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Abstract The ability to cope with heat is likely to influence species success amidst climate change. However, heat coping mechanisms are poorly understood in wild endotherms, which are increasingly pushed to their thermoregulatory limits.We take an organismal approach to this problem, unveiling how behavioural and physiological responses may allow success in the face of sublethal heat. We experimentally elevated nest temperatures for 4 h to mimic a future climate scenario (+4.5°C) during a critical period of post‐natal development in tree swallows (Tachycineta bicolor).Heat‐exposed nestlings exhibited marked changes in behaviour, including movement to cooler microclimates in the nest. They panted more and weighed less than controls at the end of the four‐hour heat challenge, suggesting panting‐induced water loss. Physiologically, heat induced high levels of heat shock protein (HSP) gene expression in the blood, alongside widespread transcriptional differences related to antioxidant defences, inflammation and apoptosis.Critically, all nestlings survived the heat challenge, and those exposed to milder heat weremorelikely to recruit into the breeding population. Early life but sub‐lethal heat may therefore act as a selective event, with the potential to shape population trajectories.Within the population, individuals varied in their physiological response to heat, namely in HSP gene expression, which exhibited higher mean and higher variance in heat‐exposed nestlings than in controls. Heat‐induced HSP levels were unrelated to individual body mass, or among‐nest differences in brood size, temperature, and behavioural thermoregulation. Nest identity explained a significant amount of HSP variation, yet siblings in the same nest differed by an average of ~4‐fold and individuals in the population differed by as much as ~100‐fold in their HSP response. This massive variation extends previous laboratory work in model organisms showing that heat shock proteins may harbour cryptic phenotypic variation.These results shed light on oft‐ignored elements of thermotolerance in wild birds at a critical stage of post‐natal development. By highlighting the scope of heat‐induced HSP gene expression and coupling it with a suite of organismal traits, we provide a framework for future testing of the mechanisms that shape species success in the face of change. Read the freePlain Language Summaryfor this article on the Journal blog.more » « less
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van_Oers, Kees (Ed.)Abstract In seasonally breeding animals, the costs and benefits of territorial aggression should vary over time; however, little work thus far has directly examined the scope and adaptive value of individual-level plasticity in aggression across breeding stages. We explore these issues using the tree swallow (Tachycineta bicolor), a single-brooded bird species in which females compete for limited nesting sites. We measured aggressiveness in nearly 100 females within 3 different stages: (1) shortly after territory-establishment, (2) during incubation, and (3) while caring for young chicks. Based on the timing, direction, and magnitude of behavioral changes between stages, we used k-means clustering to categorize each female’s behavior into a “plasticity type.” We then tested whether plasticity type and stage-specific aggression varied with key performance metrics. About 40% of females decreased aggressiveness across consecutive breeding stages to some degree, consistent with population-level patterns. 33% of females exhibited comparatively little plasticity, with moderate to low levels of aggression in all stages. Finally, 27% of females displayed steep decreases and then increases in aggression between stages; females exhibiting this pattern had significantly lower body mass while parenting, they tended to hatch fewer eggs, and they had the lowest observed overwinter survival rates. Other patterns of among-stage changes in aggressiveness were not associated with performance. These results reveal substantial among-individual variation in behavioral plasticity, which may reflect diverse solutions to trade-offs between current reproduction and future survival.more » « less
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Increasingly frequent and intense heatwaves generate new challenges for many organisms. Our understanding of the ecological predictors of thermal vulnerability is improving, yet, at least in endotherms, we are still only beginning to understand one critical component of predicting resilience: exactly how do wild animals cope with sub-lethal heat? In wild endotherms, most prior work focuses on one or a few traits, leaving uncertainty about organismal consequences of heatwaves. Here, we experimentally generated a 2.8°C heatwave for free-living nestling tree swallows (Tachycineta bicolor). Over a week-long period coinciding with the peak of post-natal growth, we quantified a suite of traits to test the hypotheses that (a) behavioral or (b) physiological responses may be sufficient for coping with inescapable heat. Heat-exposed nestlings increased panting and decreased huddling, but treatment effects on panting dissipated over time, even though heat-induced temperatures remained elevated. Physiologically, we found no effects of heat on: gene expression of three heat shock proteins in blood, muscle, and three brain regions; secretion of circulating corticosterone at baseline or in response to handling; and telomere length. Moreover, heat had a positive effect on growth and a marginal, but not significant, positive effect on subsequent recruitment. These results suggest that nestlings were generally buffered from deleterious effects of heat, with one exception: heat-exposed nestlings exhibited lower gene expression for superoxide dismutase, a key antioxidant defense. Despite this one apparent cost, our thorough organismal investigation indicates general resilience to a heatwave that may, in part, stem from behavioral buffering and acclimation. Our approach provides a mechanistic framework that we hope will improve understanding of species persistence in the face of climate change.more » « less
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Abstract Experimentally elevated testosterone (T) often leads to enhanced aggression, with examples across many different species, including both males and females. Indeed, the relationship between T and aggression is among the most well-studied and fruitful areas of research at the intersection of behavioral ecology and endocrinology. This relationship is also hypothesized to be bidirectional (i.e., T influences aggression, and aggression influences T), leading to four key predictions: (1) Individuals with higher T levels are more aggressive than individuals with lower T. (2) Seasonal changes in aggression mirror seasonal changes in T secretion. (3) Aggressive territorial interactions stimulate increased T secretion. (4) Temporary elevations in T temporarily increase aggressiveness. These predictions cover a range of timescales, from a single snapshot in time, to rapid fluctuations, and to changes over seasonal timescales. Adding further complexity, most predictions can also be addressed by comparing among individuals or with repeated sampling within individuals. In our review, we explore how the spectrum of results across predictions shapes our understanding of the relationship between T and aggression. In all cases, we can find examples of results that do not support the initial predictions. In particular, we find that Predictions 1–3 have been tested frequently, especially using an among-individual approach. We find qualitative support for all three predictions, though there are also many studies that do not support Predictions 1 and 3 in particular. Prediction 4, on the other hand, is something that we identify as a core underlying assumption of past work on the topic, but one that has rarely been directly tested. We propose that when relationships between T and aggression are individual-specific or condition-dependent, then positive correlations between the two variables may be obscured or reversed. In essence, even though T can influence aggression, many assumed or predicted relationships between the two variables may not manifest. Moving forward, we urge greater attention to understanding how and why it is that these bidirectional relationships between T and aggression may vary among timescales and among individuals. In doing so, we will move toward a deeper understanding on the role of hormones in behavioral adaptation.more » « less
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Abstract Biologists aim to explain patterns of growth, reproduction and ageing that characterize life histories, yet we are just beginning to understand the proximate mechanisms that generate this diversity. Existing research in this area has focused on telomeres but has generally overlooked the telomere's most direct mediator, the shelterin protein complex. Shelterin proteins physically interact with the telomere to shape its shortening and repair. They also regulate metabolism and immune function, suggesting a potential role in life history variation in the wild. However, research on shelterin proteins is uncommon outside of biomolecular work.Intraspecific analyses can play an important role in resolving these unknowns because they reveal subtle variation in life history within and among populations. Here, we assessed ecogeographic variation in shelterin protein abundance across eight populations of tree swallow (Tachycineta bicolor) with previously documented variation in environmental and life history traits. Using the blood gene expression of four shelterin proteins in 12‐day‐old nestlings, we tested the hypothesis that shelterin protein gene expression varies latitudinally and in relation to both telomere length and life history.Shelterin protein gene expression differed among populations and tracked non‐linear variation in latitude: nestlings from mid‐latitudes expressed nearly double the shelterin mRNA on average than those at more northern and southern sites. However, telomere length was not significantly related to latitude.We next assessed whether telomere length and shelterin protein gene expression correlate with 12‐day‐old body mass and wing length, two proxies of nestling growth linked to future fecundity and survival. We found that body mass and wing length correlated more strongly (and significantly) with shelterin protein gene expression than with telomere length.These results highlight telomere regulatory shelterin proteins as potential mediators of life history variation among populations. Together with existing research linking shelterin proteins and life history variation within populations, these ecogeographic patterns underscore the need for continued integration of ecology, evolution and telomere biology, which together will advance understanding of the drivers of life history variation in nature.more » « less
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