Abstract Pinnipeds (true seals, eared seals and walruses) are the only mammals that can hear effectively in both air and water. How and when they achieved the ability to negotiate such contrasting auditory media remains unknown. Here, we apply 3D shape and phylogenetic comparative analyses to a large dataset of extant and extinct caniform carnivorans (119 species, 217 specimens) to study the emergence of amphibious hearing in pinnipeds despite significant evolutionary constraints. We find support for the cavernous tissue as a functional and evolutionary mechanism for amphibious hearing. This tissue fills with blood during diving to equalize air pressure in the ear, enabling a shift from in-air to underwater hearing by matching the ear’s acoustic impedance to that of the surrounding water. We found that early diverging freshwater pinnipeds had impaired hearing underwater. The first ancestral marine pinnipeds could hear amphibiously but with limited hearing ranges, probably reducing attenuation and harm from loud underwater sounds. Subsequently, otariids (eared seals) and phocids (true seals) independently acquired middle ear adaptations that expanded their underwater hearing range. This iterative evolution probably facilitated the exploration of novel auditory adaptive zones by crown pinnipeds, resulting in rare acoustic abilities like ultrasonic singing, vocal learning and rhythm.
Rule et al. (Wed,) studied this question.