Abstract

Modifications in gene expression determine many of the phenotypic differentiations between closely related species. This is particularly evident in reproductive tissues, where evolution of genes is more rapid, facilitating the appearance of distinct reproductive characteristics which may lead to species isolation and phenotypic variation. Large-scale, comparative analyses of transcript expression levels have been limited until recently by lack of inter-species data mining solutions. Here, by combining expression normalisation across lineages, multivariate statistical analysis, evolutionary rate, and protein-protein interaction analysis, we investigate ortholog transcripts in the male accessory glands and testes across five closely related species in the Anopheles gambiae complex. We first demonstrate that the differentiation by transcript expression is consistent with the known Anopheles phylogeny. Then, through clustering, we discover groups of transcripts with tissue-dependent expression patterns conserved across lineages, or lineage-dependent patterns conserved across tissues. The strongest associations with reproductive function, transcriptional regulatory networks, protein-protein subnetworks, and evolutionary rate are found for the groups of transcripts featuring large expression differences in lineage or tissue-conserved patterns.

Highlights

  • Gene expression levels are quantitative molecular traits that link genotype to phenotype through modulation of molecular functions, regulating and affecting cellular and organismal fitness

  • Generation of the male reproductive transcriptome and comparison across species To study the evolutionary dynamics of gene expression in male reproductive tissues across the An. gambiae species complex, we generated transcriptomes of the male accessory glands (MAGs) and testes from five different anopheline mosquitoes: An. gambiae s.s., An. coluzzii, An. arabiensis, An. merus, and An. quadriannulatus

  • Via principal component analysis (PCA) and the construction of expression distance matrices, it was possible to investigate the phylogeny of the Anopheles complex directly from the analysis of expression divergence

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Summary

Introduction

Gene expression levels are quantitative molecular traits that link genotype to phenotype through modulation of molecular functions, regulating and affecting cellular and organismal fitness. Comparative studies focusing on gene expression differences in reproductive tissues of closely related species, where genes evolve rapidly (Swanson & Vacquier, 2002; Nielsen et al, 2005; Clark et al, 2006; Haerty & Singh, 2006; Lemos et al, 2007; Moehring et al, 2007; Turner & Hoekstra, 2008; Sundararajan & Civetta, 2011), provide insights into how genome evolution influences gene expression changes at the tissue, sex, and species-specific level and how such changes are functionally, anatomically, and physiologically integrated into and linked to fitness

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