RAD mapping reveals an evolving, polymorphic and fuzzy boundary of a plant pseudoautosomal region

Abstract

How loss of genetic exchanges (recombination) evolves between sex chromosomes is a long-standing question. Suppressed recombination may evolve when a sexually antagonistic (SA) polymorphism occurs in a partially sex-linked 'pseudoautosomal' region (or 'PAR'), maintaining allele frequency differences between the two sexes, and creating selection for closer linkage with the fully sex-linked region of the Y chromosome in XY systems, or the W in ZW sex chromosome systems. Most evidence consistent with the SA polymorphism hypothesis is currently indirect, and more studies of the genetics and population genetics of PAR genes are clearly needed. The sex chromosomes of the plant Silene latifolia are suitable for such studies, as they evolved recently and the loss of recombination could still be ongoing. Here, we used RAD sequencing to genetically map sequences in this plant, which has a large genome (c. 3 gigabases) and no available whole-genome sequence. We mapped 83 genes on the sex chromosomes, and comparative mapping in the related species S. vulgaris supports previous evidence for additions to an ancestral PAR and identified at least 12 PAR genes. We describe evidence that recombination rates have been reduced in meiosis of both sexes, and differences in recombination between S. latifolia families suggest ongoing recombination suppression. Large allele frequency differences between the sexes were found at several loci closely linked to the PAR boundary, and genes in different regions of the PAR showed striking sequence diversity patterns that help illuminate the evolution of the PAR.

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

“…The genes near the S. latifolia PAR boundary represent a much more recent translocation situation than that in mammals, and are ideal for testing whether the PAR-MSY boundary has remained in the same location. Close linkage observed between the S. latifolia MSY and genes from both addition events (Qiu et al, 2016) suggests recombination suppression after the translocations occurred (other genes added in both translocations, have remained loosely linked to the MSY boundary). However, although the translocations should not directly suppress recombination in the PAR boundary region, it is important to test this alternative.…”

“…In the plant S. latifolia, recombination suppression between the fully Y-and X-linked regions was initiated around 5-10 myr ago, but at least one region evolved suppressed recombination subsequently, forming a younger fully Y-linked male-specific (MSY) region (Bergero et al, 2007;Chibalina and Filatov, 2011). By comparing the genetic map of the S. latifolia X chromosome with mapping results in the related species Silene vulgaris, which does not have sex chromosomes, the S. latifolia PAR was inferred to have been formed by independent additions of two genomic regions to an ancestral PAR, through translocations from other chromosomes, as shown in Figure 1 Qiu et al, 2016). Several genes located near the boundary with the fully sex-linked region recombine so rarely that some variants are found only in males (Qiu et al, 2016); among these PAR boundary genes, some were added in one addition event and some in the other (Figure 1).…”

“…By comparing the genetic map of the S. latifolia X chromosome with mapping results in the related species Silene vulgaris, which does not have sex chromosomes, the S. latifolia PAR was inferred to have been formed by independent additions of two genomic regions to an ancestral PAR, through translocations from other chromosomes, as shown in Figure 1 Qiu et al, 2016). Several genes located near the boundary with the fully sex-linked region recombine so rarely that some variants are found only in males (Qiu et al, 2016); among these PAR boundary genes, some were added in one addition event and some in the other (Figure 1). …”

“…Rather than genetically mapping these genes, we used a highly sensitive population genetic approach, testing for associations between single-nucleotide polymorphisms in the PAR boundary loci and the male-determining region, using the subdivision measure K ST between males and females. K ST is the average F ST per site, computed from sequence data (Hudson Figure 1 Evolution of S. latifolia PAR, showing the origins of the PAR boundary genes studied in this paper (simplified from Figure 4 of Qiu et al (2016), and including gene locations only for these PAR boundary genes). (a) The ancestral state before the translocation events had a sex chromosome with a PAR (green region) and a region that had stopped recombining (black region, but not as separate X-linked and male-specific, or MSY, regions; different strata are not indicated in this diagram, but the black line includes all fully sex-linked regions).…”

“…et al, 1992), and reflects linkage disequilibrium due to population subdivision (Charlesworth et al, 1997), such as Y-X differentiation resulting from absent or very rare recombination. F ST has already been proposed as the best way to test for associations between alleles of partially sex-linked genes and a fully sex-linked locus (Qiu et al, , 2016Kirkpatrick and Guerrero, 2014). Importantly, this can potentially detect recombination even if it is too rare to be detectable in families, as is the case in S. latifolia for the PAR boundary loci studied here (Qiu et al, 2016).…”