Vestibular evidence for the evolution of aquatic behaviour in early cetaceans

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Abstract
Early cetaceans evolved from terrestrial quadrupeds to obligate swimmers, a change that is traditionally studied by functional analysis of the postcranial skeleton1. Here we assess the evolution of cetacean locomotor behaviour from an independent perspective by looking at the semicircular canal system, one of the main sense organs involved in neural control of locomotion2. Extant cetaceans are found to be unique in that their canal arc size, corrected for body mass, is approximately three times smaller than in other mammals. This reduces the sensitivity of the canal system, most plausibly to match the fast body rotations that characterize cetacean behaviour. Eocene fossils show that the new sensory regime, incompatible with terrestrial competence, developed quickly and early in cetacean evolution, as soon as the taxa are associated with marine environments. Dedicated agile swimming of cetaceans thus appeared to have originated as a rapid and fundamental shift in locomotion rather than as the gradual transition suggested by postcranial evidence. We hypothesize that the unparalleled modification of the semicircular canal system represented a key ‘point of no return’ event in early cetacean evolution, leading to full independence from life on land.