A test of genetic models for the evolutionary maintenance of same-sex sexual behaviour

Abstract

The evolutionary maintenance of same-sex sexual behaviour (SSB) has received increasing attention because it is perceived to be an evolutionary paradox. The genetic basis of SSB is almost wholly unknown in non-human animals, though this is key to understanding its persistence. Recent theoretical work has yielded broadly applicable predictions centred on two genetic models for SSB: overdominance and sexual antagonism. Using Drosophila melanogaster, we assayed natural genetic variation for male SSB and empirically tested predictions about the mode of inheritance and fitness consequences of alleles influencing its expression. We screened 50 inbred lines derived from a wild population for male-male courtship and copulation behaviour, and examined crosses between the lines for evidence of overdominance and antagonistic fecundity selection. Consistent variation among lines revealed heritable genetic variation for SSB, but the nature of the genetic variation was complex. Phenotypic and fitness variation was consistent with expectations under overdominance, although predictions of the sexual antagonism model were also supported. We found an unexpected and strong paternal effect on the expression of SSB, suggesting possible Y-linkage of the trait. Our results inform evolutionary genetic mechanisms that might maintain low but persistently observed levels of male SSB in D. melanogaster, but highlight a need for broader taxonomic representation in studies of its evolutionary causes.

Sexually antagonistic selection on genetic variation underlying both male and female same-sex sexual behavior

“…Consistent with our findings, Hoskins et al [ 62 ] recently found an influence of sex-linked genetic variance in male SSB on female fecundity using four inbred lines from the Drosophila Genetic Reference Panel. However, the fact that male reproductive success was not scored made it difficult to assess the relative importance of overdominance versus SA selection in maintaining genetic variance in SSB [ 62 ]. Our data suggest that both shared and sex-limited SSB alleles have strong pleiotropic effects and that sex-limited selection on this behavioral trait can have SA fitness effects via cross-trait intersexual genetic correlations.…”

“…Poor sex recognition can certainly affect rates of male-male mounting and studies in Drosophila provide an emerging understanding of the proximate basis for male SSB via this link (reviewed in: [ 27 , 28 ]). However, recent studies have only begun to uncover the underlying genetic basis of SSB in males [ 36 , 62 ] and the evolution of female SSB remains largely unexplored. Moreover, most previous studies have stopped short of exploring the link between standing genetic variation in SSB and fitness.…”

“…Theoretical work suggests that SSB in both sexes can evolve when alleles that increase fitness in one sex result in SSB in the other [ 37 ]. However, there is little empirical evidence supporting the notion that genetic variation in SSB is related to male or female fitness [ 63 ] (but see: [ 62 ]). In this study, we provided a comprehensive three-step attempt at elucidating the evolution of both male and female SSB in the seed beetle C. maculatus .…”

Testing the role of same-sex sexual behaviour in the evolution of alternative male reproductive phenotypes

“…However, SSB might also play important roles in mediating male competition (Lane, Haughan, Evans, Tregenza, & House 2016;Kuriwada 2017) and increasing relative fitness under sexual selection of males that express it (McRobert and Tompkins, 1988;Steiner, Steidle, & Ruther, 2005;Preston-Mafham, 2006;Bierbach, Jung, Hornung, Streit, & Plath, 2013). Despite these research efforts, little is known about the influence SSB might have upon evolutionary change of other traits (Bailey and Zuk, 2009;Scharf and Martin, 2013;Hoskins, Ritchie, & Bailey, 2015).…”

A prison effect in a wild population: a scarcity of females induces homosexual behaviors in males

“…In captive animals, genetic, anatomical, neurophysiological, or hormonal investigations have failed to identify clear distinctions between the mechanisms that promote SSB versus HSB (Poiani 2010;Hoskins et al 2015). Even in humans, one of the most intensively studied vertebrate species, the abundant efforts to link sexual orientation with anatomy, physiology, and genetic mechanisms have revealed complex and equivocal patterns (Banks and Gartrell 1995;Rice et al 1999;Zitzmann and Nieschlag 2001;Mustanski et al 2002;Jannini et al 2010).…”