Mammalian brain volumes vary considerably, even after controlling for body size. Although several hypotheses have been proposed to explain this variation, most research in mammals on the evolution of encephalization has focused on primates, leaving the generality of these explanations uncertain. Furthermore, much research still addresses only one hypothesis at a time, despite the demonstrated importance of considering multiple factors simultaneously. We used phylogenetic comparative methods to investigate simultaneously the importance of several factors previously hypothesized to be important in neural evolution among mammalian carnivores, including social complexity, forelimb use, home range size, diet, life history, phylogeny, and recent evolutionary changes in body size. We also tested hypotheses suggesting roles for these variables in determining the relative volume of four brain regions measured using computed tomography. Our data suggest that, in contrast to brain size in primates, carnivoran brain size may lag behind body size over evolutionary time. Moreover, carnivore species that primarily consume vertebrates have the largest brains. Although we found no support for a role of social complexity in overall encephalization, relative cerebrum volume correlated positively with sociality. Finally, our results support negative relationships among different brain regions after accounting for overall endocranial volume, suggesting that increased size of one brain regions is often accompanied by reduced size in other regions rather than overall brain expansion.

The social brain hypothesis posits that the demands of living in complex social groups require increased neural processing, and that this underlies the expansion of brain areas involved in mediation of complex social behavior. However, much of the support for the social brain hypothesis is derived from comparative studies in primates. If large brains evolved as a result of selection pressures imposed by life within complex societies, as the social brain hypothesis predicts, then gregarious nonprimate species should possess large brains and exhibit comparable expansion of brain areas mediating social behavior. Our purpose here was to test a prediction of the social brain hypothesis – that increased brain size is related to social complexity – by examining species in the carnivore family Hyaenidae. Hyaenidae contains 4 extant species that span a spectrum of social complexity: the aardwolf (Proteles cristata) is solitary during the nonbreeding season, and forms monogamous pairs during the breeding season; the striped hyena (Hyaena hyaena) lives solitarily or in small groups; the brown hyena (Parahyaena brunnea) lives in groups of up to 14 individuals; and the spotted hyena (Crocuta crocuta) lives in complex hierarchically organized groups containing up to 90 animals. Computed tomography was used to create three-dimensional endocasts based on serial analysis of coronal sections of the adult endocranium. The largest brain volume, relative to body size, is found in the spotted hyena. We found no significant variation in relative brain volume among striped hyenas, brown hyenas, and aardwolves. The spotted hyena also possesses a larger anterior cerebrum volume relative to total brain volume than is found in the other hyena species; this region is composed primarily of frontal cortex. These data are consistent with the idea that expansion of the frontal cortex is driven by the demands of processing cognitive information associated with complex social lives, but other factors may drive the evolution of large brains in hyaenids.

The purpose of this study was to examine developmental and individual variation in total endocranial volume and regional brain volumes, including the anterior cerebrum, posterior cerebrum and cerebellum/brain stem, in the spotted hyena (Crocuta crocuta). The spotted hyena is a highly gregarious animal noted for living in large, hierarchically organized groups. The social lives of male and female spotted hyenas do not differ until after puberty, when males disperse from the natal group, while females remain philopatric. Here we sought to determine whether the divergent life histories of male and female spotted hyenas are linked to differences in brain size or organization. Three-dimensional virtual endocasts were created using computed tomography from 46 spotted hyenas skulls (23 females, 22 males, 1 unknown sex) ranging in age from 1 day to 18 years. Brain volume and skull length were highly correlated (r = 0.91), and both reached asymptotic values by 34 months of age. Analyses of total endocranial volume (relative to skull length) and cerebellum/brain stem volume (relative to total endocranial volume) revealed no sex differences. However, relative anterior cerebrum volume, comprised mainly of frontal cortex, was significantly greater in adult males than adult females, and relative posterior cerebrum volume was greater in adult females than adult males. We hypothesize that the demands of neural processing underlying enhanced social cognition required for successful male transfer between matriarchical social groups at dispersal may be greater than cognitive demands on philopatric females.

Broad-based species comparisons across mammalian orders suggest a number of factors that might influence the evolution of large brains. However, the relationship between these factors and total and regional brain size remains unclear. This study investigated the relationship between relative brain size and regional brain volumes and sociality in 13 felid species in hopes of revealing relationships that are not detected in more inclusive comparative studies. In addition, a more detailed analysis was conducted of four focal species: lions (Panthera leo), leopards (Panthera pardus), cougars (Puma concolor), and cheetahs (Acinonyx jubatus). These species differ markedly in sociality and behavioral flexibility, factors hypothesized to contribute to increased relative brain size and/or frontal cortex size. Lions are the only truly social species, living in prides. Although cheetahs are largely solitary, males often form small groups. Both leopards and cougars are solitary. Of the four species, leopards exhibit the most behavioral flexibility, readily adapting to changing circumstances. Regional brain volumes were analyzed using computed tomography. Skulls (n = 75) were scanned to create three-dimensional virtual endocasts, and regional brain volumes were measured using either sulcal or bony landmarks obtained from the endocasts or skulls. Phylogenetic least squares regression analyses found that sociality does not correspond with larger relative brain size in these species. However, the sociality/solitary variable significantly predicted anterior cerebrum (AC) volume, a region that includes frontal cortex. This latter finding is despite the fact that the two social species in our sample, lions and cheetahs, possess the largest and smallest relative AC volumes, respectively. Additionally, an ANOVA comparing regional brain volumes in four focal species revealed that lions and leopards, while not significantly different from one another, have relatively larger AC volumes than are found in cheetahs or cougars. Further, female lions possess a significantly larger AC volume than conspecific males; female lion values were also larger than those of the other three species (regardless of sex). These results may reflect greater complexity in a female lion’s social world, but additional studies are necessary. These data suggest that within family comparisons may reveal variations not easily detected by broad comparative analyses.