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

Abstract

Although the mechanisms driving genome size evolution are not yet fully understood, one potentially important factor is the dynamics of the accumulation of transposable elements (TEs). Since most TEs are neutral or slightly deleterious, a negative correlation between genome size and the efficacy of selection is expected. However, previous empirical studies on closely related species with distinct life history traits (thought to undergo different selective regimes) have yielded inconsistent results. Here, we perform the first large-scale analysis of the effect of genetic drift on genome size evolution, without any prior assumption on the amount of genetic 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 the efficacy of selection (using dN/dS ratios of non-synonymous to synonymous divergence). Using an integrative approach that controls for shared evolutionary history, we reveal that genome-wide dN/dS are strongly positively correlated with genome size and TE content, particularly in GC-poor genes. This study suggests the critical importance of controlling for heterogeneity in base composition when estimating dN/dS. Furthermore, we emphasize that the lack of evidence for TE accumulation due to increased genetic drift in several previous studies may be due to a secondary effect of changes in life history traits (i.e. asexuality) 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.