Risk-averse personalities have a systemically potentiated neuroendocrine stress axis: A multilevel experiment in Parus major

Abstract

Hormonal pleiotropy—the simultaneous influence of a single hormone on multiple traits—has been hypothesized as an important mechanism underlying personality, and circulating glucocorticoids are central to this idea. A major gap in our understanding is the neural basis for this link. Here we examine the stability and structure of behavioral, endocrine and neuroendocrine traits in a population of songbirds (Parus major). Upon identifying stable and covarying behavioral and endocrine traits, we test the hypothesis that risk-averse personalities exhibit a neuroendocrine stress axis that is systemically potentiated—characterized by stronger glucocorticoid reactivity and weaker negative feedback. We show high among-individual variation and covariation (i.e. personality) in risk-taking behaviors and demonstrate that four aspects of glucocorticoid physiology (baseline, stress response, negative feedback strength and adrenal sensitivity) are also repeatable and covary. Further, we establish that high expression of mineralocorticoid and low expression of glucocorticoid receptor in the brain are linked with systemically elevated plasma glucocorticoid levels and more risk-averse personalities. Our findings support the hypothesis that steroid hormones can exert pleiotropic effects that organize behavioral phenotypes and provide novel evidence that neuroendocrine factors robustly explain a large fraction of endocrine and personality variation.

On again, off again: Acute stress response and negative feedback together predict resilience to experimental challenges

“…If individual variation in stress-induced corticosterone is positively correlated with the strength of negative feedback (as suggested by previous investigations that used similar measures of HPA activity (e.g., Schmidt et al, 2012;Baugh, Senft et al, 2017))-then correlations between stress-induced glucocorticoids and survival or stress coping capacity could be explained at least in part by stronger stress responders also having stronger negative feedback. Individual variation in measures of HPA axis activity could also reflect downstream variation in receptor densities within brain areas involved in negative feedback regulation.…”

“…Previous studies looking at the consequences of variation in the acute glucocorticoid stress response on fitness have focused almost exclusively on its magnitude (e.g., Breuner et al, 2008;Bókony et al, 2009;Ouyang, Quetting, & Hau, 2012;Vitousek, Jenkins, & Safran, 2014). Individual differences in the ability to rapidly and effectively terminate the glucocorticoid stress response have received much less attention (but see, e.g., Baugh, Senft et al, 2017;MacDougall-Shackleton, Schmidt, Furlonger, & MacDougall-Shackleton, 2013;Romero & Wikelski, 2010). When the HPA axis is activated, negative feedback is coordinated by glucocorticoids binding to glucocorticoid (GR) and mineralocorticoid (MR) receptors particularly in the hippocampus, hypothalamus and pituitary gland resulting in a decrease in circulating glucocorticoids (Breuner & Orchinik, 2001;Romero, 2004).…”

Host defences against avian brood parasitism: an endocrine perspective

“…conspecific aggression [107]) and combining it with equally fine-tuned experimental techniques for studying host responses to parasites (reviewed in [4]). To understand the endocrine basis of host defences, it is imperative to focus both on hormones as well as their receptors, as variation in both can cause differences in behaviour [38,97,98]: studies on host endocrinology to date have focused mainly on variation in hormone levels, but receptor expression for these hormones in the target tissues may yield equally illuminating findings.…”

Dexamethasone treatment supports age‐related maturation of the stress response in altricial nestling birds

“…migration-modulation hypothesis; Holberton et al 1996, Wilson et al 2017 or during development Holberton 2000, Blas et al 2006). In this sense, the negative feedback, a self-inhibitory mechanism of Cort secretion acting on the HPA axis tissues and hippocampus (Jacobson andSapolsky 1991, Romero 2004), allows modulating the adrenocortical response to stress, as demonstrated in studies explaining personality or sexual differences in HPA axis reactivity (Astheimer et al 1994, Baugh et al 2017). This regulatory mechanism may reduce the deleterious effects associated to elevated Cort levels.…”