Behavioral effects of social challenges and genomic mechanisms of social priming: What’s testosterone got to do with it?

Abstract

Social challenges from rival conspecifics are common in the lives of animals, and changes in an animal’s social environment can influence physiology and behavior in ways that appear to be adaptive in the face of continued social instability (i.e. social priming). Recently, it has become clear that testosterone, long thought to be the primary mediator of these effects, may not always change in response to social challenges, an observation that highlights gaps in our understanding of the proximate mechanisms by which animals respond to their social environment. Here, our goal is to address the degree to which testosterone mediates organismal responses to social cues. To this end, we review the behavioral and physiological consequences of social challenges, as well as their underlying hormonal and gene regulatory mechanisms. We also present a new case study from a wild songbird, the dark-eyed junco (Junco hyemalis), in which we find largely divergent genome-wide transcriptional changes induced by social challenges and testosterone, respectively, in muscle and liver tissue. Our review underscores the diversity of mechanisms that link the dynamic social environment with an organisms’ genomic, hormonal, and behavioral state. This diversity among species, and even among tissues within an organism, reveals new insights into the pattern and process by which evolution may alter proximate mechanisms of social priming.

Neurogenomic insights into paternal care and its relation to territorial aggression

“…The two experiments studied behaviors at the opposite ends of a continuum of social behavior: paternal care provokes affiliative behavior while a territorial challenge provokes aggressive behavior, and the challenge hypothesis originally posited that patterns of testosterone secretion reflects tradeoffs between parental care and territory defense, assuming that testosterone is incompatible with parental care in males 22 . Subsequent studies have shown that testosterone is not always inhibitory of parental care 35 , and that a territorial challenge activates gene regulatory pathways that do not depend on the action of testosterone 36 . Regardless of the specific neuromodulators or hormones, a mechanistic link between parental care and territory defense is likely to operate through the social behavior network in the brain because most nodes of this network express receptors for neuromodulators and hormones that are involved with both parental care and aggression 37 .…”

Bi‐directional actions of dehydroepiandrosterone and aggression in female Siberian hamsters

“…For example, in territorial California mice ( Peromyscus californicus ), winning in the home cage (Fuxjager et al, ), and repeated post‐victory surges in androgens, increase the likelihood of winning (Fuxjager et al, ). Bi‐directional feedback of behavior and physiology are hypothesized to prepare animals for future social encounters [reviewed in: (Rosvall and Peterson, )]. Thus, it is possible that ACTH challenges, in the absence of actual social interactions, are not sufficient to elicit further increases in aggression.…”

Dynamic modulation of sociality and aggression: an examination of plasticity within endocrine and neuroendocrine systems

“…In many taxonomically diverse species, prevailing in social contests triggers an androgen response that elevates aggression during subsequent social interactions, and this heightened aggression increases the likelihood of winning future contests [100][101][102]. Social interactions can also prime future responses by altering androgen receptor density and gene expression [103,104], and the androgen modulation of VP receptors in the brain [105,106].…”