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  1. 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.

     
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  2. Synopsis

    The allocation of limited resources among life history traits creates trade-offs that constrain the range of possible phenotypes of organisms. In animals, the cost of maintaining an effective immune response may reduce the ability to invest in reproduction, resulting in altered susceptibility to disease. However, not all members of a population face identical constraints because differences in an individual's environmental context or physiological state can influence the degree to which traits are negatively associated. Here, we evaluated how variation in timing of breeding, a correlate of fitness, may result in different patterns of trait associations between immunity and reproduction. We measured constitutive immunity in breeding female tree swallows (Tachycineta bicolor) using a bacteria killing assay with blood plasma to assess the relationships between bacteria killing ability (BKA), reproductive effort, and reproductive success. We found that timing of breeding can influence the association between BKA and reproductive effort, but its effects are not homogeneous among all traits. Late-breeding tree swallows with stronger BKA laid smaller clutches, a pattern that was not apparent in early breeders. Regardless of the timing of breeding, birds with stronger BKA fed their nestlings less. Despite a negative association with reproductive effort, we found no association between immunity and reproductive success. We provide evidence that individual tree swallows do not experience some trade-offs equally, and that timing of breeding likely plays a role in how costs of immunity are weighed. To understand how investment in immunity can limit life history traits, we must consider how a variation among individuals influences the relative costs of immunity.

     
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  3. Abstract

    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.

     
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  4. Abstract

    Life history theory provides a framework for understanding how trade-offs generate negative trait associations. Among nestling birds, time spent in the nest, risk of predation, and lifespan covary, but some associations are only found within species while others are only observed between species. A recent comparative study suggests that allocation trade-offs may be alleviated by disinvestment in ephemeral traits, such as nest-grown feathers, that are quickly replaced. However, direct resource allocation trade-offs cannot be inferred from interspecific trait associations without complementary intraspecific studies. Here, we asked whether there is evidence for a within-species allocation trade-off between feather quality and time spent in the nest in Tree Swallows (Tachycineta bicolor). Consistent with the idea that ephemeral traits are deprioritized, nest-grown feathers had lower barb density than adult feathers. However, despite substantial variation in fledging age among nestlings, there was no evidence for a negative association between time in the nest and feather quality. Furthermore, accounting for differences in resource availability by considering provisioning rate and a nest predation treatment did not reveal a trade-off that was masked by variation in resources. Our results are most consistent with the idea that the interspecific association between development and feather quality arises from adaptive specialization, rather than from a direct allocation trade-off.

     
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  6. Abstract

    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.

     
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  7. In response to a warming planet with earlier springs, migratory animals are adjusting the timing of essential life stages. Although these adjustments may be essential for keeping pace with resource phenology, they may prove insufficient, as evidenced by population declines in many species. However, even when species can match the tempo of climate change, other consequences may emerge when exposed to novel conditions earlier in the year. Here, using three long-term datasets on bird reproduction, daily insect availability, and weather, we investigated the complex mechanisms affecting reproductive success in an aerial insectivore, the tree swallow (Tachycineta bicolor). By examining breeding records over nearly half a century, we discovered that tree swallows have continuously advanced their egg laying by ∼3 d per decade. However, earlier-hatching offspring are now exposed to inclement weather events twice as often as they were in the 1970s. Our long-term daily insect biomass dataset shows no long-term trends over 25 y but precipitous drops in flying insect numbers on days with low ambient temperatures. Insect availability has a considerable impact on chick survival: Even a single inclement weather event can reduce offspring survival by >50%. Our results highlight the multifaceted threats that climate change poses on migrating species. The decoupling between cold snap occurrence and generally warming spring temperatures can affect reproductive success and threaten long-term persistence of populations. Understanding the exact mechanisms that endanger aerial insectivores is especially timely because this guild is experiencing the steepest and most widespread declines across North America and Europe.

     
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