Abstract

Schistosomes, the human parasites responsible for snail fever, are female-heterogametic. Different parts of their ZW sex chromosomes have stopped recombining in distinct lineages, creating “evolutionary strata” of various ages. Although the Z-chromosome is well characterized at the genomic and molecular level, the W-chromosome has remained largely unstudied from an evolutionary perspective, as only a few W-linked genes have been detected outside of the model species Schistosoma mansoni. Here, we characterize the gene content and evolution of the W-chromosomes of S. mansoni and of the divergent species S. japonicum. We use a combined RNA/DNA k-mer based pipeline to assemble around 100 candidate W-specific transcripts in each of the species. About half of them map to known protein coding genes, the majority homologous to S. mansoni Z-linked genes. We perform an extended analysis of the evolutionary strata present in the two species (including characterizing a previously undetected young stratum in S. japonicum) to infer patterns of sequence and expression evolution of W-linked genes at different time points after recombination was lost. W-linked genes show evidence of degeneration, including high rates of protein evolution and reduced expression. Most are found in young lineage-specific strata, with only a few high expression ancestral W-genes remaining, consistent with the progressive erosion of nonrecombining regions. Among these, the splicing factor u2af2 stands out as a promising candidate for primary sex determination, opening new avenues for understanding the molecular basis of the reproductive biology of this group. Keywords: sex chromosomes, evolutionary strata, W-linked gene, sex determining gene, schistosome parasites.

Highlights

  • Separate sexes are frequently determined by a specialized pair of sex chromosomes (Charlesworth et al 2005) called X and Y in species where males are heterogametic, and Z and W when females comprise the heterogametic sex (Bull1983)

  • Loss of recombination can progressively spread to larger sections of the chromosome, yielding “evolutionary strata” that have started degenerating at different time points

  • In which male and female genomic reads are broken into shorter segments (k-mers), and k-mers found in only one sex are used to identify Y/W

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Summary

Introduction

Separate sexes are frequently determined by a specialized pair of sex chromosomes (Charlesworth et al 2005) called X and Y in species where males are heterogametic (e.g. in mammals), and Z and W when females comprise the heterogametic sex (e.g. in birds) (Bull1983). Sex chromosomes arise from chromosomes containing sex-determining genes when parts of the sex-specific chromosome lose the ability to recombine (Ohno 1967; Nei 1969). Inefficient selection on this newly non-recombining Y or W chromosomal region results in the accumulation of repetitive sequences and deleterious mutations, eventually leading to extensive gene loss (Bachtrog 2013). Ancient Y/W chromosomes, such as those of mammals and birds, are typically gene-poor and heterochromatic Some genes, such as those responsible for sex-determination or sexual differentiation, as well as dosage-sensitive genes, can be preserved for large periods of time (Lahn et al 2001; Charlesworth et al 2005). Identifying genes on these chromosomes can be an important step towards understanding the mechanisms underlying differences between the sexes (Lahn et al 2001; Bellott et al 2014)

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