Abstract

Introgression is increasingly recognized as a source of genetic diversity that fuels adaptation. Its role in the evolution of sex chromosomes, however, is not well known. Here, we confirm the hypothesis that the Y chromosome in the ninespine stickleback, Pungitius pungitius, was established by introgression from the Amur stickleback, P. sinensis. Using whole genome resequencing, we identified a large region of Chr 12 in P. pungitius that is diverged between males and females. Within but not outside of this region, several lines of evidence show that the Y chromosome of P. pungitius shares a most recent common ancestor not with the X chromosome, but with the homologous chromosome in P. sinensis. Accumulation of repetitive elements and gene expression changes on the new Y are consistent with a young sex chromosome in early stages of degeneration, but other hallmarks of Y chromosomes have not yet appeared. Our findings indicate that porous species boundaries can trigger rapid sex chromosome evolution.

Highlights

  • New sex chromosomes are typically thought to originate by mutation, for instance with the transposition of a sex determining gene to an autosome

  • Reads were mapped to the reference genome of the threespine stickleback (Gasterosteus aculeatus) (Glazer et al 2015). (The chromosome numbering used throughout the manuscript refers this reference genome.) The sequences were phased bioinformatically (Browning and Browning 2007)

  • We did not find any evidence of an sex determining region (SDR) in sinensis or tymensis, either on Chr 12 or elsewhere in their genomes

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Summary

Introduction

New sex chromosomes are typically thought to originate by mutation, for instance with the transposition of a sex determining gene to an autosome (van Doorn and Kirkpatrick 2007; Vicoso and Bachtrog 2013). Based on several analyses using the microsatellites, she concluded that the Y chromosome in P. pungitius is derived from P. sinensis This situation is all the more intriguing because P. sinensis is thought to have a ZW sex determination system (Natri 2015). We confirm that the large segment of Chromosome 12 that corresponds to the putative inversion is the sex determining region in pungitius. This region is unique in the genome: it is highly diverged between males and females, and has gene trees whose topologies are characteristic of X and Y chromosomes. Examination of the new Y chromosome indicates it is in a very early stage of degeneration, and has evolved regulatory differences from the X that contribute to sex-specific gene expression

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