Widespread selection relaxation in aquatic mammals

AbstractWhile mammals are predominantly terrestrial, several lineages within them have independently transitioned to aquatic environments and exhibit a great variety of evolutionary changes, which ultimately lead to irreversible transitions to aquatic lifestyle. Such changes should also be detectable at the molecular level and, for instance, olfactory genes have been found to evolve under reduced selection and functionality in whales. However, the presence of a molecular signature related to aquatic transitions across other genes remains unknown as is the degree to which this affects only fully aquatic groups or also semiaquatic ones. Here, we use a Bayesian framework to investigate differences in the strength of purifying selection among terrestrial, semiaquatic and fully aquatic mammals using a set of 1000 orthologous genes, while accounting for shared ancestry, and controlling for body mass and effective population size. We found that selection relaxation linked to aquatic transitions is not only occurring in olfactory genes, but also detected across 20% of the other genes analysed here. This consistent trend of genes under weaker selection is inferred in both semi- and fully aquatic mammals although the pattern is stronger in the latter. While most of the genes analysed here likely remain functional in all mammals, their evolution is inferred to be neutral in a substantial number of aquatic species, consistently with genes that might be losing their functionality. The inferred widespread relaxation of selection among genes is consistent with a macroevolutionary scenario where secondary transitions to aquatic environment eventually become irreversible.