Transcriptomic analysis of mosaic brain differentiation 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 to form an adaptive mosaic of size-variable brain compartments independent of total brain size or body size. Measuring patterns of gene expression underpinning brain scaling in conjunction with anatomical brain atlases can aid in identifying influences of concerted and/or 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 remarkably polymorphic and behaviorally complex social insect, the leafcutter ant Atta cephalotes. The majority of significant differential gene expression observed among three morphologically, behaviorally, and neuroanatomically differentiated worker size groups was attributable to body size. However, we also found evidence of differential brain gene expression unexplained by worker morphological variation and transcriptomic analysis identified patterns not linearly correlated with worker size but sometimes mirroring neuropil scaling. Additionally, we identified enriched gene ontology terms associated with nucleic acid regulation, metabolism, neurotransmission, and sensory perception, further supporting a relationship between brain gene expression, brain mosaicism, and worker labor role. These findings demonstrate that differential brain gene expression among polymorphic workers underpins behavioral and neuroanatomical differentiation associated with complex agrarian division of labor in A. cephalotes.

Automated summary

By measuring patterns of gene expression and neuroanatomy, we found that the majority of gene expression differences among worker groups in leafcutter ants could be explained by body size. However, we also discovered brain gene expression differences unrelated to worker morphology, which may be related to neuropil scaling. Additionally, enriched gene ontology terms associated with nucleic acid regulation, metabolism, neurotransmission, and sensory perception further support the relationship between brain gene expression, brain mosaicism, and worker labor role. These findings demonstrate that differential brain gene expression among polymorphic workers underpins behavioral and neuroanatomical differentiation associated with complex agrarian division of labor in leafcutter ants.