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How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model.

ABSTRACT: It is widely expected that physiological and behavioral stress responses will be integrated within divergent stress-coping styles (SCS) and that these may represent opposite ends of a continuously varying reactive-proactive axis. If such a model is valid, then stress response traits should be repeatable and physiological and behavioral responses should also change in an integrated manner along a major axis of among-individual variation. While there is some evidence of association between endocrine and behavioral stress response traits, few studies incorporate repeated observations of both. To test this model, we use a multivariate, repeated measures approach in a captive-bred population of Xiphophorus birchmanni. We quantify among-individual variation in behavioral stress response to an open field trial (OFT) with simulated predator attack (SPA) and measure waterborne steroid hormone levels (cortisol, 11-ketotestosterone) before and after exposure. Under the mild stress stimulus (OFT), (multivariate) behavioral variation among individuals was consistent with a strong axis of personality (shy-bold) or coping style (reactive-proactive) variation. However, behavioral responses to a moderate stressor (SPA) were less repeatable, and robust statistical support for repeatable endocrine state over the full sampling period was limited to 11-ketotestosterone. Although post hoc analysis suggested cortisol expression was repeatable over short time periods, qualitative relationships between behavior and glucocorticoid levels were counter to our a priori expectations. Thus, while our results clearly show among-individual differences in behavioral and endocrine traits associated with stress response, the correlation structure between these is not consistent with a simple proactive-reactive axis of integrated stress-coping style. Additionally, the low repeatability of cortisol suggests caution is warranted if single observations (or indeed repeat measures over short sampling periods) of glucocorticoid traits are used in ecological or evolutionary studies focussed at the individual level.

SUBMITTER: Boulton K

PROVIDER: S-EPMC4328767 | biostudies-other | 2015 Feb

REPOSITORIES: biostudies-other

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How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model.

Boulton Kay K Couto Elsa E Grimmer Andrew J AJ Earley Ryan L RL Canario Adelino V M AV Wilson Alastair J AJ Walling Craig A CA

Ecology and evolution 20150111 3

It is widely expected that physiological and behavioral stress responses will be integrated within divergent stress-coping styles (SCS) and that these may represent opposite ends of a continuously varying reactive-proactive axis. If such a model is valid, then stress response traits should be repeatable and physiological and behavioral responses should also change in an integrated manner along a major axis of among-individual variation. While there is some evidence of association between endocri ...[more]

PMID: 25691986

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Project description:Within populations, individuals can vary in stress response, a multivariate phenomenon comprising neuroendocrine, physiological and behavioural traits.Verbal models of individual stress "coping style" have proposed that the behavioural component of this variation can be described as a single axis, with each individual's coping style being consistent across time and stress contexts.Focusing on this behavioural component of stress response and combining repeated measures of multiple traits with a novel multivariate modelling framework, we test for the existence of coping style variation and assess its stability across contexts in the Trinidadian guppy (Poecilia reticulata).Specifically, we test the following hypotheses: (1) there exists repeatable among-individual behavioural (co)variation ("personality") within a mild stress context consistent with a risk-averse-risk-prone continuum of behavioural coping style, (2) there is population-level plasticity in behaviour as a function of stressor severity, (3) there is among-individual variation in plasticity (i.e. IxE), and (4) the presence of IxE reduces cross-context stability of behavioural coping style.We found significant repeatable among-individual behavioural (co)variation in the mild stress context (open field trial), represented as an I matrix. However, I was not readily described by a simple risk-averse-risk-prone continuum as posited by the original coping style model. We also found strong evidence for population-level changes in mean behaviour with increasing stressor severity (simulated avian and piscine predation risks).Single-trait analyses did show the presence of individual-by-environment interactions (IxE), as among-individual cross-context correlations were significantly less than +1. However, multitrait analysis revealed the consequences of this plasticity variation were minimal. Specifically, we found little evidence for changes in the structure of I between mild and moderate stress contexts overall, and only minor changes between the two moderate contexts (avian vs. piscine predator).We show that a multivariate approach to assessing changes in among-individual (co)variance across contexts can prevent the over-interpretation of statistically significant, but small, individual-by-environment effects. While behavioural flexibility enables populations (and individuals) to respond rapidly to changes in the environment, multivariate personality structure can be conserved strongly across such contexts. A plain language summary is available for this article.

Project description:Based on the animal's reaction to environmental challenges, consistent but different coping styles can be identified, which in turn may have consequences for health and welfare. Therefore, profound knowledge of the complex interrelationships between individual behavioral response patterns, underlying neurobiological mechanisms and immunological effects is required. The aim of this study was to examine whether pigs with different coping styles exhibit distinct behavioral, neurobiological and immune responses to stressful situations. Therefore, pigs (n = 40) were classified as proactive, reactive or intermediate animals according to a repeatedly-performed backtest, and behavioral, neuroendocrine and immune alterations were analyzed without any stress before weaning on day 28 and after a stress treatment on day 32. Our results show that the behavioral responses in an open-field/novel-object test characterized proactive pigs as more active. There were no significant differences in adrenocorticotropic hormone and cortisol concentrations between pigs with different coping characteristics. However, we found that proactive pigs displayed significantly increased plasma noradrenaline levels in response to stress, which may reflect a higher sympathetic reactivity of these animals. Furthermore, the present study revealed coping style differences in mRNA expression of mineralocorticoid, glucocorticoid, oxytocin and arginine vasopressin receptors and the immediate early gene c-fos in stress-related brain regions. While proactive pigs responded to stress with higher mRNA expression of arginine vasopressin, mineralocorticoid and glucocorticoid receptors, reactive pigs displayed higher oxytocin receptor and c-fos mRNA expression, indicating different neurobiological mechanisms of distinct coping styles in response to stressful challenges. Moreover, we also found humoral immune differences between proactive, intermediate and reactive animals. Proactive pigs had a higher total serum IgA concentration before and after stress treatment, with a significant increase in response to stress compared to reactive and intermediate pigs. In contrast, stress-induced IgM concentrations only increased in reactive and intermediate animals, suggesting that the effects of coping style on humoral immunity may differ depending on the specific function of the immunoglobulin classes. In conclusion, this multidisciplinary study expands the concept of coping style in farm animals, particularly in terms of individual stress reactivity and disease susceptibility, and thus contributes to the understanding of the biology of animal welfare.

Dataset Information

How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model.

Publications

How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model.

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