A marker of biological age explains individual variation in the strength of the adult stress response

Abstract

The acute stress response functions to prioritize behavioural and physiological processes that maximize survival in the face of immediate threat. There is variation between individuals in the strength of the adult stress response that is of interest in both evolutionary biology and medicine. Age is an established source of this variation-stress responsiveness diminishes with increasing age in a range of species-but unexplained variation remains. Since individuals of the same chronological age may differ markedly in their pace of biological ageing, we asked whether biological age-measured here via erythrocyte telomere length-predicts variation in stress responsiveness in adult animals of the same chronological age. We studied two cohorts of European starlings in which we had previously manipulated the rate of biological ageing by experimentally altering the competition experienced by chicks in the fortnight following hatching. We predicted that individuals with greater developmental telomere attrition, and hence greater biological age, would show an attenuated corticosterone (CORT) response to an acute stressor when tested as adults. In both cohorts, we found that birds with greater developmental telomere attrition had lower peak CORT levels and a more negative change in CORT levels between 15 and 30 min following stress exposure. Our results, therefore, provide strong evidence that a measure of biological age explains individual variation in stress responsiveness: birds that were biologically older were less stress responsive. Our results provide a novel explanation for the phenomenon of developmental programming of the stress response: observed changes in stress physiology as a result of exposure to early-life adversity may reflect changes in ageing.

Keywords: Sturnus vulgaris; biological age; corticosterone; early-life adversity; stress response; telomere.

Figure 1.

Hypothesized causal relationships and resulting predicted associations.

Figure 2.

Components of variation (natal nest, host nest, residual) for each of the CORT measures in each of the two cohorts of cross-fostered birds.

Figure 3.

Summary of associations between developmental telomere attrition (ΔTL) and CORT variables. (a,c,e): 2012 cohort. (b,d,f): 2013 cohort. (a,b) Scatterplot of the association between ΔTL (more negative means greater attrition) and peak CORT. (c,d) Scatterplot of the association between ΔTL and ΔCORT. ΔCORT is the change in CORT between 15 and 30 min (where a negative value signifies a reduction in CORT). (e,f) Mean CORT at the three sample points for birds split at the median of ΔTL into those that experienced more (red open symbol, dotted line) and less developmental telomere attrition (black closed symbol, solid line). Error bars represent one standard error.

Figure 4.

Forest plots showing estimated standardized β coefficients and their 95% confidence intervals for the effects of ΔTL on each of the CORT variables in both cohorts of birds. (a) Baseline CORT; (b) peak CORT; and (c) ΔCORT. For each CORT variable, the average summary estimate (±95% confidence intervals) for the two cohorts is shown as a black diamond. Zero represents no association. Note that for peak CORT and ΔCORT the diamond does not cross zero, indicating significant average effects.