Social competition is ubiquitous in both animal and human life, and the threat from a competitor typically induces a systemic surge in the steroid hormone testosterone. While past research demonstrates clear connections among social challenges, testosterone and a suite of physiological and behavioral effects, the molecular mechanisms underlying these phenotypic changes are poorly understood. Generating an appropriate organismal response to social challenges requires large scale coordination of behavior and physiology (e.g. changes in aggression, pain tolerance, and metabolism), yet the transcriptomic mechanisms by which brain and body act together to produce a coordinated response to social challenges are unclear. The long-term goal of the proposed research is to determine how steroid hormones serve to link brain and periphery in genomic and behavioral responses to environmental contingencies. The working hypothesis is that social challenges, and their associated testosterone surges, prime individuals for success in future competition, favoring greater mobilization of energy reserves, heightened response to injury or inflammation, and greater spatial and sensory capabilities, all at the expense of self-maintenance. The objectives of this particular application are to identify how gene transcription is altered by aggressive social interactions, and to characterize how the environmental effects of a social challenge differ in brain and periphery, while engendering a coordinated organismal response to social instability. The subject is a well-studied songbird in which social challenges lead to a systemic surge in testosterone, and the effects of testosterone on many aspects of behavior and physiology are well characterized (aggression, immune function, stress, activity, etc.). By employing emerging genomic techniques, including gene set enrichment and network co-expression analyses, the proposed research will identify the effects of (1) acute social challenges and (2) persistent social instability on gene transcription, relative to unchallenged control animals. These data will reveal gene families, hubs of connectivity within gene networks, and neural and peripheral tissues that are particularly prone to socially induced plasticity. Patterns of co-variation among tissues will further reveal the precise molecular mechanisms by which social challenges prime the brain and body for a coordinated response to social instability. Knowledge of how social stressors derail normal healthy organismal function can be applied to a range of hormonally and socially induced human health issues (e.g. reproductive health, behavioral disorders of high aggression, etc.), where insights to be gained by co-discussion of social environment, brain, and periphery have yet to be fully realized.

Public Health Relevance

Because social stressors are pervasive in human and animal life, and the proposed studies will identify the genes, brain regions and peripheral organs that are particularly susceptible to either acute or persistent socially stressors, this research fills unresolved knowledge gaps about the molecular mechanisms by which socially challenging experiences engender physiological and behavioral effects. Social competition and the hormonal changes that coincide with social challenges have been linked with a variety of public health issues in humans (e.g. bullying, ADHD, conduct disorder, cardiac and reproductive health, etc.). Thus, the proposed research, which identifies the effects of social instability on organism-wide gene expression, will lay the groundwork for advances in developing new targets for the treatment and prevention of a number of behavioral and physiological disorders affecting children and adults of all ages.

National Institute of Health (NIH)
Eunice Kennedy Shriver National Institute of Child Health & Human Development (NICHD)
Exploratory/Developmental Grants (R21)
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Biobehavioral Regulation, Learning and Ethology Study Section (BRLE)
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Freund, Lisa S
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Indiana University Bloomington
Schools of Arts and Sciences
United States
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Rosvall, Kimberly A; Peterson, Mark P; Reichard, Dustin G et al. (2014) Highly context-specific activation of the HPG axis in the dark-eyed junco and implications for the challenge hypothesis. Gen Comp Endocrinol 201:65-73
Rosvall, Kimberly A; Peterson, Mark P (2014) Behavioral effects of social challenges and genomic mechanisms of social priming: What's testosterone got to do with it? Curr Zool 60:791-803
Rosvall, Kimberly A (2013) Proximate perspectives on the evolution of female aggression: good for the gander, good for the goose? Philos Trans R Soc Lond B Biol Sci 368:20130083