Neurogenomic landscape of social status-dependent cooperative display behavior

The neurogenomic mechanisms mediating male-male reproductive cooperative behaviors are unknown. We leveraged extensive transcriptomic and behavioral data on a neotropical bird (Pipra filicauda) that perform cooperative courtship displays to understand these mechanisms. Cooperative display is modulated by testosterone, it promotes cooperation in non-territorial birds, but suppresses cooperation in territory holders. We sought to understand the neurogenomic underpinnings of these three related traits: social status, cooperative behavior, and testosterone phenotype. To do this, we profiled gene expression in 10 brain nuclei spanning the social decision-making network (SDMN), and two key endocrine tissues that regulate social behavior. We associated gene expression with each birds behavioral and endocrine profile derived from three years of repeated measures taken from free-living birds in the Ecuadorian Amazon. We found distinct landscapes of constitutive gene expression were associated with social status, testosterone phenotype, and cooperation, reflecting the modular organization and engagement of neuroendocrine tissues. Sex-steroid and neuropeptide signaling appeared to be important in mediating status-specific relationships between testosterone and cooperation, suggesting shared regulatory mechanisms with male aggressive and sexual behaviors. We also identified differentially regulated genes involved in cellular activity and synaptic potentiation, suggesting multiple mechanisms underpin these genomic states. Finally, we identified SDMN-wide gene expression differences between territorial and floater males that could form the basis of "status-specific" neurophysiological phenotypes, potentially mediated by testosterone and growth hormone. Overall, our findings provide new, systems-level insights into the mechanisms of cooperative behavior and suggest that differences in neurogenomic state are the basis for individual differences in social behavior.