Baboons (Papio anubis) living in larger social groups have bigger brains

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Abstract

The evolutionary origin of Primates' exceptionally large brains is still highly debated. Two competing explanations have received much support: the ecological hypothesis and the social brain hypothesis (SBH). We tested the SBH in (n = 82) baboons (Papio anubis) belonging to the same research centre but housed in groups with size ranging from 2 to 63 individuals. We found that baboons living in larger social groups had larger brains. This effect was driven mainly by white matter volume and to a lesser extent by grey matter volume but not by the cerebrospinal fluid. In comparison, the size of the enclosure, an ecological variable, had no such effect. In contrast to the current re-emphasis on potential ecological drivers of primate brain evolution, the present study provides renewed support for the social brain hypothesis and suggests that the social brain plastically responds to group size. Many factors may well influence brain size, yet accumulating evidence suggests that the complexity of social life might be an important determinant of brain size in primates.

Introduction

Two evolutionary hypotheses that propose to explain the exceptionally large size of Primate's brains have received much empirical support (Dunbar, 1998), the ecological hypothesis (EH) and the social brain hypothesis (SBH). Both hypotheses assume that energetically costly increases in relative brain size were driven by selection for higher cognitive abilities (Aiello & Wheeler, 1995; Isler & van Schaik, 2006). However, the ecological hypothesis posits that higher cognitive abilities were demanded by novel types of foraging (DeCasien, Williams, & Higham, 2017; González-Forero & Gardner, 2018; Louail, Gilissen, Prat, Garcia, & Bouret, 2019). For instance, comparisons between folivorous and frugivorous primates have shown that frugivory is associated with an increase in relative brain volume (Clutton-Brock & Harvey, 1980; DeCasien et al., 2017). In contrast, the social brain hypothesis (SBH), originating from the Machiavellian intelligence hypothesis, proposes that the increase in brain size has been driven by the cognitive demands of primate's complex social life (Byrne & Whiten, 1988; Dunbar, 1998; Humphrey, 1976; see Whiten, 2018 for an historical account). The SBH is supported by a positive relationship between brain size and social group size across primate species, suggesting a constraint imposed by the brain volume on the size of social groups (Dunbar, 1992, Dunbar, 2009; Sawaguchi & Kudo, 1990). However, most comparative studies supporting the ecological or the social hypothesis are correlational and were done across species. Since ecology, social life and group size are tightly linked in nature, the teasing apart of the different factors is difficult (Dunbar & Shultz, 2017; Healy & Rowe, 2007).

More recently, the SBH has been tested within primate species rather than across species (Dunbar, 2012). If social life is assumed to be the driving force behind the evolution of large brains, we should expect the brain to respond to changes in the social life of individuals through neuroplasticity. Individuals with less social partners should therefore have less voluminous brains than individuals with more social partners. In humans, studies have shown that social network size significantly correlates with grey matter density of regions constituting the social brain (for a review see Adolphs, 2009), including the amygdala and posterior superior temporal sulcus (STS) (Bickart, Wright, Dautoff, Dickerson, & Barrett, 2011; Kanai, Bahrami, Roylance, & Rees, 2012; Kwak, Joo, Youm, & Chey, 2018; Lewis, Rezaie, Brown, Roberts, & Dunbar, 2011; Powell, Lewis, Roberts, García-Fiñana, & Dunbar, 2012). Furthermore, in rhesus macaques (Macaca mulatta), Sallet et al. (2011) have shown that social network size correlates with the grey matter densities in some regions of the social brain (n = 23) and Noonan et al. (2014) have found that individual dominance status correlates with the density in some of these areas (n = 25).

The study of non-human primates in captivity is of prime importance because it allows to experimentally test the effect of social group size on brain volume in primates while controlling for ecological factors and other correlates of brain volume or social life. Consequently, the aim of the present study was to test the intraspecific predictions of the SBH regarding the relationships between social group size and brain size in captive olive baboons (Papio anubis) while controlling for environmental and individual variables. We tested a large sample of captive olive baboons (n = 82) to determine whether group size (range: 2—63 individuals) influences brain size (range: 117-189 cm3) as measured through in vivo magnetic resonance imagery (MRI) acquisitions (see methods). We used enclosure size (range: 9—304 m2) as an ecological control variable because home range size has been shown to have an influence on brain structures in primates (Clutton-Brock & Harvey, 1980; Sawaguchi, 1990) and because other ecological factors, such as diet for instance, are controlled for in captivity. Furthermore, home range and social group size are tightly linked in nature and substantially correlated in our sample (rτ = 0.60, z = 7.82, p < .001). Enclosure size is thus an excellent non-social ecological control variable for our study in captivity. We also used the volume of the cerebrospinal fluid (CSF) as a control for individual differences in morphology (such as body size).

Section snippets

Results

In a first analysis (Fig. 1), we noted that the baboons' overall brain volume was smaller when they were housed with a small group in a small enclosure (the “Loge” enclosures in our facility) compared to when they lived in a larger group with a large enclosure (the “Parc” enclosures; one-sided t-test, t(80) = −1.71,p = .046). This small but significant difference observed at the time of scanning could potentially be explained by an effect of group size or enclosure size (or both) on brain

Discussion

Why are primate brains inordinately large? Two competing hypotheses (ecological and social) have both received empirical support but the correlational nature of the studies and the tight relationship between ecological and social variables in nature makes it difficult to draw definitive conclusions on the evolutionary origin of primates' large brains (Dunbar & Shultz, 2017). To tease apart these two hypotheses we studied the effect of social group size on brain size in a large sample of captive

Species and subjects

Olive baboons (Papio anubis), N = 82 including 28 males, from 2 to 26 years old.

The baboons lived in different social groups, including at least two adults and one or two adult males. Most of the baboons were born, and stayed, within their birth group. However, animal movements between groups happened before the study period for (1) subadult males when they reached sexual maturity, in order to avoid male-male conflicts or direct inbreeding, (2) weaned juveniles when enclosures had reached

Acknowledgements

The project has received funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program grant agreement No 716931 (716931 - GESTIMAGE - ERC-2016-STG, P.I. Adrien Meguerditchian), from the French “Agence Nationale de le Recherche” (ANR-12-PDOC-0014-01, LangPrimate Project, P.I. Adrien Meguerditchian) as well as from grants ANR-16-CONV-0002 (ILCB), ANR-11-LABX-0036 (BLRI) and ANR-11-IDEX-0001-02 (A*MIDEX).

We are very grateful to the CNRS

Author contributions

N.C. supervised the present study. A.M. and N.C. prepared the paper. N.C. analysed the results. D.M. and K.M. analysed MRI data. A.M. supervised MRI acquisitions and MRI data analyses. M.R. designed MRI sequences, B.N. designed the baboons’ health monitoring programs during MRI acquisitions, J.-L.A. supervised and coordinated the MRI sessions.

Data availability

The data analysed in this article are freely available on the Open Science Foundation website, with the following DOI 10.17605/OSF.IO/Y9E64.

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