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Social networks can vary in their organization and dynamics, with implications for ecological and evolutionary processes. Understanding the mechanisms that drive social network dynamics requires integrating individual‐level biology with comparisons across multiple social networks.Testosterone is a key mediator of vertebrate social behaviour and can influence how individuals interact with social partners. Although the effects of testosterone on individual behaviour are well established, no study has examined whether hormone‐mediated behaviour can scale up to shape the emergent properties of social networks.We investigated the relationship between testosterone and social network dynamics in the wire‐tailed manakin, a lekking bird species in which male–male social interactions form complex social networks. We used an automated proximity system to longitudinally monitor several leks and we quantified the social network structure at each lek. Our analysis examines three emergent properties of the networks—social specialization (the extent to which a network is partitioned into exclusive partnerships), network stability (the overall persistence of partnerships through time) and behavioural assortment (the tendency for like to associate with like). All three properties are expected to promote the evolution of cooperation. As the predictor, we analysed the collective testosterone of males within each social network.Social networks that were composed of high‐testosterone dominant males were less specialized, less stable and had more negative behavioural assortment, after accounting for other factors. These results support our main hypothesis that individual‐level hormone physiology can predict group‐level network dynamics. We also observed that larger leks with more interacting individuals had more positive behavioural assortment, suggesting that small groups may constrain the processes of homophily and behaviour‐matching.Overall, these results provide evidence that hormone‐mediated behaviour can shape the broader architecture of social groups. Groups with high average testosterone exhibit social network properties that are predicted to impede the evolution of cooperation. [ABSTRACT FROM AUTHOR]

Many studies have identified the reproductive benefits of cooperative behaviors, yet few have identified the mechanisms that underlie these behaviors. Mechanistic studies can inform our understanding of why some individuals are more or less cooperative, as well as identify the physiological constraints imposed upon the evolution of reproductive traits. Male wire-tailed manakins (Pipra filicauda) exhibit cooperative courtship behaviors and more cooperative territory holders have been shown to exhibit higher reproductive success. To begin to understand the proximate basis of cooperative display behaviors, we conducted both an observational study and an experimental study. Because coordinated courtship displays underlie this form of cooperation, our study also examined both the hormonal and social drivers of individual variation in courtship behavior more broadly (e.g., courtship display rates). Our observational study revealed that males with higher testosterone levels performed fewer cooperative display bouts. In addition, our experimental study demonstrated that the proportion of a male's courtship displays that were cooperative decreased after being administered a testosterone-filled hormone implant. We found no relationship between an individual's courtship display effort (i.e., display rate and time spent performing courtship displays) and circulating testosterone in either study. However, more cooperative males spent a greater proportion of time performing courtship displays than did less cooperative males, suggesting that testosterone may indirectly mediate courtship display behaviors by influencing a territory holder's cooperative behavior. Overall, both our observational and experimental results suggest that reduced cooperative behavior is a cost of maintaining high levels of testosterone for territory-holding males. [ABSTRACT FROM AUTHOR]

The evolution of behavior relies on changes at the level of the genome; yet the ability to attribute a behavioral change to a specific, naturally occurring genetic change is rare in vertebrates. In the white-throated sparrow (Zonotrichia albicollis), a chromosomal polymorphism (ZAL2/2m) is known to segregate with a behavioral phenotype. Individuals with the ZAL2m haplotype engage in more territorial aggression and less parental behavior than individuals without it. These behaviors are thought to be mediated by sensitivity to sex steroids, and the chromosomal rearrangement underlying the polymorphism has captured a prime candidate gene: estrogen receptor 1 (ESR1), which encodes estrogen receptor a (ERα). We therefore hypothesized that the behavioral effects of the ZAL2m rearrangement are mediated by polymorphism in ESR1. We report here that (i) the ESR1 promoter region contains fixed polymorphisms distinguishing the ZAL2m and ZAL2 alleles; (ii); those polymorphisms regulate transcription efficiency in vitro and therefore potentially do the same in vivo (iii); the local expression of ERα in the brain depends strongly on genotype in a free-living population; and (iv) ERα expression in the medial amygdala and medial preoptic area may fully mediate the effects of genotype on territorial aggression and parenting, respectively. Thus, our study provides a rare glimpse of how a chromosomal polymorphism has affected the brain and social behavior in a vertebrate. Our results suggest that in this species, differentiation of ESR1 has played a causal role in the evolution of phenotypes with alternative life-history strategies. [ABSTRACT FROM AUTHOR]

The vertebrate basal forebrain and midbrain contain a set of interconnected nuclei that control social behavior. Conserved anatomical structures and functions of these nuclei have now been documented among fish, amphibians, reptiles, birds and mammals, and these brain regions have come to be known as the vertebrate social behavior network (SBN). While it is known that nuclei (nodes) of the SBN are rich in steroid and neuropeptide activity linked to behavior, simultaneous variation in the expression of neuroendocrine genes among several SBN nuclei has not yet been described in detail. In this study, we use RNA‐seq to profile gene expression across seven brain regions representing five nodes of the vertebrate SBN in a passerine bird, the wire‐tailed manakin Pipra filicauda. Using weighted gene co‐expression network analysis, we reconstructed sets of coregulated genes, showing striking patterns of variation in neuroendocrine gene expression across the SBN. We describe regional variation in gene networks comprising a broad set of hormone receptors, neuropeptides, steroidogenic enzymes, catecholamines and other neuroendocrine signaling molecules. Our findings show heterogeneous patterns of brain gene expression across nodes of the avian SBN and provide a foundation for future analyses of how the regulation of gene networks may mediate social behavior. These results highlight the importance of region‐specific sampling in studies of the mechanisms of behavior. [ABSTRACT FROM AUTHOR]

The neurogenomic mechanisms mediating male–male reproductive cooperative behaviours remain unknown. We leveraged extensive transcriptomic and behavioural data on a neotropical bird species (Pipra filicauda) that performs cooperative courtship displays to understand these mechanisms. In this species, the cooperative display is modulated by testosterone, which promotes cooperation in non‐territorial birds, but suppresses cooperation in territory holders. We sought to understand the neurogenomic underpinnings of three related traits: social status, cooperative display behaviour 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 behaviour. We associated gene expression with each bird's behavioural 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 signalling appeared to be important in mediating status‐specific relationships between testosterone and cooperation, suggesting shared regulatory mechanisms with male aggressive and sexual behaviours. 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 behaviour and suggest that differences in neurogenomic state are the basis for individual differences in social behaviour. [ABSTRACT FROM AUTHOR]