As the global climate changes, temperatures are rising, snow is melting earlier, and rainfall is becoming more variable, and these climatic changes may create an ecological mismatch. While prior work has shown how animals respond to these changes physiologically and behaviorally, few have specifically investigated antipredator behavior, an essential activity. In many species, there are direct fitness tradeoffs between allocating time and energy to antipredator vigilance and foraging. To discover how these tradeoffs are affected by climate change, we studied how temperature, snowmelt date, and rainfall affected the proportion of time yellow-bellied marmots (Marmota flaviventer) allocated to vigilance during bouts of foraging. While snowmelt and temperature did not explain variation in vigilance, rainfall did. Higher rainfall in the week prior to a focal observation was associated with higher vigilance, possibly reflecting more abundant food that affords the luxury of increasing antipredator vigilance while foraging. Such an effect might be consequential at the population level given the importance of foraging and antipredator behaviors for a highly time restrictive hibernating species. Further research is necessary to determine consequences at the population level and whether and how these findings extend to other species.

Society formation and maintenance in yellow-bellied marmots

ABSTRACTThe period before sexual maturity is a sensitive life stage where most development and change occur. Studies in humans and other animals show that early adverse experiences contribute to poor health and survival. However, the mechanisms are still unclear. Some have found that early life adversity (ELA) can lead to elevated glucocorticoids later in life, dysregulate the stress response, and increase the impact of later stressors. However, most animal studies have focused on individual stressors. Protecting wild populations that are exposed to multiple stressors requires a better understanding of the physiological consequences of several co‐occurring stressors. We used a cumulative adversity index (CAI) to ask whether early adverse experiences were associated with increased levels of adult fecal glucocorticoid metabolites (FGM) in wild female yellow‐bellied marmots (Marmota flaviventer). We found a significant interaction between adversity and elevation that explained variation in FGMs. Thus, we infer that ELA can modulate FGMs, but contrary to similar research in other mammals, the trend was toward downregulation under more environmentally relaxed conditions (lower elevation). Our results highlight the value of studying the relative importance of early and later stressors in the physiology of different wild taxa when investigating the mechanisms of early life adversity.

How phenotypes are shaped by multilevel selection-the theoretical framework proposing natural selection occurs at more than one level of biological organization-is a classic debate in biology. Though social behaviours are a common theoretical example for multilevel selection, it is unknown if and how multilevel selection acts on sociality in the wild. We studied the relative strength of multilevel selection on both individual behaviour and group social structure, quantified with social networks and 19 years of data from a wild, free-living mammal, the yellow-bellied marmot (Marmota flaviventer). Contextual analysis (exploring the impact of individual and group social phenotypes on individual fitness, relative to each other) revealed multilevel selection gradients in specific fitness and life history contexts, with selection for group social structure being just as strong, if not stronger, than individual social behaviour. We also found antagonistic multilevel selection gradients within and between levels, potentially explaining why increased sociality is not as beneficial or heritable in this system compared with other social taxa. Thus, the evolutionary dynamics of hierarchical or nested biological traits should be assessed at multiple levels simultaneously to tell a more accurate and comprehensive story. Overall, we provide empirical evidence suggesting that multilevel selection acts on social relationships and structures in the wild and provide direct evidence for a classic, unanswered question in biology.

One of the most explored factors mediating antipredator behavior is group size, which generally predicts individuals in larger social groups allocate less time to antipredator vigilance while foraging. However, group size alone does not capture the full complexity of sociality. An individual's 'sense of security', or their perceived risk of predation, is also influenced by an individual's social connections. Further, group social structure - the pattern of all social interactions in a group - could explain additional variation in perceptions of security for the individuals that reside in the group. Using the time allocated to vigilance during foraging and flight initiation distance (FID) to quantify individuals' social security, we explored whether individual yellow-bellied marmots (Marmota flaviventer) in tightly connected social groups looked less while foraging and had shorter FIDs. Using linear mixed effect models, we found modest support for the Social Security Hypothesis; individuals in more socially reciprocal groups may spend less time looking for predators while foraging. No measure of group social structure explained variation in FID. Measures of the immediate environment (the number of individuals within 10 m for vigilance and the distance from burrow and alert distance for FID) had effect sizes an order of magnitude greater than measures of social structure, suggesting an individual's immediate environment has more of an impact on their antipredator behavior than the structure of their social group.

The gut microbiome has a well-documented relationship with host fitness, physiology, and behavior. However, most of what is known comes from captive animals where diets and environments are more homogeneous or controlled. Studies in wild populations that experience dynamic environments and have natural life history variation are less common but are key to understanding the drivers of variation in the gut microbiome. Here we examine a wild population of yellow-bellied marmots (Marmota flaviventer), an obligate winter hibernator, to quantify multivariate associations between host-associated factors (e.g., age, sex, environmental harshness, and social behavior) and gut microbial composition. Across 5 years and 143 individuals, we found that males had a higher relative abundance of microbes associated with mass gain and cellulose digestion, which suggests a metabolic investment in mass gain (such as phylum Firmicutes and family Lachnospiraceae). By contrast, females had higher relative abundances of microbes associated with inflammation and metabolism (from microbial groups such as Tenericutes and Ruminococcus), possibly reflecting the importance of lactation and offspring investment. Post hoc analyses of lactating females showed a negative relationship with the abundance of microbes associated with mass gain but a positive relationship with microbes associated with metabolic energy, suggesting a trade-off between investment in pups and maternal mass gain. Older animals also had reduced Proteobacteria relative abundance, a phylum associated with reduced inflammation. Results demonstrate that sex and age-based traits, not sociality or environmental harshness, are associated with microbe-mediated metabolism and inflammation in a wild, hibernating mammal.

Emitting alarm calls may be costly, but few studies have asked whether calling increases a caller’s risk of predation and survival. Since observing animals calling and being killed is relatively rare, we capitalized on over 24,000 h of observations of marmot colonies and asked whether variation in the rate that yellow-bellied marmots (Marmota flaviventer) alarm called was associated with the probability of summer mortality, a proxy for predation. Using a generalized mixed model that controlled for factors that influenced the likelihood of survival, we found that marmots who called at higher rates were substantially more likely to die over the summer. Because virtually all summer mortality is due to predation, these results suggest that calling is indeed costly for marmots. Additionally, the results from a Cox survival analysis showed that marmots that called more lived significantly shorter lives. Prior studies have shown that marmots reduce the risk by emitting calls only when close to their burrows, but this newly quantified survival cost suggests a constraint on eliminating risks. Quantifying the cost of alarm calling using a similar approach in other systems will help us better understand its true costs, which is an essential value for theoretical models of calling and social behavior.

Climate change and its resulting effects on seasonality are known to alter a variety of animal behaviors including those related to foraging, phenology, and migration. Although many studies focus on the impacts of phenological changes on physiology or fitness enhancing behaviors, fewer have investigated the relationship between variation in weather and phenology on risk assessment. Fleeing from predators is an economic decision that incurs costs and benefits. As environmental conditions change, animals may face additional stressors that affect their decision to flee and influence their ability to effectively assess risk. Flight initiation distance (FID)—the distance at which animals move away from threats—is often used to study risk assessment. FID varies due to both internal and external biotic and physical factors as well as anthropogenic activities. We asked whether variation in weather and phenology is associated with risk-taking in a population of yellow-bellied marmots (Marmota flaviventer). As the air temperature increased marmots tolerated closer approaches, suggesting that they either perceived less risk or that their response to a threat was thermally compromised. The effect of temperature was relatively small and was largely dependent upon having a larger range in the full data set that permitted us to detect it. We found no effects of either the date that snow disappeared or July precipitation on marmot FID. As global temperatures continue to rise, rainfall varies more and drought becomes more common, understanding climate-related changes in how animals assess risk should be used to inform population viability models.

METHODS: Validating an immunoassay to measure fecal glucocorticoid metabolites in yellow-bellied marmots

Life history trade-offs are one of the central tenets of evolutionary demography. Trade-offs, depicting negative covariances between individuals' life history traits, can arise from genetic constraints, or from a finite amount of resources that each individual has to allocate in a zero-sum game between somatic and reproductive functions. While theory predicts that trade-offs are ubiquitous, empirical studies have often failed to detect such negative covariances in wild populations. One way to improve the detection of trade-offs is by accounting for the environmental context, as trade-off expression may depend on environmental conditions. However, current methodologies usually search for fixed covariances between traits, thereby ignoring their context dependence. Here, we present a hierarchical multivariate 'covariance reaction norm' model, adapted from Martin (2023), to help detect context dependence in the expression of life-history trade-offs using demographic data. The method allows continuous variation in the phenotypic correlation between traits. We validate the model on simulated data for both intraindividual and intergenerational trade-offs. We then apply it to empirical datasets of yellow-bellied marmots (Marmota flaviventer) and Soay sheep (Ovis aries) as a proof-of-concept showing that new insights can be gained by applying our methodology, such as detecting trade-offs only in specific environments. We discuss its potential for application to many of the existing long-term demographic datasets and how it could improve our understanding of trade-off expression in particular, and life history theory in general.

Protecting populations contending with co-occurring stressors requires a better understanding of how multiple early-life stressors affect the fitness of natural systems. However, the complexity of such research has limited its advancement and prevented us from answering new questions. In human studies, cumulative risk models predict adult health risk based on early adversity exposure. We apply a similar framework in wild yellow-bellied marmots (Marmota flaviventer). We tested cumulative adversity indices (CAIs) across different adversity types and time windows. All CAIs were associated with decreased pup survival and were well supported. Moderate and acute, but not standardized CAIs were associated with decreased lifespan, supporting the cumulative stress hypothesis and the endurance of early adversity. Multivariate models showed that differences in lifespan were driven by weaning date, precipitation, and maternal loss, but they performed poorly compared with CAI models. We highlight the development, utility, and insights of CAI approaches for ecology and conservation.

In group-living species, reproductive variation among individuals of the same sex is widespread. By identifying the mechanisms underlying this reproductive skew, we gain fundamental insights into the evolution and maintenance of sociality. A common mechanism, social control, is typically studied by quantifying dominance, which is one of many attributes of sociality that describes how individuals exert influence on others and is an incomprehensive measure of social control as it accounts only for direct relationships. Here, we use the global reaching centrality (GRC), which quantifies the degree of hierarchy in a social network by accounting for both direct and indirect social relationships. Using a wild, free-living population of adult female yellow-bellied marmots (Marmota flaviventris), we found a positive relationship between the reproductive skew index and GRC: more despotic social groups have higher reproductive skew. The GRC was stronger predictor for skew than traditional measures of social control (i.e. dominance). This allows deeper insights into the diverse ways individuals control other group members' reproduction, a core component in the evolution of sociality. Future studies of skew across taxa may profit by using more comprehensive, network-based measures of social control.

Across animal systems, abiotic environmental features, including timing of seasonal events and weather patterns, affect fitness. An individual’s degree of social integration also has fitness consequences, but we lack an understanding of how abiotic features relate to patterns of individual sociality. A deeper understanding of this relationship could be developed from studying systems where these two links with fitness have already been identified. We explored the relationship between individual social behavior and seasonal timing, seasonal length, and weather patterns. We used social network analysis on a sixteen-year dataset of a wild population of hibernating yellow-bellied marmots (Marmota flaviventer). We fit a series of generalized linear mixed models and found that longer growing seasons before winter hibernation and longer winters were associated with increased individual sociality in the following spring. However, later snowmelt was associated with decreased sociality that spring. We found no relationship between individual sociality and various measures of precipitation and temperature. This suggests that seasonal timing and length may be a more important driver of sociality than weather patterns in this system, both as a lag and contemporary effect. Seasonal timing and length may mediate the opportunity or intensity of social interactions. The entwined relationships between the seasonal schedule and weather, and the seemingly contradictory role of winter length and snowmelt, suggests the timing of seasons and its relationship with sociality is complex and further exploration of environment-sociality relationships is required across taxa.Significance statementWhile the adaptive benefits of social behavior are well studied, less is known about how features of the abiotic environment drive variation in individual social behavior. Given increasing stochasticity in the timing of seasonal events and weather patterns, mapping the environment-sociality relationship will provide important insights to the drivers of sociality in the wild. This is particularly salient for species most vulnerable to climate and environmental change, such as seasonal hibernators, like yellow-bellied marmots (Marmota flaviventer). We found that features of seasonal duration were positively associated with increased sociality, whereas the timing of seasonal onset was negatively associated. This work provides empirical evidence towards an important gap in the behavioral ecology literature.

Dispersal is an important individual decision which may influence individual fitness as well as population viability. The social cohesion hypothesis posits more social individuals remain at home, which is supported by prior work across taxa. However, how the sociality and connectivity of the group an individual resides in-their group social structure-relates to dispersal decisions has not been explored. We extend the social cohesion hypothesis to predict individuals residing in more social groups would remain at home, and we quantified the affiliative and agonistic social network structure of female yellow-bellied marmots (Marmota flaviventer), a facultatively social ground-dwelling squirrel, where about half of all females disperse. Using mixed-effects models, we found no support for the hypothesis that affiliative group structure explained any variation in a marmot's decision to disperse. We did find marmots in groups with less agonistic centralization (around one or few individuals) were less likely to disperse. The former finding may result from limited ability to perceive group structure whereas the latter may reflect individuals in less agonistically centralized groups are less likely to be reproductively suppressed. These results suggest individual dispersal decisions are more impacted by individual sociality and not that of their social group. Thus, the social cohesion hypothesis may not scale to the level of the group. Further work is required to determine whether dispersal decisions in obligately social species are influenced by group social structure.

Abstract Obtaining body condition is an important life history challenge that directly impacts individual fitness and is particularly important for hibernating animals, whose maintenance of adequate body fat and mass is essential for survival. It is well-documented that host-associated microorganisms play a vital role in animal physiology and behavior. Recent work demonstrates that gut microbes are associated with fat accumulation and obesity, particularly the phyla Firmicutes and Bacteroidetes. The focus of most microbiome studies has been on human health or involved lab-reared animals used as a model system. However, these microbes likely are important for individual fitness in wild populations and provide potential mechanistic insights into the adaptability and survival of wildlife. Here we tested whether symbiotic microorganisms within the phyla of Firmicutes and Bacteroidetes were associated with summer mass gain in an exceptionally well-studied wild population of yellow-bellied marmots (Marmota flaviventer) by analyzing 207 fecal samples collected over 5 summer active seasons. Results showed that marmots with higher mass gain rates had a greater relative abundance of Firmicutes. In contrast, a higher relative abundance of Bacteroidetes was associated with lower mass gain rates, but only for marmots living in harsher environments. Similar patterns were found at the family level where Ruminococcaceae, a member of Firmicutes, was associated with higher mass gain rates, and Muribaculaceae, a member of Bacteroidetes, was associated with lower mass gain rates in harsher environments. Although correlative, these results highlight the potential importance of symbiotic gut microbiota to mass gain in the wild—a trait associated with survival and fitness in many taxonomic groups.

With global climates changing rapidly, animals must adapt to new environmental conditions with altered weather and phenology. The key to adapting to these new conditions is adjusting the timing of reproduction to maximize fitness. Using a long-term dataset on a wild population of yellow-bellied marmots (Marmota flaviventer) at the Rocky Mountain Biological Laboratory (RMBL), we investigated how the timing of reproduction changed with changing spring conditions over the past 50 years. Marmots are hibernators with a 4-month active season. It is thus crucial to reproduce early enough in the season to have time to prepare for hibernation, but not too early, as snow cover prevents access to food. Importantly, climate change in this area has, on average, increased spring temperatures by 5°C and decreased spring snowpack by 50 cm over the past 50 years. We evaluated how female marmots adjust the timing of their reproduction in response to changing conditions and estimated the importance of both microevolution and plasticity in the variation in this timing. We showed that, within a year, the timing of reproduction is not as tightly linked to the date a female emerges from hibernation as previously thought. We reported a positive effect of spring snowpack but not of spring temperature on the timing of reproduction. We found inter-individual variation in the timing of reproduction, including low heritability, but not in its response to changing spring conditions. There was directional selection for earlier reproduction since it increased the number and proportion of pups surviving their first winter. Taken together, the timing of marmot reproduction might evolve via natural selection; however, plastic changes will also be extremely important. Further, future studies on marmots should not operate under the assumption that females reproduce immediately following their emergence.

The gut microbiome has a well-documented relationship with host fitness. Greater microbial diversity and abundance of specific microbes have been associated with improved fitness outcomes. Intestinal microbes also may be associated with patterns of social behaviour. However, these associations have been largely studied in captive animal models; we know less about microbiome composition as a potential driver of individual social behaviour and position in the wild. We used linear mixed models to quantify the relationship between fecal microbial composition, diversity and social network traits in a wild population of yellow-bellied marmots (Marmota flaviventer). We focused our analyses on microbes previously linked to sociability and neurobehavioural alterations in captive rodents, primates and humans. Using 5 years of data, we found microbial diversity (Shannon–Wiener and Faith's phylogenetic diversity) has a modest yet statistically significant negative relationship with the number of social interactions an individual engaged in. We also found a negative relationship between Streptococcus spp. relative abundance and two social network measures (clustering coefficient and embeddedness) that quantify an individual's position relative to others in their social group. These findings highlight a potentially consequential relationship between microbial composition and social behaviour in a wild social mammal.

Is flight initiation distance associated with longer-term survival in yellow-bellied marmots, Marmota flaviventer?

The (surprising) importance of males in a matrilineal society: behavioural insights from a topological knockout study

Species with different ecological niches will likely exhibit distinct responses to a changing environment. Differences in the magnitude of niche specialization may also indicate which species may be more vulnerable to environmental change, as many life‐history characteristics are known to affect climate change vulnerability. We characterized the niche space of three sympatric high‐elevation ground‐dwelling squirrels, yellow‐bellied marmot (Marmota flaviventer), Belding's ground squirrel (Urocitellus beldingi), and golden‐mantled ground squirrel (Callospermophilus lateralis), in the alpine and upper subalpine regions of the Sierra Nevada in California. We used 5879 observations of individual squirrels, collected from 4 years (2009–2012) of transect survey data, to quantify which ecogeographical variable types (climate, topography, or landcover) were most important in defining the niche of each species. We conducted Ecological Niche Factor Analysis to quantify the niche and generate indices of “marginality” (magnitude of selection) and “specialization” (narrowness of niche space). All three species demonstrated differential use of niche space when compared to the available niche space. Moreover, the relative importance of the variables shaping the niche differed among these species. For example, the presence of meadows was important in defining the niche for U. beldingi and M. flaviventer, but the presence of conifers was important to C. lateralis. Precipitation was important in defining the niche for all three species, positively so for U. beldingi, and negatively for the other two species. The niche breadth of these three species was also positively associated with geographic range size. Mammals in high‐elevation mountain systems often are perceived as vulnerable to climate shifts, but our results underscore the importance of also including non‐climate‐based factors in defining the niche. The overall magnitude of niche selection for all three species was driven by a combination of topographic, climatic, and landcover factors; thus, efforts to forecast areas where these species can persist in the future need to evaluate from more than just a climatic perspective.