Abstract
Selection is expected to work differently in autosomal and X-linked genes because of their ploidy difference and the exposure of recessive X-linked mutations to haploid selection in males. However, it is not clear whether these expectations apply to recently evolved sex chromosomes, where many genes retain functional X- and Y-linked gametologs. We took advantage of the recently evolved sex chromosomes in the plant Silene latifolia and its closely related species to compare the selective pressures between hemizygous and non-hemizygous X-linked genes as well as between X-linked genes and autosomal genes. Our analysis, based on over 1000 genes, demonstrated that, similar to animals, X-linked genes in Silene evolve significantly faster than autosomal genes—the so-called faster-X effect. Contrary to expectations, faster-X divergence was detectable only for non-hemizygous X-linked genes. Our phylogeny-based analyses of selection revealed no evidence for faster adaptation in X-linked genes compared to autosomal genes. On the other hand, partial relaxation of purifying selection was apparent on the X-chromosome compared to the autosomes, consistent with a smaller genetic diversity in S. latifolia X-linked genes (πx = 0.016; πaut = 0.023). Thus, the faster-X divergence in S. latifolia appears to be a consequence of the smaller effective population size rather than of a faster adaptive evolution on the X-chromosome. We argue that this may be a general feature of “young” sex chromosomes, where the majority of X-linked genes are not hemizygous, preventing haploid selection in heterogametic sex.
Highlights
Sex chromosomes are unusual in many respects, as they are subject to sex-biased inheritance and differences in effective population size (Ne ), ploidy, and recombination rate between the sexes—all of which can affect the evolution of sex-linked genes
To better understand the evolution of sex-linked genes and the role of natural selection in this process, we investigated the patterns of genetic diversity, substitution rates, and natural selection in X-linked and autosomal genes of the dioecious flowering plant Silene latifolia and closely related species which evolved separate sexes [26] and de novo sex chromosomes in the last 11 million years [27]
Our results indicate that the evolution of X-linked genes in S. latifolia and its dioecious relatives is dominated by relaxation of selection due to a smaller effective population size of the X-chromosome compared to the autosomes
Summary
Sex chromosomes are unusual in many respects, as they are subject to sex-biased inheritance and differences in effective population size (Ne ), ploidy, and recombination rate between the sexes—all of which can affect the evolution of sex-linked genes. The molecular evolution of Y (or W)-linked genes is strongly influenced by the lack of recombination, which results in gradual genetic degeneration of the sex-specific chromosome [1]. X (or Z)-linked genes recombine in the homogametic sex, preventing degeneration. X (or Z)-chromosomes do have their fair share of distinctive features [2]. X (or Z)-chromosomes spend two-thirds of the time in the homogametic sex (assuming 50:50 sex ratios), which results in gradual “feminisation”. Of the X-chromosome [3,4,5] and “masculinisation” of the Z-chromosome [6].
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