Abstract

Sex-biased genes are central to the study of sexual selection, sexual antagonism, and sex chromosome evolution. We describe a comprehensive de novo assembled transcriptome in the common frog Rana temporaria based on five developmental stages and three adult tissues from both sexes, obtained from a population with karyotypically homomorphic but genetically differentiated sex chromosomes. This allows the study of sex-biased gene expression throughout development, and its effect on the rate of gene evolution while accounting for pleiotropic expression, which is known to negatively correlate with the evolutionary rate. Overall, sex-biased genes had little overlap among developmental stages and adult tissues. Late developmental stages and gonad tissues had the highest numbers of stage- or tissue-specific genes. We find that pleiotropic gene expression is a better predictor than sex bias for the evolutionary rate of genes, though it often interacts with sex bias. Although genetically differentiated, the sex chromosomes were not enriched in sex-biased genes, possibly due to a very recent arrest of XY recombination. These results extend our understanding of the developmental dynamics, tissue specificity, and genomic localization of sex-biased genes.

Highlights

  • Sexual dimorphism is almost ubiquitous in sexual organisms

  • We have analyzed genes that are differentially expressed between the sexes in terms of (a) their tissue specificity, (b) their progression and turnover during embryonic development and adulthood, (c) their rate of evolution, and (d) their enrichment on sex chromosomes

  • We have found that the global transcriptome profiles primarily clustered by tissue or developmental stage, and less by sex

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Summary

Introduction

Sexual dimorphism is almost ubiquitous in sexual organisms. The genetic basis underlying sex differences often involves many genes and is very complex [1]. Males and females share the majority of their genome, which creates intralocus conflicts at many genes [2]. Differential gene expression between the sexes is an important mechanism for the resolution of intralocus conflicts and is responsible for the majority of sex-specific phenotypes [2,3]. Differences in gene expression influence the variation in the degree of sexual dimorphism, as elegantly demonstrated by the transcriptomic comparison between subordinate and dominant male turkeys [4]. Sex-biased gene expression is widespread in animals [5,6,7,8,9,10]

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