(2nd Place) Elaborated division of labor is facilitated by neuropeptide interplay in the leafcutter ant

Social insects offer powerful models to investigate the link between epigenetic regulation of genes and behavior because distinct tasks are segregated among nearly genetically identical females. Workers of the leafcutter ant genus Atta exhibit an extreme example of this task partitioning, wherein behaviors are typically segregated among highly phenotypically distinct individual castes. Here, we provide the first molecular characterization of the different castes and identify specific neuropeptides as mediators of caste division of labor in A. cephalotes. First, we find that the neuropeptide CCAP is highly expressed in the brain of the leaf cutter caste, and injection into Supermajor leads to leaf movement/carrying behavior. Second, we identify neuroparsin-A (NPA) as a regulator of brood caretaking behavior. NPA showed elevated expression in forager castes relative to caretaking castes. Injection of NPA peptides into the brain of nurses suppressed caretaking behavior. By contrast, knockdown of neuroparsin-A in the brain of supermajors resulted in the acquisition of caretaking behavior as well as a shift in the transcriptome towards a nurse-like state. Importantly, caretaking was rescued when NPA injection in nurses was paired with knockdown of the putative receptor for NPA. Comparison of A. cephalotes RNAseq data with the transcriptome of a eusocial mammal (Naked Mole Rat) revealed global similarities in transcriptional differences between foraging and caretaking castes, despite the absence of a direct NPA ortholog in mammals. We propose that neuroparsin-A governs caretaking behavior in leafcutter ants, by controlling conserved mechanisms of behavioral regulation shared between insects and mammals.