Abstract

Sexual dimorphism requires regulation of gene expression in developing organisms. These developmental differences are caused by differential expression of genes and isoforms. The effect of expressing a gene is also influenced by which other genes are simultaneously expressed (functional interactions). However, few studies have described how these processes change across development. We compare the dynamics of differential expression, isoform switching and functional interactions in the sexual development of the model parasitoid wasp Nasonia vitripennis, a system that permits genome wide analysis of sex bias from early embryos to adults. We find relatively little sex-bias in embryos and larvae at the gene level, but several sub-networks show sex-biased functional interactions in early developmental stages. These networks provide new candidates for hymenopteran sex determination, including histone modification. In contrast, sex-bias in pupae and adults is driven by the differential expression of genes. We observe sex-biased isoform switching consistently across development, but mostly in genes that are already differentially expressed. Finally, we discover that sex-biased networks are enriched by genes specific to the Nasonia clade, and that those genes possess the topological properties of key regulators. These findings suggest that regulators in sex-biased networks evolve more rapidly than regulators of other developmental networks.

Highlights

  • Sexual differentiation during development involves many genes that are shared between sexes and must be caused by different use of the same genes

  • We present an investigation of sex biased gene expression and co-expression from early development to adulthood in an insect

  • We make a first detailed comparison of the interplay between gene expression and isoform switching over Nasonia’s sexual development, and note that sex-biased isoform switching is in most cases present in loci that already show sex-biased gene expression

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Summary

Introduction

Sexual differentiation during development involves many genes that are shared between sexes (i.e. genes on the autosomes) and must be caused by different use of the same genes. Numerous organisms lack sex-chromosomes altogether, demonstrating that genes located exclusively on sex-specific chromosomes are not necessary for the evolution of phenotypic differences between sexes [1,10,11,12,13,14]. Phenotypic differences between sexes seem to evolve whenever the selective pressures between the two are different (sexually antagonistic selection or conflict, see [15,16,17,18]). Characterizing differences in gene expression throughout the development of sexually dimorphic phenotypes is necessary to understand the regulatory variation that enables phenotypic diversification when selection on genes differ in males and females (i.e. there are conflicting selection pressures)

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