Partial sex linkage and linkage disequilibrium on the guppy sex chromosome

Abstract

The guppy Y chromosome has been considered a model system for the evolution of suppressed recombination between sex chromosomes, and it has been proposed that complete sex-linkage has evolved across about 3 Mb surrounding the sex-determining locus of this fish, followed by recombination suppression across a further 7 Mb of the 23 Mb XY pair, forming younger evolutionary strata. Sequences of the guppy genome show that Y is very similar to the X chromosome, making it important to understand which parts of the Y are completely non-recombining, and whether there is indeed a large completely non-recombining region. Here, we describe new evidence that supports a different interpretation of the data that suggested the presence of such a region. We analysed PoolSeq data in samples from multiple natural populations from Trinidad. This yields evidence for linkage disequilibrium (LD) between sequence variants and the sex-determining locus. Downstream populations have higher diversity than upstream ones (which display the expected signs of bottlenecks). The associations we observe conform to predictions for a genome region with infrequent recombination that carries one or more sexually antagonistic polymorphisms. They also suggest the region in which the sex-determining locus must be located. However, no consistently male-specific variants were found, supporting the suggestion that any completely sex-linked region may be very small.

Comparison of methodological approaches to the study of young sex chromosomes: A case study in Poecilia

“…reticulata data, and although they did uncover a pattern that is broadly consistent with Stratum II, it was not statistically different across populations (Charlesworth et al, 2020 ). Qiu et al ( 2022 ) and Fraser et al ( 2020 ) identified small male‐specific regions largely consistent with the regions identified by Almeida et al ( 2021 ). However, because of scaffold orientation differences and population‐specific inversions, the male‐specific regions in Fraser et al ( 2020 ) are in different physical locations on the X chromosome.…”

“…(2019) did not report evidence for Stratum I in their own P. reticulata data, and although they did uncover a pattern that is broadly consistent with Stratum II, it was not statistically different across populations (Charlesworth et al, 2020). Qiu et al (2022) and Fraser et al…”

Sex Chromosome Heteromorphism and the Fast-X Effect in Poeciliids

“…Previous work has indicated that P. reticulata and P. wingei share the same male-heterogametic sex chromosome system (Nanda et al 2014; Morris et al 2018; Darolti et al 2019). Analyses of coverage differences between males and females indicate that Y degeneration is restricted to the distal end of the sex chromosomes, in a region ancestral to P. reticulata and P. wingei (designated as Stratum I) (Wright et al 2017; Darolti et al 2019; Darolti et al 2020; Fraser et al 2020; Qiu et al 2022), and suggest that Y degeneration is slightly more exaggerated in P. wingei compared to P. reticulata . This nonrecombining region coincides with the previously mapped location of the sex determining region in P. reticulata (Winge 1922; Winge 1927; Winge and Ditlevsen 1947; Traut and Winking 2001; Tripathi et al 2009) and is also found across six natural guppy populations from Trinidad (Almeida et al 2021).…”

The Development of Genetic Sex Identification Markers and Evidence of a Male Heterogametic Sex Determination System in Red Shiner

“…This lineage specificity is a testament to the many polymorphisms that can surround potential sex-determining regions and the frequency of sex chromosome recombination and turnovers that can occur in species with homomorphic sex chromosomes (Gamble et al 2015;Brelsford et al 2017;Palmer et al 2019). Incomplete linkage disequilibrium and recombination often stop evolutionary strata from developing in the sex-determining chromosomes (Palmer et al 2019;Qiu et al 2022), which can prevent allelic fixation in a sex and result in only partially sex-linked markers. In addition, variance in the concordance of a putatively sex-linked marker with phenotype can be due to deletions, insertions, mutations, and null alleles that occur on or near sex-linked loci (Volff and Schartl 2001;Gao et al 2010;Fontaine et al 2017).…”

“…2019; Qiu et al. 2022), which can prevent allelic fixation in a sex and result in only partially sex‐linked markers. In addition, variance in the concordance of a putatively sex‐linked marker with phenotype can be due to deletions, insertions, mutations, and null alleles that occur on or near sex‐linked loci (Volff and Schartl 2001; Gao et al.…”