Abstract

The social brain hypothesis (SBH) posits that the demands imposed on individuals by living in cohesive social groups exert a selection pressure favouring the evolution of large brains and complex cognitive abilities. Using volumetry and the isotropic fractionator to determine the size of and numbers of neurons in specific brain regions, here we test this hypothesis in African mole-rats (Bathyergidae). These subterranean rodents exhibit a broad spectrum of social complexity, ranging from strictly solitary through to eusocial cooperative breeders, but feature similar ecologies and life history traits. We found no positive association between sociality and neuroanatomical correlates of information-processing capacity. Solitary species are larger, tend to have greater absolute brain size and have more neurons in the forebrain than social species. The neocortex ratio and neuronal counts correlate negatively with social group size. These results are clearly inconsistent with the SBH and show that the challenges coupled with sociality in this group of rodents do not require brain enlargement or fundamental reorganization. These findings suggest that group living or pair bonding per se does not select strongly for brain enlargement unless coupled with Machiavellian interactions affecting individual fitness.

Highlights

  • The social brain hypothesis (SBH) contends that the demands imposed on individuals by living in cohesive social groups exert a selection pressure favouring the evolution of large brains and complex cognitive abilities[1]

  • While it might be possible that subterranean microphthalmic mammals are somehow aberrant in the way their brains are built, we show that this is not a concern in the choice of molerats as our model group

  • Despite examining measures ranging from overall brain size to neuronal numbers, we found no differences between the social grades in any of the relative measures, whether previously reported[13,62], or tested for the first time

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Summary

Introduction

The social brain hypothesis (SBH) contends that the demands imposed on individuals by living in cohesive social groups exert a selection pressure favouring the evolution of large brains and complex cognitive abilities[1]. One way to limit the effects of biological heterogeneity and statistical interference is to study brain evolution within closely related but behaviourally diverse clades[21] We use this approach and test the SBH in African mole-rats (Rodentia: Bathyergidae). Social species live in stable, multigenerational families in which only few individuals (often just a single bonded pair) reproduce and most of their offspring stay permanently within the family as non-reproductive helpers Members of this cohesive group cooperate through digging and maintaining the burrows, foraging for food and bringing it to communal storage, engaging in colony defence against intruders and predators, and taking care of the pups – grooming, huddling, returning them to the nest chamber when they wander off and providing them with cecotrophs[22,39,40,41,42,43]. Manipulative or Machiavellian behaviour is likely selected against in mole-rat colonies with monopolized reproduction because it would harm an individual’s inclusive fitness

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