A cerebellar substrate for cognition evolved multiple times independently in mammals

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Abstract

Given that complex behavior evolved multiple times independently in different lineages, a crucial question is whether these independent evolutionary events coincided with modifications to common neural systems. To test this question in mammals, we investigate the lateral cerebellum, a neurobiological system that is novel to mammals, and is associated with higher cognitive functions. We map the evolutionary diversification of the mammalian cerebellum and find that relative volumetric changes of the lateral cerebellar hemispheres (independent of cerebellar size) are correlated with measures of domain-general cognition in primates, and are characterized by a combination of parallel and convergent shifts towards similar levels of expansion in distantly related mammalian lineages. Results suggest that multiple independent evolutionary occurrences of increased behavioral complexity in mammals may at least partly be explained by selection on a common neural system, the cerebellum, which may have been subject to multiple independent neurodevelopmental remodeling events during mammalian evolution.

Data availability

The brain data and the phylogeny that were used in the analyses are available as source data files (Figure 2 - source data 1, and Figure 3 - source data 1). Behavioral data for primates is available from Figure 2 Deaner RO, Van Schaik CP, Johnson V. 2006. Do some taxa have better domain-general cognition than others? A meta-analysis of nonhuman primate studies. Evolutionary Psychology 4: 149-196.

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Jeroen B Smaers

Department of Anthropology, Stony Brook University, Stony Brook, United States

For correspondence
jeroen.smaers@stonybrook.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-1741-9839
Alan H Turner

Department of Anatomical Sciences, Stony Brook University, Stony Brook, United States

Competing interests
The authors declare that no competing interests exist.
Aida Gómez-Robles

Department of Genetics, Evolution and Environment, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Chet C Sherwood

Department of Anthropology, The George Washington University, Washington, DC, United States

Competing interests
The authors declare that no competing interests exist.

Funding

Wenner Gren Foundation (Grant 9209)

Jeroen B Smaers

James S. McDonnell Foundation (220020293)

Chet C Sherwood

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.