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

Our understanding of how sensory structure design 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 outside the nest. Strong differences in worksite light conditions are predicted to influence sensory and processing requirements for vision. Analyzing confocal scans of worker eyes and brains, we found that eye structure and visual neuropils appear to have been 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, indicating peripheral sensory adaptation to ambient rainforest light. Optic lobes and mushroom body collars were disproportionately small in minims. Within the optic lobe, lamina and lobula relative volumes increased with worker size whereas medulla volume decreased. Visual system phenotypes thus correspond to task specializations in dark or light environments and illustrate a functional neuroplasticity underpinning division of labor in this socially complex agricultural ant.