Origins of male homosexuality

Male homosexuality has always puzzled evolutionary biologists. It has 30-45% heritability, so there must be some genetic predisposition (Bailey et al., 2000). But how could such a predisposition get passed down from generation to generation? It ought to die out, by its very nature.

Well, not all predispositions are fully expressed. This observation led the economist and evolutionary psychologist Ed Miller to propose that male homosexuality has survived by means of a balanced polymorphism (Miller, 2000). In the human species, the male has to invest more in his offspring, particularly if the female is less able to feed herself and her offspring through food gathering, as in non-tropical environments. To change male behavior in this direction, the fastest way, with the least genetic change, is to partially feminize the male brain. This could be done through heterozygote advantage at some gene loci: if only one allele is changed, a man would become more child-oriented while still being heterosexual; if both alleles are changed, he would also become feminized in his sexual orientation.

But heterosis effects are absent at most loci. There is usually a simple dominant/recessive mode of action. Nonetheless, a balanced polymorphism is still possible through additive effects over many loci. If a certain proportion have alleles for mental feminization, a man will take more interest in his children without becoming feminized in his object of sexual interest. There may, however, be more than one ‘right’ mix of feminization/non-feminization alleles (the number of possible permutations being a function of the number of relevant genes). Even if all men in one generation have the right mix, reshuffling of genes from their generation to the next would produce some male offspring who are too feminized and others not enough.

Of course, this situation would be gradually corrected by natural selection. The ‘right’ mixes would not be exactly equal in their adaptive value. Natural selection would tend to favor some over others and eventually there would be fixation of one mix of alleles. But this would take a long time and paternal investment varies in importance even among the relatively young populations of Homo sapiens—itself a young species.

So this is Miller’s theory: male homosexuality is the tail end of a balanced polymorphism due to selection for men who invest more in rearing their children and provisioning their families. Santtila et al. (2009) tried to test this theory, which they describe as follows:

Miller (2000) speculates that if a typical man inherits only a few of the alleles partially preventing androgenization, he would express more kindness, sensitivity, tendermindedness, and empathy. Only occasionally would a sufficient number of these alleles come together to produce homosexuality. Heterosexual carriers of these alleles would be better fathers and more attractive mates as men with such traits are less likely to harm their partner or children (Miller, 2000). These traits in men would help them to attract women and, thus, lead to greater reproductive success, ensuring the survival of the alleles in the gene pool. A heterosexual man without any of these alleles would exhibit traits such as ruthlessness, selfishness, insensitivity, and cruelty, making them unattractive to women.

This isn’t quite what Miller had in mind. Yes, a heterosexual carrier would be less likely to harm his partner and children, but a more critical factor would be his willingness to provide for them. Nor is it necessary to assume that such men are preferred as mates. Their greater reproductive success would come from the higher survival rate of their children. We’re talking natural selection here, not sexual selection.

This misunderstanding affected Santilla et al.’s experimental design. Heterosexual men with homosexual brothers were questioned on a wide range of behaviors: psychopathy, sexual aggression, sexual coercion, sexual activity, and number of children. No questions were asked about interest in children or willingness to care for them. Number of children might inversely correlate with paternal investment (some could die through neglect or insufficient care), but only if there are enough of them. Nowadays, family size is too small for this factor to be significant. Indeed, the heterosexual subjects had each fathered less than one child on average.

No significant differences were found between the heterosexual ‘carriers’ and a control heterosexual group. But it’s not clear to me that a difference should be expected, given the experimental design.

References

Bailey, J.M., M.P. Dunne, & N.G. Martin. (2000). Genetic and environmental influences on sexual orientation and its correlates in an Australian twin sample. Journal of Personality and Social Psychology, 78, 524-536.

Miller, E.M. (2000). Homosexuality, birth order and evolution: Toward an equilibrium reproductive economics of homosexuality. Archives of Sexual Behavior, 29, 1-34.

Santtila, P., A-L. Högbacka, P. Jern, A. Johansson, M. Varjonen, K. Witting, B. von der Pahlen, N. K. Sandnabba. (2009). Testing Miller’s theory of alleles preventing androgenization as an evolutionary explanation for the genetic predisposition for male homosexuality. Evolution and Human Behavior, 30, 58-65.