A new model has been proposed to explain the evolutionary origin and maintenance of male homosexuality in human populations in the context of Darwinian Evolution by invoking the idea of sexually antagonistic selection. This was proposed in an article released on June 17, 2008 in the open access journal PLoS ONE.

Homosexuality in males is widely considered to be influenced by factors that are both psychosocial and genetic. The latter is suggested by a few items. Namely, the high correlation of sexual orientation in identical twins points to a genetic component. Additionally, there is a higher frequency of homosexuality in males who belong to a maternal line of male homosexuals. These same effects have not, however, been shown for female homosexuality — so these two phenomena very likely have different origins and dynamics.

This report, written by an Italian research team made up of Andrea Camperio Ciani and Giovanni Zanzotto at the University of Padova and Paolo Cermelli at the University of Torino, explores a number of different hypotheses for the potential genetic basis of male homosexuality. These included: the genetic maternal effect on sons; the heterozygote advantage, such as in malarial resistance, in which hybrids for a trait have desirable traits; and sexually antagonistic selection.

Under Darwinian evolutionary models, genes that are passed on to offspring are preserved or amplified in the population while those that do not decrease in frequency. Generally, homosexual males reproduce less than heterosexual males, so a genetic basis for male homosexuality is difficult to explain. However, work published in 2004 by Camperio Ciani and collaborators indicated that females in the maternal line of male homosexuals were more fertile than other women.

This led the team to consider sexually antagonistic selection to provide an explanation. In this type of selection, a reproductive advantage is experienced by one sex while a reproductive disadvantage occurs in the other sex. Previously, this sort of evolution has been documented in insects, birds, and some mammals, but it has never been seen in humans.

A large set of models were examined by the researchers and excluded individually if they implied that alleles would go extinct too easily or overtake the population. The paper concluded that the only model that fit the empirical data was based on sexually antagonistic selection, based in particular on two genes, at least one of which must be on the X chromosome, which determines the maternal genes in male babies. This model implies that there is an interaction between male homosexuality and increased female fertility. This complex dynamic results in the maintenance of male homosexuality at a stable but low frequency, as well as a hereditary effect on male homosexuality through the female line.

This model could potentially change the focus of opinions on male homosexuality. For instance, perhaps homosexuality should not be seen as a trait that is detrimental to a population because of the reduced male reproduction it implies, but rather in context of providing gender specific benefits by promoting female fertility. This could be an explanation for the evolutionary origin of this genetic trait in humans.

Sexually antagonistic characteristics are only just being widely recognized in the human population. It is understood as one of the key mechanisms by which higher levels of genetic variation can be maintained in populations. This could be the first example of many potentially sexually antagonistic traits to be found in humans. This in particular could help create better understanding of the many genetically based sexual conflicts in humans, most of which are as of yet unexplained.

Notably, if the genetic mechanism behind male homosexuality is as described in this model, there are interesting implications on the overall fertility of a population. That is, the proportion of male homosexuals in a population could signal a corresponding proportion of females with higher fecundity — this alone could account for a positive net increase in the fertility of a whole population when compared to populations without such a system. This increase will become higher as the population baseline fertility decreases, meaning that these genes could provide a buffering effect on factors that would otherwise lower the overall fertility of a population.

Sexually Antagonistic Selection in Human Male Homosexuality.
Camperio Ciani A, Cermelli P, Zanzotto G
PLoS ONE 3(6): e2282.
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Written by Anna Sophia McKenney