Biology subjects

Ryder, T. B.

Publications and source records attributed to Ryder, T. B..

8 recordsLinked to original sources

bioRxiv2022

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.

evolutionary biology↗

bioRxiv2020

Reciprocal social ties drive stable cooperation within a social network

Social reciprocity is thought to be the most important driver of cooperation among non-kin, but its effects within complex social networks where individuals choose their partners have not been studied. Here, we test whether reciprocation can explain social dynamics in a bird species where males form coalitions to court females, the wire-tailed manakin (Pipra filicauda). In our study population, approximately a third of male-male social interactions involve one male leaving his territory to interact and display with the owner of another territory; this directional behaviour provides benefits to the recipient at a cost to the visiting male. We characterize social ties among pairs of territory holders according to the directionality of their interactions, and show here 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 of the territories. An individual-level analysis revealed that a males 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 social partnerships one year later. Together, these results demonstrate that reciprocity is associated with stability in complex social networks where partner choice is flexible. LAY SUMMARYO_ST_ABSWhen animals are free to choose their partners, how does reciprocity influence social dynamics?C_ST_ABSIn the wire-tailed manakin, males form coalitions with other males to help attract mates. We tracked male social networks and found that some males form reciprocal partnerships where each male leaves its territory to display at the others territory. These bidirectional partnerships are particularly strong and stable, indicating that reciprocity is associated with stability in complex social networks.

animal behavior and cognition↗

bioRxiv2019

Gender bias in research teams and the underrepresentation of women in science

Why are females still underrepresented in science? The social factors that affect career choices and trajectories are thought to be important but are poorly understood. We analyzed author gender in a sample of >61,000 scientific articles in the biological sciences to evaluate the factors that shape the formation of research teams. We find that authorship teams are more gender-assorted than expected by chance, with excess homotypic assortment accounting for up to 7% of published articles. One possible mechanism that could explain gender assortment and broader patterns of female representation is that women may focus on different research topics than men (i.e., the \"topic preference\" hypothesis). An alternative hypothesis is that researchers may consciously or unconsciously prefer to work within same-gender teams (the \"gender homophily\" hypothesis). Using network analysis, we find no evidence to support the topic preference hypothesis, because the topics of female-authored articles are no more similar to each other than expected within the broader research landscape. Instead, consistent with a model of moderate gender homophily, we find that the prevalence of matched-gender teams increases as a discipline moves towards gender parity. This can occur because latent preferences are more easily fulfilled in a gender-diverse environment. Finally, we show that female authors pay a substantial citation cost to work in gender-matched teams. Notably, the prevalence of homotypic assortment is predicted to increase in the future if more disciplines shift towards gender parity. These data indicate that social preferences can have important downstream consequences for the retention of women and other underrepresented groups in science.

scientific communication and education↗

bioRxiv2019

Extended hormone-phenotypes shape the structure, stability, and assortment of social networks

O_LISocial 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. C_LIO_LITestosterone is a key mediator of vertebrate social behavior and can influence how individuals interact with social partners. Although the effects of testosterone on individual behavior are well established, no study has examined whether hormone-mediated behavior can scale up to shape the emergent properties of social networks. C_LIO_LIWe 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 behavioral assortment (the tendency for like to associate with like). All three properties are expected to promote the evolution of cooperation. As the predictor, we analyzed the collective testosterone of males within each social network. C_LIO_LISocial networks that were composed of high-testosterone dominant males were less specialized, less stable, and had more negative behavioral 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 behavioral assortment, suggesting that small groups may constrain the processes of homophily and behavior-matching. C_LIO_LIOverall, these results provide evidence that hormone-mediated behavior 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. C_LI

animal behavior and cognition↗

bioRxiv2019

Reciprocity and behavioral heterogeneity govern the stability of social networks

The dynamics of social networks can determine the transmission of information, the spread of diseases, and the evolution of behavior. Despite this broad importance, a general framework for predicting social network stability has not been proposed. Here, we present longitudinal data on the social dynamics of a cooperative bird species, the wire-tailed manakin, to evaluate the potential causes of temporal network stability. We find that when partners interact less frequently, and when the breadth of social connectedness within the network increases, the social network is subsequently less stable. Social connectivity was also negatively associated with the temporal persistence of coalition partnerships on an annual timescale. This negative association between connectivity and stability was surprising, especially given that individual manakins who were more connected also had more stable partnerships. This apparent paradox arises from a within-individual behavioral trade-off between partnership quantity and quality. Crucially, this trade-off is easily masked by behavioral variation among individuals. Using a simulation, we show that these results are explained by a simple model that combines among-individual behavioral heterogeneity and reciprocity within the network. As social networks become more connected, individuals face a trade-off between partnership quantity and maintenance. This model also demonstrates how among-individual behavioral heterogeneity, a ubiquitous feature of natural societies, can improve social stability. Together, these findings provide unifying principles that are expected to govern diverse social systems. Significance StatementIn animal societies, social partnerships form a dynamic network that can change over time. Why are some social network structures more stable than others? We addressed this question by studying a cooperative bird species in which social behavior is important for fitness, similar to humans. We found that stable social networks are characterized by more frequent interactions, but sparser connectivity throughout the network. Using a simulation, we show how both results can be explained by a simple model of reciprocity. These findings indicate that social stability is governed by a trade-off whereby individuals can either maintain a few high-quality partners, or increase partner number. This fundamental trade-off may govern the dynamics and stability of many societies, including in humans.

animal behavior and cognition↗

bioRxiv2018

Testosterone drives status-specific patterns of cooperation and transmission of behavior in a social network

Stable 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 males 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.

animal behavior and cognition↗

bioRxiv2018

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.

neuroscience↗

bioRxiv2018

Dynamic network partnerships and social contagion drive cooperation

Both reciprocity and positive assortment (like with like) are predicted to promote the evolution of cooperation, yet how partners influence each others behavior within dynamic networks is not well understood. One way to test this question is to partition phenotypic variation into differences among individuals in the expression of cooperative behavior (the \"direct effect\"), and plasticity within individuals in response to the social environment (the \"indirect effect\"). A positive correlation between these two sources of variation, such that more cooperative individuals elicit others to cooperate, is predicted to facilitate social contagion and selection on cooperative behavior. Testing this hypothesis is challenging, however, because it requires repeated measures of behavior across a dynamic social landscape. Here, we use an automated data-logging system to quantify the behavior of 179 wire-tailed manakins, birds that form cooperative male-male coalitions, and we use multiple-membership models to test the hypothesis that dynamic network partnerships shape within-individual variation in cooperative behavior. Our results show strong positive correlations between a birds own sociality and his estimated effect on his partners, consistent with the hypothesis that cooperation begets cooperation. These findings support the hypothesis that social contagion can facilitate selection for cooperative behavior within social networks.

animal behavior and cognition↗