Comparative genomics of 77 species of Drosophila
Although the mechanisms driving genome size evolution are not yet fully understood, one potentially important factor is the dynamics of accumulation of transposable elements (TEs). Since most of them are neutral or slightly deleterious, a negative correlation between genome size and selection efficacy is expected. However, previous empirical studies on closely related species with contrasted life history traits (thought to undergo contrasted selection efficacies) have yielded inconsistent results. Here, we perform the first large-scale analysis of the effect of drift on genome size evolution, without any prior assumption on the amount of drift. We reconstructed a phylogeny based on whole-genome data (2,242 genes) for 77 Drosophilid species to examine correlations between genome size, TE content, and measures of selection efficacy (especially using dN/dS ratios of non-synonymous to synonymous divergence). Using an integrative approach that controls for shared history, we find that genome-wide dN/dS are strongly positively correlated with genome size and TE content, particularly in GC-poor genes. This study highlights the critical importance of controlling for heterogeneity in base composition when testing the controversial correlation between dN/dS and genome size. Furthermore, we performed a literature review highlighting that the absence of evidence for TE accumulation in association with increased genetic drift in previous studies may be attributed to a secondary effect of changes in life history traits on TE dynamics. In conclusion, this work provides evidence for TE proliferation in fly genomes when purifying selection is reduced, shedding new light on the role of TEs and genetic drift in the evolution of genome architecture.