Genomic and anatomical comparisons of skin support independent adaptation to life in water by cetaceans and hippos.

The macroevolutionary transition from terra firma to obligatory inhabitance of the marine hydrosphere has occurred twice in the history of Mammalia: Cetacea and Sirenia. In the case of Cetacea (whales, dolphins, and porpoises), molecular phylogenies provide unambiguous evidence that fully aquatic cetaceans and semiaquatic hippopotamids (hippos) are each other's closest living relatives. Ancestral reconstructions suggest that some adaptations to the aquatic realm evolved in the common ancestor of Cetancodonta (Cetacea + Hippopotamidae). An alternative hypothesis is that these adaptations evolved independently in cetaceans and hippos. Here, we focus on the integumentary system and evaluate these hypotheses by integrating new histological data for cetaceans and hippos, the first genome-scale data for pygmy hippopotamus, and comprehensive genomic screens and molecular evolutionary analyses for protein-coding genes that have been inactivated in hippos and cetaceans. We identified eight skin-related genes that are inactivated in both cetaceans and hippos, including genes that are related to sebaceous glands, hair follicles, and epidermal differentiation. However, none of these genes exhibit inactivating mutations that are shared by cetaceans and hippos. Mean dates for the inactivation of skin genes in these two clades serve as proxies for phenotypic changes and suggest that hair reduction/loss, the loss of sebaceous glands, and changes to the keratinization program occurred ∼16 Ma earlier in cetaceans (∼46.5 Ma) than in hippos (∼30.5 Ma). These results, together with histological differences in the integument and prior analyses of oxygen isotopes from stem hippopotamids ("anthracotheres"), support the hypothesis that aquatic skin adaptations evolved independently in hippos and cetaceans. [Display omitted] • Cetaceans and hippos have differences in the thickness and organization of the skin • Genomic screens identified 8 skin genes that are inactivated in hippos and cetaceans • None of these 8 genes share inactivating mutations in hippos and cetaceans • Aquatic skin adaptations evolved independently in hippos and cetaceans Springer et al. perform genomic and anatomical comparisons to determine whether aquatic adaptations of the skin in hippos and cetaceans are shared derived or convergent features in these two clades. The results of these comparisons support the hypothesis that aquatic adaptations of the skin are convergent characters in hippos and cetaceans. [ABSTRACT FROM AUTHOR]