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ABSTRACT The ability of organisms to effectively respond to challenges is critical for survival. We investigated how an acute stressor affected corticosterone, mitochondrial function, and DNA oxidative damage in a wild population of Leach's storm‐petrels (Hydrobates leucorhous). We conducted a standardized 20‐min handling procedure on storm‐petrel chicks and collected baseline and post‐handling blood samples. We measured plasma corticosterone and red blood cell DNA oxidative damage levels through the detection of a mutated DNA base 8‐Hydroxy‐2'‐deoxyguanosine (8‐OHdG). In addition, we quantified six measures of mitochondrial aerobic metabolism from red blood cells. Overall, the handling stressor increased plasma corticosterone levels and decreased mitochondrial efficiency to produce ATP. Although the increase in corticosterone was inversely related to the change in DNA oxidative damage, the decrease in mitochondrial efficiency was positively correlated with the change in DNA oxidative damage. Thus, over an acute stress response, individuals who had the largest increase in corticosterone also had the least amount of oxidative damage. In addition, individuals who prioritized ATP production during the acute stress also showed higher levels of oxidative damage. This work highlights the complex pathways by which corticosterone and mitochondrial efficiency affect oxidative damage during acute stress, providing new insights into the trade‐offs underlying physiological responses in wild animals.
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Damage-Fitness Model: Evaluation and synthesis
Abstract Decades of research into stress responses have highlighted large variation among individuals, populations, and species, and the sources of this variation have been a center of research across disciplines. The most common measure of the vertebrate stress response is glucocorticoids. However, the predictive power of glucocorticoid responses to fitness is surprisingly low. This is partly because the hormone levels rapidly change in response to stressor exposure and elevated levels at one time point can indicate either that glucocorticoids are helping the organism cope with the stressor or that dysregulation of hormone release is harming the organism. Meaning, the fitness consequences of the stressor depends on how efficient the stress responses are at negating the harmful impacts of stressors to cells and tissues. To encompass the idea of the efficiency of stress responses and to integrate cellular and organismal stress responses, a new theoretical model called the Damage-Fitness Model was developed. The model focuses on the downstream effects of stress responses and predicts that the accumulation of damage in cells and tissues (e.g., persistent damage to proteins, lipids, and DNA) negatively impacts fitness components. In this mini-review, we examine evidence supporting the Damage-Fitness Model and explore new directions forward.
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- PAR ID:
- 10129459
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 59
- Issue:
- 2
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 282 to 291
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Synopsis Glucocorticoids facilitate the integration of environmental information and coordination of organismal responses to perturbations. Circulating glucocorticoids are hypothesized to depend on an individual’s environment and condition (i.e., state) to facilitate surviving challenges while minimizing fitness costs. Studies specifically focused on sources of individual variation in circulating glucocorticoids are critical to understanding state-dependent modulation of glucocorticoids and integrated phenotypes more broadly. Such studies can also provide insight into the evolution and adaptive significance of circulating glucocorticoids. Here, we repeatedly sample individuals before and during food restriction to identify how and when food availability and intrinsic differences (i.e., body condition and telomere length), including those of social partners, covary with glucocorticoids in captive Red Crossbills (Loxia curvirostra), a nomadic songbird that specializes on foraging for conifer seeds. Conifer seeds are ephemeral resources produced during unpredictable, but locally synchronous, masting events. Fluctuating food availability and social cues, change the behavior and glucocorticoid physiology of Red Crossbills. Pairs consisting of an adult and juvenile were food restricted using an environmental manipulation known to induce socially mediated changes in glucocorticoid signaling. Baseline and stress-induced glucocorticoids were measured before and during food restriction. Amongst adults, stress-induced glucocorticoids declined following food restriction and positively covaried with telomere length, independent of food availability. These results support the hypothesis that the acute glucocorticoid response is adaptively modulated based on environmental conditions and individual differences in state as measured by telomere length. Under food restriction, juvenile baseline glucocorticoids negatively covaried with body condition and the telomere lengths of adult social partners. The covariation between adult telomere lengths and juvenile baseline glucocorticoids suggests that telomere lengths of adults may relate to adult phenotypes, a hypothesis supported by the covariation between adult telomeres and stress-induced glucocorticoids. Further, as patterns were absent before food restriction, our results demonstrate how environmental challenges can reveal the importance of intrinsic differences to organismal responses and social cues. This study leverages a non-model organism experiencing an ecologically relevant environmental challenge to exemplify how intrinsic differences, including those of social partners, can modulate an endocrine mediator of organismal responses to environmental perturbations.more » « less
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Abstract It is frequently hypothesized that animals employ a generalized “stress response,” largely mediated by glucocorticoid (GC) hormones, such as corticosterone, to combat challenging environmental conditions. Under this hypothesis, diverse stressors are predicted to have concordant effects across biological levels of an organism. We tested the generalized stress response hypothesis in two complementary experiments with juvenile and adult male Eastern fence lizards (Sceloporus undulatus). In both experiments, animals were exposed to diverse, ecologically-relevant, acute stressors (high temperature or red imported fire ants, Solenopsis invicta) and we examined their responses at three biological levels: behavioral; physiological (endocrine [plasma corticosterone and blood glucose concentrations] and innate immunity [complement and natural antibodies]); and cellular responses (gene expression of a panel of five heat-shock proteins in blood and liver) at 30 or 90 min post stress initiation. In both experiments, we observed large differences in the cellular response to the two stressors, which contrasts the similar behavioral and endocrine responses. In the adult experiment for which we had innate immune data, the stressors affected immune function independently, and they were correlated with CORT in opposing directions. Taken together, these results challenge the concept of a generalized stress response. Rather, the stress response was context specific, especially at the cellular level. Such context-specificity might explain why attempts to link GC hormones with life history and fitness have proved difficult. Our results emphasize the need for indicators at multiple biological levels and whole-organism examinations of stress.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/icb/icz060
