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Animals encounter many novel and unpredictable challenges when moving into new areas including pathogen exposure. Because effective immune defenses against such threats can be costly, plastic immune responses could be particularly advantageous, as such defenses can be engaged only when context warrants activation. DNA methylation is a key regulator of plasticity via its effects on gene expression. In vertebrates, DNA methylation occurs exclusively at CpG dinucleotides, and typically, high DNA methylation decreases gene expression, particularly when it occurs in promoters. The CpG content of gene regulatory regions may therefore represent one form of epigenetic potential (EP), a genomic means to capacitate gene expression and hence adaptive phenotypic plasticity. Non-native populations of house sparrows (Passer domesticus) - one of the world's most cosmopolitan species – have high EP in the promoter of a key microbial surveillance gene, Toll-like receptor 4 (TLR4), compared to native populations. We previously hypothesized that high EP may enable sparrows to balance the costs and benefits of inflammatory immune responses well, a trait critical to success in novel environments. In the present study, we found support for this hypothesis: house sparrows with high EP in TLR4 promoter were better able to resist a pathogenic Salmonella enterica infection than sparrows with low EP. These results support the idea that high EP contributes to invasion and perhaps adaptation in novel environments, but the mechanistic details whereby these organismal effects arise remain obscure.

 

Climate change is dramatically altering our planet, yet our understanding of mechanisms of thermal tolerance is limited in wild birds. We characterized natural variation in heat shock protein (HSP) gene expression among tissues and populations of free-living Tree Swallows (Tachycineta bicolor). We focused on HSPs because they prevent cellular damage and promote recovery from heat stress. We used quantitative PCR to measure gene expression of 3 HSPs, including those in the HSP70 and HSP90 families that have robust experimental connections to heat in past literature. First, to evaluate how tissues and, by extension, the functions that they mediate, may vary in their thermal protection, we compared HSP gene expression among neural and peripheral tissues. We hypothesized that tissues with particularly vital functions would be more protected from heat as indicated by higher HSP gene expression. We found that brain tissues had consistently higher HSP gene expression compared to the pectoral muscle. Next, we compared HSP gene expression across 4 distinct populations that span over 20° of latitude (>2,300 km). We hypothesized that the more southern populations would have higher HSP gene expression, suggesting greater tolerance of, or experience with, warmer local conditions. We observed largely higher HSP gene expression in more southern populations than northern populations, although this pattern was more striking at the extremes (southern Indiana vs. Alaska), and it was stronger in some brain areas than others (ventromedial telencephalon vs. hypothalamus). These results shed light on the potential mechanisms that may underlie thermal tolerance differences among populations or among tissues.

 

The social environment that individuals experience appears to be a particularly salient mediator of stress resilience, as the nature and valence of social interactions are often related to subsequent health, physiology, microbiota, and overall stress resilience. Relatively few studies have simultaneously manipulated the social environment and ecological challenges under natural conditions. Here, we report the results of experiments in wild tree swallows (Tachycineta bicolor) in which we manipulated both ecological challenges (predator encounters and flight efficiency reduction) and social interactions (by experimental dulling of a social signal). In two experiments conducted in separate years, we reversed the order of these treatments so that females experienced either an altered social signal followed by a challenge or vice‐versa. Before, during, and after treatments were applied, we tracked breeding success, morphology and physiology (mass, corticosterone, and glucose), nest box visits via an RFID sensor network, cloacal microbiome diversity, and fledging success. Overall, we found that predator exposure during the nestling period reduced the likelihood of fledging and that signal manipulation sometimes altered nest box visitation patterns, but little evidence that the two categories of treatment interacted with each other. We discuss the implications of our results for understanding what types of challenges and what conditions are most likely to result in interactions between the social environment and ecological challenges.

 

Abstract Flexibility in the regulation of the hypothalamic–pituitary–adrenal (HPA) axis is an important mediator of stress resilience as it helps organisms adjust to, avoid, or compensate for acute and chronic challenges across changing environmental contexts. Glucocorticoids remain the favorite metric from medicine to conservation biology to attempt to quantify stress resilience despite the skepticism around their consistency in relation to individual health, welfare, and fitness. We suggest that a cochaperone molecule related to heat shock proteins and involved in glucocorticoid receptor activity, FKBP5, may mediate HPA flexibility and therefore stress resilience because it affects how individuals can regulate glucocorticoids and therefore capacitates their abilities to adjust phenotypes appropriately to prevailing, adverse conditions. Although the molecule is well studied in the biomedical literature, FKBP5 research in wild vertebrates is limited. In the present article, we highlight the potential major role of FKBP5 as mediator of HPA axis flexibility in response to adversity in humans and lab rodents. 

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.