Proximate Mechanisms Influencing Individual Variation in Cooperative Behavior

Cooperation is a complex behavior in which individuals act in ways that increase the fitness of others, at some cost to themselves. In cooperatively breeding vertebrates, helpers capable of reproducing forgo their own reproduction to assist raising offspring produced by breeders. Cooperative breeding in many species is facultative. In such cases, breeders within a single population differ in whether they are assisted by helpers, and potential helpers differ in whether they join a group and provide alloparental care. A major challenge in the study of cooperative breeding behavior is understanding why individuals differ in their cooperative tendency and their contributions to cooperative activities. The ultimate causes of variation in cooperative breeding behavior are increasingly well understood. Our understanding of the underlying physiological mechanisms and behaviors associated with individual differences in cooperative tendency remains poorly studied. In order to understand why cooperative behavior varies within a population, it is necessary to consider the proximate mechanisms associated with variation in cooperative breeding behavior from both the breeders’ and potential helpers’ perspectives. I investigated proximate mechanisms underlying individual variation in cooperative breeding behavior in a wild, color-marked population of facultative, cooperatively breeding brown-headed nuthatches (Sitta pusilla). The study population was located in north Florida at Tall Timbers Research Station. In this population, cooperation varies among breeders and helpers. Approximately 30% of breeding pairs are assisted by at least one second-year, male helper. Second year males also vary in their cooperative tendency, some males become helpers, others attempt to breed independently, and some do not associate with a social group. From 2013-2018, I used observations and experiments to investigate (1) how helpers contribute to breeders’ reproductive effort and how breeders alter their own investment when assisted by a helper, (2) how breeders’ prior nesting success and cooperative status affect subsequent helper recruitment, (3) how potential helpers’ early life physiological mechanisms influence individual variation in cooperation, and (4) how variation in aggressive behavior among breeders influences variation in cooperative behavior. Breeders assisted by helpers did not reduce their investment in offspring production or care, and as a result, nestlings raised by cooperative groups received more food, weighed more, and were more likely to fledge compared to nestlings raised by just the breeding pair. Variation in cooperation among breeders was not explained by differences in breeders’ prior nesting success or cooperative status. Eight-three percent of breeders that recruited helpers had fledged offspring the previous breeding season, yet 56% of unassisted breeders had also fledged young the previous year. These data suggest fledging young is neither necessary nor sufficient in explaining variation in cooperative behavior among breeders. Furthermore, variation in aggressive behavior was unrelated to variation in helper recruitment among breeders. Breeders’ aggressive behavior in response to a heterospecific competitor model was unrelated to breeders’ current cooperative status, and did not predict future recruitment of helpers. These data suggest that, while we thought that aggression and cooperation would represent a behavioral conflict, they do not. Variation in cooperation behavior among potential helpers was related to variation in hormone concentrations, and not variation in relatedness among group members. For potential helpers, variation in nestling corticosterone (the primary stress hormone in birds), not relatedness, predicted which individuals became helpers. Nestlings with lower levels of stress-induced corticosterone were more likely to become helpers, but were not significantly more related to the breeding male compared to their non-helping siblings. My dissertation research investigated proximate mechanisms that influence individual variation in the decision to cooperate, a relatively unexplored aspect of cooperative breeding behavior. This study is one of the first to document a link between glucocorticoids and future helping, and demonstrates that variation in the expression of cooperative behavior may be due to individual differences in underlying physiological mechanisms and behaviors, not relatedness alone. This research contributes to our understanding of variation in cooperative behavior and cooperation among unrelated individuals.