Parallel loss of sweet and umami taste receptor function from phocids and otarioids suggests multiple colonizations of the marine realm by pinnipeds

Abstract Aim Pinnipeds are thought to have evolved from a North Pacific ancestor, although some fossil evidence suggests a nonmarine Arctic origin and separate invasions into the North Pacific and North Atlantic. We here set out to test differing hypotheses about the origin of pinnipeds through identification and age estimation of pinniped marine invasions. Location Arctic, North America, North Atlantic, North Pacific. Taxon Pinnipeds (seals, sea lions, walruses and their fossil relatives). Methods Because evidence indicates that taste loss in marine mammals and birds results from adaptation to the marine environment, we examined 16 representative pinnipeds for loss‐of‐function mutations in the TAS1R1 , TAS1R2 and TAS1R3 genes encoding the sweet T1R2–T1R3 and umami (savory) T1R1–T1R3 receptors, and used the loss‐of‐function events of these receptors as indicators of marine invasion. Results Numerous loss‐of‐function mutations were found in each pinniped TAS1R (22 in TAS1R1 , 21 in TAS1R2 and 42 in TAS1R3 ). Six mutations were shared by all phocids and six other mutations by all otarioids (otariids and odobenids), but none by all phocids and all otarioids. Selective pressures on TAS1R1 , TAS1R2 and TAS1R3 were estimated to have been relaxed, respectively, 16.3, 20.1 and 19.8 million years ago (Myra) in phocids, and 12.1, 18.1 and 18.2 Myra in otarioids. Main conclusions All TAS1R s, T1R1–T1R3 and T1R2–T1R3 are nonfunctional in all extant pinnipeds. Both receptors lost their function approximately 20 Myra in the Phocidae lineage and approximately 18 Myra in the Otarioidea lineage. Both lineages have colonized the marine realm independently, which entails nonmarine origins of both Pinnipedia and its stem lineage. Combined with fossil evidence, molecular findings here suggest an Arctic centre of long‐lasting (approximately 38–18 Myra) nonmarine pinniped evolution and at least five separate marine invasions, with the extinct (enaliarctid, Desmatophocidae, Kolponomos ) and Otarioidea lineages entering the North Pacific and the Phocidae lineage the North Atlantic.