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  1. Abstract

    The gut microbiome impacts host health and fitness, in part through the diversification of gut metabolic function and pathogen protection. Elevations in glucocorticoids (GCs) appear to reduce gut microbiome diversity in experimental studies, suggesting that a loss of microbial diversity may be a negative consequence of increased GCs. However, given that ecological factors like food availability and population density may independently influence both GCs and microbial diversity, understanding how these factors structure the GC-microbiome relationship is crucial to interpreting its significance in wild populations. Here, we used an ecological framework to investigate the relationship between GCs and gut microbiome diversity in wild North American red squirrels (Tamiasciurus hudsonicus). As expected, higher GCs predicted lower gut microbiome diversity and an increase in metabolic taxa. Surprisingly, but in line with prior empirical studies on wild animals, gastrointestinal pathogens decreased as GCs increased. Both dietary heterogeneity and an upcoming food pulse exhibited direct effects on gut microbiome diversity, whereas conspecific density and reproductive activity impacted diversity indirectly via changes in host GCs. Our results provide evidence of a gut–brain axis in wild red squirrels and highlight the importance of situating the GC-gut microbiome relationship within an ecological framework.

     
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  2. Abstract

    Long‐term studies of wild animals provide the opportunity to investigate how phenotypic plasticity is used to cope with environmental fluctuations and how the relationships between phenotypes and fitness can be dependent upon the ecological context.

    Many previous studies have only investigated life‐history plasticity in response to changes in temperature, yet wild animals often experience multiple environmental fluctuations simultaneously. This requires field experiments to decouple which ecological factor induces plasticity in fitness‐relevant traits to better understand their population‐level responses to those environmental fluctuations.

    For the past 32 years, we have conducted a long‐term integrative study of individually marked North American red squirrelsTamiasciurus hudsonicusErxleben in the Yukon, Canada. We have used multi‐year field experiments to examine the physiological and life‐history responses of individual red squirrels to fluctuations in food abundance and conspecific density.

    Our long‐term observational study and field experiments show that squirrels can anticipate increases in food availability and density, thereby decoupling the usual pattern where animals respond to, rather than anticipate, an ecological change.

    As in many other study systems, ecological factors that can induce plasticity (such as food and density) covary. However, our field experiments that manipulate food availability and social cues of density (frequency of territorial vocalizations) indicate that increases in social (acoustic) cues of density in the absence of additional food can induce similar life‐history plasticity, as does experimental food supplementation.

    Changes in the levels of metabolic hormones (glucocorticoids) in response to variation in food and density are one mechanism that seems to induce this adaptive life‐history plasticity.

    Although we have not yet investigated the energetic response of squirrels to elevated density or its association with life‐history plasticity, energetics research in red squirrels has overturned several standard pillars of knowledge in physiological ecology.

    We show how a tractable model species combined with integrative studies can reveal how animals cope with resource fluctuations through life‐history plasticity.

     
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  3. In fluctuating environments, phenotypic mismatching may reflect an error-avoidance bias that enhances a mother squirrel’s overall lifetime fitness. 
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  4. While cooperative interactions among kin are a key building block in the societies of group-living species, their importance for species with more variable social environments is unclear. North American red squirrels ( Tamiasciurus hudsonicus ) defend individual territories in dynamic neighbourhoods and are known to benefit from living among familiar conspecifics, but not relatives. However, kin-directed behaviours may be restricted to specific genealogical relationships or strongly mediated by geographical distance, masking their influence at broader scales. Using distance between territories as a proxy for the ability of individuals to interact, we estimated the influence of primary kin (parents, offspring, siblings) on the annual survival and reproductive success of red squirrels. This approach revealed associations between fitness and access to kin, but only for certain genealogical relationships and fitness components. For example, females had enhanced annual survival when living closer to their daughters, though the reverse was not true. Most surprising was the finding that males had higher annual reproductive success when living closer to their father, suggesting possible recognition and cooperation among fathers and sons. Together, these findings point to unexpected nuance in the fitness consequences of kinship dynamics for a species that is territorial and largely solitary. 
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