Same sex attraction — A Darwinian paradox, no more

Like most human behavioural traits, a preference for same-sex sexual relationships can be informed in part by learning and environmental / developmental experiences.  A role for genes is also now abundantly clear.  So-called ‘gay genes’ have not yet been precisely identified, but pedigree and twin studies have shown that homosexuality tends to run in families (reviewed in Ngun etal. 2011), and a recent genetic analysis of 409 pairs of gay brothers links sexual orientation in men with particular regions of the human genome (Sanders et al. 2015).  The pressing question then — described often as a ‘Darwinian paradox’ — is how do we account for the common occurrence of homosexuality in evolutionary terms, given that it would seem to present a severe limitation on evolutionary fitness through one’s direct lineage? Several explanations and speculations have been offered (see the very accessible review in Barash 2012) — and many illustrate, as the saying goes: ‘things are not always as they seem’.

For male homosexuality, one of the best explanations so far comes from recent studies suggesting that female relatives of gay men generally have more offspring than the female relatives of straight men.   In other words, there are genetic factors transmitted through the maternal line (partly linked to the X-chromosome) that increase the probability of becoming homosexual in males, but they promote higher fecundity in females (Camperio-Ciani et al. 2004, Iemmola and Camperio-Ciani 2009).  Hence, the genetic factors that “… influence homosexual orientation in males are not selected against because they increase fecundity in female carriers, thus offering a solution to the Darwinian paradox and an explanation of why natural selection does not progressively eliminate homosexuals” (Iemmola and Camperio-Ciani 2009).

A similar hypothesis (that applies to either male or female homosexuality) is suggested by Zietsch et al. (2008):

“The genes influencing homosexuality have two effects.  First, and most obviously, these genes increase the risk for homosexuality, which ostensibly has decreased Darwinian fitness.  Countervailing this, however, these same genes appear to increase sex-atypical gender identity, which our results suggest may increase mating success in heterosexuals. This mechanism, called antagonistic pleiotropy, might maintain genes that increase the risk for homosexuality because they increase the number of sex partners in the relatives of homosexuals.” … “The traits most reliably associated with homosexuality relate to masculinity–femininity; homosexual men tend to be more feminine than heterosexual men, and homosexual women tend to be more masculine than heterosexual women.”

In other words, this ‘sex atypicality’ may be advantageous when expressed in heterosexuals.  Do some (perhaps many) females tend to be more attracted to males with certain feminine behavioral traits such as tenderness, considerateness, and kindness?  In this study, the results indeed show that “... psychologically masculine females and feminine men are (a) more likely to be nonheterosexual but (b), when heterosexual, have more opposite-sex sexual partners” (Zietsch et al. 2008).

Another, more general hypothesis for homosexuality is that same-sex attraction never really imposed a significant penalty on fitness in our deep ancestral past, because heterosexual sex was still routinely practiced in spite of it.  There are two very different contexts in which this effect would be expected: 

Bivariate trait space continuum for sexual orientation (Aarssen 2015)

The first obtains from just straightforward bisexuality, i.e. where ancestral sex lives commonly involved a mix of both same-sex and heterosexual activity but in varying proportions (informed in part by genotypic variability) ranging from bisexual with a more dominant opposite-sex attraction, to bisexual with a more dominant same-sex attraction.  But random mating within this mix would also have produced genetic variants that informed strictly homosexual as well as strictly heterosexual orientations — with only the latter of the two strongly favoured by natural selection. 

Nevertheless, despite being strongly disfavoured by natural selection, strict homosexuality would have persisted in low frequency simply because of genetic factors informing same-sex attraction that were inherited from bisexual ancestors.  Under this hypothesis, homosexuality is not really a Darwinian paradox at all; instead it, along with asexuality, were just periodic maladaptive genotypic by-products of ancestral gene transmission.

Most ancestral bisexuals, however, were probably female. Research has shown that men are generally attracted to one sex or the other, whereas women are more likely than men to have a bisexual orientation. According to one hypothesis, a ‘fluid sexuality’ that enabled same-sex sexual behavior in women made it easier for women to raise children together. 

Painting of King Solomon and his wives

by Giovanni Venanzi di Pesaro (1627-1705)

This, according to Kuhle (2013): "… would have been particularly beneficial to ancestral women when their male mates were unable to adequately care, protect, and provide because they were injured, away on prolonged hunts, or preoccupied finding, courting, and mating with other women.  The latter scenario was particularly likely to occur within polygynous mating systems. ...

If so, it is possible that men’s relative lack of aversion to a female mate’s homosexual, rather than heterosexual, affair … and men’s common fantasy of simultaneously mating with multiple women … is an outgrowth of a male psychology designed to promote their mates’ same-sex sexual behavior.”

The latter would have commonly benefitted the offspring of not just bisexual women, but also the men who fathered these offspring, many of whom were often not around to help raise them.  Ironically, therefore, for many of our male ancestors, it was probably better for their own genetic fitness, if their partners were bisexual.

The second context for predicting successful heterosexual practice (and hence gene transmission) — despite the presence of same sex attraction — applies even in the case of strong preference for same-sex encounters, including strict homosexuality.  According to what we might call the ‘failed disfavouring selection’ hypothesis (Aarssen 2015), female homosexuality probably never had widespread opportunity to be strongly disfavoured by natural selection.  This is because, throughout much (probably most) of human history, males were to a large extent in control of the sexual activity and fertility of females.  Many or most women, therefore, were essentially forced — by patriarchal subjugation, socio-cultural expectations, and / or religious imperatives — to mate with men and bear their (frequently many) offspring, regardless of their sexual orientation. [The same would also have been true regardless of the intensity of female sexual impulse (drive)]. 

Accordingly, so called ‘gay genes’ in many of our female ancestors — including those that might have been inherited by their sons as well as their daughters — were never significantly limited in their transmission success to future generations.  And so in this context, the prevalence of homosexuality today is (again) not really a Darwinian paradox at all.

Importantly however, women more than ever are now in control of both their fertility and their sex lives, and their empowerment for this and other basic human rights continues to grow rapidly on a global scale.  For our predecessors, choosing successfully to be a practicing homosexual meant zero gene transmission through direct lineage.  But today this is not necessarily the case, with reproductive technologies for sperm banks and in-vitro fertilization (and perhaps, in the future, human cloning).  But unless the latter become widely practiced as a popular cultural norm, the widespread mating and reproductive freedom for women today means that selection against an exclusively or predominantly lesbian orientation may soon be ramping up (Aarssen & Altman 2006).  If female bisexuality, remains alive and well, however, so also would some homosexuality (because of genetic inheritance from bisexual maternal ancestors).

The above scenario is a good example of how some traits — like homosexuality, the generally weaker sexual impulse in females compared with males, and the child-free culture — rather than a consequence of being favoured by natural selection in the ancestral past, may instead be a consequence of not having been disfavoured by natural selection.

References

Aarssen LW (2015) What Are We? Exploring the Evolutionary Roots of Our Future. Queen’s University, Kingston.

Aarssen LW, Altman S (2006) Explaining below-replacement fertility and increasing childlessness in wealthy countries: Legacy drive and the “transmission competition” hypothesis. Evolutionary Psychology 4: 290-302.

Barash DP (2012) Homo Mysterious: Evolutionary Puzzles of Human Nature. Oxford University Press, Oxford.

Camperio-Ciani A, Corna F, Capiluppi C (2004) Evidence for maternally inherited factors favouring male homosexuality and promoting female fecundity. Proceedings of the Royal Society of London, Series B: Biological Sciences 271: 2217–2221.

Iemmola F, Camperio-Ciani A (2009) New evidence of genetic factors influencing sexual orientation in men: female fecundity increase in the maternal line. Archives of Sexual Behavior 38: 393–399.

Kuhle BX (2013) Born Both Ways: The alloparenting Hypothesis for sexual fluidity in women. Evolutionary Psychology 11: 304-323.

Ngun TC, Ghahramani N, Sa´nchez FJ, Bocklandt S, Vilain E (2011) The genetics of sex differences in brain and behavior. Frontiers in Neuroendocrinology 32: 227–246.

Sanders AR, Martin ER, Beecham GW, Guo S, Dawood K, Rieger G, Badner JA, Gershon ES, Krishnappa RS, Kolundzija AB, Duan J, Gejman PV, Bailey JM (2015) Genome-wide scan demonstrates significant linkage for male sexual orientation. Psychological Medicine 45: 1379-1388.

Zietscha BP, Morley KI, Shekar SN, Verweij KJH, Keller MC, Macgregor S, Wright MJ, Bailey JM, Martin NG (2008) Genetic factors predisposing to homosexuality may increase mating success in heterosexuals. Evolution and Human Behavior 29: 424–433.