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Primate mosaic brain evolution reflects selection on sensory and cognitive specialization

Nature Ecology & Evolution volume 3, pages 1483–1493 (2019)Cite this article

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Abstract

The mammalian brain is composed of numerous functionally distinct structures that vary in size within and between clades, reflecting selection for sensory and cognitive specialization. Primates represent a particularly interesting case in which to examine mosaic brain evolution since they exhibit marked behavioural variation, spanning most social structures, diets and activity periods observed across mammals. Although studies have consistently demonstrated a trade-off between visual and olfactory specialization in primates, studies of some regions (for example, the neocortex) have produced conflicting results. Here, we analyse the socioecological factors influencing the relative size of 33 brain regions, using updated statistical techniques and data from more species and individuals than previous studies. Our results confirm that group-living species and those with high-quality diets have expanded olfactory or visual systems, depending on whether they are nocturnal or diurnal. Conversely, regions associated with spatial memory are expanded in solitary species and those with low-quality diets, suggesting a trade-off between visual processing and spatial memory. Contrary to previous work, we show that diet quality predicts relative neocortex size at least as well as, if not better than, social complexity. Overall, our results demonstrate that primate brain structure is largely driven by selection on sensory and cognitive specializations that develop in response to divergent socioecological niches.

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Fig. 1: Relative region size differs between primate species due to variation in diets, social systems and activity patterns.
Fig. 2: The relative sizes of specific brain regions increase across primate species according to suborder and socioecology.

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The authors declare that all data supporting the findings of this study are available in the paper and its Supplementary Information.

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Acknowledgements

We thank C. Sherwood and R. Barton for helpful advice and K. Chiou for his artistic skill. For training in phylogenetic comparative methods, J.P.H. thanks the AnthroTree Workshop, which was supported by the NSF (grant no. BCS-0923791) and the National Evolutionary Synthesis Center (NSF grant no. EF-0905606). This material is based on work supported by the National Science Foundation Graduate Research Fellowship (grant no. DGE1342536) and the New York University MacCracken Fellowship Program.

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Authors and Affiliations

  1. Department of Anthropology, New York University, New York, NY, USA

    Alex R. DeCasien & James P. Higham

  2. New York Consortium in Evolutionary Primatology, New York, NY, USA

    Alex R. DeCasien & James P. Higham

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Contributions

A.R.D. designed the project and performed the analyses with input from J.P.H. A.R.D. compiled the data. Both authors wrote the manuscript.

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Correspondence to Alex R. DeCasien.

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Supplementary information

Supplementary Materials

Supplementary Figs. 1 and 2, list of tables, notes for tables, methods and appendix.

Reporting Summary

Supplementary Data 1

This file includes all neuroanatomical and socioecological (activity period, diet, DQI, social system and group size) data used in this study. Data sources and relevant notes are also included.

Supplementary Tables 1–12

10kTrees26 consensus tree BIC comparisons.

Supplementary Tables 13–24

10kTrees26 consensus tree PGLS/ANOVA results.

Supplementary Tables 25–28

10kTrees26 consensus tree PGLS/ANOVA results within activity pattern.

Supplementary Tables 29–32

Results across block of 1,000 trees from 10kTrees26—Bayesian MCMC analysis.

Supplementary Tables 33–36

Ref. 27 consensus tree BIC comparisons.

Supplementary Tables 37–40

Ref. 27 consensus tree PGLS/ANOVA results.

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DeCasien, A.R., Higham, J.P. Primate mosaic brain evolution reflects selection on sensory and cognitive specialization. Nat Ecol Evol 3, 1483–1493 (2019). https://doi.org/10.1038/s41559-019-0969-0

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