Different ways of evolving tool-using brains in teleosts and amniotes

Abstract

In mammals and birds, tool-using species are characterized by a high degree of encephalization with a relatively large telencephalon containing a higher proportion of total brain neurons compared to other species. Some teleost species in the wrasse family have convergently evolved tool-using abilities. In this study, we compared the brains of tool-using wrasses with various teleost species from a broad phylogenetic range. Using the isotropic fractionator, we show that in the tool-using wrasses, the telencephalon and the ventral part of the forebrain and midbrain are significantly enlarged compared to other teleost species but do not contain a larger proportion of cells. Instead, we found with tract tracing and selective neuronal fiber visualization that this size difference is due to large fiber tracts connecting the dorsal part of the telencephalon (pallium) to the inferior lobe (IL), a ventral mesencephalic structure absent in amniotes. The high degree of connectivity between the IL and the pallium in tool-using wrasses suggests that this unique teleostean structure could contribute to higher-order cognitive functions. Given remarkable differences in their overall brain organization, we conclude that, unlike in amniotes, the evolution of non-telencephalic structures might have been key in the emergence of higher-order cognitive functions in teleosts.