Evidence for a mechanism of phenotypic integration of behaviour and innate immunity in a wild rodent: implications for animal personality and ecological immunology

Abstract

If a single mechanism influences multiple traits, it may facilitate functional integration or impede optimal trait expression to produce consistent individual differences and correlations among those traits. The fields of animal personality and ecological immunology each aim to understand variation and covariation of behavioural and immune traits. Studying these traits together may provide additional insight into patterns of (co)variation than studying behaviours or immunity in isolation, as trade-offs between behaviour and immunity are likely. Hormonal mechanisms may be involved in the variation and covariation between behavioural and immune traits, and the role of receptors in particular has rarely been tested in wild animals. In wild-caught Belding's ground squirrels, Urocitellus beldingi, we delivered mifepristone to experimentally block the actions of glucocorticoid receptors (GRs), a component of the stress response. Then we evaluated whether cortisol binding with GRs affects the plasticity of behavioural and immune traits, consistent individual differences and phenotypic integration of exploratory behaviour, activity, antipredator behaviour, response to restraint and bacteria-killing ability, a measure of innate immunity. Mifepristone treatment abolished relationships between faecal glucocorticoid metabolite levels and both exploratory behaviour and bacteria-killing ability. This result indicates that cortisol binding with GRs is a mechanism of plasticity of those traits. Mifepristone also affected relationships among traits. Specifically, mifepristone treatment significantly modulated the relationships between bacteria-killing ability and two behaviours, exploration and activity. This result supports the hypothesis that the GR–cortisol binding is a mechanism of phenotypic integration. Together, these results suggest that GR–cortisol binding balances the often observed trade-off between behaviour and immunity to produce patterns of (co)variation of behavioural and immune traits seen in nature.