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Neuron numbers link innovativeness with both absolute and relative brain size in birds

Abstract

A longstanding issue in biology is whether the intelligence of animals can be predicted by absolute or relative brain size. However, progress has been hampered by an insufficient understanding of how neuron numbers shape internal brain organization and cognitive performance. On the basis of estimations of neuron numbers for 111 bird species, we show here that the number of neurons in the pallial telencephalon is positively associated with a major expression of intelligence: innovation propensity. The number of pallial neurons, in turn, is greater in brains that are larger in both absolute and relative terms and positively covaries with longer post-hatching development periods. Thus, our analyses show that neuron numbers link cognitive performance to both absolute and relative brain size through developmental adjustments. These findings help unify neuro-anatomical measures at multiple levels, reconciling contradictory views over the biological significance of brain expansion. The results also highlight the value of a life history perspective to advance our understanding of the evolutionary bases of the connections between brain and cognition.

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Fig. 1: Framework linking cognition, neuron numbers and brain size.
Fig. 2: Neurons and innovation propensity.
Fig. 3: Neuron numbers and brain mass as a function of body size.
Fig. 4: Neuron numbers as a function of absolute and relative brain size.
Fig. 5: Neurons and development in species belonging to low-slope and highest slope grades.

Data availability

The data used in the analyses of this paper are archived in zenodo (https://doi.org/10.5281/zenodo.6460346).

Code availability

The R code used for the analyses of this paper are archived in zenodo (https://doi.org/10.5281/zenodo.6460346).

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Acknowledgements

This research was funded by MINECO (PID2020-119514GB-I00 to D.S.), the Czech Science Foundation (18-15020 to P.N.), the Grant Agency of Charles University (1438217 to M.K.) and the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie postdoctoral fellowship (grant agreement no. 838998 to F.S.). F.S. and J.G.P. were supported by the postdoctoral fellowship program Beatriu de Pinós (2020 BP 00067 and 2020 BP 00147, Government of Catalonia). We thank A. Iwaniuk, S. Reader, S. Ducatez and J. Morand-Ferron for discussions and the R team and package contributors for facilitating analytical tools. We also thank J. Louys for facilitating bird silhouettes. This paper is dedicated to J. Morand-Ferron.

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L.L. and F.S. proposed the study. D.S., L.L., F.S. and P.N. conceived the study. D.S. and T.E.M. elaborated the life history framework. P.N., S.O., L.M., M.K., Y.Z. and C.O. collected the neuro-anatomical data, L.L. the innovation data and J.G.P., F.S. and E.C. the endocast data. D.S. designed and conducted the analyses, with contributions from F.S., L.L., P.N. and T.E.M. D.S. wrote the manuscript and all authors edited and approved it.

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Correspondence to Daniel Sol, Louis Lefebvre or Pavel Němec.

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Nature Ecology & Evolution thanks Onur Güntürkün, Cristian Gutierrez-Ibanez and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Sol, D., Olkowicz, S., Sayol, F. et al. Neuron numbers link innovativeness with both absolute and relative brain size in birds. Nat Ecol Evol 6, 1381–1389 (2022). https://doi.org/10.1038/s41559-022-01815-x

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