Associations between glucocorticoids and sociality across a continuum of vertebrate social behavior

Abstract

The causes and consequences of individual differences in animal behavior and stress physiology are increasingly studied in wild animals, yet the possibility that stress physiology underlies individual variation in social behavior has received less attention. In this review, we bring together these study areas and focus on understanding how the activity of the vertebrate neuroendocrine stress axis (HPA‐axis) may underlie individual differences in social behavior in wild animals. We first describe a continuum of vertebrate social behaviors spanning from initial social tendencies (proactive behavior) to social behavior occurring in reproductive contexts (parental care, sexual pair‐bonding) and lastly to social behavior occurring in nonreproductive contexts (nonsexual bonding, group‐level cooperation). We then perform a qualitative review of existing literature to address the correlative and causal association between measures of HPA‐axis activity (glucocorticoid levels or GCs) and each of these types of social behavior. As expected, elevated HPA‐axis activity can inhibit social behavior associated with initial social tendencies (approaching conspecifics) and reproduction. However, elevated HPA‐axis activity may also enhance more elaborate social behavior outside of reproductive contexts, such as alloparental care behavior. In addition, the effect of GCs on social behavior can depend upon the sociality of the stressor (cause of increase in GCs) and the severity of stress (extent of increase in GCs). Our review shows that the while the associations between stress responses and sociality are diverse, the role of HPA‐axis activity behind social behavior may shift toward more facilitating and less inhibiting in more social species, providing insight into how stress physiology and social systems may co‐evolve.

The influence of stress hormones and aggression on cooperative behaviour in subordinate meerkats

“…One hypothesis that could explain our results is that there are sex differences in the central distribution of GRs or receptors for other components involved the neuroendocrine stress axis (69) that in turn modify how GCs alter cooperative behaviour. For example, increased production of corticotropin-releasing factor (CRF) in the mesolimbic system due to elevated GCs could promote fear and anxiety of conspecifics thereby reducing social behaviour (27,28). CRF receptors in females may be hypersensitive compared to males (68) such that there is a lower threshold in females than males at which GCs cause a reduction in social behaviour.…”

“…For instance, mifepristone is a selective GR antagonist that can lower the expression of behaviours influenced by GCs such as reducing the expression of anti-social behaviours in humans (social withdrawal behaviour) that are associated with major depression, anxiety, or post-traumatic stress (26). How exactly changes in GCs or their genomic (binding to MRs or GRs) or non-genomic consequences affect behaviour is an active area of research (27). Previous studies suggest the possibility that increased GCs can reduce social behaviour by affecting the activity of neural circuits in the mesolimbic pathway such as promoting fear of conspecifics (28) or altering the reward value of social interactions (29)(30).…”

Early-life manipulation of cortisol and its receptor alters stress axis programming and social competence

“…Affiliative behaviours and glucocorticoid levels have been shown to be related in other vertebrates [84]. For example, in bonobos (Pan paniscus), aggressive conflicts increase HPA axis activity and promote affiliative behaviours between victims of the conflict and conspecifics [84]. Furthermore, in rhesus macaques (Macaca mulatta), playful behaviours in young males correlate with lower cortisol levels [85].…”

Corticosterone administration targeting a hypo-reactive HPA axis rescues a socially-avoidant phenotype in scarcity-adversity reared rats

“…, Fries et al, 2005; Heim et al, 2000). While prior studies have linked poverty-related adversity to reduced cortisol secretion in children and adults (Bernard et al, 2015; Karb et al, 2012; Zalewski et al, 2012), the subsequent consequences of hypocortisolism on social behavior remain poorly understood (for review see Charmandari et al, 2003; Gunnar and Vazquez, 2001; Miller, 2018; Raulo and Dantzer, 2018; van Goozen et al, 2007). Furthermore, animal models are needed to discern the causality/directionality of relations between adversity exposure, HPA axis activity, and social development, as well as to explicitly test these relations as a function of developmental timing.…”