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

Clare Andrews, Daniel Nettle, Maria Larriva, Robert Gillespie, Sophie Reichert, Ben O. Brilot, Thomas Bedford, Pat Monaghan, Karen A. Spencer, Melissa Bateson

Research output: Contribution to journalJournal Article

6 Citations (Scopus)

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.
Original languageEnglish
JournalRoyal Society Open Science
Volume4
Issue number9
DOIs
Publication statusPublished - 27 Sep 2017
Externally publishedYes

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stress response
biomarkers
telomeres
corticosterone
Sturnus vulgaris
birds
medicine
erythrocytes
hatching
physiology
chicks
Biological Sciences

Keywords

  • Biological age
  • Corticosterone
  • Early-life adversity
  • Stress response
  • Sturnus vulgaris
  • Telomere

Cite this

Andrews, Clare ; Nettle, Daniel ; Larriva, Maria ; Gillespie, Robert ; Reichert, Sophie ; Brilot, Ben O. ; Bedford, Thomas ; Monaghan, Pat ; Spencer, Karen A. ; Bateson, Melissa. / A marker of biological age explains individual variation in the strength of the adult stress response. In: Royal Society Open Science. 2017 ; Vol. 4, No. 9.
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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.",
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Andrews, C, Nettle, D, Larriva, M, Gillespie, R, Reichert, S, Brilot, BO, Bedford, T, Monaghan, P, Spencer, KA & Bateson, M 2017, 'A marker of biological age explains individual variation in the strength of the adult stress response', Royal Society Open Science, vol. 4, no. 9. https://doi.org/10.1098/rsos.171208

A marker of biological age explains individual variation in the strength of the adult stress response. / Andrews, Clare; Nettle, Daniel; Larriva, Maria; Gillespie, Robert; Reichert, Sophie; Brilot, Ben O.; Bedford, Thomas; Monaghan, Pat; Spencer, Karen A.; Bateson, Melissa.

In: Royal Society Open Science, Vol. 4, No. 9, 27.09.2017.

Research output: Contribution to journalJournal Article

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T1 - A marker of biological age explains individual variation in the strength of the adult stress response

AU - Andrews, Clare

AU - Nettle, Daniel

AU - Larriva, Maria

AU - Gillespie, Robert

AU - Reichert, Sophie

AU - Brilot, Ben O.

AU - Bedford, Thomas

AU - Monaghan, Pat

AU - Spencer, Karen A.

AU - Bateson, Melissa

PY - 2017/9/27

Y1 - 2017/9/27

N2 - 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.

AB - 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.

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KW - Corticosterone

KW - Early-life adversity

KW - Stress response

KW - Sturnus vulgaris

KW - Telomere

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DO - 10.1098/rsos.171208

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VL - 4

JO - Royal Society Open Science

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SN - 2054-5703

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ER -