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.

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Brain evolution is hypothesized to be driven by neuroarchitectural requirements for behavioral performance. Assessments of such needs should be informed by the nature of sensory and motor processes underpinning behavior. We developed a novel metric to estimate the relative neuroanatomical investments required to perform tasks varying in sensorimotor and processing demands across polymorphic and polyethic workers of the leafcutter ant Atta cephalotes and quantified brain size and structure to examine their correspondence with our computational approximations. Investment in multi-sensory integration and motor requirements for task performance was estimated to be greatest for media workers whose leaf-harvesting repertoire involves the most diverse and demanding sensory and motor processes, including plant discrimination, leaf cutting, and fragment transportation. Volumetric analysis of confocal brain images revealed that absolute brain size increased with worker size and compartmental scaling allometries among functionally specialized brain compartments differed among polymorphic workers. The mushroom bodies, centers of sensory integration and learning, and the antennal lobes, which process olfactory inputs, were significantly larger in medias than in minim workers (fungal gardeners) and major workers ("soldiers"), which had lower estimated task-related neural demands. Minims had a proportionally larger central complex, perhaps to control navigation in subterranean fungal garden chambers. These results indicate that variation in task performance requirements has selected for adaptive variation in brain size and mosaic scaling.