Corticosterone exposure is associated with long-term changes in DNA methylation, physiology and breeding decisions in a wild bird.

When facing challenges, vertebrates activate a hormonal stress response that can dramatically alter behaviour and physiology. Although this response can be costly, conceptual models suggest that it can also recalibrate the stress response system, priming more effective responses to future challenges. Little is known about whether this process occurs in wild animals, particularly in adulthood, and if so, how information about prior experience with stressors is encoded. One potential mechanism is hormonally mediated changes in DNA methylation. We simulated the spikes in corticosterone that accompany a stress response using non-invasive dosing in tree swallows (Tachycineta bicolor) and monitored the phenotypic effects 1 year later. In a subset of individuals, we characterized DNA methylation using reduced representation bisulfite sequencing shortly after treatment and a year later. The year after treatment, experimental females had stronger negative feedback and initiated breeding earlier-traits that are associated with stress resilience and reproductive performance in our population-and higher baseline corticosterone. We also found that natural variation in corticosterone predicted patterns of DNA methylation. Finally, corticosterone treatment influenced methylation on short (1-2 weeks) and long (1 year) time scales; however, these changes did not have clear links to functional regulation of the stress response. Taken together, our results are consistent with corticosterone-induced priming of future stress resilience and support DNA methylation as a potential mechanism, but more work is needed to demonstrate functional consequences. Uncovering the mechanisms linking experience with the response to future challenges has implications for understanding the drivers of stress resilience.

Experimentally elevated corticosterone does not affect bacteria killing ability of breeding female tree swallows (Tachycineta bicolor).

The immune system can be modulated when organisms are exposed to acute or chronic stressors. Glucocorticoids (GCs), the primary hormonal mediators of the physiological stress response, are suspected to play a crucial role in immune modulation. However, most evidence of stress-associated immunomodulation does not separate the effects of glucocorticoid-dependent pathways from those of glucocorticoid-independent mechanisms on immune function. In this study, we experimentally elevated circulating corticosterone, the main avian glucocorticoid, in free-living female tree swallows (Tachycineta bicolor) for one to two weeks to test its effects on immune modulation. Natural variation in bacteria killing ability (BKA), a measure of innate constitutive immunity, was predicted by the interaction between timing of breeding and corticosterone levels. However, experimental elevation of corticosterone had no effect on BKA. Therefore, even when BKA is correlated with natural variation in glucocorticoid levels, this relationship may not be causal. Experiments are necessary to uncover the causal mechanisms of immunomodulation and the consequences of acute and chronic stress on disease vulnerability. Findings in other species indicate that acute increases in GCs can suppress BKA; but our results support the hypothesis that this effect does not persist over longer timescales, during chronic elevations in GCs. Direct comparisons of the effects of acute vs. chronic elevation of GCs on BKA will be important for testing this hypothesis.

Manipulation of a social signal affects DNA methylation of a stress-related gene in a free-living bird.

Social status directly affects the health of humans and other animals. Low status individuals receive more antagonistic encounters, have fewer supportive relationships, and have worse health outcomes. However, the physiological and cellular processes that mediate the relationship between the social environment and health are incompletely known. Epigenetic regulation of the HPA axis, the neuroendocrine pathway that activates in response to stressors, may be one process that is sensitive to the social environment. Here, we experimentally manipulated plumage, a key social signal in female tree swallows (Tachycineta bicolor) and quantified methylation of four genes in the HPA axis before and after treatment. We found that dulling the white breast plumage affected methylation in one gene, CRHR1; however, the effect depended on the original brightness of the bird. Methylation in this gene was correlated with baseline corticosterone levels, suggesting that DNA methylation of CRHR1 helps regulate glucocorticoid production in this species. Methylation in two other genes, FKBP5 and GR, changed over the course of the experiment, independent of treatment. These results show that methylation of these genes is labile into adulthood and suggest that epigenetic regulation of the HPA axis could help birds respond to current environmental conditions.

Among-population variation in telomere regulatory proteins and their potential role as hidden drivers of intraspecific variation in life history.

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.

Understanding spatiotemporal effects of food supplementation on host-parasite interactions using community-based science.

Supplemental feeding can increase the overall health of animals but also can have variable effects on how animals defend themselves against parasites. However, the spatiotemporal effects of food supplementation on host-parasite interactions remain poorly understood, likely because large-scale, coordinated efforts to investigate them are difficult. Here, we introduce the Nest Parasite Community Science Project, which is a community-based science project that coordinates studies with bird nest box 'stewards' from the public and scientific community. This project was established to understand broad ecological patterns between hosts and their parasites. The goal of this study was to determine the effect of food supplementation on eastern bluebirds (Sialia sialis) and their nest parasite community across the geographic range of the bluebirds from 2018 to 2021. We received 674 nests from 69 stewards in 26 states in the eastern United States. Nest box stewards reported whether or not they provided mealworms or suet near nesting bluebirds, then they followed the nesting success of the birds (number of eggs laid and hatched, proportion that hatched, number and proportion of nestlings that successfully fledged). We then identified and quantified parasites in the nests. Overall, we found that food supplementation increased fledging success. The most common nest parasite taxon was the parasitic blow fly (Protocalliphora sialia), but a few nests contained fleas (Ceratophyllus idius, C. gallinae and Orchopeas leucopus) and mites (Dermanyssus spp. and Ornithonyssus spp.). Blow flies were primarily found at northern latitudes, where food supplementation affected blow fly prevalence. However, the direction of this effect varied substantially in direction and magnitude across years. More stewards fed bluebirds at southern latitudes than at northern latitudes, which contradicts the findings of other community-based science projects. Overall, food supplementation of birds was associated with increased host fitness but did not appear to play a consistent role in defence against these parasites across all years. Our study demonstrates the importance of coordinated studies across years and locations to understand the effects of environmental heterogeneity, including human-based food supplementation, on host-parasite dynamics.

Gene expression in the female tree swallow brain is associated with inter- and intra-population variation in glucocorticoid levels.

Studies of the evolutionary causes and consequences of variation in circulating glucocorticoids (GCs) have begun to reveal how they are shaped by selection. Yet the extent to which variation in circulating hormones reflects variation in other important regulators of the hypothalamic-pituitary-adrenal (HPA) axis, and whether these relationships vary among populations inhabiting different environments, remain poorly studied. Here, we compare gene expression in the brain of female tree swallows (Tachycineta bicolor) from populations that breed in environments that differ in their unpredictability. We find evidence of inter-population variation in the expression of glucocorticoid and mineralocorticoid receptors in the hypothalamus, with the highest gene expression in a population from an extreme environment, and lower expression in a population from a more consistent environment as well as in birds breeding at an environmentally variable high-altitude site that are part of a population that inhabits a mixture of high and low altitude habitats. Within some populations, variation in circulating GCs predicted differences in gene expression, particularly in the hypothalamus. However, some patterns were present in all populations, whereas others were not. These results are consistent with the idea that some combination of local adaptation and phenotypic plasticity may modify components of the HPA axis affecting stress resilience. Our results also underscore that a comprehensive understanding of the function and evolution of the stress response cannot be gained from measuring circulating hormones alone, and that future studies that apply a more explicitly evolutionary approach to important regulatory traits are likely to provide significant insights.

Birds advancing lay dates with warming springs face greater risk of chick mortality.

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.

Cold temperatures induce priming of the glucose stress response in tree swallows.

Capricious environments often present wild animals with challenges that coincide or occur in sequence. Conceptual models of the stress response predict that one threat may prime or dampen the response to another. Although evidence has supported this for glucocorticoid responses, much less is known about the effects of previous challenges on energy mobilization. Food limitation may have a particularly important effect, by altering the ability to mobilize energy when faced with a subsequent challenge. We tested the prediction that challenging weather conditions, which reduce food availability, alter the energetic response to a subsequent acute challenge (capture and restraint). Using a three-year dataset from female tree swallows measured during three substages of breeding, we used a model comparison approach to test if weather (temperature, wind speed, and precipitation) over 3- or 72-hour timescales predicted baseline and post-restraint glucose levels, and if so which environmental factors were the strongest predictors. Contrary to our predictions, weather conditions did not affect baseline glucose; however, birds that had experienced lower temperatures over the preceding 72 h tended to have higher stress-induced glucose when faced with an acute stressor. We also saw some support for an effect of rainfall on stress-induced glucose: around the time that eggs hatched, birds that had experienced more rainfall over the preceding 72 h mounted lower responses. Overall, we find support in a wild animal for the idea that the glucose stress response may be primed by exposure to prior challenges.

The relative speed of the glucocorticoid stress response varies independently of scope and is predicted by environmental variability and longevity across birds.

The acute glucocorticoid response is a key mediator of the coordinated vertebrate response to unpredictable challenges. Rapid glucocorticoid increases initiate changes that allow animals to cope with stressors. The scope of the glucocorticoid response - defined here as the absolute increase in glucocorticoids - is associated with individual differences in performance and varies across species with environment and life history. In addition to varying in scope, responses can differ enormously in speed; however, relatively little is known about whether speed and absolute glucocorticoid levels covary, how selection shapes speed, or what aspects of speed are important. We used corticosterone samples collected at 5 time points from 1750 individuals of 60 species of birds to ask i) how the speed and scope of the glucocorticoid response covary and ii) whether variation in absolute or relative speed is predicted by environmental context or life history. Among species, faster absolute glucocorticoid responses were strongly associated with a larger scope. Despite this covariation, the relative speed of the glucocorticoid response (standardized within species) varied independently of absolute scope, suggesting that selection could operate on both features independently. Species with faster relative glucocorticoid responses lived in locations with more variable temperature and had shorter lifespans. Our results suggest that rapid changes associated with the speed of the glucocorticoid response, such as those occurring through non-genomic receptors, might be an important determinant of coping ability and we emphasize the need for studies designed to measure speed independently of absolute glucocorticoid levels.

Individual variation in natural or manipulated corticosterone does not covary with circulating glucose in a wild bird.

Animals respond to sudden challenges with a coordinated set of physiological and behavioral responses that enhance the ability to cope with stressors. While general characteristics of the vertebrate stress response are well described, it is not as clear how individual components covary between or within individuals. A rapid increase in glucocorticoids coordinates the stress response and one of the primary downstream results is an increase in glucose availability via reduced glucose utilization. Here, we asked whether between- and within-individual variation in corticosterone directly predict variation in glucose. We collected 2673 paired glucose and corticosterone measures from 776 tree swallows (Tachycineta bicolor) from four populations spanning the species range. In adults, glucose and corticosterone both increased during a standardized restraint protocol in all four populations. Moreover, in one population experimentally increasing a precursor that stimulates corticosterone release resulted in a further increase in both measures. In contrast, nestlings did not show a robust glucose response to handling or manipulation. Despite this group-level variation, there was very little evidence in any population that between-individual variation in corticosterone predicted between-individual variation in glucose regulation. Glucose was moderately repeatable within individuals, but within-individual variation in glucose and corticosterone were unrelated. Our results highlight the fact that a strong response in one aspect of the coordinated acute stress response (corticosterone) does not necessarily indicate that specific downstream components, such as glucose, will show similarly strong responses. These results have implications for understanding the evolution of integrated stress response systems.

Developmental temperature predicts the adult response to stressors in a free-living passerine.

Early-life conditions can have substantial effects on the ways animals respond to stressors as adults. In particular, thermal conditions during development affect juveniles' responses to stressors, and there is evidence that these effects may extend into adulthood. However, these effects remain poorly understood, especially in free-living organisms. We test the prediction that ambient temperatures during laying, embryonic development and nestling development affect the hormonal mediators of the response to stressors in adults. To do so, we use a long-term dataset of tree swallows (Tachycineta bicolor) with records from both natal development and adult breeding. We found a strong, negative relationship between ambient temperature during early development (incubation) and an individual's corticosterone (CORT) response to stress later in life (while incubating her own young). Thermal conditions during other stages of natal development also showed a weak relationship with baseline CORT during provisioning. In a post hoc analysis, we found no evidence that ambient temperature during development differentially influenced the survival and recruitment of juveniles with different CORT phenotypes. Our results show that thermal conditions during development can have long-term effects on how individuals respond to stressors.

Genome-wide variation in DNA methylation is associated with stress resilience and plumage brightness in a wild bird.

Individuals often differ in their ability to cope with challenging environmental and social conditions. Evidence from model systems suggests that patterns of DNA methylation are associated with variation in coping ability. These associations could arise directly if methylation plays a role in controlling the physiological response to stressors by, among other things, regulating the release of glucocorticoids in response to challenges. Alternatively, the association could arise indirectly if methylation and resilience have a common cause, such as early-life conditions. In either case, methylation might act as a biomarker for coping ability. At present, however, relatively little is known about whether variation in methylation is associated with organismal performance and resilience under natural conditions. We studied genome-wide patterns of DNA methylation in free-living female tree swallows (Tachycineta bicolor) using methylated DNA immunoprecipitation (MeDIP) and a tree swallow genome that was assembled for this study. We identified areas of the genome that were differentially methylated with respect to social signal expression (breast brightness) and physiological traits (ability to terminate the glucocorticoid stress response through negative feedback). We also asked whether methylation predicted resilience to a subsequent experimentally imposed challenge. Individuals with brighter breast plumage and higher stress resilience had lower methylation at differentially methylated regions across the genome. Thus, widespread differences in methylation predicted both social signal expression and the response to future challenges under natural conditions. These results have implications for predicting individual differences in resilience, and for understanding the mechanistic basis of resilience and its environmental and social mediators.

Apparent inbreeding preference despite inbreeding depression in the American crow.

Although matings between relatives can have negative effects on offspring fitness, apparent inbreeding preference has been reported in a growing number of systems, including those with documented inbreeding depression. Here, we examined evidence for inbreeding depression and inbreeding preference in two populations (Clinton, New York, and Davis, California, USA) of the cooperatively breeding American crow (Corvus brachyrhynchos). We then compared observed inbreeding strategies with theoretical expectations for optimal, adaptive levels of inbreeding, given the inclusive fitness benefits and population-specific magnitude of inbreeding depression. We found that low heterozygosity at a panel of 33 microsatellite markers was associated with low survival probability (fledging success) and low white blood cell counts among offspring in both populations. Despite these costs, our data were more consistent with inbreeding preference than avoidance: The observed heterozygosity among 396 sampled crow offspring was significantly lower than expected if local adults were mating by random chance. This pattern was consistent across a range of spatial scales in both populations. Adaptive levels of inbreeding, given the magnitude of inbreeding depression, were predicted to be very low in the California population, whereas complete disassortative mating was predicted in the New York population. Sexual conflict might have contributed to the apparent absence of inbreeding avoidance in crows. These data add to an increasing number of examples of an "inbreeding paradox," where inbreeding appears to be preferred despite inbreeding depression.

Traffic noise exposure alters nestling physiology and telomere attrition through direct, but not maternal, effects in a free-living bird.

Anthropogenic impacts, such as noise pollution from transportation networks, can serve as stressors to some wildlife species. For example, increased exposure to traffic noise has been found to alter baseline and stress-induced corticosterone levels, reduce body condition and reproductive success, and increase telomere attrition in free-living birds. However, it remains unknown if alterations in nestling phenotype are due to direct or indirect effects of noise exposure. For example, indirect (maternal) effects of noise may occur if altered baseline and stress-induced corticosterone in mothers results in differential deposition of yolk steroids or other components in eggs. Noise exposure may also alter nestling corticosterone levels directly, given that nestlings cannot escape the nest during development. Here, we examined maternal versus direct effects of traffic noise exposure on baseline and stress-induced corticosterone levels, and body condition (as measured by size-corrected mass) in nestling tree swallows (Tachycineta bicolor). We used a two-way factorial design and partially cross-fostered eggs between nests exposed to differing levels (i.e. amplitudes) of traffic noise. For nestlings that were not cross-fostered, we also investigated the effects of traffic noise on telomere dynamics. Our results show a positive relationship between nestling baseline and stress-induced corticosterone and nestling noise exposure, but not maternal noise exposure. While we did not find a relationship between noise and body condition in nestlings, nestling baseline corticosterone was negatively associated with body condition. We also found greater telomere attrition for nestlings from nests with greater traffic noise amplitudes. These results suggest that direct, rather than maternal, effects result in potentially long-lasting consequences of noise exposure. Reduced nestling body condition and increased telomere attrition have been shown to reduce post-fledging survival in this species. Given that human transportation networks continue to expand, strategies to mitigate noise exposure on wildlife during critical periods (i.e. breeding) may be needed to maintain local population health in free-living passerines, such as tree swallows.

The lingering impact of stress: brief acute glucocorticoid exposure has sustained, dose-dependent effects on reproduction.

Acutely stressful experiences can have profound and persistent effects on phenotype. Across taxa, individuals differ remarkably in their susceptibility to stress. However, the mechanistic causes of enduring stress effects, and of individual differences in stress susceptibility, are poorly understood. Here, we tested whether brief, acute increases in glucocorticoid hormones have persistent effects on phenotype, and whether effects differ according to the magnitude or duration of elevation. We used a novel method to non-invasively manipulate hormone levels on short time scales: the application of corticosterone gel to a model egg secured in the nest. Free-living female tree swallows (Tachycineta bicolor) exposed to several brief corticosterone increases during incubation showed dose-dependent differences in behaviour throughout the reproductive period. Birds receiving treatments that simulated higher or longer acute stress responses later provisioned larger broods at lower rates; the resulting offspring were smaller in size. Treatment did not influence female body condition, oxidative stress, reproductive success or inter-annual survival, but exposed females maintained higher baseline corticosterone after treatments ceased. Overall, these results indicate that brief, acute elevations in glucocorticoids in adulthood can have long-term consequences. Furthermore, individuals that mount a greater or longer acute stress response may be more likely to experience lingering effects of stress.

Major histocompatibility complex variation and blood parasites in resident and migratory populations of the common yellowthroat.

Genes of the major histocompatibility complex (MHC) are a critical part of the adaptive immune response, and the most polymorphic genes in the vertebrate genome, especially in passerine birds. This diversity is thought to be influenced by exposure to pathogens which can vary in relation to numerous factors. Migratory behaviour may be a particularly important trait to consider because migratory birds are exposed to a greater number of different pathogens and parasites at both breeding (i.e. temperate) and overwintering (i.e. tropical and subtropical) areas, as well as at stopover sites during migration. Thus, migrants are predicted to have greater MHC diversity than residents. We compared MHC variation, at both class I and II, and levels of haemosporidian infection between one resident and two migratory populations of the common yellowthroat (Geothlypis trichas). We found that residents were less likely to be infected with haemosporidian parasites and had lower MHC diversity at class I; however, variation at MHC class II was greater in residents than migrants, contrary to our prediction. These patterns were not likely to be caused by differences in population demography as genomewide heterozygosity (based on 9225 single nucleotide polymorphisms) was high in all three populations and not correlated with MHC variation. Our different results for MHC class I and II suggest that studies of immune gene variation in relation to life history need to consider that there could be different selection pressures arising from intracellular (class I) and extracellular (class II) pathogens in different populations.

Effects of experimental chronic traffic noise exposure on adult and nestling corticosterone levels, and nestling body condition in a free-living bird.

Transportation noise affects urbanized, rural, and otherwise unaltered habitats. Given expanding transportation networks, alterations in the acoustic landscapes experienced by animals are likely to be pervasive and persistent (i.e. chronic). It is important to understand if chronic noise exposure alters behavior and physiology in free-living animals, as it may result in long-lasting impacts, such as reduced reproductive success. Here, we experimentally tested the effects of chronic traffic noise on baseline and stress-induced corticosterone (the primary avian glucocorticoid), parental feeding behavior, and fitness proxies in breeding tree swallows (Tachycineta bicolor). Our results show that chronic traffic noise is related to altered corticosterone in both adult female and nestling tree swallows, suggesting that noise may be a stressor in both groups. In adult females, our results suggest that traffic noise is related to a limited ability to respond to subsequent acute stressors (i.e. reduced stress-induced corticosterone levels after handling). Further, our results show no evidence of habituation to noise during the breeding season, as the negative relationship between traffic noise and adult female stress-induced corticosterone became stronger over time. In nestlings, we found a positive relationship between traffic noise exposure and baseline corticosterone. Finally, we found a negative relationship between traffic noise and nestling body condition, despite no detectable effects of noise on nestling provisioning (e.g. parental feeding rate, or insect bolus size/composition). These results highlight the potential long-term consequences of chronic noise exposure, as increased baseline corticosterone and reduced nestling body condition in noise-exposed areas may have negative, population-level consequences.

Efficacy of negative feedback in the HPA axis predicts recovery from acute challenges.

The glucocorticoid stress response mediates a suite of physiological and behavioural changes that allow vertebrates to cope with transient stressors. Chronically elevated glucocorticoid levels are known to result in a variety of organismal costs, but relatively little is known about the downstream effects of mounting a series of brief, acute spikes in circulating glucocorticoids. Conceptual models of stress suggest that repeated acute stressors might produce 'wear-and-tear' on the stress-response system when encountered in sequence. We used a novel technique to experimentally induce acute corticosterone spikes on either three or six consecutive days in incubating tree swallows. Consistent with the 'wear-and-tear' hypothesis, we found that (i) a sequence of corticosterone spikes produced cumulative effects on corticosterone regulation, (ii) treatment frequency predicted the severity of consequences, and (iii) individual variation in the ability to terminate the stress response through negative feedback predicted the duration of physiological disruption in the group that experienced the most frequent challenges. Our results illustrate the importance of assessing multiple aspects of the hormonal stress response and have implications for understanding both individual and population resilience to repeated transient stressors.

Age and infection history are revealed by different ornaments in a warbler.

Female preference for older or more disease-resistant males are both possible outcomes of parasite-mediated sexual selection, but the extent to which infection alters the development of ornaments to yield signals of male age and health has rarely been explored. In a longitudinal study of 61 male common yellowthroats (Geothlypis trichas), age-related increases in the size of the melanin-based mask and carotenoid-based bib were not correlated among young males, likely owing to differences in how blood parasites affect ornament development. Infection with trypanosomes and hemosporidians in a male's first breeding season was associated with slower growth of the mask; uninfected males attained large masks in their second breeding season, while infected males attained large masks in their third breeding season. In contrast, the bib size of males increased every year regardless of infection. As a consequence, different populations of males are identified by the largest ornaments-older males in the case of bib and a combination of older males and young, uninfected males in the case of mask. Although mask is thus the more informative trait with respect to male health, females prefer large bibs in our population. If infection is opportunistic, young, uninfected males may not possess good genes for parasite resistance but simply good luck, and it may benefit females to prefer older males who are more likely to have withstood prior episodes of selection. A "pure" signal of age may be a more reliable signal of resistance to parasites than an ornament whose expression is modulated by infection.

The repeatability of glucocorticoids: A review and meta-analysis.

Glucocorticoids are highly conserved hormones that mediate a suite of responses to changing conditions in vertebrates. Recent work has focused on understanding how selection operates on glucocorticoid secretion in natural populations. Because heritability is rarely estimated and difficult to measure in the wild, many studies report within-individual repeatability as an estimate of stable between individual differences in glucocorticoid secretion. We conducted a systematic review and meta-analysis on estimates of within-individual glucocorticoid repeatability to elucidate general patterns of repeatability, and to test for relationships between covariates and estimates of repeatability. To this end, we collected 203 estimates of within-individual glucocorticoid repeatability drawn from 71 separate studies and 55 species. Overall, we found moderate levels of repeatability (0.29). We also found that repeatability varied by sample type. Long-term measures (e.g., fecal and feather samples) and acute stress-induced plasma glucocorticoids had higher repeatability (long-term: 0.44, stress-induced: 0.38), than baseline glucocorticoid levels (0.18). Repeatability also decreased with increasing time between repeated sampling events. Despite significant overall repeatability, there was substantial heterogeneity in estimates from different studies, suggesting that repeatability of glucocorticoid secretion varies substantially across systems and conditions. We discuss the implications of our results for understanding selection on glucocorticoid traits and suggest that continuing work should focus on evaluating the repeatability of within-individual glucocorticoid reaction norms.