Abstract
In species with polygenic sex determination (PSD), multiple male- and female-determining loci on different proto-sex chromosomes segregate as polymorphisms within populations. The extent to which these polymorphisms are at stable equilibria is not yet resolved. Previous work demonstrated that PSD is most likely to be maintained as a stable polymorphism when the proto-sex chromosomes have opposite (sexually antagonistic) fitness effects in males and females. However, these models usually consider PSD systems with only two proto-sex chromosomes, or they do not broadly consider the dominance of the alleles under selection. To address these shortcomings, I used forward population genetic simulations to identify selection pressures that can maintain PSD under different dominance scenarios in a system with more than two proto-sex chromosomes (modeled after the house fly). I found that overdominant fitness effects of male-determining proto-Y chromosomes are more likely to maintain PSD than dominant, recessive, or additive fitness effects. The overdominant fitness effects that maintain PSD tend to have proto-Y chromosomes with sexually antagonistic effects (male-beneficial and female-detrimental). In contrast, dominant fitness effects that maintain PSD tend to have sexually antagonistic multi-chromosomal genotypes, but the individual proto-sex chromosomes do not have sexually antagonistic effects. These results demonstrate that sexual antagonism can be an emergent property of the multi-chromosome genotype without individual sexually antagonistic chromosomes. My results further illustrate how the dominance of fitness effects has consequences for both the likelihood that PSD will be maintained as well as the role sexually antagonistic selection is expected to play in maintaining the polymorphism.
Highlights
Sex determination is the developmental process by which a genetic signal or environmental cue initiates sexually dimorphic gene regulatory pathways to produce phenotypically different males and females (Bachtrog et al 2014)
Overdominant fitness effects are the most likely to maintain polygenic sex determination (PSD), with >40% of fitness values maintaining proto-sex chromosomes at a frequency >0.1% after 1000 generations
Recessive, or overdominant fitness effects maintain PSD, there is a broad range of frequencies at which the proto-Y chromosomes (YM and IIIM) can segregate as polymorphisms (Figure 2 and Supplementary Figure S3)
Summary
Sex determination is the developmental process by which a genetic signal or environmental cue initiates sexually dimorphic gene regulatory pathways to produce phenotypically different males and females (Bachtrog et al 2014). Master regulators can be found on sex chromosomes, and the evolutionary transitions of sex determiners can drive turnover of the sex chromosomes (Abbott et al 2017) These evolutionary transitions include a period of polygenic sex determination (PSD), during which multiple master sex-determining loci on different chromosomes segregate as polymorphisms within species (Moore and Roberts 2013). Models that do allow for stable PSD often predict that opposing selection pressures in males and females (i.e., sexually antagonistic selection) may be important for maintaining the polymorphism (Bull 1983; Rice 1986; van Doorn and Kirkpatrick 2007; Meisel et al 2016). It is possible that variable selection pressures across heterogeneous environments could maintain PSD (Bateman and Anholt 2017)
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