Chromosomal Context Affects the Molecular Evolution of Sex-linked Genes and Their Autosomal Counterparts in Turtles and Other Vertebrates

Abstract

Sex chromosomes evolve differently from autosomes because natural selection acts distinctly on them given their reduced recombination and smaller population size. Various studies of sex-linked genes compared with different autosomal genes within species support these predictions. Here, we take a novel alternative approach by comparing the rate of evolution between subsets of genes that are sex-linked in selected reptiles/vertebrates and the same genes located in autosomes in other amniotes. We report for the first time the faster evolution of Z-linked genes in a turtle (the Chinese softshell turtle Pelodiscus sinensis) relative to autosomal orthologs in other taxa, including turtles with temperature-dependent sex determination (TSD). This faster rate was absent in its close relative, the spiny softshell turtle (Apalone spinifera), thus revealing important lineage effects, and was only surpassed by mammalian-X linked genes. In contrast, we found slower evolution of X-linked genes in the musk turtle Staurotypus triporcatus (XX/XY) and homologous Z-linked chicken genes. TSD lineages displayed overall faster sequence evolution than taxa with genotypic sex determination (GSD), ruling out global effects of GSD on molecular evolution beyond those by sex-linkage. Notably, results revealed a putative selective sweep around two turtle genes involved in vertebrate gonadogenesis (Pelodiscus-Z-linked Nf2 and Chrysemys-autosomal Tspan7). Our observations reveal important evolutionary changes at the gene level mediated by chromosomal context in turtles despite their low overall evolutionary rate and illuminate sex chromosome evolution by empirically testing expectations from theoretical models. Genome-wide analyses are warranted to test the generality and prevalence of the observed patterns.