Shared and Species-Specific Patterns of Nascent Y Chromosome Evolution in Two Guppy Species.

Jake Morris,Alison E Wright,Natasha I Bloch,Judith E Mank,Iulia Darolti

doi:10.3390/genes9050238

Jake Morris, Alison E Wright + Show 3 more

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https://doi.org/10.3390/genes9050238

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Abstract

Sex chromosomes form once recombination is halted around the sex-determining locus between a homologous pair of chromosomes, resulting in a male-limited Y chromosome. We recently characterized the nascent sex chromosome system in the Trinidadian guppy (Poecilia reticulata). The guppy Y is one of the youngest animal sex chromosomes yet identified, and therefore offers a unique window into the early evolutionary forces shaping sex chromosome formation, particularly the rate of accumulation of repetitive elements and Y-specific sequence. We used comparisons between male and female genomes in P. reticulata and its sister species, Endler’s guppy (P. wingei), which share an ancestral sex chromosome, to identify male-specific sequences and to characterize the degree of differentiation between the X and Y chromosomes. We identified male-specific sequence shared between P. reticulata and P. wingei consistent with a small ancestral non-recombining region. Our assembly of this Y-specific sequence shows substantial homology to the X chromosome, and appears to be significantly enriched for genes implicated in pigmentation. We also found two plausible candidates that may be involved in sex determination. Furthermore, we found that the P. wingei Y chromosome exhibits a greater signature of repetitive element accumulation than the P. reticulata Y chromosome. This suggests that Y chromosome divergence does not necessarily correlate with the time since recombination suppression. Overall, our results reveal the early stages of Y chromosome divergence in the guppy.

Highlights

Sex chromosomes, where chromosome complement determines whether an individual develops as a male or female, have evolved independently in many diverse lineages [1,2]
We first assembled male-specific k-mers shared in both species (Y-mers) into contigs, uncovering substantial homology to the X chromosome, consistent with only recent recombination suppression between the two chromosomes. From this Y-mer assembly, we identified a significant enrichment of genes that have been implicated in pigmentation, as well as two plausible candidate genes that may be involved in sex determination
We observed an excess of male-specific k-mers above ~30× coverage in both P. reticulata and P. wingei (Supplementary Figure S1), consistent with small but detectable amounts of male-specific sequence on the Y in both species

Summary

Introduction

Sex chromosomes, where chromosome complement determines whether an individual develops as a male or female, have evolved independently in many diverse lineages [1,2]. In addition to permitting X and Y chromosome divergence, the loss of recombination for the male-specific Y chromosome leads to a range of evolutionary processes, including rapid loss of gene activity, high rates of pseudogenization, and accumulation of repetitive elements [7,11,12,13,14]. These processes can lead to major differences in size and gene content between the X and Y, and in old, highly heteromorphic sex.

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