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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. 

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. 

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. 

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. 

Abstract Competitive interactions often occur in series; therefore animals may respond to social challenges in ways that prepare them for success in future conflict. Changes in the production of the steroid hormone testosterone (T) are thought to mediate phenotypic responses to competition, but research over the past few decades has yielded mixed results, leading to several potential explanations as to why T does not always elevate following a social challenge. Here, we measured T levels in tree swallows (Tachycineta bicolor), a system in which females compete for limited nesting cavities and female aggression is at least partially mediated by T. We experimentally induced social challenges in two ways: (1) using decoys to simulate territorial intrusions and (2) removing subsets of nesting cavities to increase competition among displaced and territory-holding females. Critically, these experiments occurred pre-laying, when females are physiologically capable of rapidly increasing circulating T levels. However, despite marked aggression in both experiments, T did not elevate following real or simulated social challenges, and in some cases, socially challenged females had lower T levels than controls. Likewise, the degree of aggression was negatively correlated with T levels following a simulated territorial intrusion. Though not in line with the idea that social challenges prompt T elevation in preparation for future challenges, these patterns nevertheless connect T to territorial aggression in females. Coupled with past work showing that T promotes aggression, these results suggest that T may act rapidly to allow animals to adaptively respond to the urgent demands of a competitive event. 

Abstract Telomeres are emerging as correlates of fitness‐related traits and may be important mediators of ecologically relevant variation in life history strategies. Growing evidence suggests that telomere dynamics can be more predictive of performance than length itself, but very little work considers how telomere regulatory mechanisms respond to environmental challenges or influence performance in nature. Here, we combine observational and experimental data sets from free‐living tree swallows (Tachycineta bicolor) to assess how performance is predicted by the telomere regulatory gene POT1, which encodes a shelterin protein that sterically blocks telomerase from repairing the telomere. First, we show that lower POT1 gene expression in the blood was associated with higher female quality, that is, earlier breeding and heavier body mass. We next challenged mothers with an immune stressor (lipopolysaccharide injection) that led to “sickness” in mothers and 24 h of food restriction in their offspring. While POT1 did not respond to maternal injection, females with lower constitutive POT1 gene expression were better able to maintain feeding rates following treatment. Maternal injection also generated a 1‐day stressor for chicks, which responded with lower POT1 gene expression and elongated telomeres. Other putatively stress‐responsive mechanisms (i.e., glucocorticoids, antioxidants) showed marginal responses in stress‐exposed chicks. Model comparisons indicated that POT1 mRNA abundance was a largely better predictor of performance than telomere dynamics, indicating that telomere regulators may be powerful modulators of variation in life history strategies. 

Abstract Seasonal plasticity in aggression is likely to be shaped by the contexts in which aggression is beneficial, as well as the constraints inherent in its underlying mechanisms. In males, seasonal plasticity in testosterone (T) secretion is thought to underlie seasonal plasticity in conspecific aggression, but it is less clear how and why female aggression may vary across different breeding stages. Here, we integrate functional and mechanistic perspectives to begin to explore seasonal patterns of conspecific aggression in female tree swallows (Tachycineta bicolor), a songbird with intense female–female competition and T‐mediated aggression. Female tree swallows elevate T levels during early breeding stages, coinciding with competition for nest boxes, after which time T levels are roughly halved. However, females need to defend ownership of their nesting territory throughout the breeding season, suggesting it may be adaptive to maintain aggressive capabilities, despite low T levels. We performed simulated territorial intrusions using 3D‐printed decoys of female tree swallows to determine how their aggressive response to a simulated intrusion changes across the breeding season. First, we found that 3D‐printed decoys produce data comparable to stage‐matched studies using live decoys, providing researchers with a new, more economical method of decoy construction. Further, female aggressiveness remained relatively high through incubation, a period of time when T levels are quite low, suggesting that other mechanisms may regulate conspecific female aggression during parental periods. By showing that seasonal patterns of female aggression do not mirror the established patterns of T levels in this highly competitive bird, our findings provide a unique glimpse into how behavioural mechanisms and functions may interact across breeding stages to regulate plasticity. 

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.