Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis

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. How can males and females of the same species be so different, despite sharing the same genes? Several explanations for this question rely on the presence of sex-specific chromosomes (XY or ZW), but this is not always the case. Wasps lack sex chromosomes; individuals that carry a single copy of the genome develop into males, while individuals that carry two copies develop into females. Since male and female wasps have the same set of genes, differences between the sexes must be caused by different uses of the same genes (bias) between sexes. We thus choose to study how sex-biased gene networks work and evolve in wasps. We detect bias across several gene-gene interactions at the earliest stages of development, when few individual genes are biased. This suggests that bias in the balance between genes, rather than bias in individual genes, can trigger developmental differences between sexes. We also find that potential regulatory genes in sex-biased networks evolve faster than regulators in networks that are shared between males and females. Together, our findings suggest that re-wiring interactions in gene networks play a key role in the functioning and evolution of differences between sexes.