The neuroplasticity of division of labor: worker polymorphism, compound eye structure and brain organization in the leafcutter ant Atta cephalotes

Abstract

Our understanding of how the design of peripheral sensory structures is coupled with neural processing capacity to adaptively support division of labor is limited. Workers of the remarkably polymorphic fungus-growing ant Atta cephalotes are behaviorally specialized by size: the smallest workers (minims) tend fungi in dark subterranean chambers while larger workers perform tasks mainly outside the nest. These strong differences in worksite light conditions are predicted to influence sensory and processing requirements for vision. We found that eye structure and visual neuropils have been be selected to maximize task performance according to light availability. Minim eyes had few ommatidia, large interommatidial angles and eye parameter values, suggesting selection for visual sensitivity over acuity. Large workers had larger eyes with disproportionally more and larger ommatidia, and smaller interommatidial angles and eye parameter values, reflecting peripheral sensory adaptation to ambient rainforest light. Additionally, optic lobe and mushroom body collar volumes were disproportionately small in minims, and within the optic lobe, lamina and lobula relative volumes increased with worker size whereas the medulla decreased. Visual system phenotypes thus correspond to task specializations in dark or light environments and reflect a functional neuroplasticity underpinning division of labor in this socially complex agricultural ant.