An official website of the United States government
Abstract Vertebrates respond to a diversity of stressors by rapidly elevating glucocorticoid (GC) levels. The changes in physiology and behavior triggered by this response can be crucial for surviving a variety of challenges. Yet the same process that is invaluable in coping with immediate threats can also impose substantial damage over time. In addition to the pathological effects of long-term exposure to stress hormones, even relatively brief elevations can impair the expression of a variety of behaviors and physiological processes central to fitness, including sexual behavior, parental behavior, and immune function. Therefore, the ability to rapidly and effectively terminate the short-term response to stress may be fundamental to surviving and reproducing in dynamic environments. Here we review the evidence that variation in the ability to terminate the stress response through negative feedback is an important component of stress coping capacity. We suggest that coping capacity may also be influenced by variation in the dynamic regulation of GCs—specifically, the ability to rapidly turn on and off the stress response. Most tests of the fitness effects of these traits to date have focused on organisms experiencing severe or prolonged stressors. Here we use data collected from a long-term study of tree swallows (Tachycineta bicolor) to test whether variation in negative feedback, or other measures of GC regulation, predict components of fitness in non-chronically stressed populations. We find relatively consistent, but generally weak relationships between different fitness components and the strength of negative feedback. Reproductive success was highest in individuals that both mounted a robust stress response and had strong negative feedback. We did not see consistent evidence of a relationship between negative feedback and adult or nestling survival: negative feedback was retained in the best supported models of nestling and adult survival, but in two of three survival-related analyses the intercept-only model received only slightly less support. Both negative feedback and stress-induced GC levels—but not baseline GCs—were individually repeatable. These measures of GC activity did not consistently covary across ages and life history stages, indicating that they are independently regulated. Overall, the patterns seen here are consistent with the predictions that negative feedback—and the dynamic regulation of GCs—are important components of stress coping capacity, but that the fitness benefits of having strong negative feedback during the reproductive period are likely to manifest primarily in individuals exposed to chronic or repeated stressors.
more »
« less
Quantifying the Autonomic Response to Stressors—One Way to Expand the Definition of “Stress” in Animals
Abstract Quantifying how whole organisms respond to challenges in the external and internal environment (“stressors”) is difficult. To date, physiological ecologists have mostly used measures of glucocorticoids (GCs) to assess the impact of stressors on animals. This is of course too simplistic as Hans Seyle himself characterized the response of organisms to “noxious stimuli” using multiple physiological responses. Possible solutions include increasing the number of biomarkers to more accurately characterize the “stress state” of animal or just measuring different biomarkers to more accurately characterize the degree of acute or chronic stressors an animal is experiencing. We focus on the latter and discuss how heart rate (HR) and heart rate variability (HRV) may be better predictors of the degree of activation of the sympathetic–adrenal–medullary system and complement or even replace measures of GCs as indicators of animal health, welfare, fitness, or their level of exposure to stressors. The miniaturization of biological sensor technology (“bio-sensors” or “bio-loggers”) presents an opportunity to reassess measures of stress state and develop new approaches. We describe some modern approaches to gathering these HR and HRV data in free-living animals with the aim that heart dynamics will be more integrated with measures of GCs as bio-markers of stress state and predictors of fitness in free-living animals.
more »
« less
- Award ID(s):
- 1749627
- PAR ID:
- 10222709
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 60
- Issue:
- 1
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 113 to 125
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Stress resilience is defined as the ability to rebound to a homeostatic state after exposure to a perturbation. Organisms modulate various physiological mediators to respond to unpredictable changes in their environment. The gut microbiome is a key example of a physiological mediator that coordinates a myriad of host functions including counteracting stressors. Here, we highlight the gut microbiome as a mediator of host stress resilience in the framework of the reactive scope model. The reactive scope model integrates physiological mediators with unpredictable environmental changes to predict how animals respond to stressors. We provide examples of how the gut microbiome responds to stressors within the four ranges of the reactive scope model (i.e., predictive homeostasis, reactive homeostasis, homeostatic overload, and homeostatic failure). We identify measurable metrics of the gut microbiome that could be used to infer the degree to which the host is experiencing chronic stress, including microbial diversity, flexibility, and gene richness. The goal of this perspective piece is to highlight the underutilized potential of measuring the gut microbiome as a mediator of stress resilience in wild animal hosts.more » « less
-
Stephanidis C., Antona M. (Ed.)The objective of this study is to develop and use a virtual reality game as a tool to assess the effects of realistic stress on the behavioral and physiological responses of participants. The game is based on a popular Steam game called Keep Talking Nobody Explodes, where the players collaborate to defuse a bomb. Varying levels of difficulties in solving a puzzle and time pressures will result in different stress levels that can be measured in terms of errors, response times, and other physiological measurements. The game was developed using 3D programming tools including Blender and a virtual reality development kit (VRTK). To measure response times accurately, we added LSL (Lab Stream Layer) Markers to collect and synchronize physiological signals, behavioral data, and the timing of game events. We recorded Electrocardiogram (ECG) data during gameplay to assess heart rate and heart-rate variability (HRV) that have been shown as reliable indicators of stress. Our empirical results showed that heart rate increased significantly while HRV reduced significantly when the participants under high stress, which are consistent with the prior mainstream stress research. This VR game framework is publicly available in GitHub and allows researchers to measure and synchronize other physiological signals such as electroencephalogram, electromyogram, and pupillometry.more » « less
-
ABSTRACT Developing animals display a tremendous ability to change the course of their developmental path in response to the environment they experience, a concept referred to as developmental plasticity. This change in behavior, physiology or cellular processes is primarily thought to allow animals to better accommodate themselves to the surrounding environment. However, existing data on developmental stress and whether it brings about beneficial or detrimental outcomes show conflicting results. There are several well-referred hypotheses related to developmental stress in the current literature, such as the environmental matching, silver spoon and thrifty phenotype hypotheses. These hypotheses speculate that the early-life environment defines the capacity of the physiological functions and behavioral tendencies and that this change is permanent and impacts the fitness of the individual. These hypotheses also postulate there is a trade-off among organ systems and physiological functions when resources are insufficient. Published data on avian taxa show that some effects of developmental nutritional and thermal stressors are long lasting, such as the effects on body mass and birdsong. Although hypotheses on developmental stress are based on fitness components, data on reproduction and survival are scarce, making it difficult to determine which hypothesis these data support. Furthermore, most physiological and performance measures are collected only once; thus, the physiological mechanisms remain undertested. Here, we offer potential avenues of research to identify reasons behind the contrasting results in developmental stress research and possible ways to determine whether developmental programming due to stressors is beneficial or detrimental, including quantifying reproduction and survival in multiple environments, measuring temporal changes in physiological variables and testing for stress resistance later in life.more » « less
-
ABSTRACT Considerable progress has been made in understanding the physiological basis for variation in the life‐history patterns of animals, particularly with regard to the roles of oxidative stress and hormonal regulation. However, an underappreciated and understudied area that could play a role in mediating inter‐ and intraspecific variation of life history is endoplasmic reticulum (ER) stress, and the resulting unfolded protein response (UPRER). ER stress response and the UPRERmaintain proteostasis in cells by reducing the intracellular load of secretory proteins and enhancing protein folding capacity or initiating apoptosis in cells that cannot recover. Proper modulation of the ER stress response and execution of the UPRERallow animals to respond to intracellular and extracellular stressors and adapt to constantly changing environments. ER stress responses are heritable and there is considerable individual variation in UPRERphenotype in animals, suggesting that ER stress and UPRERphenotype can be subjected to natural selection. The variation in UPRERphenotype presumably reflects the way animals respond to ER stress and environmental challenges. Most of what we know about ER stress and the UPRERin animals has either come from biomedical studies using cell culture or from experiments involving conventional laboratory or agriculturally important models that exhibit limited genetic diversity. Furthermore, these studies involve the assessment of experimentally induced qualitative changes in gene expression as opposed to the quantitative variations that occur in naturally existing populations. Almost all of these studies were conducted in controlled settings that are often quite different from the conditions animals experience in nature. Herein, we review studies that investigated ER stress and the UPRERin relation to key life‐history traits including growth and development, reproduction, bioenergetics and physical performance, and ageing and senescence. We then ask if these studies can inform us about the role of ER stress and the UPRERin mediating the aforementioned life‐history traits in free‐living animals. We propose that there is a need to conduct experiments pertaining to ER stress and the UPRERin ecologically relevant settings, to characterize variation in ER stress and the UPRERin free‐living animals, and to relate the observed variation to key life‐history traits. We urge others to integrate multiple physiological systems and investigate how interactions between ER stress and oxidative stress shape life‐history trade‐offs in free‐living animals.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icaa009
