The Mechanisms of Female Nonheterosexuality

Nonheterosexual behavior in humans is virtually ubiquitous around the world, even in cultures that discourage or punish the practice. Seemingly maladaptive and yet consistently present in the population, the origins of homosexuality have been studied for decades. However, an overwhelming majority of research thus far has been conducted on male homosexuals, with only passing interest in female nonheterosexuality. It is known that female homosexuality does not originate from the same genetic pathways as male homosexuality (Hu et al. 1995), and what little research has been done into kin selection showed no support for the inclusive fitness explanations based on a study of female homosexuals in Thailand (Hu et al. 2023). Furthermore, male sexuality is considered more binary than female sexuality, with many more women identifying as “somewhat” homosexual, bisexual, or having a degree of sexual fluidity throughout their lives, as compared to men (Norris et al. 2015). Even women who report themselves as “completely heterosexual” typically experience some degree of genital arousal to erotic images of either sex (Chivers 2017). Clearly, female nonheterosexuality is meaningfully different from male homosexuality. My question is thus: is there an explanation for the origin of female homosexuality? Through this paper, I will examine two hypotheses: one, that female nonheterosexual behavior is adaptive and enables strong female-female bonding and increased paternity certainty, or two, that female nonheterosexual behavior is an occasional result of antagonistic pleiotropy or prenatal conditions that lead to maladaptive sexual preference.

Before reviewing the literature around these hypotheses, I believe it is necessary to discuss the two most common forms of female nonheterosexuality: “butch” and “femme”. While not every nonheterosexual woman identifies with these labels, at least 73% report association with one of the two (Loulan and Thomas 1990). Furthermore, many more women identify as “femme” than “butch”, and while almost all butches describe themselves as purely homosexual, nearly half of femmes identify as bisexual (Rosario et al. 2007). Both butch and femme nonheterosexuals have developed cultural niches within Western society that may impact their mating strategies and same-sex sexual behavior. Simultaneously, there are studied differences in psychology and physiology between women who identify as butch versus femme. Butch women typically display more “masculine” patterns of mate guarding and jealousy (Bassett et al. 2010), as well as a masculinized hypothalamus (Byne et al. 2001). Additionally, the majority of women who identified as “butch lesbians” exclusively prefer to date femme-type nonheterosexuals rather than each other.  Luoto et al. 2018 suggests that the “butch” type of female nonheterosexual derives almost exclusively from masculinizing prenatal hormones and is largely unrelated to the “femme” type in terms of origin. Based on their evidence cited, I am inclined to agree with this hypothesis that there are multiple female nonheterosexual types, and that the butch type is meaningfully distinct. My arguments that follow will therefore focus primarily on the “femme” type of female nonheterosexual, which make up the majority of the female nonheterosexual population and whose origins are more poorly understood.

Female nonheterosexuality as potentionally adaptive has been approached from multiple angles. One such perspective is the “polygyny hypothesis”, which posits that nonheterosexuality in women facilitated conflict resolution in polygynous relationships (Kanazawa 2016). This hypothesis has been met with considerable skepticism, as there is no evidence that examples of female same-sex sexual activity in polygynous marriages reduced competition or tension between co-wives (Jeffery et al. 2019). I also disagree with female nonheterosexuality as a response to polygyny once you consider the historical context of how fraught co-wife relationships have been across cultures. Instead, I find another explanation, the “alloparenting hypothesis” to be much more scientifically supported. The dominant mating strategy for males is the “multiple matings” strategy, which decreases the likelihood of each offspring receiving sufficient paternal care (Schacht and Bell 2016). Women, therefore, must do much of the provisioning for their children alone, which in nearly every scenario leads to reduced fitness (either through infanticide or fewer existing children reaching adulthood.) The alloparenting hypothesis suggests that, because men are unreliable sources of parental care, women instead seek pair bonds with other women. Bisexuality allows women to mate with desirable, “good gene” men that are unlikely to sufficiently provision for them, and then raise offspring in stable, sexually-reinforced relationships with other women (Kuhle and Radtke 2013). Sexual fluidity also allows women in previously heterosexual (male-provisioned) relationships that have been abandoned (due to male death, divorce, or promiscuity) more potential options to find a new partner. Especially because men typically marry women younger than themselves and do not want to provision for step-children (Buss 1989), older women with dependent children who have become unexpectedly widowed may have no options for assistance except other women. The potential for sexual fluidity thus becomes a valuable “fallback” for otherwise heterosexual women. Alloparenting is additionally supported by evidence from primates such as squirrel monkeys and macaques and in at least one great ape species, the bonobo. Alloparenting in these communities is typically a reciprocal provisioning of other females’ children, with provisioned females helping provide for their alloparents’ offspring later on (Furuichi 2011). Relationships between bisexual women could thus function similarly: women mate with genetically desirable men, then assist in provisioning for one another within a pair bond, increasing both of their fitnesses compared to what they could achieve as single females. This specific pattern has been observed by the female-female pair bonding of albatrosses who cooperatively raise male-sired chicks (Bailey and Zuk 2009). Of course, homosexual women who avoid matings with men do not directly benefit from alloparenting their bisexual partner’s children, nor is this an example of kin selection. Alloparenting, therefore, is only adaptive for women who are willing to reciprocally raise children conceived in heterosexual couplings or born in formerly male-provisioned relationships, thus favoring the more sexually-fluid “femme” phenotype of nonheterosexual women.

I also think that, when discussing alloparenting, it is important I mention that female-female relationships do not necessarily have to be sexual in nature to fulfill heterosexual roles. When asked, many women report having a “best” same-sex friendship that is as intimate, passionate, and fulfilling as a heterosexual romance. These friendships, though rarely sexual, also involve physical intimacy such as hand holding, lap-sitting, and cuddling that we may otherwise associate with romance (Diamond 2002). Many nonheterosexual women cite these friendships as sources of self-discovery for their own sexuality, and even in heterosexual relationships prefer the “friendship-first” model of finding potential partners, where romance emerges from an existing friendship (Thompson 2006). Female sexual fluidity, therefore, may be a means of maintaining these supportive same-sex relationships through physical intimacy and romantic-like emotional connection. Though not necessarily a replacement for a heterosexual relationship, these extremely strong female-female bonds create a social safety net for women should they lack a male provisioner. 

There exists another prevalent hypothesis for adaptive female nonheterosexuality: male mate choice. In a 2016 study, over 50% of men reported that they would be sexually excited by their female partners admitting to same-sex attractions (Apostolou 2016b). Additionally, men were found to be less jealous of women with prior same-sex partners than male partners, and parents were less “distressed” by nonheterosexual daughters compared to sons. A follow-up study found that 34% of male participants desired that their long-term partner actively engage in same-sex sexual encounters, compared to 6% of female respondents. Male respondents were also twenty-five times more likely to desire their short-term partners to engage in same-sex sexual encounters compared to female respondents (Apostolou et al. 2017). The authors hypothesized that males responded positively to same-sex infidelity because it reduced risk of cuckoldry. Provisioning males cannot mate guard at all times, leading to risk of their mates “stepping out”. However, even if women are seeking sexual satisfaction with other women, a male can be confident that any offspring are still genetically his. Additionally, a male may hope that these same-sex encounters will give him increased access to his partner’s partner, opening up new mating opportunities (Apostolou et al. 2017). In a study taking place in both China and Britain, male respondents overwhelmingly exhibited higher tolerance and forgiveness for same-sex sexual infidelity compared to heterosexual infidelity, while women were equally likely to end the relationship. Seventy percent of male respondents also indicated that they would prefer their partner to have a same-sex affair over a heterosexual one, compared to only 35% of women, which I believe supports the hypothesis for male preference for same-sex infidelity as a means to reduce paternity uncertainty (Wang and Apostolou 2019). When asked what they consider to be cheating in a relationship, significantly fewer men than women indicated that they believed oral sex, communal showering, and erotic messaging between their partner and a same-sex friend to be a form of infidelity (Compton and Bowman 2017). Similarly, both men and women reported lower rates of jealousy in response to instances of same-sex infidelity compared to heterosexual infidelity (Sagarin et al. 2003). Overall, the evidence suggests men are more tolerant of nonheterosexual infidelity than infidelity which may result in cuckoldry; in many instances, this prospect may even be enjoyed by men who are excited by lesbian encounters involving their otherwise heterosexual partner. Sexually fluid women who are willing to limit any EPCs to other women may therefore be more desirable to provisioning males, receive more offspring support because of increased paternity certainty, and feel physically safer in a relationship by reducing male jealousy and aggressive mate guarding behaviors. This improves her fitness, passing down nonheterosexual genes.

These results from male respondents are compelling to me as evidence that many men may prefer nonheterosexual mates, though it’s of note that men almost never list nonheterosexuality as a desirable trait for a mate without first being prompted (Luoto et al. 2018). Once again, this hypothesis only explains the prevalence for the “femme” type of women that is sexually desirable to men and willing and able to participate in a heterosexual relationship. A butch woman who is both socially masculine and unlikely to willingly associate with a man would not receive the fitness benefits of being provisioned by an invested male, further supporting my conclusion that femme and butch “types” of nonheterosexual women arise from different pathways and are under different selective pressures. As for the mate choice hypothesis, I believe that it is a plausible explanation for the apparent male excitement by female nonheterosexuality, a phenomenon that is widely documented. Lesbians and “female-female” sexual activity is common in American male-targeted pornographic content, while gay men were rare in woman-targeted content (Winnick 1985); college-aged men overwhelmingly reported finding more “erotic value” in lesbian pornography, compared to male-male erotica (Louderback and Whitley 1996). There is certainly a culture of sexual fetishization and tolerance for female nonheterosexuality that, in some cases, leads to male encouragement of nonheterosexual behavior. However, I do wonder if male arousal and tolerance was, itself, an adaptation to an existing phenomenon of widespread female nonheterosexuality, or even the result of the more-recent cultural fetishization of same-sex sexual relationships between women that plays to the male desire for multiple accessible mates.

My alternative hypothesis that female nonheterosexuality is non-adaptive is supported by some evidence of antagonistic pleiotropy. In Italy, nonheterosexual women were located through Internet interest groups; to avoid self-sampling bias, participants were not told the exact nature of the study, and asked to report on sexual history, pedigree size, and fecundity. Heterosexual control groups were found and interviewed in a similar manner. The results found that lesbian women have, on average, four times reduced personal fitness compared to their heterosexual relatives. However, nonheterosexual women almost always had larger pedigrees and higher fecundity on both the maternal and paternal sides of their family, such that the fitness loss was offset (Camperio-Ciani et al. 2018). Though genes were not identified, the consistency of the results supported the hypothesis of genetic polymorphism occasionally leading to homosexual tendencies when a specific combination of genes that otherwise select for fecundity are passed down to an individual. Using newspaper advertisements to locate homosexual probands, another study found that nonheterosexual women typically have more nonheterosexual sisters than heterosexual women (Bailey and Benishay 1993). Similar research suggested that nonheterosexual women also had, on average, more homosexual brothers than heterosexual peers (Bailey and Bell 1993). Based on an Australian twin study, behavioral genes that may predispose an individual to homosexuality were found to be potentially linked to increasing reproductive success in their heterosexual relatives (Zietsch et al. 2008). These data support the hypothesis that some genes, though they occasionally produce a low-fitness individual, also increase fertility for the majority of a lineage and are maintained by balancing selection in the population. As we discuss these results, however, I think it’s important I mention the potential for selection bias; it is possible that women with larger families are more able to express themselves, or that nonheterosexual women with nonheterosexual siblings feel safer coming out. These results might show correlation without causation, and I do believe there are likely familial dynamics enabling multiple nonheterosexual siblings to live more openly with mutual support. That said, I am also personally convinced of some genetic basis to nonheterosexuality based on the research that is available. Furthermore, as these studies made no distinction between butch or femme when discussing the pedigrees of nonheterosexual women, I can only speculate on whether these same fecundity genes are ubiquitous across female nonheterosexuals. Given the distinct physiological differences between many butch-identifying lesbians compared to femme women, I believe that there are key genetic differences not only between nonheterosexual and heterosexual women, but between butch and femme-identifying nonheterosexuals as well. 

An additional female-specific genetic hypothesis for the prevalence of female nonheterosexuality is weak selection. The weak selection pressures hypothesis posed by Apostolou 2016 argues that, because female sexuality and marriages have been restricted by family and male control for much of modern human development, “fitness-depressing” homosexual genes have never been strongly selected against because nonheterosexual women were forced into heterosexual roles. This, the author posits, explains the high rates and varied forms of female nonheterosexuality due to maladaptive genes “hitchhiking” through the population. While possible, I find this hypothesis overall implausible, as it does not account for male attraction to same-sex behavior, higher fecundity in nonheterosexual pedigrees, or the pronounced differences between butch and femme nonheterosexuals.

Finally, prenatal hormone exposure has been studied in regards to same-sex behavior for both men and women. Many nonheterosexual women have been hypothesized to have high androgen exposure in the womb, which is oftentimes reflected in their physiology, such as “masculinized” digit-length compared to heterosexual women and masculinized regions of the brain (Breedlove 2017). Estrogen can also act as a masculinizing hormone, making any variation in typical prenatal hormones possibly “disruptive” to sexual development. Luoto et al. 2018 theorized that different combinations of these hormones in utero can lead to the observed gradient of female sexualities, including butch and femme phenotypes. Hormonal influence on sexual orientation has been further supported by several pharmaceutical studies. One found that nearly 25% of girls whose mothers were treated with synthetic estrogen diethylstilbestrol (DES) while pregnant reported nonheterosexuality as adults (Ehrhardt et al. 1985). Another found that mothers of nonheterosexual daughters consistently consumed more amphetamine-based diet pills and/or synthetic thyroid medications while pregnant than their peers with heterosexual daughters. Increased prescription drug use during the first trimester of pregnancy was also unusually high across many mothers of nonheterosexual children, leading to speculation that drugs which impact either the mother’s or the fetus’ immune system interfere with the “proper” feminization of fetal brains (Ellis and Hellberg 2005). I find the evidence that prenatal hormones influence sexual orientation to be quite compelling. However, I do not believe that the vast majority of these hormonal fluctuations are completely “accidental” as the result of aberrant maternal conditions, but rather caused by genetic factors which are in turn selected for due to resulting adaptive benefits.

Based on the evidence I have reviewed here, I believe that femme-type female nonheterosexuality is an adaptive trait that has been selected for over the course of human evolution. Femme-type nonheterosexuality— often associated with hetero-typical female physiology and bisexuality— enables women more options for support and provisioning when confronted by unreliable males. Even when these close female bonds are not innately sexual, they are still reinforced by a degree of intimacy and pseudo-romantic connection not often shared by male-male friendships. Male mate preference for female sexual fluidity may have developed in response to this phenomenon, or it may have been acting as an existing selective pressure. The genetic component of female nonheterosexuality additionally appears to confer reproductive benefits to a woman’s heterosexual kin, which only further integrates nonheterosexuality into the population. Butch-type female nonheterosexual is a bit more cryptic, given that an overwhelming proportion of butches identify as strictly lesbian. It is possible that the butch phenotype results from an overexposure to androgens in utero or a genetic matrix which otherwise makes a woman more sexually fluid, or that butch and femme come about by entirely different mechanisms. More research into the nuances of female nonheterosexuality will be required to answer these questions. Still, based on what research has been done, I do believe that femme-type female nonheterosexuality is adaptive, and a certain degree of sexual fluidity benefits a woman, while the genes contributing to it benefit her pedigree.

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