Neurobiological adaptations supporting vocal plasticity have accumulated in the marine carnivores

The evolutionary neurobiology of mammalian vocal learning is poorly understood. Pinnipeds are among the most promising model clades for addressing this knowledge gap^1–4. The whole clade has been adaptively endowed with exquisite volitional breathing control to which the monachinae seals add developmental call plasticity and the phocinae add the capability for formant and frequency modulation and potentially mimicry^5–10. Until now, there were no comparative neurobiological data on vocal behavior in this clade. Here, using histology and ex vivo dMRI tractography, we provide strong first evidence for a phylogenetic spectrum of accumulative neural adaptations supporting aspects of volitional vocal control across pinniped species. Otariids and phocid seals, but not coyotes, showed robust direct cortical vocal motor connectivity to the brainstem nucleus ambiguus. This pathway may have evolved to facilitate volitional breathing, submerged prey consumption, and underwater call production for an amphibious lifestyle in a basal pinniped prior to exaptation for vocal production learning in select clades. Phocid seals, but not otariids, showed a robust arcuate-like auditory-premotor cortical pathway potentially related to developmental call learning. Harbor seals (branch phocinae) showed hypertrophic connectivity in the pathway between anterior ventrolateral thalamus and vocal premotor cortex, one part of the striatal-thalamocortical anterior forebrain circuit related to vocal motor reward learning in birds^11,12. Thalamic-premotor connectivity is specifically implicated in human language production and vocal mimicry in parrots^13,14.