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.

Highlights

  • The vertebrate stress response is highly conserved across taxa and functions to prioritize immediate survival over non-essential activities in the face of acute threats [1,2]

  • Using two cohorts of adult European starlings that had previously been subjected to an experimental manipulation of early-life adversity, we tested the hypothesis that the rate of biological ageing, measured via the extent to which erythrocyte telomeres had shortened during development, explained individual variation in adult stress responsiveness

  • We predicted that birds whose developmental telomere attrition, and biological ageing, had been accelerated by exposure to early-life adversity would respond to stress as adults as if they were older than their chronological age, and show an attenuated response to an acute stressor

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Summary

Introduction

The vertebrate stress response is highly conserved across taxa and functions to prioritize immediate survival over non-essential activities in the face of acute threats [1,2] This change in priorities is mediated via the release of glucocorticoid hormones that temporarily suppress behaviour not critical to immediate survival, including foraging, self-maintenance, courtship, mating and parental care, while simultaneously promoting behaviour that aids avoiding, combating or escaping threats [3]. The concept of biological age has been proposed to capture this variation in life expectancy [17], and we, propose that biological age could explain individual differences in the stress responsiveness of adult animals of the same chronological age

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