Gender-Nonspecific Sexual Responses in Women
In "What is sexual orientation and do women have one?", Michael Bailey (2009) described sexual orientation as "a mechanism, analogous to a compass, that directs our sexuality", noting the following sex difference:
"Men, but not women, have a category specific sexual arousal pattern, one that is usually directed much more strongly to members of one sex than to those of the other. For example, almost all men who identify as homosexual are more sexually aroused by men than by women. In contrast, the arousal pattern of heterosexual women tends to be bisexual, and thus irrelevant to most women’s partner choices. That is, women who identify them selves as heterosexual tend to be similarly aroused by male and female sexual stimuli. The category specific male sexual arousal pattern is the primary sexual motivation that directs male sexual activity to certain kinds of individuals (most often women, but sometimes men) rather than others. Indeed, I contend that a man’s category specific sexual arousal pattern is his sexual orientation. Most women lack this strong directional motivation, and so it is not surprising that their sexual behavior is more malleable and sexually fluid."
Because sexual orientation is a multidimensional construct, it is appropriate to refer to this category-specificity of sexual response as gender-specificity when relative attraction to males and females is the subject of study (Chivers, 2016).
Meredith Chivers (2016) reviewed the research on gender-specificity of sexual response, summarizing the effects of sex and sexual orientation:
"For gynephilic women, sexual responses are typically gender-specific at most stages of sexual response. For androphilic women, a more textured pattern is revealed...In sum, androphilic women's early stimulus processing, genital response, autonomic responses, and responsive solitary sexual desire is gender-nonspecific, whereas their later stimulus processing, affective, and subjective responses, reward area activation, and responsive partnered desire are more gender-specific."
Androphilic women are generally nonspecific across the various stages of sexual response, including: visual attention, cognitive measures, neural responses, pupil dilation, and genital response. However, there are some key exceptions. Androphilic women have been found to be gender-specific when viewing men and women's faces (Imhoff et al., 2010)(Nummenmaa et al., 2012)(Hahn et al., 2015) and when processing odorous stimuli (putative human pheromones) through the hypothalamus (Savic et al., 2001)(Savic et al., 2005)(Berglund et al., 2006). Gender-specific activations of brain regions associated with sexual activity have been reported in androphilic and gynephilic women, although these are "much less" gender-specific than in androphilic and gynephilic men (Sylva et al., 2013). Androphilic women also show gender-specific patterns when viewing prepotent (sexually aroused) genitals, showing greater neural response, dwell time, and vaginal vasocongestion to male torsos and erect penises (Ponseti et al., 2006)(Nummenmaa et al., 2012)(Spape et al., 2014). At that, genital response can be measured in three different ways: vaginal vasocongestion, clitoral erection, and vaginal lubrication. Where vaginal vasocongestion and clitoral erection are generally nonspecific (Huberman & Chivers, 2015) (Suschinsky et al., 2020), vaginal lubrication has been found to be gender-specific in androphilic women (Sawatsky et al., 2018). Smooth regression splines have also been able to detect gender-specific vaginal responses in androphilic women (Pulverman et al., 2015)(but see my Commentary).
To explain this sex difference in arousal, Chivers (2016) proposes ten different hypotheses. Of these, the Preparation Hypothesis that women's bodies produce nonspecific sexual responses to all sexual stimuli, in order to protect the body from injuries caused by unwanted sex. In their review of the Preparation Hypothesis, Lalumière et al. (2022) concluded that "the evidence is favorable but not entirely convincing".
In addition to gender-specificity, there are sex differences and sexual orientation effects when it comes to the concordance between self-reported sexual attraction and physiological sexual arousal. Women are generally less concordant then men, with androphilic women being the least concordant (Chivers & Blumenstock, 2024)(Chivers et al., 2010). This raises the question as to whether physiological sexual arousal is an accurate measure of sexual orientation in females, or if it is measuring something else entirely.
As summarized by Diamond & Rosky (2016):
"Does this mean that all women are "really" bisexual without being consciously aware of it? Not necessarily: Discrepancies between one's genital arousal to a sexual stimulus and one's psychological experience of arousal are common, especially in women, and it is not clear how to interpret these discrepancies. (Bailey, 2009; Bailey, Rieger & Rosenthal, 2011; Chivers, Seto, Lalumiere, Laan & Grimbos, 2010; Rieger et al., 2005; Rosenthal, Sylva, Safron, & Bailey, 2011; Rosenthal et al., 2012; Suschinsky, Lalumiere, & Chivers, 2009). Further complicating the picture is the fact that women show more gender-specific genital responses (i.e., greater arousal to their preferred gender) when sexual stimuli consistent of static images of exposed genitals rather than extended videos of individuals engaged in sexual activity (Bouchard, Timmers, & Chivers, 2015) [this seems to be an error; presumably, Diamond & Rosky meant to refer to Ponseti et al., 2006 or Spape et al., 2014]. These findings underscore a point made earlier: There is no agreed-upon direct measure of sexual orientation, which makes it impossible to interpret self-reports of "choice" (as well as change) in sexual orientation."
While it is doubtful that gender-nonspecificity is a measurement artefact (Chivers et al., 2016)(Suschinsky et al., 2020), Diamond (2008) proposes an elegant solution to this conundrum. There are two states associated with sexual response: proceptivity ("motivation to initiate sexual activity") and arousability ("capacity to become aroused to sexual stimuli"). Where proceptivity is a proactive trait, arousability is a reactive trait. In males, proceptivity is always high, due to males' "continuously high androgen levels". In females, proceptivity is only high during ovulation, where it is mediated by the monthly hormonal cycle. When female proceptivity is cyclical, female arousability is constant, possibly due to the Preparation Hypothesis.
Diamond (2008) explains:
"Because proceptivity represents a strong motivation to initiate sexual behavior, it would be important (evolutionarily speaking) for this response to be targeted only toward potentially reproductive partners and, therefore, it is reasonable to expect that this form of sexual desire is innately coded for “sex of partner.” Yet, the same would not be true for arousability. As long as urges to initiate mating were reliably targeted toward reproductive partners in the EEA, there would be little or no selection pressure to code “sex of partner” into arousability."
This could explain why female same-sex sexual attractions and sexual behaviors occur, not just in humans but other primates. There is some evidence in support of this hypothesis from studies on androphilic women and nonheterosexual women (Suschinsky et al., 2014)(Diamond & Wallen, 2011)(Chivers, 2016). Since the study on nonheterosexual women relied on self-report, it ought to be verified through physiological measures. If true, physiological sexual arousal is not the best measure of female sexual orientation, because it is also necessary to measure proceptivity.
The difference between proceptivity and arousability could explain why "all women may be capable of desiring periodic sexual contact with women" (Diamond & Alley, 2019). VanderLaan et al. (2023) also suggest that, in females, "same-sex sexuality might hinge to a greater extent on sociocultural factors". In recent years, several authors have proposed various evolutionary explanations for female same-sex sexual attraction and sexual behavior (Diamond, 2008)(Apostolou, 2022)(Luoto & Rantala, 2022)(Semenyna et al., 2022)(Frederick et al., 2023)(Raymond & Crochet, 2023).
Taken together, it might be an inaccuracy to describe the typical female as heterosexual or (exclusively) androphilic. Typical female sexuality appears to work very differently from typical male sexuality, where female sexual orientation can be "person-based" instead of "sex-based".
Gynephilia as Male-Shifted Sexuality
While appealing, Diamond's (2008) theory raises a few questions. If proceptivity is mediated by hormone levels, why are gynephilic women more gender-specific in their sexual arousal?
Gynephilic females are (near) exclusively homosexual in their sexual attractions, showing greater gender-specificity than androphilic females but less gender-specificity than gynephilic males (Bailey, 2009) (Bailey et al., 2016) (Chivers, 2016) (Rieger et al., 2016). Interestingly, gynephilic women are more gender-specific when shown less intense sexual stimuli (Chivers et al., 2007). Chivers (2016) describes finding gender-specific responses to prepotent female stimuli (engorged and lubricated vulvas) in gynephilic women, but this study only involved 4 participants (Timmers et al., 2013). If female proceptivity is distinct from female arousability, the Preparation Hypothesis suggests that all gynephilic women should have some arousability towards male stimuli (Lalumière et al., 2022). This does not necessarily translate to sexual attraction towards males, as it remains unclear whether physiological sexual arousal is an accurate measurement of female sexual orientation.
What can be stated objectively is that gynephilic females show intermediate patterns of physiological arousal, between that of the typical (heterosexual) male and the typical ("heterosexual") female. These patterns are observed in terms of gynephilia (arousal to the female sex), gender-specificity, arousal to visual stimuli (Bailey et al., 1994), "person-based" vs "sex-based" attractions, and longitudinal sexual fluidity.
Suppose that gynephilia, gender-specificity, "sex-based"-ness, and stability of sexual attractions are all traits of male-typical sexuality. If male-shifted brain sexual differentiation can cause these traits to manifest in a female, this would explain why they are associated with each other. Each trait only appears in an incomplete form, due to the androgynous biology of a male-shifted female. We would also expect the degree of each trait to be a function of "male-shifted"-ness, whether that be number of genetic polymorphisms, dose and timing of prenatal androgen exposure, etc.
If gender-specificity is "organized" during an early developmental period and later "activated" by hormone levels, this could explain the differences in proceptivity between gynephilia and androphilia. It is also possible that Diamond's (2008) hypothesis is insufficient in explaining the nonspecificity of androphilic women's arousal.
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