Collaborative Research: Social Environment Effects on Hormones and the Integrated Behavioral Phenotype

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Animals must adjust their behaviors and other traits to a constantly changing social environment. For example, the strategies and the signals that individuals use to attract mates and breed often depend on an individual's social status relative to others in the population, and that status can fluctuate as group composition changes and/or other individuals change in rank. Accordingly, the hormonal and genetic mechanisms that underlie such behaviors and signals are likely to be sensitive to social conditions. Yet, we know relatively little about these mechanisms, particularly in wild populations living under natural conditions. This project will examine the mechanisms that allow for behavioral flexibility, and the ways that those mechanisms evolve, using Australian fairy-wrens (genus Malurus) as a model system. These study species are uniquely suited to this research because they show pronounced variation, across both individuals and populations, in the visual signals that individuals use to attract mates, and a great deal is known about the effects of hormones (particularly androgens like testosterone) on the development of these signals. This project will use a state-of-the-art semi-automated radio tracking system to continuously monitor social interactions among individuals to examine the effects of those interactions on hormones and gene expression in the brain, and use experimental manipulation of social conditions in the field to demonstrate the underlying causes. Comparisons across populations and across the sexes will be conducted, making this one of the first studies to examine the role and regulation of breeding signals in females. Overall, this research will contribute to a better understanding of the hormonal and genetic mechanisms that allow individuals to adjust to a constantly changing social environment. In addition this work will build capacity in Papua New Guinea, a richly biodiverse region of considerable conservation concern, through key partnerships and direct involvement of locals in research, educational outreach, and interchange activities. Public educational materials also will be created, including short videos presenting results from the research as well as the process of doing the research, for broad dissemination through proven and highly visited internet channels. Thus, this project will have broad impacts on both conservation and public understanding of science.A central goal of the animal behavior research agenda is to identify the role of androgens and other hormones in regulating expression of ornaments and associated reproductive behaviors, yet to date these roles remain unclear. One view, which has received relatively little attention from behavioral ecologists, is that androgens are phenotypic integrators that act to produce an adaptive multi-dimensional phenotype that is well suited to its social environment. This collaborative project will build on previous research with two sister species of Malurus fairy-wren that exhibit intraspecific variation in male and female ornamentation, making this system uniquely suited for examining these issues. The project consists of three inter-related studies that, together and synergistically, will address key questions regarding how androgens modulate expression of breeding signals and associated behaviors. First, high-density data on social interactions, collected from an automated telemetry array in conjunction with experimental manipulation of social environment, will be used to examine the role of social interactions and early-life conditions in regulating individual androgen levels and breeding phenotype. Second, a combination of observational, genomic and hormone manipulation approaches will be used to examine the extent to which androgens affect whole suites of characters to produce an integrated reproductive phenotype. Finally, hormone implant experiments and genomic analyses across the sexes and across two closely related species will reveal the degree of evolutionary constraint on hormonal mechanisms regulating ornament elaboration and behavior. By bridging the gap between the ways that behavioral ecologists and endocrinologists view hormones, this project will transform the ways that we view the role of hormones in regulating phenotypic integration and signaling.