Evolution of neurometabolic frugality in harvester ants

Abstract

Despite the importance of neurometabolic costs in brain size evolution, quantitative data on brain metabolic rates are lacking. We measured ex vivo brain metabolic rates among species of the ant genus Pogonomyrmex to differentiate the roles of sociality and body size in brain evolution in a phylogenetic context. Worker body size and colony size (a proxy for social complexity) vary significantly among Pogonomyrmex species and were positively correlated. However, sociality was not a determinant of brain energetics. Worker body size strongly affected brain metabolism: 38% of resting metabolic rate was attributable to brain metabolism in species with the smallest workers, compared to 6% in species with the largest workers. More derived species had strikingly lower mass-specific brain metabolic costs, suggesting that increases in worker body size have selected for neurometabolic frugality through reductions in brain mass-specific metabolic rate. Additionally, smaller worker body sizes may require higher brain mass-specific energetic costs to achieve comparable performance by absolutely smaller brains. Our study shows that the social brain hypothesis does not explain patterns of brain size in Pogonomyrmex, but body size and evolutionary history strongly influence brain evolution in regard to both size and metabolic cost.