Effective population size does not explain long-term variation in genome size and transposable element content in animals

Abstract

Animal genomes exhibit a remarkable variation in size, but the evolutionary forces responsible for such variation are still debated. As the effective population size (Ne) reflects the intensity of genetic drift, it is expected to be a key determinant of the fixation rate of nearly-neutral mutations. Accordingly, the Mutational Hazard Hypothesis postulates lineages with low Ne to have bigger genome sizes due to the accumulation of slightly deleterious transposable elements (TEs), and those with high Ne to maintain streamlined genomes as a consequence of a more effective selection against TEs. However, the existence of both empirical confirmation and refutation using different methods and different scales precludes ts general validation. Using high-quality public data, we estimated genome size, TE content and rate of non-synonymous to synonymous substitutions (dN/dS) as Ne proxy for 807 species including vertebrates, molluscs and insects. After collecting available life-history traits, we tested the associations among population size proxies, TE content and genome size, while accounting for phylogenetic non-independence. Our results confirm TEs as major drivers of genome size variation, and endorse life-history traits and dN/dS as reliable proxies for Ne. However, we do not find any evidence for increased drift to result in an accumulation of TEs across animals. Within more closely related clades, only a few isolated and weak associations emerge in fishes and birds. Our results outline a scenario where TE dynamics vary according to lineage-specific patterns, lending no support for genetic drift as the predominant force driving long-term genome size evolution in animals.