Abstract

In social animals, hierarchical rank governs food availability, territorial rights and breeding access. Rank order can change rapidly and typically depends on dynamic aggressive interactions. Since the neuromodulator corticotrophin releasing factor (CRF) integrates internal and external cues to regulate the hypothalamic-pituitary adrenal (HPA) axis, we analyzed the CRF system during social encounters related to status. We used a particularly suitable animal model, African cichlid fish, Astatotilapia burtoni, whose social status regulates reproduction. When presented with an opportunity to rise in rank, subordinate A. burtoni males rapidly change coloration, behavior, and their physiology to support a new role as dominant, reproductively active fish. Although changes in gonadotropin-releasing hormone (GnRH1), the key reproductive molecular actor, have been analyzed during social ascent, little is known about the roles of CRF and the HPA axis during transitions. Experimentally enabling males to ascend in social rank, we measured changes in plasma cortisol and the CRF system in specific brain regions 15 minutes after onset of social ascent. Plasma cortisol levels in ascending fish were lower than subordinate conspecifics, but similar to levels in dominant animals. In the preoptic area (POA), where GnRH1 cells are located, and in the pituitary gland, CRF and CRF1 receptor mRNA levels are rapidly down regulated in ascending males compared to subordinates. In the Vc/Vl, a forebrain region where CRF cell bodies are located, mRNA coding for both CRFR1 and CRFR2 receptors is lower in ascending fish compared to stable subordinate conspecifics. The rapid time course of these changes (within minutes) suggests that the CRF system is involved in the physiological changes associated with shifts in social status. Since CRF typically has inhibitory effects on the neuroendocrine reproductive axis in vertebrates, this attenuation of CRF activity may allow rapid activation of the reproductive axis and facilitate the transition to dominance.

Highlights

  • Social interactions shape the behavior, physiology and reproductive capacity of many animals, especially those living in social groups characterized by dominance hierarchies

  • In the case of the social system of the African cichlid fish Astatotilapia burtoni, when a subordinate individual ascends in social rank, rapid and dramatic changes occur in behavior (3–5 minutes), physiology, and neural activity (30 minutes) as the individual assumes its new dominant phenotype

  • corticotrophin releasing factor (CRF) family mRNA levels in the Vc/ventral telencephalon (Vl) CRF1 receptor levels in Vc/Vl were lower in ascending males compared to both subordinate and dominant males [analysis of variance (ANOVA), F(2,40) = 5.612, P,0.0071; Student-Newman-Keuls, P,0.05] (Fig. 3A)

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Summary

Introduction

Social interactions shape the behavior, physiology and reproductive capacity of many animals, especially those living in social groups characterized by dominance hierarchies. In such species, lower social rank is associated with submissive behavior, reduced reproductive opportunity, and increased hypothalamic-pituitary adrenal (HPA) (hypothalamic-pituitary-interrenal, HPI, axis in fishes) axis activity. The HPA/I axis, which signals via the neuropeptide corticotrophin releasing factor (CRF, known as corticotrophin releasing hormone, CRH), is well known for its role in the stress response [1] This HPA/I axis coordinates behavioral, endocrine, autonomic, immune and reproductive responses to stressors [2]. The timing and downstream effects of social ascent on reproductive physiology have been well documented in A. burtoni [10,11,12,13], but the role of CRF during this status transition has not been examined

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