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Individual Differences in the Biological Basis of Androphilia in Mice And Hormones and Behavior 111 (2019) 23–30 Contents lists available at ScienceDirect Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh Review article Individual differences in the biological basis of androphilia in mice and men T ⁎ Ashlyn Swift-Gallant Neuroscience Program, Michigan State University, 293 Farm Lane, East Lansing, MI 48824, USA Department of Psychology, Memorial University of Newfoundland, St. John's, NL A1B 3X9, Canada ARTICLE INFO ABSTRACT Keywords: For nearly 60 years since the seminal paper from W.C Young and colleagues (Phoenix et al., 1959), the principles Androphilia of sexual differentiation of the brain and behavior have maintained that female-typical sexual behaviors (e.g., Transgenic mice lordosis) and sexual preferences (e.g., attraction to males) are the result of low androgen levels during devel- Androgen opment, whereas higher androgen levels promote male-typical sexual behaviors (e.g., mounting and thrusting) Sexual behavior and preferences (e.g., attraction to females). However, recent reports suggest that the relationship between Sexual preferences androgens and male-typical behaviors is not always linear – when androgen signaling is increased in male Sexual orientation rodents, via exogenous androgen exposure or androgen receptor overexpression, males continue to exhibit male- typical sexual behaviors, but their sexual preferences are altered such that their interest in same-sex partners is increased. Analogous to this rodent literature, recent findings indicate that high level androgen exposure may contribute to the sexual orientation of a subset of gay men who prefer insertive anal sex and report more male- typical gender traits, whereas gay men who prefer receptive anal sex, and who on average report more gender nonconformity, present with biomarkers suggestive of low androgen exposure. Together, the evidence indicates that for both mice and men there is an inverted-U curvilinear relationship between androgens and sexual pre- ferences, such that low and high androgen exposure increases androphilic sexual attraction, whereas relative mid-range androgen exposure leads to gynephilic attraction. Future directions for studying how individual differences in biological development mediate sexual behavior and sexual preferences in both mice and humans are discussed. 1. Introduction down to more androgens results in more masculine behavior; however, recent evidence points to a more complex nonlinear relationship be- The neuroendocrine basis of sexual behavior and sexual preferences tween androgens and male-typical sexual preferences, and here I will is well studied in rodents. The research indicates that gonadal hor- review the literature suggesting that high androgen signaling promotes mones act during critical periods in development to organize neural androphilia (i.e., sexual preference for male partners) in male rodents. I structures in a sex-typical fashion (e.g., Morris et al., 2004). In adult- will then discuss how these findings may apply to humans, and review hood, activational or transient effects of hormones further act on these the recent literature suggesting multiple biological pathways (i.e., in- sexually differentiated brain structures to promote sex-typical beha- cluding high androgen signaling) underlie androphilia in men. viors, including sexual behavior towards opposite-sex partners. The landmark paper by Phoenix et al. (1959) demonstrated that male-ty- 2. Androphilia and androgens in mice pical sexual behaviors like mounting are increased in female guinea pigs androgenized during embryonic development, whereas female 2.1. From hormone manipulation to transgenic mouse models: androgens, sexual behaviors, like lordosis, are decreased in these females even sexual behavior and sexual preferences in rodents when primed with estrus-inducing hormone regimens in adulthood. Since this formative study, a plethora of evidence has emerged sup- Hormone manipulation studies were the first line of evidence to porting the role of androgen action during early critical periods in de- suggest that androgen action during early development organize the velopment as well as in puberty (reviewed in Schulz and Sisk, 2016), for brain and behavior in a sex-typical fashion. Females exposed to an- masculinizing and defeminizing neural circuits and adult sex-typed drogens during early critical periods display male-typical sexual beha- behaviors. By and large, the story of sexual differentiation seems to boil viors in adulthood; Phoenix et al. (1959), first reported these findings in ⁎ Department of Psychology, Memorial University of Newfoundland, 232 Elizabeth Ave, St. John's, NL A1B 3X9, Canada. E-mail address: [email protected]. https://doi.org/10.1016/j.yhbeh.2018.12.006 Received 31 July 2018; Received in revised form 21 November 2018; Accepted 11 December 2018 Available online 27 December 2018 0018-506X/ © 2018 Elsevier Inc. All rights reserved. A. Swift-Gallant Hormones and Behavior 111 (2019) 23–30 guinea pigs, and many others have replicated these findings in mice and the enzyme aromatase to assess estrogenic effects on behavior; indeed, rats (for review, see Cooke et al., 1998). In male rodents, removal of such studies have indicated that androgen action via ERs contributes to gonadal androgens during early development (e.g., Gerall et al., 1967), the display of male-typical sexual behavior and sexual preferences (e.g., or prenatal and postnatal treatment with anti-androgens (e.g., fluta- Brand et al., 1991; Clemens and Gladue, 1978; for review in rats, see mide: Clemens et al., 1978; Casto et al., 2003; cyproterone acetate: Bakker et al., 1996; in mice, see Bodo, 2008; Brock and Bakker, 2011; Ward and Renz, 1972), results in dramatic decreases in male-typical for review comparing mice and rats, see Bonthuis et al., 2010). How- sexual behaviors (i.e., decreased mounting, intromissions and ejacula- ever, a second limitation of androgen or estrogen manipulation studies tion), and increased female-typical behaviors such as lordosis (e.g., is that simply manipulating circulating hormones may not alter hor- Gladue and Clemens, 1978; Ward and Renz, 1972) when treated with mone levels in the brain; for example, removal of both gonadal and hormone regimens that typically induce receptivity in females (i.e., adrenal hormones at birth does not seem to alter the neural endocrine estradiol and progesterone). Similarly, sexual preferences, as measured environment, even 3 days following gonad and adrenal removal by simultaneous exposure to male and female partner or sexual odor (Konkle and McCarthy, 2011); these findings could be accounted for by stimuli, are mediated by androgens: male-typical levels of androgen de novo steroid synthesis in the brain (Robel and Baulieu, 1995; re- exposure during early development increases preference for female viewed in Diotel et al., 2018 and Forger et al., 2016). Neural hormone sexual stimuli, whereas the absence of or low-level androgen exposure implantations were first to address the role of hormones directly in the leads to a preference for male sexual stimuli (e.g., Domınguez-Salazar brain for behavior (e.g., Davidson, 1966; for review see McEwen et al., et al., 2002; Stern, 1970). Together, such studies suggest that low level 1979; Frye, 2001), and modern transgenic technology (and sponta- androgen exposure during development results in female-typical sexual neous mutations of the androgen receptor gene) has allowed for the behaviors and preferences, while higher male-typical androgen levels refined testing of the effects of androgenic signaling compared to es- promote male-typical sexual behaviors and preferences in adult mice trogenic signaling on sexual behaviors by targeting hormone receptors. and rats (see Table 1). With transgenic mouse models, we can ensure hormone sensitivity is There are a couple caveats to consider when evaluating these early altered specifically in neural tissue, even if hormone synthesis con- androgen manipulation studies; for one, androgens can act via both tinues in the brain following gonadectomy. androgenic and estrogenic signaling pathways. Testosterone, the pri- Prior to modern transgenic technology, Lyon and Hawkes (1970) mary androgen produced by the gonads, can be metabolized into either described the condition of testicular feminization mutation (Tfm) in the more potent androgen dihydrotestosterone (DHT) or, with the help mice, in which XY chromosomal male mice showed a female phenotype of the enzyme aromatase, converted to estrogens (Naftolin, 1994; re- at birth. It was later discovered that these rodents have a single nu- viewed in Roselli et al., 2009). Thus, it is difficult to parse out the ef- cleotide deletion in the androgen receptor gene, causing a frameshift fects of androgen action via the androgen receptor (AR) versus the es- mutation that renders AR nonfunctional (Charest et al., 1991). Males trogen receptors (ERs). Many studies have manipulated estrogens and with this mutation present as females in their somatic features, having a Table 1 Endocrine mediation of male-typical and female-typical sexual behaviors and preferences. Endocrine manipulation Male-typical sexual Female-typical sexual Gynephilia Androphilia References behavior behavior Neonatal decrease in T in males For review, see Cooke et al. (1998) Neonatal increase in T in males a e.g., Henley et al. (2010) and Cruz and Pereira (2012) Estrogenic manipulations Global ERα KO in males Ogawa et al. (1998) and Wersinger and Rissman (2000) Global ERβ KO in males
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