Abstract

Chromosome rearrangements (CRs) are perceived to be related to sex chromosome evolution, but it is a matter of controversy whether CRs are the initial causative mechanism of suppressed recombination for sex differentiation. The early stages of sex chromosome evolution in amphibians may represent intermediate states of differentiation, and if so, they potentially shed light on the ultimate cause of suppressed recombination and the role of CRs in sex chromosome differentiation. In this paper, we showed that sex determination differs among 16 populations of spiny frog (Quasipaa boulengeri), in which individuals have normal and rearranged chromosomes caused by reciprocal translocation. In eastern areas, without translocation, genetic differentiation between sexes was relatively low, suggesting unrestricted recombination. In comparison, in western populations that have both normal and translocated chromosomes, a male-heterogametic system and lack of X-Y recombination were identified by male-specific alleles and heterozygote excess. However, such genetic differentiation between sexes in western populations was not directly related to karyotypes, as it was found in individuals with both normal and translocated karyotypes. In the western Sichuan Basin, male-specific and translocation-specific allelic frequency distributions suggested that recombination of sex-differentiation ceased in all populations, but recombination suppression caused by translocation did not exist in some populations. Combined with phylogenetic inference, this indicated that the establishment of sex-linkage had taken place independently of reciprocal translocation, and translocation was not the ultimate cause of sex chromosome differentiation. Furthermore, comparison of the genetic diversity of alleles on Y chromosomes, X chromosomes, and autosomes in western populations showed a reduction of effective population size on sex chromosomes, which may be caused by reciprocal translocation. It indicates that, although it is not the ultimate cause of recombination suppression, reciprocal translocation may enhance sex chromosome differentiation.

Highlights

  • A commonly invoked theory explaining the origin of sex chromosomes states that the appearance of a sex-determining gene would make a pair of autosomes become protosex chromosomes (Charlesworth et al, 2005; Bachtrog, 2013)

  • In populations of the western Sichuan Basin, the sex specificity of allelic distributions, the highly negative fixation indices (FIS) value, the high FST value between males and females, and the cluster analyses all showed that these six sex-linked loci were associated with sex and lay on the non-recombining region of sex chromosomes

  • The X and Y chromosomes of Q. boulengeri were differentiated to different degrees and could not recombine freely, leading to stable genetic sex determination (GSD)

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Summary

Introduction

A commonly invoked theory explaining the origin of sex chromosomes states that the appearance of a sex-determining gene would make a pair of autosomes become protosex chromosomes (Charlesworth et al, 2005; Bachtrog, 2013). Empirical studies have highlighted that recombination suppression plays a key role in the evolution of sex chromosomes, eventually leading to the differentiation of the sex chromosomes (Wright et al, 2016). Another model predicts that chromosome rearrangements (CRs) are part of crucial dynamics in sex chromosome differentiation (Ohno, 1967; Miura et al, 2012). Recent studies highlighted that CRs are derived and not the cause of sex chromosome differentiation (Natri et al, 2013; Sun et al, 2017)

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