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.

A marker of biological ageing predicts adult risk preference in European starlings, Sturnus vulgaris

“…Telomere attrition rather than absolute telomere length may be the better predictor of longevity (Boonekamp et al 2014) and hence biological ageing. Our finding aligns with mounting evidence from birds that developmental telomere attrition is a stronger predictor of adult phenotypic outcomes than a single cross-sectional measurement of adult telomere length (reviewed in Andrews, Nettle, Larriva, et al 2017). Since we measured telomere length in juveniles (day 56) and risk preference in adulthood (>day 260), in future studies it would be useful to acquire telomere length measures contemporaneously with behavioral measures of decision-making for closer comparison to the data on humans.…”

“…Since we measured telomere length in juveniles (day 56) and risk preference in adulthood (>day 260), in future studies it would be useful to acquire telomere length measures contemporaneously with behavioral measures of decision-making for closer comparison to the data on humans. However, we note that developmental telomere attrition predicted adult telomere length in 2 separate cohorts of starlings (Bateson, Brilot, et al 2015; Andrews, Nettle, Larriva, et al 2017) as well as in jackdaws (Boonekamp et al 2014). …”

“…Our starling studies taken together indirectly imply the reverse association, that is greater developmental telomere attrition was predictive of greater impulsivity but also of greater aversion to risk. In another prior study on previous starling cohorts, we found that birds undergoing greater developmental telomere attrition had an attenuated hypothalamic-pituitary-adrenal (HPA) axis glucocorticoid hormone stress response (Andrews, Nettle, Larriva, et al 2017). Within neuroeconomics, evidence is emerging for a role for glucocorticoids as mediators of human financial risk-taking (Coates et al 2010; Kandasamy et al 2014).…”

“…That telomere attrition rather than developmental manipulation best predicted the phenotypic outcome is in agreement with what would be expected if telomere attrition serves as an integrative measure of the combined experiences during development (not limited only to our manipulation) and individual variation in sensitivity to those experiences (Bateson 2016). We have previously found telomere attrition to be the better predictor of a range of phenotypic outcomes in starlings compared to developmental manipulations themselves (Bateson, Brilot, et al 2015; Nettle, Andrews, et al 2015; Andrews, Nettle, Larriva, et al 2017). …”

Developmental history and stress responsiveness are related to response inhibition, but not judgement bias, in a cohort of European starlings (Sturnus vulgaris)

“…Briefly, we used a standardised capture-handling-restraint protocol employed previously in European starlings (Andrews et al 2017). Birds had not been disturbed for 2 h prior to sampling.…”