Abstract
Women’s capacity for sexual fluidity is at least as interesting a phenomenon from the point of view of evolutionary biology and behavioral endocrinology as exclusively homosexual orientation. Evolutionary hypotheses for female nonheterosexuality have failed to fully account for the existence of these different categories of nonheterosexual women, while also overlooking broader data on the causal mechanisms, physiology, ontogeny, and phylogeny of female nonheterosexuality. We review the evolutionary-developmental origins of various phenotypes in the female sexual orientation spectrum using the synergistic approach of Tinbergen’s four questions. We also present femme-specific and butch-specific hypotheses at proximate and ultimate levels of analysis. This review article indicates that various nonheterosexual female phenotypes emerge from and contribute to hormonally mediated fast life history strategies. Life history theory provides a biobehavioral explanatory framework for nonheterosexual women’s masculinized body morphology, psychological dispositions, and their elevated likelihood of experiencing violence, substance use, obesity, teenage pregnancy, and lower general health. This pattern of life outcomes can create a feedback loop of environmental unpredictability and harshness which destabilizes intrauterine hormonal conditions in mothers, leading to a greater likelihood of fast life history strategies, global health problems, and nonheterosexual preferences in female offspring. We further explore the potential of female nonheterosexuality to function as an alloparental buffer that enables masculinizing alleles to execute their characteristic fast life history strategies as they appear in the female and the male phenotype. Synthesizing life history theory with the female sexual orientation spectrum enriches existing scientific knowledge on the evolutionary-developmental mechanisms of human sex differences.
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Notes
Brown et al. (2002b) recorded almost equal numbers of butches (n = 87) and femmes (n = 89) in a U.S. sample of predominantly or exclusively homosexual women. In Chinese lesbian samples, butches consistently and significantly outnumber femmes (Zheng et al., 2018, and references therein). Perhaps surprisingly, a sample of Chinese bisexuals consisted of equal numbers of femmes, butches, and androgynous women (Zheng et al., 2018).
In a Spanish sample, however, sexual sensation seeking (as opposed to general sensation seeking) was lower in self-identified lesbians (n = 90) than in heterosexual women (n = 92) (Gil-Llario, Morell-Mengual, Ballester-Arnal, Giménez-García, & Castro-Calvo, 2015). Notably, bisexual women were excluded from the study due to a low sample size (n = 4) (Gil-Llario et al., 2015). Another study found that bisexual women had higher sexual sensation-seeking scores than either lesbian or heterosexual women (Stief, Rieger, & Savin-Williams, 2014).
That is, willingness, attitudes, and desires associated with uncommitted sexual behavior.
See Swaab and Hofman (1988) for another interpretation of the developmental mechanism underlying SDN dimorphism, namely that the size of the SDN decreases due to postnatal cell death. Note that the authors used the term “SDN” rather than “INAH3.” It was only in future research that the term “INAH3” became established (Byne et al., 2001).
See Spencer et al. (2017) who, despite reporting higher aggression in CAH girls than in unaffected girls, found that amniotic fluid testosterone was not a significant predictor of aggression. Spencer et al. suggest that amniotic fluid testosterone may not be a sensitive measure of prenatal androgen exposure.
This is aligned with the finding of a recent meta-analysis that lesbians have 9% higher wages than heterosexual women (Klawitter, 2015). This difference appears to be driven by higher work intensity, i.e., more working hours for lesbians than heterosexuals, which may, in part, be explained by more frequent childbearing (and child rearing) in heterosexual women (Sabia, Wooden, & Nguyen, 2017).
See Rahman and Wilson (2003) for null findings between digit ratios of butches and femmes in a sample that was substantially smaller than that of Brown et al. (2002b). Rahman and Wilson (2003), however, reported a general replication of the finding that homosexual women had more masculine 2D:4D than heterosexual women. See also Vásquez-Amézquita et al. (2018) for a failure to replicate the finding between digit ratio and sexual orientation in a sample of 16 nonheterosexual women from Colombia (who scored 5 or 6 on the Kinsey scale, i.e., mainly or exclusively homosexual). This may have been caused by the researchers’ failure to distinguish between butches and femmes, or the small sample sizes of heterosexual (n = 21) and nonheterosexual women (n = 16).
Skorska et al. (2015) compared 52 exclusively or near-exclusively homosexual women with 134 heterosexual women. Skorska et al. did not distinguish between butch and femme women, which may have confounded the results.
Though see Rieger et al. (2016, not controlling for butch/femme differences) for findings that suggest that even exclusively homosexual (Kinsey 6) women experience some genital arousal when shown erotic material of men.
An adaptation can be defined as an inherited and reliably developing characteristic that came into existence as a feature of a species through natural selection because it facilitated reproductive fitness during the period of its evolution (Buss, Haselton, Shackelford, Bleske, & Wakefield, 1998; Tooby & Cosmides, 1992). See Lewis et al. (2017) for a broad, more recent discussion.
Byproducts are phenomena that exist because they are intrinsically coupled with an adaptation, despite having no function in and of themselves (see Lewis et al., 2017 for a more detailed discussion).
Kanazawa (2017) only analyzed women up to 29 years of age. Our review indicates that the lifetime fitness of nonheterosexual women is no higher than that of heterosexual women (recent findings in an Italian population indicate that nonheterosexual women in fact have lower reproductive fitness than heterosexual women: Camperio Ciani et al., 2018). Early reproduction is characteristic for fast LH strategies, and so Kanazawa’s data lends support to our hypothesis about female homosexuality being an outcome of selection for fast LH strategies.
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Acknowledgements
Parts of this article were presented at the 46th Annual Behavior Genetics Meeting, Brisbane, Australia in 2016. The authors wish to thank the members of the University of Auckland Language, Cognition and Culture Lab for valuable comments on earlier drafts. Constructive inputs from anonymous reviewers helped us improve this article. The authors are particularly thankful to Paul Vasey for his thoughtful editorial contributions.
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A travel grant (S.L.) was provided by the Behavior Genetics Association to present this research at 46th Annual Behavior Genetics Meeting, Brisbane, Australia.
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Luoto, S., Krams, I. & Rantala, M.J. A Life History Approach to the Female Sexual Orientation Spectrum: Evolution, Development, Causal Mechanisms, and Health. Arch Sex Behav 48, 1273–1308 (2019). https://doi.org/10.1007/s10508-018-1261-0
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DOI: https://doi.org/10.1007/s10508-018-1261-0