| Popis: |
The neurogenomic mechanisms mediating cooperation in animals are understudied. Here we leverage extensive transcriptomic and behavioral data on birds that perform cooperative courtship displays to better understand the mechanisms underlying cooperative behaviors. Males of the neotropical wire-tailed manakin (Pipra filicauda) form cooperative display coalitions and their cooperative behaviors are modulated by testosterone in a status-specific manner. That is, testosterone promotes cooperation in non-territorial birds, but suppresses it 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 known to regulate social behavior. We associated gene expression with each bird’s detailed behavioral and endocrine profile derived from 3 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 appear to be important in mediating status-specific relationships between testosterone and cooperation, which suggests shared regulatory mechanisms with male aggressive and sexual behaviors. We also identify differentially regulated genes that are involved in cellular activity and synaptic potentiation, suggesting that multiple mechanisms underpin these genomic states. Finally, we identify 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 behavior, and suggest that differences in neurogenomic state are the basis for individual differences in social behavior.Significance StatementCooperative behavior is an important determinant of fitness in many animals, yet its neurogenomic underpinnings remain poorly understood. We leveraged an unprecedented dataset describing gene expression in multiple brain nuclei and endocrine tissues from male wire-tailed manakins (Pipra filicauda) characterized for social status, behavior, and testosterone phenotype in the Ecuadorian Amazon. In this species, testosterone influences an unusual male-male cooperative display, but the nature of the relationship between cooperation and circulating testosterone depends on social status. We found evidence that individual behavioral phenotypes are determined by a complex neurogenomic landscape across interconnected brain nuclei. We show, on a transcriptomic scale, that brain modularity and hormone pleiotropy drive status-specific differences in gene expression resulting individual differences in cooperative behavior. |
