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.

Keywords: animal personality; cooperation; cooperative breeding; glucocorticoids; hypothalamic‐pituitary‐adrenal axis; pair‐bond; parental care; social behavior; stress.

Figure 1

Different categories of social behavior discussed in this review. Categories range from initial social tendencies (proactive personality) to social behavior occurring in reproductive contexts (parental care, sexual pair‐bonding) and lastly to social behavior occurring in a nonreproductive contexts (nonsexual bonding, group‐level cooperation)

Figure 2

A predictive framework for the effects of glucocorticoids (GCs) on different categories of social behavior. (a) At the level of initial social tendencies to approach conspecifics (proactive personality), increasing GCs are expected to be inversely associated with social behavior (“The inhibitory role of GCs”). (b) In the context of parental care, GCs may affect this form of social behavior in a nonlinear fashion, facilitating it in moderate levels but inhibiting it at very low or very high levels. (c) In the context of pair‐bonding or affiliative behavior, GCs may inhibit social behavior in sexual contexts but facilitate it in nonsexual contexts (see Figure 1 for description of these two types of affiliation). The latter trend is likely limited to a threshold level of GCs beyond which GCs no longer promote social behavior. Furthermore, solely nonsocial environmental stressors are likely to have more negative effect on affiliation than social stressors. (d) In the context of group‐level cooperation, GCs increase social behavior without a threshold level (“The facilitating role of GCs”)

Figure 3

Summary of evidence between measures of glucocorticoids (GCs) and proactivity in wild vertebrates. Studies measuring stress‐induced or integrated GCs show proactivity is mostly negatively correlated with GCs, whereas studies measuring baseline GCs show mostly no correlation. Sociality of the species is not associated with the relationship between GCs and proactivity. Counts are comparisons where any measure of GCs and proactivity were investigated and in some cases there was more than one comparison per study (see Table S1)

Figure 4

Summary of evidence on the associations between measures of glucocorticoids (GCs) and parental care in wild vertebrates. Most comparisons showed that parental care is negatively associated with GCs when they are elevated within the stress induced range or given a high dose of experimental GCs whereas positive correlations are apparent in comparisons with GCs on lower baseline range (baseline GCs or low dose experimental GCs). Counts are comparisons where any measure of GCs and parental care were investigated and in some cases there was more than one comparison per study (see Table S2)

Figure 5

Summary of evidence between measures of glucocorticoids (GCs) and nonsexual pair‐bonding behavior in wild vertebrates. Most studies support our prediction that GCs have a positive effect on pair‐bonding behavior (affiliation) where increased affiliative behavior between two conspecific is associated with a subsequent reduction in GCs (Affiliation effects on GCs). Some studies also supported the prediction that elevations in GCs caused an increase in the expression of nonsexual pair‐bonding behavior (GCs effect on affiliation). Counts are comparisons where any measure of GCs and nonsexual bonding behavior were investigated and in some cases there was more than one comparison per study (see Table S3)

Figure 6

Summary of studies on the associations between measures of glucocorticoids (GCs) and alloparental behavior in wild and captive cooperative breeders. While most studies from captive studies found no correlation between alloparental behavior and GCs, the majority of the evidence from wild animals shows GCs are positively associated with alloparental behavior. Counts are comparisons where any measure of GCs and alloparental behavior were investigated and in some cases there was more than one comparison per study (see Table S4)