Social Status Predicts How Sex Steroid Receptors Regulate Complex Behavior across Levels of Biological Organization

Abstract

Social status strongly affects behavior and physiology, in part mediated by gonadal hormones, although how each sex steroid acts across levels of biological organization is not well understood. We examine the role of sex steroids in modulating social behavior in dominant (DOM) and subordinate (SUB) males of a highly social fish, Astatotilapia burtoni. We first used agonists and antagonists to each sex steroid receptor and found that androgens and progestins modulate courtship behavior only in DOM, whereas estrogens modulate aggressive behavior independent of social status. We then examined the hormonal and physiological responses to sex steroid receptor antagonist treatment and uncovered substantial changes in circulating steroid hormone levels and gonad size only in SUB, not in DOM. Consistent with status-based physiological sensitivities to drug manipulation, we found that neuropeptide and steroid receptor gene expression in the preoptic area was sensitive only in SUB. However, when we compared the transcriptomes of males that received either vehicle or an estrogen receptor antagonist, 8.25% of all genes examined changed expression in DOM in comparison with only 0.56% in SUB. Finally, we integrate behavior, physiology, and brain gene expression to infer functional modules that underlie steroid receptor regulation of behavior. Our work suggests that environmentally induced changes at one level of biological organization do not simply affect changes of similar magnitude at other levels, but that instead very few key pathways likely serve as conduits for executing plastic responses across multiple levels.