Abstract

Sex chromosomes evolve once recombination is halted between a homologous pair of chromosomes. The dominant model of sex chromosome evolution posits that recombination is suppressed between emerging X and Y chromosomes in order to resolve sexual conflict. Here we test this model using whole genome and transcriptome resequencing data in the guppy, a model for sexual selection with many Y-linked colour traits. We show that although the nascent Y chromosome encompasses nearly half of the linkage group, there has been no perceptible degradation of Y chromosome gene content or activity. Using replicate wild populations with differing levels of sexually antagonistic selection for colour, we also show that sexual selection leads to greater expansion of the non-recombining region and increased Y chromosome divergence. These results provide empirical support for longstanding models of sex chromosome catalysis, and suggest an important role for sexual selection and sexual conflict in genome evolution.

Highlights

  • Sex chromosomes evolve once recombination is halted between a homologous pair of chromosomes

  • Our results suggest that recombination suppression between the X and Y spread quickly in the recent history of this sex chromosome system, possibly driven by the presence of sexually antagonistic alleles related to sexual selection

  • We used individuals from natural and laboratory populations in conjunction with analysis of coverage, single nucleotide polymorphisms (SNPs) and expression differences between males and females in this model system to test the role of sexual conflict in recombination suppression between the X and Y chromosomes

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Summary

Introduction

Sex chromosomes evolve once recombination is halted between a homologous pair of chromosomes. Using replicate wild populations with differing levels of sexually antagonistic selection for colour, we show that sexual selection leads to greater expansion of the non-recombining region and increased Y chromosome divergence These results provide empirical support for longstanding models of sex chromosome catalysis, and suggest an important role for sexual selection and sexual conflict in genome evolution. Colour is sexually antagonistic in guppies, as brightly coloured males are more attractive to females and more visible to predators, but brightly coloured females gain no fitness advantage and only suffer increased predation[10,11,12] In this system, current models of sex chromosome evolution predict that recombination would be selected against between the sex determining locus and linked loci involved in colouration. Because many vertebrate sex chromosomes show progressive spread of the non-recombining region[18,19,20,21], the large size of the guppy non-recombining region and male-specific regions suggest substantial divergence between the X and Y

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