Abstract

AbstractThe sexes experience different selective pressures, which can lead to highly divergent phenotypes that are achieved via sex‐biased gene expression. The effect of sexual dimorphism on the degree of sex‐bias in gene expression can be studied in species characterized by sexually selected alternative male phenotypes. We analyzed gene expression in the bulb mite Rhizoglyphus robini (Acari, Acaridae), in which more sexually dimorphic, aggressive fighter males, possessing thickened legs of the third pair which are used to kill rivals, coexist with unarmored scrambler males. We sequenced transcriptomes of adult females and both types of males and de‐novo assembled 114,456 transcriptome‐based gene models (TGMs). Significantly more TGMs had male‐biased expression than female‐biased expression. Among TGMs that were over expressed in one, but not both, male morphs (compared to expression in females), we found about four times more fighter‐biased genes than scrambler‐biased genes. This demonstrates that the degree of expression bias reflects the degree of sexually selected dimorphism. However, the number of sex‐biased genes was much higher than the number of genes differentially expressed between male morphs, and most male‐biased genes were shared between morphs, suggesting that selection pressures act similarly on males irrespective of their morph. Furthermore, we found that male‐biased genes evolved at a faster rate than female‐biased genes, as evidenced by a higher rate of both gene‐turnover and amino acid substitution, indicating that sexual selection, acting more strongly on males, accelerates the rate of molecular evolution. Interestingly, gene turnover was relatively higher, but amino acid substitution rate relatively lower among fighter‐biased genes, suggesting that different components of sexual selection may have different effects on the evolution of sex‐biased genes.

Highlights

  • The sexes, which are defined by the types of gametes they produce, experience different selective pressures that often result in highly divergent phenotypes

  • While the sexes may differ with respect to the loci associated with sex chromosomes, divergent phenotypes are mostly achieved by sex-bias in gene expression patterns, defined as the predominant or exclusive expression of genes in one sex

  • We obtained 137,151 transcripts in the original Trinity assembly. These were reduced to 114,456 transcriptome-based gene models (TGMs) after applying the pipeline for merging transcripts likely derived from the same genomic location. 96,826 TGMs were found in fighter males, 100,157 in scrambler males, and 84,600 in females

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Summary

Introduction

The sexes, which are defined by the types of gametes they produce, experience different selective pressures that often result in highly divergent phenotypes. Sexual dimorphism is thought to be driven to a large extent by sexual selection, a process arising from reproductive competition, and leading to the evolution of traits that facilitate access to partners of the opposite sex and their gametes. This process, acting mostly on males, has led to the emergence of a vast diversity of sexually dimorphic traits, such as body size, weapons, sexual ornaments or ejaculate traits (reviewed in Andersson 1994). Reproductive competition sometimes leads to the emergence of alternative reproductive phenotypes in males, where large, often armored, territorial males coexist with less sexually dimorphic phenotypes adopting nonaggressive ways to secure access to females (reviewed in Gross 1996; Brockmann 2001; Oliveira et al 2008)

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