Relaxed purifying selection is associated with an accumulation of transposable elements in flies

Abstract

Although the mechanisms driving the evolution of genome size are not yet fully understood, one potentially important factor is the dynamics of the accumulation of mobile selfish genetic elements called transposable elements (TEs). Since most of these sequences are neutral or slightly deleterious, a negative correlation between genome size and selection efficacy is expected. However, previous studies based on empirical data from closely related species with contrasting life history traits (thought to result in contrasting levels of selection efficacy) have yielded inconsistent results, leaving this issue controversial. In this study, we perform the first large-scale analysis of the effect of drift on genome size evolution, without any prior assumption about the amount of drift in each sampled species. 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). We highlight a strong phylogenetic inertia in genome size and confirm that TEs are the major components of genome size. 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 evolutionary rates and genome size. Furthermore, our review of previous studies reveals that the absence of evidence for TE accumulation in association with increased genetic drift 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 and genetic drift increases, shedding new light on the role of transposable elements and genetic drift in the evolution of genome architecture.