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1. HPA flexibility and FKBP5 : promising physiological targets for conservation

   https://doi.org/10.1098/rstb.2022.0512  

   Zimmer, Cédric ; Jimeno, Blanca ; Martin, Lynn B. ( March 2024 , Philosophical Transactions of the Royal Society B: Biological Sciences)

   Hypothalamic–pituitary–adrenal axis (HPA) flexibility is an emerging concept recognizing that individuals that will cope best with stressors will probably be those using their hormones in the most adaptive way. The HPA flexibility concept considers glucocorticoids as molecules that convey information about the environment from the brain to the body so that the organismal phenotype comes to complement prevailing conditions. In this context, FKBP5 protein appears to set the extent to which circulating glucocorticoid concentrations can vary within and across stressors. Thus,FKBP5expression, and the HPA flexibility it causes, seem to represent an individual's ability to regulate its hormones to orchestrate organismal responses to stressors. AsFKBP5expression can also be easily measured in blood, it could be a worthy target of conservation-oriented research attention. We first review the known and likely roles of HPA flexibility and FKBP5 in wildlife. We then describe putative genetic, environmental and epigenetic causes of variation in HPA flexibility andFKBP5expression among and within individuals. Finally, we hypothesize how HPA flexibility andFKBP5expression should affect organismal fitness and hence population viability in response to human-induced rapid environmental changes, particularly urbanization.

   This article is part of the theme issue ‘Endocrine responses to environmental variation: conceptual approaches and recent developments’.

    

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2. On again, off again: Acute stress response and negative feedback together predict resilience to experimental challenges

   https://doi.org/10.1111/1365-2435.13281  

   Zimmer, Cedric ; Taff, Conor C. ; Ardia, Daniel R. ; Ryan, Thomas A. ; Winkler, David W. ; Vitousek, Maren N. ; Angelier, ed., Frédéric ( January 2019 , Functional Ecology)

   Individuals often vary markedly in their ability to cope with stressors, but the drivers of this variation remain poorly understood. Many studies have tested relationships among individual variation in glucocorticoid levels and the response to challenges—often finding inconsistent patterns; however, few have addressed whether variation in the capacity to terminate the stress response through negative feedback is associated with stress resilience.

   While conceptual models predict that interactions among different components of hypothalamic–pituitary–adrenal (HPA) axis regulation may be important predictors of the phenotypic and fitness effects of stress, we are aware of no previous experimental tests of this hypothesis.

   We investigate whether individual variation in HPA axis regulation is related to resilience to experimental challenges in free‐living tree swallows (Tachycineta bicolor). We mimicked salient natural challenges by temporarily reducing flight efficiency or increasing perceived predation risk during incubation, and determined whether HPA axis responsiveness prior to treatments predicted resilience.

   Females that exhibited both a robust HPA axis activation and strong negative feedback were less likely to abandon nests during incubation.

   Our results suggest that exhibiting a strong HPA axis activation coupled with effective negative feedback may predict stress resilience. Therefore, the ability to turn on and then off the HPA axis efficiently may be important for fitness.

   Our results also suggest that the interactions between different components of the HPA axis may provide greater insight into differences in stress coping capacity.

   Aplain language summaryis available for this article.

    

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3. Gut Microbiome as a Mediator of Stress Resilience: A Reactive Scope Model Framework

   https://doi.org/10.1093/icb/icac030  

   Houtz, Jennifer L. ; Taff, Conor C. ; Vitousek, Maren N. ( May 2022 , Integrative And Comparative Biology)

   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.

    

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4. The impact of parental and developmental stress on DNA methylation in the avian hypothalamic–pituitary–adrenal axis

   https://doi.org/10.1111/mec.17291  

   Siller Wilks, Stefanie J. ; Heidinger, Britt J. ; Westneat, David F. ; Solomon, Joseph ; Rubenstein, Dustin R. ( February 2024 , Molecular Ecology)

   The hypothalamic–pituitary–adrenal (HPA) axis coordinates an organism's response to environmental stress. The responsiveness and sensitivity of an offspring's stress response may be shaped not only by stressors encountered in their early post‐natal environment but also by stressors in their parent's environment. Yet, few studies have considered how stressors encountered in both of these early life environments may function together to impact the developing HPA axis. Here, we manipulated stressors in the parental and post‐natal environments in a population of house sparrows (Passer domesticus) to assess their impact on changes in DNA methylation (and corresponding gene expression) in a suite of genes within the HPA axis. We found that nestlings that experienced early life stress across both life‐history periods had higher DNA methylation in a critical HPA axis gene, the glucocorticoid receptor (NR3C1). In addition, we found that the life‐history stage when stress was encountered impacted some genes (HSD11B1, NR3C1andNR3C2) differently. We also found evidence for the mitigation of parental stress by post‐natal stress (inHSD11B1andNR3C2). Finally, by assessing DNA methylation in both the brain and blood, we were able to evaluate cross‐tissue patterns. While some differentially methylated regions were tissue‐specific, we found cross‐tissue changes inNR3C2andNR3C1, suggesting that blood is a suitable tissue for assessing DNA methylation as a biomarker of early life stress. Our results provide a crucial first step in understanding the mechanisms by which early life stress in different life‐history periods contributes to changes in the epigenome of the HPA axis.

    

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5. Maternal glucocorticoids have minimal effects on HPA axis activity and behavior of juvenile wild North American red squirrels

   https://doi.org/10.1242/jeb.236620  

   Westrick, Sarah E. ; van Kesteren, Freya ; Boutin, Stan ; Lane, Jeffrey E. ; McAdam, Andrew G. ; Dantzer, Ben ( May 2021 , Journal of Experimental Biology)

   ABSTRACT As a response to environmental cues, maternal glucocorticoids (GCs) may trigger adaptive developmental plasticity in the physiology and behavior of offspring. In North American red squirrels (Tamiasciurus hudsonicus), mothers exhibit increased GCs when conspecific density is elevated, and selection favors more aggressive and perhaps more active mothers under these conditions. We tested the hypothesis that elevated maternal GCs cause shifts in offspring behavior that may prepare them for high-density conditions. We experimentally elevated maternal GCs during gestation or early lactation. We measured two behavioral traits (activity and aggression) in weaned offspring using standardized behavioral assays. Because maternal GCs may influence offspring hypothalamic–pituitary–adrenal (HPA) axis dynamics, which may in turn affect behavior, we also measured the impact of our treatments on offspring HPA axis dynamics (adrenal reactivity and negative feedback), and the association between offspring HPA axis dynamics and behavior. Increased maternal GCs during lactation, but not gestation, slightly elevated activity levels in offspring. Offspring aggression and adrenal reactivity did not differ between treatment groups. Male, but not female, offspring from mothers treated with GCs during pregnancy exhibited stronger negative feedback compared with those from control mothers, but there were no differences in negative feedback between lactation treatment groups. Offspring with higher adrenal reactivity from mothers treated during pregnancy (both controls and GC-treated) exhibited lower aggression and activity. These results suggest that maternal GCs during gestation or early lactation alone may not be a sufficient cue to produce substantial changes in behavioral and physiological stress responses in offspring in natural populations. 

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