The repeatability of glucocorticoids: A review and meta-analysis

Taff, Conor C.; Schoenle, Laura A.; Vitousek, Maren N.

doi:10.1016/j.ygcen.2018.01.011

Cited by 103 publications

(98 citation statements)

References 61 publications

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“…www.nature.com/scientificreports www.nature.com/scientificreports/ the external environment suggests that endocrine phenotypes might be more variable than other traits, corticosterone measures exhibit similar levels of variability to other phenotypic measures among populations 101 and are generally repeatable across studies (r = 0.29 102 ). Ecological similarities across lakes that are unrelated to predation regime might offer an explanation for the dominance of particular steroids across multiple factors as well as the similar factor loadings across regimes (CPC results).…”

Section: Discussionmentioning

confidence: 99%

Effects of predation risk on egg steroid profiles across multiple populations of threespine stickleback

McGhee

Paitz

Baker

et al. 2020

Sci Rep

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Predation often has consistent effects on prey behavior and morphology, but whether the physiological mechanisms underlying these effects show similarly consistent patterns across different populations remains an open question. In vertebrates, predation risk activates the hypothalamic-pituitaryadrenal (HPA) axis, and there is growing evidence that activation of the maternal HPA axis can have intergenerational consequences via, for example, maternally-derived steroids in eggs. Here, we investigated how predation risk affects a suite of maternally-derived steroids in threespine stickleback eggs across nine Alaskan lakes that vary in whether predatory trout are absent, native, or have been stocked within the last 25 years. Using liquid chromatography coupled with mass spectroscopy (LC-MS/ MS), we detected 20 steroids within unfertilized eggs. Factor analysis suggests that steroids covary within and across steroid classes (i.e. glucocorticoids, progestogens, sex steroids), emphasizing the modularity and interconnectedness of the endocrine response. Surprisingly, egg steroid profiles were not significantly associated with predator regime, although they were more variable when predators were absent compared to when predators were present, with either native or stocked trout. Despite being the most abundant steroid, cortisol was not consistently associated with predation regime. Thus, while predators can affect steroids in adults, including mothers, the link between maternal stress and embryonic development is more complex than a simple one-to-one relationship between the population-level predation risk experienced by mothers and the steroids mothers transfer to their eggs. Predation is a potent force that shapes phenotypes over evolutionary and developmental time 1,2. A major question in evolutionary biology is the extent to which selective pressures such as predation pressure have predictable effects on prey phenotypes and the role of natural selection in shaping consistent patterns of plasticity and/or the independent evolution of similar traits in closely related lineages (i.e. parallelism 3-6). Examining whether different populations of prey respond to predators in the same manner has offered insights into this question 7. For example, traits that protect prey and/or enable quick escape from predators often show evidence of parallelism across replicate populations with similar predation regimes (e.g. morphology 7,8 ; antipredator behavior 9,10). Predation pressure has also been shown to affect life history traits (e.g. age and size at maturity, offspring size and number), often in a parallel manner across populations with similar predation regimes 11,12. Despite the many studies comparing morphology, behavior, and life history traits among populations that differ in predation risk, less is known about the predictability of changes in physiological mechanisms underlying these phenotypic responses to predation pressure. The physiological response to acute and chronic stressors such as predation risk is highly conserv...

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Section: Discussionmentioning

confidence: 99%

Effects of predation risk on egg steroid profiles across multiple populations of threespine stickleback

McGhee

Paitz

Baker

et al. 2020

Sci Rep

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“…The overall goal of our study was to determine whether aspects of HPA axis function predict stress resilience. We predicted that individual variation in response to the standardized restraint stressor would be associated with the response to experimental challenges because HPA axis activity is relatively consistent within individuals over time (e.g., Baugh, Davidson et al, 2017;Taff, Schoenle, & Vitousek, 2018), including in this population (Vitousek, Taff, Hallinger, Zimmer, & Winkler, 2018) and can predict the behavioural response to natural challenges (e.g., Vitousek et al, 2014). We predicted that (a) females that respond to a standardized restraint stressor with a greater elevation in CORT would be more strongly impacted by experimental challenges, and thus have a higher probability of abandoning nests during incubation.…”

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confidence: 99%

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

et al. 2019

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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. A plain language summary is available for this article.

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“…All analyses were performed in R version 3.5.1 (R Core Team, 2018) and meta-analyses were performed using the package metafor (Viechtbauer, 2010). Before performing any analyses, we used the escalc function in metafor to convert the correlation coefficients r to the standardized, normally distributed effect size Fisher’s Z and to calculate the sampling variance for each effect size (as described in Holtmann, Lagisz, & Nakagawa, 2016; Taff, Schoenle, & Vitousek, 2018). Results were back-transformed to r to support easier interpretation.…”

Section: Methodsmentioning

confidence: 99%

“…When considering the numerous empirical studies addressing these relationships using similar fitness measures, variation in environmental conditions as well as individuals’ physiological conditions, life history strategy and evolutionary history have made it challenging to draw generalizable conclusions. Previous qualitative reviews of GC-fitness relationships (Breuner, Patterson, & Hahn, 2008; Bonier et al ., 2009a; Crespi et al ., 2013; Schoenle, Zimmer, & Vitousek, 2018a) suggest that the relationships between GCs and both survival and reproductive success are not consistent and vary across these contexts. However, we know of no comparative studies to date that have investigated how context affects GC-fitness relationships.…”

Section: Introductionmentioning

confidence: 99%

Does variation in glucocorticoid regulation predict fitness? A phylogenetic meta-analysis

Schoenle

Zimmer

Miller

et al. 2019

Preprint

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Glucocorticoid hormones (GCs) are central mediators of metabolism and the response to challenges. Because circulating levels of GCs increase in response to challenges, within-population variation in GCs could reflect individual variation in condition or experience. At the same time, individual variation in the degree to which GCs increase in response to challenges (which is relatively consistent within individuals over time) could have causal effects on stress coping capacity, and the ability to survive and reproduce. Although a number of studies in vertebrates have tested whether within-population variation in GCs predicts components of fitness, it is not clear whether there are consistent patterns across taxa. Here we present the first phylogenetic meta-analysis testing whether within-population variation in GCs is associated with components of fitness across vertebrates. At the same time, we introduce and test predictions about an overlooked but potentially important mediator of GC-fitness relationships: life history context. We suggest that strong context-dependence in the fitness benefit of maintaining elevated GCs could obscure consistent patterns between GCs and fitness across taxa. Meta-analyses revealed that across vertebrates, baseline and stress-induced GCs were consistently negatively correlated with reproductive success. This relationship did not differ depending on life history context. In contrast, the relationships between GCs and survival were highly context dependent, differing according to life history strategy. Both baseline and stress-induced GCs were more strongly negatively associated with survival in longer-lived populations and species. Stress-induced GCs were also more negatively associated with survival in organisms that engage in relatively more valuable reproductive attempts. Fecal GCs did not predict survival or reproductive success. We also used a meta-analytic approach to test whether experimental increases in GCs had consistent causal effects on fitness. Experimental increases in GCs reduced both survival and reproductive success, although the latter relationship was not significant when accounting for phylogeny. Overall, these results support the prediction that GC-fitness relationships can be strongly context dependent, and suggest that incorporating life history may be particularly important for understanding GC-survival relationships. Future studies that explore the role of other aspects of context (e.g., the nature and frequency of stressors, environmental variation) within and across species could provide important insights how and when variation in GC regulation predicts fitness.

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The repeatability of glucocorticoids: A review and meta-analysis

Cited by 103 publications

References 61 publications

Effects of predation risk on egg steroid profiles across multiple populations of threespine stickleback

Effects of predation risk on egg steroid profiles across multiple populations of threespine stickleback

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

Does variation in glucocorticoid regulation predict fitness? A phylogenetic meta-analysis

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