Social context-dependent relationships between mouse dominance rank and plasma hormone levels

Abstract

The associations between social status and endogenous testosterone and corticosterone have been well-studied across taxa, including rodents. Dominant social status is typically associated with higher levels of circulating testosterone and lower levels of circulating corticosterone but findings are mixed and depend upon numerous contextual factors. Here, we determine that the social environment is a key modulator of these relationships in Mus musculus. In groups of outbred CD-1 mice living in stable dominance hierarchies, we found no evidence of simple linear associations between social rank and corticosterone or testosterone plasma levels. However, in social hierarchies with highly despotic alpha males that socially suppress other group members, testosterone levels in subordinate males were significantly lower than in alpha males. In less despotic hierarchies, where all animals engage in high rates of competitive interactions, subordinate males had significantly elevated testosterone compared to agonistically inhibited subordinates from despotic hierarchies. Subordinate males from highly despotic hierarchies also had elevated levels of corticosterone compared to alpha males. In pair-housed animals, the relationship was the opposite, with alpha males exhibiting elevated levels of corticosterone compared to subordinate males. Notably, subordinate males living in social hierarchies had significantly higher levels of plasma corticosterone than pair-housed subordinate males, suggesting that living in a large group is a more socially stressful experience for less dominant individuals. Our findings demonstrate the importance of considering social context when analyzing physiological data related to social behavior and using ethologically relevant behavioral paradigms to study the complex relationship between hormones and social behavior.

Quantitative trait locus mapping and analysis of heritable variation in affiliative social behavior and co‐occurring traits

“…Yet, because social approach precedes adult‐initiated partner sniffing, the lack of tighter correlation of these aspects of sociability across strains was somewhat unexpected. The expression of social behaviors depends importantly upon the interplay between the magnitude of internal social drives and the specific social (eg, age, sex, familiarity of the partner) and environmental (familiarity, safety, size) context . Thus, we suggest that rank‐order variation across tasks is likely because of important task differences, including differences in partner attributes (juvenile, adult), behavioral requirements (chamber exploration, presence of novel objects), and ethological relevance of behaviors (direct interaction vs restricted partner access).…”

Stress‐Induced Depression: Is Social Rank a Predictive Risk Factor?

“…Indeed, during social reorganization in baboons, dominant individuals show the greatest psychological stress compared to their subordinates counterparts . In outbred CD1 mice, dominants display lower corticosterone levels than subordinates, that are more physiologically stressed, in highly despotic social groups . In contrast, dominant mice show greater plasma corticosterone than subordinates in pair‐housed conditions .…”

“…In outbred CD1 mice, dominants display lower corticosterone levels than subordinates, that are more physiologically stressed, in highly despotic social groups . In contrast, dominant mice show greater plasma corticosterone than subordinates in pair‐housed conditions . Noteworthy, subordinates from social structures generated by the visible burrow system (VBS) in rats display a blunted corticosterone response to acute novel stressor following 14‐day chronic social stress in the visible burrow system suggesting that subordinates are more vulnerable to subsequent stressors than dominant rats.…”

“…To what extent differences in methodology for assessing dominance–submissive relationships are critical to conclude about the vulnerability to stress linked to a particular social rank. Given that social behaviors depend on a range of interacting environmental, individual, and social factors, it would be important to assess vulnerability in social rank establishment through other models and procedures (e.g., Refs. ).…”

“…However, in inbred mice maintained under equivalent experimental and husbandry conditions, individual differences could be due to the exposure of differential factors during early development (e.g., differences in maternal care or in social interactions between siblings) or to specifics related to the social organization within the homecage. In fact, social behaviors depend on a range of interacting environmental, individual, and social factors . There might be a priori differences that predispose individuals to attain a specific social rank order.…”