The origin and evolution of amphibious hearing in pinnipeds

Summary Seals (pinnipeds) are the only mammals that can hear 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 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, which fills with blood during diving to equalise air pressure in the ear, enables a shift from in-air to underwater hearing by matching the acoustic impedance of the ear to that of the surrounding water. Early diverging freshwater pinnipeds had impaired hearing underwater. The first marine pinnipeds could hear amphibiously but were limited by a functional tradeoff between hearing abilities and the need to prevent damage 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 likely facilitated the exploration of novel auditory adaptive zones by crown pinnipeds, resulting in rare acoustic abilities like ultrasonic singing, vocal learning, and keeping rhythm.