Sequence diversity patterns suggesting balancing selection in partially sex‐linked genes of the plant Silene latifolia are not generated by demographic history or gene flow

Abstract

DNA sequence diversity in genes in the partially sex-linked pseudoautosomal region (PAR) of the sex chromosomes of the plant Silene latifolia is higher than expected from within-species diversity of other genes. This could be the footprint of sexually antagonistic (SA) alleles that are maintained by balancing selection in a PAR gene (or genes) and affect polymorphism in linked genome regions. SA selection is predicted to occur during sex chromosome evolution, but it is important to test whether the unexpectedly high sequence polymorphism could be explained without it, purely by the combined effects of partial linkage with the sex-determining region and the population's demographic history, including possible introgression from Silene dioica. To test this, we applied approximate Bayesian computation-based model choice to autosomal sequence diversity data, to find the most plausible scenario for the recent history of S. latifolia and then to estimate the posterior density of the most relevant parameters. We then used these densities to simulate variation to be expected at PAR genes. We conclude that an excess of variants at high frequencies at PAR genes should arise in S. latifolia populations only for genes with strong associations with fully sex-linked genes, which requires closer linkage with the fully sex-linked region than that estimated for the PAR genes where apparent deviations from neutrality were observed. These results support the need to invoke selection to explain the S. latifolia PAR gene diversity, and encourage further work to test the possibility of balancing selection due to sexual antagonism.

Population genetics of sexual conflict in the genomic era

“…Partial sex-linkage is predicted to lead to more sexually antagonistic alleles 72,77,78 than expected for autosomal regions, but fewer than expected for fully sex-linked regions. Consistent with this prediction, population genetic approaches have shown that there is evidence of increased variation (Tajima's D) for genes on the PAR of Silene latifolia, a dioecious plant 40,41 , which is presumably the result of balancing selection from sexual conflict. Preliminary data from studies of guppies is consistent with the Silene results 54 , suggesting this pattern might be a widespread.…”

“…Provisional data generated using this method suggests that a substantial proportion of the genome is subject to sexual conflict 29 which may exert a constraint on the evolution of sexual dimorphism. Published studies show that putative sexually antagonistic loci are distributed non-randomly across different genomic regions 40,41 , which is discussed further below.…”

“…Preliminary 29 and published studies 25,38,40,41 of sexual conflict have measured nucleotide diversity with Tajima's D (Box 2), which estimates the proportion of nucleotide sites in a given sequence that are polymorphic within a population. This approach is based on the assumption that balancing selection from sexual conflict will lead to the maintenance of multiple alleles, which will in turn cause higher than expected levels of sequence diversity compared to regions not under balancing selection.…”

“…Provisional data generated using this method suggests that a substantial proportion of the genome is subject to sexual conflict 29 which may exert a constraint on the evolution of sexual dimorphism. Published studies show that putative sexually antagonistic loci are distributed non-randomly across different genomic regions 40,41 , which is discussed further below.This technique gives little insight into the source of sexual conflict, as nucleotide diversity alone cannot distinguish sexual conflict over reproductive fitness from conflict over viability or survival (Fig. 2).…”

Recombination provides evidence for ancient hybridisation in the Silene aegyptiaca (Caryophyllaceae) complex

“…These are expected to result in intrinsic genetic isolation fairly early in the speciation continuum, such that secondary contact is unlikely to result in gene flow (Coyne and Orr 2004;Seehausen et al 2014;Nosil et al 2008;Servedio et al 2011;Muir et al 2012;Guirao-Rico et al 2017). Given that hybridisation appears to be the cause of recombination (either in vivo or in vitro) in these Silene individuals, and that the species involved are distinct (Toprak et al 2016), it appears that secondary contact has resulted in some but limited gene flow.…”