American Society of Naturalists

T. Brandt Ryder, Roslyn Dakin, Ben J. Vernasco, Brian S. Evans, Brent M. Horton, and Ignacio T. Moore (Jan 2020)

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Testosterone helps male birds ascend in social status, but too much is detrimental to their cooperative behavior

Cooperation has fascinated biologists for hundreds of years. Why are some individuals more cooperative and others more competitive? What underlies these differences in behavior and how do those individual differences contribute to stable cooperative societies? Although biologists have long known that hormones shape behavior, our understanding of the mechanisms that enable behavioral flexibility in cooperative social networks remains virtually unstudied.

Ryder et al. studied the hormonal basis of variation in cooperative behavior in a lekking tropical birds. Leks are a social system where males join together and display to attract females. Using a novel biologging system, the researchers autonomously collected data on the cooperative social networks (i.e., who interacts with whom and the frequency of those interactions). These data were combined with repeated measures of circulating testosterone to ask if circulating hormones drive individual differences in cooperative tendencies.

The researchers found that testosterone, a hormone long known for its mediation of aggression, can also influence social behavior in a cooperative social system. High testosterone was associated with increased cooperative tendencies in young, non-territorial males, but it was antagonistic to those same behaviors once a male acquired his own territorial at the lek. This research highlights how hormones can have diverse effects on behavior, depending upon an animal’s life stage, and it underscores the importance of testosterone in context-dependent behavioral flexibility.

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Abstract

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 and competition for status are both 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.