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. 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, 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. Such tracts were not present in other teleost species such as trout, zebrafish, or the Astyanax surface fish. The high degree of connectivity between the IL and the pallium in tool-using wrasses suggests that this unique teleostean structure contributes to higher-order cognitive functions. Considering how remarkably different their overall brain organization is, 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.

How smart wasT. rex? Testing claims of exceptional cognition in dinosaurs and the application of neuron count estimates in palaeontological research

“…4D). Interestingly, brain cell densities (suggestive of high neuron counts but including endothelial and glia cells) on par with or even higher than those of telluravian birds have recently been identified among ectotherm teleost fish, with comparatively small relative brain sizes (Estienne et al, 2024). All of this suggests that metabolic rate and neuronal density are not tightly coupled and that endothermy cannot be used as a proxy for the latter.…”

“…4D). Interestingly, brain cell densities (suggestive of high neuron counts but including endothelial and glia cells) on par with or even higher than those of telluravian birds have recently been identified among ectotherm teleost fish, with comparatively small relative brain sizes (Estienne et al, 2024).…”

“…Second comparisons between groups of extant vertebrates, especially birds and mammals, strongly suggest that there is no uniform relationship between neuron density and relative brain size or elevated metabolic rates (Kverkova et al, 2022; see also Estienne et al, 2024).…”

“…Second comparisons between groups of extant vertebrates, especially birds and mammals, strongly suggest that there is no uniform relationship between neuron density and relative brain size or elevated metabolic rates (Kverkova et al, 2022; see also Estienne et al, 2024). We will elaborate on this aspect in the Discussion section but would like to state at this point already that it is not straight-forward to assume avian neuron densities in Mesozoic theropods simply because they exhibited endothermy or a potential increase in relative brain size.…”

Evolution of the visual system in ray-finned fishes

“…The IL can be quite large, in some species like Synchiropus or Eurypegasus the IL is even larger than the entire telencephalon (Gebhardt & Hofmann, 2023). The large size of the IL in wrasses has been noted also by Estienne et al (2023). They concluded that the NG-IL system is a derived feature in ray-finned fishes and has no counterpart in tetrapods.…”