Behavioral performance and division of labor influence brain mosaicism in the leafcutter ant Atta cephalotes

Abstract

Brain evolution is hypothesized to be driven by behavioral selection on neuroarchitecture. We developed a novel metric of relative neuroanatomical investments involved in performing tasks varying in sensorimotor and processing demands across polymorphic task-specialized workers of the leafcutter ant Atta cephalotes and quantified brain size and structure to examine their correlation with our computational approximations. Investment in multisensory and motor integration for task performance was estimated to be greatest for media workers, whose highly diverse repertoire includes leaf-quality discrimination and leaf-harvesting tasks that likely involve demanding sensory and motor processes. Confocal imaging revealed that absolute brain volume increased with worker size and functionally specialized compartmental scaling differed among workers. The mushroom bodies, centers of sensory integration and learning and memory, and the antennal lobes, olfactory input sites, were larger in medias than in minims (gardeners) and significantly larger than in majors ("soldiers"), both of which had lower scores for involvement of olfactory processing in the performance of their characteristic tasks. Minims had a proportionally larger central complex compared to other workers. These results support the hypothesis that variation in task performance influences selection for mosaic brain structure, the independent evolution of proportions of the brain composed of different neuropils.

Keywords: Distributed cognition; Mushroom body; Sensory processing; Social brain evolution; Task performance.