 83, 14–22.

• Swift-Gallant, A., Johnson, B. A., Di Rita, V., & Breedlove, S. M. (2020). Through a glass, darkly: Human digit ratios reflect prenatal androgens, imperfectly. Hormones and Behavior, 120, 104686. doi: 10.1016/j.yhbeh.2020.104686

• Swift-Gallant, A., & Monks, D. A. (2017). Androgenic mechanisms of sexual differentiation of the nervous system and behavior. Frontiers in Neuroendocrinology, 46, 32–45.

• Zadina, J. E., Dunlap, J. L., & Gerall, A. A. (1979). Modifications induced by neonatal steroids in reproductive organs and behavior of male rats. Journal of Comparative and Physiological Psychology, 93(2), 314–322.