Sociality does not drive the evolution of large brains in eusocial African mole-rats

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.

Brain atlas of the African mole‐ratFukomys anselli

“…Superficially, the brains look very much like other rodent brains and the encephalization index is similar to that of surface‐dwelling rodents. Total neuron and glia cell numbers in African mole‐rats conform to scaling rules established for other rodents (with the exception of the naked mole‐rat, see below; Kverková et al, ). Immunohistochemical analysis of the cholinergic, putative catecholaminergic, and serotoninergic neuron systems of two mole‐rat species ( Cryptomys hottentotus pretoriae, Bathyergus suillus ) by Bhagwandin, Fuxe, Bennett, and Manger (), concluded in line with former studies that their brains, in principle, exhibit the same complement of homologous nuclei as in other rodents.…”

“…The brain of Fukomys anselli (body mass: 50–120 g) resembles a rat brain but is less elongated in shape (Figure ). With an average adult brain mass of 1.15 ± 0.06 g (mean ± SD , n = 6) it is about two thirds the size of a rat brain (body mass: 300–500 g; Herculano‐Houzel, ), but more than double the size of a naked mole‐rat brain (body mass: 40–60 g; Kverková et al, ) or mouse brain (body mass: 15–40 g; Herculano‐Houzel, ). The brain mass of the individuals used in the present study compares well to that reported for a similar sample size of Ansell's mole‐rats in a recent study (Kverková et al, ).…”

“…With an average adult brain mass of 1.15 ± 0.06 g (mean ± SD , n = 6) it is about two thirds the size of a rat brain (body mass: 300–500 g; Herculano‐Houzel, ), but more than double the size of a naked mole‐rat brain (body mass: 40–60 g; Kverková et al, ) or mouse brain (body mass: 15–40 g; Herculano‐Houzel, ). The brain mass of the individuals used in the present study compares well to that reported for a similar sample size of Ansell's mole‐rats in a recent study (Kverková et al, ). Macroscopic inspection of the Ansell's mole‐rat brains (Figure ) revealed several features related to the underground lifestyle, such as very thin optic nerves, a delicate optic chiasm but well‐developed trigeminal nerves, ganglia, and branches (Figure ).…”

“…Indeed, this species is so distinct from other African mole‐rats that it has recently been proposed to constitute its own rodent family, Heterocephalidae (Patterson & Upham, ). Furthermore, the brain of the naked mole‐rat has been shown to differ from other African mole‐rat brains and general rodent brain scaling rules in that it is relatively smaller and has fewer neurons than expected for a rodent of its body size (Kverková et al, ). It is therefore likely that the naked mole‐rat brain is not representative for subterranean mammals.…”

Artificial selection on brain size leads to matching changes in overall number of neurons

“…Moreover, neuronal density often shows a pattern of negative allometry with body and brain size across species (Herculano-Houzel et al 2015a;Olkowicz et al 2016). Hence, small-bodied species with smaller absolute brain size show higher neuronal densities than larger species with larger absolute brain size, although exceptions from this rule have been observed (Kverková et al 2018). Whether this negative allometry pattern also exists within species or whether neuronal density is a species-specific characteristic is currently unknown (but see Herculano-Houzel et al 2015b).…”