Abstract
A variety of social, developmental, biological and genetic factors influence sexual orientation in males. Thus, several hypotheses have attempted to explain the sustenance of genetic factors that influence male homosexuality, despite decreased fecundity within the homosexuals. Kin selection, the existence of maternal effects and two forms of balancing selection, sexually antagonistic selection and overdominance, have been proposed as compensatory mechanisms for reduced homosexual fecundity. Here, we suggest that the empirical support for kin selection and maternal effects cannot account for the low universal frequency and stability of the distribution of homosexuals. To identify the responsible compensatory mechanism, we analyzed fecundity in 2,100 European female relatives, i.e., aunts and grandmothers, of either homosexual or heterosexual probands who were matched in terms of age, culture and sampling strategy. Female relatives were chosen to avoid the sampling bias of the fraternal birth order effect, which occurs when indirectly sampling mothers though their homosexual sons. We observed that the maternal aunts and grandmothers of homosexual probands were significantly more fecund compared with the maternal aunts and maternal grandmothers of the heterosexual probands. No difference in fecundity was observed in the paternal female lines (grandmothers or aunts) from either of the two proband groups. Moreover, due to the selective increase in maternal female fecundity, the total female fecundity was significantly higher in homosexual than heterosexual probands, thus compensating for the reduced fecundity of homosexuals. Altogether, these data support an X-linked multi-locus sexually antagonistic hypothesis rather than an autosomal multi-locus overdominance hypothesis.
Highlights
The origin and causes of male homosexuality remain largely debated, and several mechanisms have been proposed to explain this condition
Research Question The aims of this study are to determine the balancing selection mechanisms, if any, which allow the persistence of genetic factors that influence male homosexuality in the population
To match for, religious, ethnic and socio-cultural variables that might influence the demography, the subjects were recruited from various associations for homosexual men, such as discotheques and beaches, and the heterosexual proband control group was sampled from after-work clubs, discotheques, and beaches located in the same geographical region, controlling for the ages of the subjects
Summary
The origin and causes of male homosexuality remain largely debated, and several mechanisms have been proposed to explain this condition. The evidence-based assumption of even a partial genetic predisposition for homosexuality in males generates evolutionary questions and presents several factors that contradict the Darwinian assumption that natural selection should progressively eliminate factors reducing individual fecundity and fitness. This contradiction results in a Darwinian paradox because homosexual men are less fecund and produce fewer offspring than heterosexual men. Studies on homosexual brothers employing DNA linkage analyses suggest an increased rate of homosexuality in the maternal line [10] This conclusion has prompted the comparison of X-chromosomes in brothers, which can only be maternally inherited. It is well accepted that homosexual males reproduce significantly less than their heterosexual counterparts [17,18,19]
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