The large‐X effect in plants: increased species divergence and reduced gene flow on the Silene X‐chromosome

Abstract

The disproportionately large involvement of the X-chromosome in the isolation of closely related species (the large-X effect) has been reported for many animals, where X-linked genes are mostly hemizygous in the heterogametic sex. The expression of deleterious recessive mutations is thought to drive the frequent involvement of the X-chromosome in hybrid sterility, as well as to reduce interspecific gene flow for X-linked genes. Here, we evaluate the role of the X-chromosome in the speciation of two closely related plant species - the white and red campions (Silene latifolia and S. dioica) - that hybridize widely across Europe. The two species evolved separate sexes and sex chromosomes relatively recently (~10(7) years), and unlike most animal species, most X-linked genes have intact Y-linked homologs. We demonstrate that the X-linked genes show a very small and insignificant amount of interspecific gene flow, while gene flow involving autosomal loci is significant and sufficient to homogenize the gene pools of the two species. These findings are consistent with the hypothesis of the large-X effect in Silene and comprise the first report of this effect in plants. Nonhemizygosity of many X-linked genes in Silene males indicates that exposure of recessive mutations to selection may not be essential for the occurrence of the large-X effect. Several possible causes of the large-X effect in Silene are discussed.

Recombination changes at the boundaries of fully and partially sex-linked regions between closely related Silene species pairs

“…On the basis of all site types, divergence is invariably low, and the PAR genes studied here have mean net divergence D a of 0.25%, and include no fixed differences between the species, while shared variants are common, similar to the published results for autosomal and X-linked genes (Supplementary Table S2), and consistent with incomplete isolation between the two species. Net divergence D a ranges from only 0.55% for 20 autosomal genes (Muir et al, 2012), or 0.27% in a larger sample of genes recently studied in three populations of each species (Hu and Filatov, 2015), to 0.51% for X-linked genes (Hu and Filatov, 2015). K ST values for the six PAR genes studied here nevertheless indicate differentiation between S. latifolia and S. dioica (Supplementary Table S2).…”

“…The S. dioica XY chromosomes are homologous with those of S. latifolia (Nicolas et al, 2005), and have indistinguishable morphology and arm ratios (Grabowska-Joachimiak and Joachimiak, 2002). The two species hybridize readily, producing fertile progeny, consistent with nonrearranged chromosomes, and there is evidence for ongoing gene flow (Muir et al, 2012;Hu and Filatov, 2015). If the translocation events outlined above occurred in a common ancestor of these species and directly suppressed recombination between the added regions and the MSY region, the PAR boundary genes should also show close linkage to the MSY in S. dioica.…”

“…In S. dioica, we detected no variation in E521, despite testing several pairs of PCR primers to exclude the possibility that a highly diverged allele is present and is not amplified. Excluding E521, whose low diversity in S. dioica will increase K ST , the mean K ST value for the five other PAR genes studied here is 0.084 (with 95% confidence intervals 0.034-0.128), versus the estimated values of 0.154 for autosomal genes, or 0.381 for X-linked genes (Hu and Filatov, 2015).…”

“…However, the difference we find between S. latifolia and S. dioica cannot be explained by an N e difference. The estimated silent site nucleotide diversity values for autosomal genes differ very slightly between S. latifolia and S. dioica, based on estimates from large numbers of genes (Hu and Filatov, 2015). Diversity estimates for silent sites are most appropriate for assessing effective population sizes, and the largest difference in such diversity estimates so far published is 7% (in the estimated value of π in Muir et al (2012)), which is too small to explain the observed difference in associations of variants in the PAR boundary genes with the MSY between S. latifolia and S. dioica (the alternative diversity estimate in the same paper, Watterson's theta, yielded a slight difference in the opposite direction).…”

Genetic Diversity on the Sex Chromosomes

“…2011). Curiously, however, introgression is reduced on the Silene X chromosome, relative to the autosomes, between S. latifolia and S. dioica , suggesting that the large-X effect is also acting in plants (Hu and Filatov 2016; Box1), although its expected effects on diversity have not been investigated.…”