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.
Highlights
Upon exposure to a social or environmental challenge, individuals within a population often differ consistently in their behavioral response
Single behaviors are often linked within an individual with other behaviors. These consistent individual differences and trait correlations are the basis for the concept of animal personality, which has been demonstrated in a wide variety of species
Using semi-natural enclosures, we studied wild-caught great tits (Parus major), a species that has been the subject of extensive investigation in animal personality and, more recently, of intra-population variation in glucocorticoid physiology (Hau et al, 2016)
Summary
Upon exposure to a social or environmental challenge, individuals within a population often differ consistently in their behavioral response (reviewed in Réale et al, 2007; Bell et al, 2009; Dall et al, 2012). Single behaviors (e.g. aggressiveness) are often linked within an individual with other behaviors (e.g. exploration; reviewed in Groothuis and Carere, 2005) These consistent individual differences and trait correlations are the basis for the concept of animal personality (similar to ‘coping styles’, ‘behavioral syndromes’), which has been demonstrated in a wide variety of species (van Oers and Naguib, 2013). Glucocorticoids (hereafter CORT) are proposed to be key steroids involved in one of the major axes of personality: the shy-bold continuum (Øverli et al, 2007; Carere et al, 2010) In part, this hypothesis rests on the pleiotropic nature of steroids—these endocrine products circulate throughout the organism and bind to multiple receptor types across diverse tissues. A single hormone can simultaneously affect multiple targets, thereby precisely modulating the expression of several behaviors (Ketterson and Nolan, 1999)
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