Schistosome W-Linked Genes Inform Temporal Dynamics of Sex Chromosome Evolution and Suggest Candidate for Sex Determination.

Melissa Wilson,Mikhail A Moldovan,Marion A L Picard,Marwan Elkrewi,Beatriz Vicoso

doi:10.1093/molbev/msab178

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

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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