Transcriptomic evidence of mosaic brain evolution underlying complex division of labor in a social insect

Concerted developmental programming may constrain changes in component structures of the brain, thus limiting the ability of selection on individual brain compartments to form an adaptive mosaic independent of total brain size or body size. Measuring patterns of gene expression underpinning brain scaling can distinguish between concerted and mosaic evolution. Species exhibiting exceptional size and behavioral polyphenisms provide excellent systems to test predictions of brain evolution models by quantifying brain gene expression. We examined patterns of brain gene expression in a highly polymorphic and behaviorally complex social insect, the leafcutter ant Atta cephalotes. Consistent with expectations of concerted evolution, approximately ~50% of differential gene expression observed among three morphologically, behaviorally, and neuroanatomically differentiated worker size groups was attributable to body size. Additionally, we found strong evidence of differential brain gene expression that could not be explained by body size variation. Transcriptomic results coupled patterns of worker size and allometric brain compartment scaling with task performance to identify patterns of gene expression not explained by worker size, instead supporting mosaicism. Additionally, we observed enriched gene ontology terms associated with nucleic acid regulation, metabolism, neurotransmission, and sensory perception, further supporting a role for brain gene expression with worker social role. Our findings demonstrate that differential brain gene expression among polymorphic workers is linked to behavioral and neuroanatomical differentiation underpinning complex agrarian division of labor in A. cephalotes.