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Vitousek, M. N.

Publications and source records attributed to Vitousek, M. N..

13 recordsLinked to original sources

Geographical variation in plasma bactericidal ability of breeding tree swallows (Tachycineta bicolor)

Immune defenses may vary across environments due to differences in life history or abiotic and biotic characteristics, but few studies have compared the strength of immune responses across broad geographical gradients. Here we investigated how bacteria killing ability (BKA), a measure of constitutive innate immune function, varies among populations of tree swallows (Tachycineta bicolor) inhabiting different environments. We hypothesized that populations living in unpredictable environments, which also have shorter breeding seasons and thus fewer opportunities to renest in the event of reproductive failure, would invest in reproduction at the expense of immunity. To test this hypothesis, we measured BKA and monitored reproductive activity in four populations located across most of the breeding range of tree swallows, in Tennessee, New York, Wyoming and Alaska. Consistent with our predictions, BKA was lowest in Alaska and Wyoming and highest in Tennessee. In most populations BKA was also lower during incubation than during nestling provisioning, and lower in males than in females. These results suggest that the high reproductive investment seen in populations experiencing more unpredictable breeding conditions may come at a cost to immune function. While reduced immune investment could increase susceptibility to parasites, this potential cost is likely offset by lower parasite pressure in these environments, limiting the need for maintaining strong constitutive innate defenses like BKA.

ecology↗

Developmental cold exposure increases the ability to maintain body temperature during future cold challenges in a free-living altricial bird

Developing in suboptimal temperatures can have widespread negative effects in organisms, but early exposure to thermal challenges can also trigger increased investment in thermoregulatory capacity. Within birds, the effects of cold exposure during incubation may differ between precocial and altricial species due to differences in the ontogeny of thermoregulation. To date, most of the evidence showing that embryonic cold exposure shapes future thermoregulatory capacity comes from a few precocial species in laboratory settings. Less is known about sensitivity to low-temperature incubation in altricial species which only become fully endothermic after hatching. In this study, we tested the effects of cold temperatures during embryonic development by temporarily cooling the nest boxes of free-living tree swallows (Tachycineta bicolor) during late incubation and subsequently exposing nestlings to an acute cold challenge. Cold exposure during early development made nestlings better at maintaining their body temperatures during the acute challenge. Developmentally cold-exposed birds also had higher thyroxine (T4) levels when sampled at lower ambient temperatures, whereas control birds showed the opposite relationship. Among nestlings that failed to maintain their body temperature during the acute cold challenge, developmentally cold-exposed nestlings secreted more corticosterone during the acute cold challenge than control nestlings. Despite these changes, cold-exposed birds did not differ from controls in cold-induced metabolic rates, body mass, or bacteria killing ability. These results are, to our knowledge, the first to show that developmental cold exposure increases the capacity to maintain body temperature during future cold challenges in a songbird. These findings suggest that experiencing even a mild decline in ambient temperatures during embryonic development could prime birds to cope more effectively with harsh or variable environmental conditions later in life.

ecology↗

Organismal robustness and resilience influence the ability to cope with cold snaps

Coping with challenges often requires maintaining performance during poor conditions (robustness) and reestablishing normal performance following disturbance (resilience). Trade-offs between performance under normal and challenging conditions may generate variation in stress coping capacity, but there is little empirical data from wild populations. We studied robustness and resilience to temperature in tree swallows (Tachycineta bicolor) using a 39-year dataset that included >75,000 hours of behavioral data. Cold snaps had profound and sustained impacts on fitness; effects on nestlings were mediated by the behavioral robustness and resilience of parents. Parental robustness was predicted by developmental cold exposure and current endocrine state. As expected, trade-offs between peak performance and behavioral robustness influenced susceptibility. Selection on trade-offs may generate population differences in vulnerability to changing temperature regimes.

ecology↗

The mouse gut microbiota responds to predator odor and predicts host behavior

Chronic stressors can alter the mammalian gut microbiota in ways that mediate host stress responses, but the impacts of acute stressors on these interactions are less well understood. Here, we show that brief exposure of wild-derived mice to predator odor altered gut-microbiota composition, which in turn predicted host behavior. We investigated the individual and combined effects of 15-minute exposures to synthetic fox fecal odor and 30 days of chronic social isolation, an established chronic stressor. Using ethological assays, visceral adipose tissue transcriptomics, and genome-resolved metagenomics, we found that predator-odor exposure significantly affected mouse behavior, gene expression, and gut microbiota. Predator odor-responsive bacteria were associated with the expression of genes involved in anti-microbial defense, and host behavioral responses were predicted by random forest models trained on gut-microbiota profiles. These findings indicate interactions between the gut microbiota and wild-mouse responses to the threat of predation, an ecologically relevant acute stressor.

microbiology↗

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

When facing challenges, vertebrates activate an evolutionarily conserved hormonal stress response that can dramatically alter behavior 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 to DNA methylation. We simulated the spikes in corticosterone that accompany an acute stress response using non-invasive dosing in female tree swallows (Tachycineta bicolor) and monitored the phenotypic effects one year later, and DNA methylation both shortly after treatment and a full 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 stress-induced corticosterone predicted patterns of DNA methylation, including methylation of the MC2R gene, which encodes the adrenocorticotropic hormone receptor. Finally, corticosterone treatment causally influenced methylation on short (1-2 weeks) and long (1 year) time scales; however, many of 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. Uncovering the mechanisms linking experience with the response to future challenges has implications for understanding the drivers of stress resilience. SIGNIFICANCEA stress response to an environmental challenge can preserve an individuals fitness and may even prime them to survive similar challenges in the future. What mechanisms underlie priming is unclear, but epigenetic alterations to stress-related genes are one possibility. We experimentally tested whether increasing corticosterone in free-living swallows had lasting phenotypic or epigenetic effects. A year after treatment, females who received corticosterone had altered stress physiology and bred earlier than control birds, traits that are associated with higher fitness. Treatment also altered DNA methylation and methylation of the MC2R gene was correlated with stress physiology. This study adds to a growing body of literature suggesting that epigenetic changes are key to animals response to a changing environment.

physiology↗

Joint effects of social interactions and environmental challenges on physiology, internal microbiome, and reproductive performance in tree swallows (Tachycineta bicolor).

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 environment 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), social interactions 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 social interactions, 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.

physiology↗

Developmental stage-dependent effects of perceived predation risk on physiology and fledging success of tree swallows (Tachycineta bicolor)

The risk of predation directly affects physiology, behavior, and fitness of wild birds. Social interactions with conspecifics may affect how individuals respond to stressors such as predators. Strong social connections could help individuals recover from a stressful experience; however, competitive interactions also have the potential to exacerbate stress. Few studies have investigated the interaction between environmental stressors and the social landscape in wild bird populations. Here, we experimentally simulated predation attempts on breeding female tree swallows (Tachicyneta bicolor). At the same time, we manipulated female breast plumage color, a key social signal. Simulated predation events on tree swallows negatively affected their nestlings condition, telomere lengths, and fledging success. However, the effects of experimental manipulations were timing-dependent: simulated predation during the early nestling period was more detrimental than "predation" during incubation. Contrary to our expectations, manipulation of the social environment did not affect the response of tree swallows to simulated predation. However, manipulating female plumage during the nestling period did affect nestling size, indicating an effect of the social environment on reproductive success. Our data demonstrate that transient stressors on breeding female birds can have carry-over effects on their nestlings, some of which may be long-lasting.

ecology↗

Within-individual consistency and between-individual variation in the shapes of eggs laid by tree swallows (Tachycineta bicolor)

Bird eggs come in a wide variety of shapes and recent large-scale studies across species have renewed interest in understanding the factors that generate and maintain this diversity. However, these advances largely overlook the fact that egg shape also varies dramatically within species: between populations, between individuals, and between eggs produced by the same individual. We measured the shape and size of 1382 eggs produced by 205 tree swallows (Tachycineta bicolor) in 259 nests with many females having eggs measured in two or three years. We found that intra-specific variation in the asymmetry and ellipticity of tree swallow eggs spanned the range of typical egg shapes from 69% of species reported in a recent comparative study. Variation in shape and size was largely explained by individual identity, as the repeatability of egg shape and size was remarkably high both for eggs produced within a clutch and for clutches produced in successive years. All characteristics of mother and daughter eggs were positively correlated, although with a sample size of only 15 pairs these relationships were not significant. Female mass and structural size were correlated with the size of eggs produced, but not with their shape. Older females produced eggs that were larger, more asymmetrical, and less elliptical; this pattern was driven by a combination of both longitudinal changes in egg characteristics as females aged and by differential overwinter survival of females with particular egg characteristics. We found no evidence that any aspect of shape or size that we measured was related to nestling measurements or fate. Finally, we found that the patterns of covariation in aspects of egg size and shape between-individuals differed from that observed within-individuals, suggesting that the mechanisms driving egg shape variation might differ across these levels. A complete understanding of avian egg shapes will need to incorporate variation at multiple scales and we discuss the interpretation of our results in light of recent large-scale comparative studies that focus only on mean species egg shapes.

zoology↗

Environmental variability and longevity predict the speed of the acute glucocorticoid response 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 1,750 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. As predicted by a recent model, 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.

physiology↗

Investigating a trade-off between the quality of nest grown feathers and pace of development in an altricial bird.

Life history theory provides a framework for understanding how trade-offs generate negative trait associations. Among nestling birds, developmental rate, 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 inter-specific trait-associations without complementary intra-specific studies. Here, we asked whether there is evidence for a within-species allocation trade-off between feather quality and developmental speed 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 developmental pace 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 inter-specific association between development and feather quality arises from adaptive specialization, rather than from a direct allocation trade-off.

ecology↗

Environmental unpredictability shapes glucocorticoid regulation across populations of tree swallows

Responding appropriately to challenges is an important contributor to fitness. Variation in the regulation of glucocorticoid hormones, which mediate the phenotypic response to challenges, can therefore influence the ability to persist in a given environment. We compared stress responsiveness in four populations of tree swallows (Tachycineta bicolor) along an environmental gradient to evaluate support for different selective pressures in driving the evolution of glucocorticoid regulation. In accordance with the environmental unpredictability hypothesis, stronger stress responses were seen in more unpredictable environments. Contrary to the reproductive value hypothesis, the stress response was not lower in populations engaging in more valuable reproductive attempts. Populations with stronger stress responses also had stronger negative feedback, which supports a "mitigating" rather than a "magnifying" effect of negative feedback on stress responses. These results suggest that combining a robust stress response with strong negative feedback may be important for persisting in unpredictable or rapidly changing environments.

evolutionary biology↗

Plumage manipulation alters the integration of social behavior, physiology, internal microbiome, and fitness.

Signals often covary with physiological and behavioral traits to form an axis of integrated phenotypic variation associated with reproductive performance. This pattern of phenotypic integration could result from intrinsic between-individual differences that are causally related to signal production, physiology, and behavior. Alternatively, signal expression itself might generate dynamic feedback between physiology, behavior, and the experienced social environment, resulting in an integrated phenotype. Here, we manipulated the plumage of female tree swallows (Tachycineta bicolor) to decouple the expression of a social signal from any pre-existing behavioral or physiological differences. We collected a time series of physiological samples, monitored social interactions with a sensor network, and tracked reproductive performance. Relative to sham controls, dulled females experienced an altered social environment; overall, these females were visited more by conspecific females and less by males. Dulled females subsequently changed their own behavior by initiating fewer interactions and increasing nestling provisioning. These differences resulted in an altered internal microbiome and glucose levels and, ultimately, dulled females produced more offspring. Moreover, dulled females produced larger clutches than control females in the year after the manipulation. Thus, signal variation alone--independent from any pre-existing differences--had a sustained causal affect on a suite of integrated traits. This finding suggests that dynamic feedback may play an important role in coordinating an integrated signaling phenotype. Our results have implications for understanding how variation in signal expression arises and is maintained and the extent to which the information encoded in signals is contingent upon their use in a social environment.

zoology↗

Does variation in glucocorticoid regulation predict fitness? A phylogenetic meta-analysis.

Glucocorticoid hormones (GCs) are central mediators of metabolism and the response to challenges. Because circulating levels of GCs increase in response to challenges, within-population variation in GCs could reflect individual variation in condition or experience. At the same time, individual variation in the degree to which GCs increase in response to challenges (which is relatively consistent within individuals over time) could have causal effects on stress coping capacity, and the ability to survive and reproduce. Although a number of studies in vertebrates have tested whether within-population variation in GCs predicts components of fitness, it is not clear whether there are consistent patterns across taxa. Here we present the first phylogenetic meta-analysis testing whether within-population variation in GCs is associated with components of fitness across vertebrates. At the same time, we introduce and test predictions about an overlooked but potentially important mediator of GC-fitness relationships: life history context. We suggest that strong context-dependence in the fitness benefit of maintaining elevated GCs could obscure consistent patterns between GCs and fitness across taxa. Meta-analyses revealed that across vertebrates, baseline and stress-induced GCs were consistently negatively correlated with reproductive success. This relationship did not differ depending on life history context. In contrast, the relationships between GCs and survival were highly context dependent, differing according to life history strategy. Both baseline and stress-induced GCs were more strongly negatively associated with survival in longer-lived populations and species. Stress-induced GCs were also more negatively associated with survival in organisms that engage in relatively more valuable reproductive attempts. Fecal GCs did not predict survival or reproductive success. We also used a meta-analytic approach to test whether experimental increases in GCs had consistent causal effects on fitness. Experimental increases in GCs reduced both survival and reproductive success, although the latter relationship was not significant when accounting for phylogeny. Overall, these results support the prediction that GC-fitness relationships can be strongly context dependent, and suggest that incorporating life history may be particularly important for understanding GC-survival relationships. Future studies that explore the role of other aspects of context (e.g., the nature and frequency of stressors, environmental variation) within and across species could provide important insights how and when variation in GC regulation predicts fitness.

evolutionary biology↗