Primate brain size is predicted by diet but not sociality
Alex R. DeCasien, Scott A. Williams & James P. Higham
Nature Ecology & Evolution 1, Article number: 0112 (2017)
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Biological anthropology Social evolution
Abstract
The social brain hypothesis posits that social complexity is the primary driver of primate cognitive complexity, and that social pressures ultimately led to the evolution of the large human brain. Although this idea has been supported by studies indicating positive relationships between relative brain and/or neocortex size and group size, reported effects of different social and mating systems are highly conflicting. Here, we use a much larger sample of primates, more recent phylogenies, and updated statistical techniques, to show that brain size is predicted by diet, rather than multiple measures of sociality, after controlling for body size and phylogeny. Specifically, frugivores exhibit larger brains than folivores. Our results call into question the current emphasis on social rather than ecological explanations for the evolution of large brains in primates and evoke a range of ecological and developmental hypotheses centred on frugivory, including spatial information storage, extractive foraging and overcoming metabolic constraints.
Primates, especially anthropoids, have relatively large brains compared to other mammals. These observations have led researchers to propose various explanations for the evolution of increased brain size in the primate lineage. Accordingly, numerous comparative analyses have been undertaken with the goal of identifying social and/or ecological variables that explain interspecific variation in overall brain size, or of specific brain regions1.
Early studies suggested that ecological factors, such as diet, explain relative brain size variation in non-human primates2,3,4,5. This is consistent with the idea that processing of meat and other foods contributed to subsequent increases in hominin brain size6, 7 by fulfilling corresponding higher energy requirements8,9,10,11. Later comparative studies emphasized the role of social factors. In particular, the social brain hypothesis posits that social complexity is the primary driver of cognitive complexity among primates, and that social pressures associated with maintaining group cohesion ultimately led to the evolution of the large human brain12,13,14,15. This hypothesis has been supported by studies indicating positive relationships between relative brain and/or neocortex size and mean group size2,14,15,16,17.
However, research investigating the relationships between relative brain size and different social and mating system types, which may differ in their relative social complexity, has produced highly conflicting results17,18. Some studies have shown that polygynandrous primate species have the largest brains3,17, consistent with the idea that systems that promote the most interactions and relationships between the greatest numbers of individuals might be the most cognitively demanding. Conversely, other studies have shown that monogamous species have the largest brains18, and have argued that monogamy may require greater deception and manipulation abilities18 for obtaining extra-pair copulations, produce a relatively high cost of cuckoldry, and/or require conflict resolution and coordination abilities for bond maintenance17.
These conflicting results suggest that methodological issues may have led different researchers to different conclusions. Throughout the comparative study of primate brain size evolution, species sample sizes used in analyses have been small and idiosyncratic, while the statistical techniques available have improved considerably since early analyses. For example, many early studies used residuals as data, which can cause bias if the control variable co-varies with other variables in the analysis; the use of multiple regression with the confounding variable incorporated as a covariate is now recommended instead19. In addition, many studies used a phylogeny20 that has become outdated and set all branch lengths to 1—a relatively radical branch length transformation that presumes an evolutionary pattern in which changes occur at the time of speciation in both daughter species.
We assembled a much larger and more representative sample of primates (>140 spp., more than tripling the sample size of previous studies) and tested whether multiple measures of sociality (mean group size, social and mating system separately) explain variation in brain size after controlling for body size, diet and phylogenetic history. Although some studies have used relative neocortex size rather than whole brain size, this information is not available for a large sample of primate species; in any case, the neocortex scales hyper-allometrically with brain size21. In its original form, the social brain hypothesis was formulated to explain primate intelligence12,13 and was later discussed as an attempt to explain brain size14,15,22. The subsequent focus on the neocortex was not always based on a priori reasoning, but because neocortex analyses sometimes showed the strongest correlations with the social variables under examination14. Regions outside the neocortex are also involved in complex cognitive functions (for example, cerebellum23, hippocampus24, striatum25) and studies show that overall brain size predicts global cognitive ability across non-human primates24,26. Furthermore, studies by the main proponents of the social brain hypothesis continue to present analyses of relative total brain size17,22,24, consistent with the interpretation that the social brain hypothesis does indeed aim to explain evolutionary increases not only in neocortex ratio, but in overall brain size.
Acknowledgements
We thank M. Shattuck for help with data compilation, H. Kaplan for providing access to additional data, R. Raaum for statistical advice, and R. Peterson and M. Petersdorf for encouragement and feedback on previous versions of the manuscript. For training in phylogenetic comparative methods, J.P.H. thanks the AnthroTree Workshop, which is supported by the National Science Foundation (NSF; BCS-0923791) and the National Evolutionary Synthesis Center (NSF grant EF-0905606). This material is based on work supported by the NSF Graduate Research Fellowship (grant DGE1342536).
Author information
Affiliations
Department of Anthropology, New York University, 25 Waverly Place, New York, New York 10003, USA
Alex R. DeCasien, Scott A. Williams & James P. Higham
New York Consortium in Evolutionary Primatology, New York, New York 10024, USA
Alex R. DeCasien, Scott A. Williams & James P. Higham
Contributions
A.R.D. designed the project and performed the analyses with input from J.P.H. and S.A.W. A.R.D. and S.A.W. collected the data. All three authors wrote the manuscript.
Competing interests
The authors declare no competing financial interests.
Corresponding author
Correspondence to Alex R. DeCasien.
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