Reciprocal social ties drive stable cooperation within a social network

ABSTRACTSocial reciprocity is thought to be the most important driver of cooperation among non-kin, but its effects on complex social networks in the wild have not been studied. Here, we test whether reciprocation can explain social dynamics in a cooperative bird, the wire-tailed manakin (Pipra filicauda). Over three years of study, we observed that territory holding males engaged in far more reciprocated (bidirectional) partnerships with other territory holders than expected by chance. Reciprocated partnerships were also stronger (i.e., the partners interacted more frequently) than non-reciprocated partnerships, controlling for spatial proximity. Furthermore, we show that a male’s social contribution to a given partner was predictive of the number of social interactions he received from that same partner. Finally, we show that reciprocation predicted the long-term stability of a partnership one year later. Together, these results demonstrate that reciprocity can stabilize cooperation within a broader social network.

Reduced cooperative behavior as a cost of high testosterone in a lekking passerine bird

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.

Testosterone modulates status-specific patterns of cooperation in a social network

SummaryStable cooperation requires plasticity whereby individuals are able to express competitive or cooperative behaviors depending on social context. To date, however, the physiological mechanisms that underlie behavioral variation in cooperative systems are poorly understood. We studied hormone-mediated behavior in the wire-tailed manakin (Pipra filicauda), a gregarious songbird whose cooperative partnerships are crucial for fitness. We used automated telemetry to monitor > 36,000 cooperative interactions among male manakins over three field seasons, and we examined how circulating testosterone affects cooperation using > 500 hormone samples. Observational data show that in non-territorial floater males, high testosterone is associated with increased cooperative behaviors and subsequent ascension to territorial status. In territory-holding males, however, both observational and experimental evidence demonstrate that high testosterone antagonizes cooperation. Moreover, circulating testosterone explains significant variation (2-8%) in social behavior within each status class. Collectively, our findings show that the hormonal control of cooperation depends on a male’s social status. We propose that the status-dependent reorganization of hormone-regulatory pathways can facilitate stable cooperative partnerships, and thus provide direct fitness benefits for males.

Co-regulation of hormone receptors, neuropeptides, and steroidogenic enzymes across the vertebrate social behavior network

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 (WGCNA), we reconstructed sets of coregulated genes, revealing striking patterns of variation in neuroendocrine gene expression across the SBN. We describe regional expression variation networks comprising a broad set of hormone receptors, neuropeptides, steroidogenic enzymes, catecholamines, and other neuroendocrine signaling molecules. Our findings highlight how heterogeneity of brain gene expression across the SBN can provide functional insights into the neuroendocrine and genetic mechanisms that underlie vertebrate social behavior.

Climate, demography and lek stability in an Amazonian bird

Lekking is a rare, but iconic mating system where polygynous males aggregate and perform group displays to attract females. Existing theory postulates that demographic and environmental stability are required for lekking to be an evolutionarily viable reproductive strategy. However, we lack empirical tests for the hypotheses that lek stability is facilitated by age-specific variation in demographic rates, and by predictable, abundant resources. To address this knowledge gap, we use multistate models to examine how two demographic elements of lek stability—male survival and recruitment—vary with age, social status and phase of the El Niño Southern Oscillation (ENSO) in a Neotropical frugivorous bird, the wire-tailed manakin ( Pipra filicauda ) . Our results show that demographic and environmental conditions were related to lek stability in the Ecuadorean Amazon. Apparent annual survival probability of territorial males was higher than that of non-territorial floaters, and recruitment probability increased as males progressed in an age-graded queue. Moreover, annual survival of territorial males and body condition of both floaters and territory holders were higher following years with El Niño conditions, associated with reduced rainfall and probably higher fruit production in the northern Neotropics, and lower after years with wet, La Niña conditions that predominated our study. Recruitment probabilities varied annually, independent of ENSO phase, and increased over our study period, but the annual mean number of territorial males per lek declined. Our results provide empirical support for hypothesized demographic and environmental drivers of lek dynamics. This study also suggests that climate-mediated changes in resource availability can affect demography and subsequent lek stability in a relatively buffered, lowland rainforest.

Proximity data-loggers increase the quantity and quality of social network data

Social network analysis is an ideal quantitative tool for advancing our understanding of complex social behaviour. However, this approach is often limited by the challenges of accurately characterizing social structure and measuring network heterogeneity. Technological advances have facilitated the study of social networks, but to date, all such work has focused on large vertebrates. Here, we provide proof of concept for using proximity data-logging to quantify the frequency of social interactions, construct weighted networks and characterize variation in the social behaviour of a lek-breeding bird, the wire-tailed manakin, Pipra filicauda . Our results highlight how this approach can ameliorate the challenges of social network data collection and analysis by concurrently improving data quality and quantity.