Commentary Apostolou (2022) "The Evolution of Female Same-Sex Attraction"

Recently, I've been reading through the articles published in The Cambridge Handbook of Evolutionary Perspectives on Sexual Psychology Volume 4: Controversies, Applications, and Nonhuman Primate Extensions (2022). I highly recommend these to anyone with an interest in female sexuality, and by extension female-to-male transsexuality.

The topic of this blog post is Chapter 2: "The Evolution of Female Same-Sex Attraction", Menelaos Apostolou. This was a very interesting read, but I have a couple of minor comments.

Apostolou (2022) claims that "The most common type of female same-sex attraction is heterosexual orientation with same-sex attraction [mostly-androphilic] (7.9 percent), followed by homosexuality [gynephilic] (3.0 percent) and bisexuality [ambiphilic] (2.1 percent)." As there is no source provided, I don't know how he derived these figures. Semenyna et al. (2022) report different figures, where ~85% of women are androphilic, ~7-10% are mostly-androphilic, ~2-4% are ambiphilic, and ~1% are gynephilic. These figures are derived from: Bailey et al. (2016), Diamond (2016), Rahman et al. (2019), Savin-Williams & Vrangalova (2013). 

A non-critique, but Apostolou (2022) states that "many women who experience same-sex attractions may experience a change in their attractions over time." While true, it is worth noting that self-reported changes to sexual attraction do not necessarily suggest a true change or fluidity of sexual orientation itself.

"In contrast to most men, most women require emotional involvement to engage in a sexual relationship...It is therefore important to understand that defining a bisexual woman’s sexual orientation merely by asking which sex she is attracted to at an arbitrary point in time may be misleading. One may be erroneously led to believe that her sexual orientation has under gone shifts from heterosexual to homosexual or to bisexual in the course of her life. This is because romantic love causes one to focus one’s energy and attention solely on the object of one’s love...Should the love object be male, the woman might be inclined to identify as heterosexual. Should the love object be female, the woman may be inclined to identify as homosexual. If feelings of romantic love towards that person subside, the woman’s “momentary sexual orientation” may undergo another shift, giving a muddled view about her sexual orientation. This does not ultimately boil down to sexual malleability nor to fundamental changes in the woman’s sexual orientation...but to the fact that nonheterosexual women’s attractions are sometimes person-based rather than sex-based. Determining women’s sexual orientation through an introspective sense of their sexual orientation at an arbitrary point in time can therefore be problematic if a person-based attraction should at that specific point in time bias it to one end of the male–female gender spectrum." (Luoto et al., 2022)

This exhausts all of my minor comments. 

Apostolou (2022) describes three important concepts pertaining to the evolutionary origins of female nonheterosexuality. First is the concept of mutation-selection balance equilibrium, described like so:

"Although the genetic material is replicated with high fidelity, copy errors or mutations do occur. Mutations are a likely source of the genetic predisposition for same-sex attraction. In particular, a gene that codes for a mechanism regulating sexual attraction that is normally expressed in men, experiences a mutation that gives rise to an allele that is expressed in both sexes or only in women. In effect, women who carry the allele will experience same-sex attractions. Assuming that same-sex attraction impairs women's reproductive success, we expect that alleles predisposing for same-sex attraction would experience negative selection pressure that would cause them to be removed from the gene pool. Yet, because the mutation rate is positive (i.e., new mutations would be generated in every generation), at any given point in time, there would be an equilibrium frequency of alleles that predispose for same-sex attraction, which is determined by the balance between mutation rate and the rate that selection removes these alleles from the gene pool."

Apostolou (2022) goes on to explain why negative selection pressure would have been weak against female nonheterosexuality. He argues that said genes would be 'shielded' against selection 50% of the time, when they are expressed in males instead of females. Additionally, hundreds or thousands of alleles might code for sexual orientation. If true, a single mutant allele would have a "very small phenotypic effect". Because the negative selection pressure against any given gene would be "very weak", these mutant alleles could accumulate over time, increasing mutant-selection balance equilibrium. 

As Diamond (2021) notes, there is evidence to support the "small phenotypic effect" hypothesis: "In September 2019, the largest-ever genome-wide-association study (GWAS) of same-gender sexuality [same-sex sexual behavior] was published in Science (Ganna et al., 2019)...overall their analyses indicated that thousands of other genetic variants, each with tiny effects, significantly contributed to the likelihood of ever engaging in same-gender [same-sex] sexual behavior.""

Apostolou (2022)'s discussion of weak negative selection pressure is compelling, as he accounts for the oft-neglected status of women in the ancestral context of humanity. His descriptions of 'regulation of mating', 'male-male competition', and 'social pressures' all describe how "heterosexual contact is forced on women" , in what feminists refer to as compulsory heterosexuality. This drastically reduces negative selection pressure against female same-sex attraction, as women of all sexual orientations were forced to have children. There is some support for this in research on rhesus macaques, which has found that "restrictive social conditions" can suppress the expression of masculinized sexuality in females (Wallen, 2022). If this is applicable to humans, "suppressed" females might not express nonheterosexuality during their lifetime, but pass those genes down to their daughters.

Apostolou (2022) also describes positive selection pressures hypotheses, which describe why ancestral men might have preferred to mate with same-sex attracted women. The first hypothesis is that same-sex attracted men and women might have had a preference for each other due to being similar in their nonheterosexuality. The second hypothesis is to protect against cuckoldry, while the third is to increase sexual access to women. Whether these hypotheses are correct is unknown to me, but Apostolou (2022) provides compelling empirical data to support the theory that men have evolved to prefer mostly-androphilic women (i.e., heterosexual women who are slightly same-sex attracted, Kinsey=1,2).

Apostolou (2022) summarizes his hypotheses like so:

"There are many genes that code for mechanisms that regulate attraction. Genes that code for attraction toward women are expressed in men and remain silent in women. Some of these genes have mutated so that they are also expressed in women, resulting in those women who carry them to experience same-sex attractions. These attractions reduce reproductive output, so they are selected against. A positive mutation rate tends to introduce such alleles into the gene pool, and a negative selection rate tends to remove them, so that, at any point in time, there would be several such alleles in the gene pool that the positive mutation rate has introduced and negative selection has not yet removed. For a given rate of positive mutation, the equilibrium frequency of these alleles and, thus, the relative prevalence of female same-sex attraction in the population, depends on the strength of the negative selection." 

"...in ancestral human societies, there were several factor, such as arranged marriage, that weakened considerably negative selection pressures on female same-sex attraction...there were factors, such as a male preference for same-sex attraction in women, which have contributed to reducing negative selection pressures by adding a positive selection component. Although factors including arranged marriage and men monopolizing women by force have largely disappeared from contemporary postindustrial societies, the transition to postindustrialism was too recent in evolutionary terms for selection forces to have adjusted the equilibrium of mutant alleles to present conditions. Thus, the observed prevalence of female same-sex attraction predominantly reflects the ancestral human condition. These weak negative and positive selection hypotheses predict that female same-sex attraction would be in a relative minority of the female population, and it would be predominantly found in heterosexual women, a prediction which fits the observed prevalence rates."

Recommended to those interested in the evolutionary origins of female nonheterosexuality.

EDIT: Originally, I had the following written as a minor comment (previously called "nit-pick"):

On the subject of kin selection theory, Apostolou (2022) claims that "With one exception (Vasey et al., 2007), studies failed to provide evidence in support of this prediction for men (Abild et al., 2014Bobrow & Bailey, 2001Camperio Ciani et al., 2016Rahman & Hull, 2005Vasey & VanderLaan, 2012), and to my knowledge, there has not been any attempt to test this prediction in women."

In contrast, Frederick et al. (2023) describe how "Studies in Samoa and Java (Indonesia) have found evidence consistent with the theory", citing: Nila et al. (2018), VanderLaan & Vasey (2012), Vasey & VanderLaan (2010), and VanderLaan et al. (2012). Although Apostolou (2022) mentions the work Vasey & VanderLaan conducted in Samoa, he neglects to mention Nila et al. (2018)'s work in Java (Indonesia). Frederick et al. (2023) describe how cultural differences might be at play, where the theory's applicability could depend on "how accepted and integrated these androphilic men are in the population (Vasey et al., 2020)."

This was a major error on my part, as I failed to review Nila et al.'s research in Java. Nila et al. (2018) found only found a little evidence consistent with kin selection theory. As stated plainly in the abstract: "Kin selection reduced the direct reproductive cost of homosexual men by 20%, so suggesting that kin selection alone is insufficient to explain the maintenance of male homosexuality". 

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References

Abild, M. L., VanderLaan, D. P., & Vasey, P. L. (2014). Does geographic proximity influence the expression of avuncular tendencies in Canadian androphilic males?. Journal of Cognition and Culture, 14(1-2), 41-63. https://brill.com/view/journals/jocc/14/1-2/article-p41_3.xml

Apostolou M. The Evolution of Female Same-Sex Attraction. In: Shackelford TK, ed. The Cambridge Handbook of Evolutionary Perspectives on Sexual Psychology. Cambridge Handbooks in Psychology. Cambridge University Press; 2022:28-51.

Bailey, J. M., Vasey, P. L., Diamond, L. M., Breedlove, S. M., Vilain, E., & Epprecht, M. (2016). Sexual Orientation, Controversy, and Science. Psychological Science in the Public Interest, 17(2), 45-101. https://doi.org/10.1177/1529100616637616 (Original work published 2016)

Bobrow, D., & Bailey, J. M. (2001). Is male homosexuality maintained via kin selection?. Evolution and Human Behavior, 22(5), 361-368. https://doi.org/10.1016/S1090-5138(01)00074-5

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Diamond, L. M. (2016). Sexual fluidity in male and females. Current Sexual Health Reports, 8(4), 249-256. https://doi.org/10.1007/s11930-016-0092-z

Diamond, L. M. (2021). The New Genetic Evidence on Same-Gender Sexuality: Implications for Sexual Fluidity and Multiple Forms of Sexual Diversity. The Journal of Sex Research, 58(7), 818–837. https://doi.org/10.1080/00224499.2021.1879721

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Ganna, A., Verweij, K. J., Nivard, M. G., Maier, R., Wedow, R., Busch, A. S., ... & Zietsch, B. P. (2019). Large-scale GWAS reveals insights into the genetic architecture of same-sex sexual behavior. Science, 365(6456), eaat7693. https://doi.org/10.1126/science.aat7693

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