Marmots Marmota Research Articles

Beneficial effects of group size on oxidative balance in a wild cooperative breeder

Social factors have important effects on individuals’ fitness, yet the proximate mechanisms remain virtually unknown. Oxidative stress, which results from the imbalance between the systemic effect of reactive oxygen species on molecules and an organism’s capacity to restore oxidative balance, is one potential mechanism mediating such effects. Although individuals’ oxidative balance seems to be affected by their social status, the effects of social environment, and particularly group size and composition, on oxidative balance have seldom been determined in wild populations. Here, we investigated the influence of group size and composition on the oxida- tive balance of wild dominant Alpine marmots (Marmota marmota). We simultaneously measured an index of circulating oxidative damage to lipids (thiobarbituric acid reactive substances) and specific activity of the main enzymatic antioxidant defense (superoxide dismutase). Our results showed a marked decrease in both oxidative damage and antioxidant activity in individuals from larger groups, highlighting a beneficial effect of group size on individuals’ oxidative balance. We discussed the possibility that these physiological benefits originate from social thermoregulation alleviating the cost of hibernation. This study extends our understanding of the proxi- mate factors underpinning the evolution of sociality and opens up novel perspectives within the field of evolutionary ecology.

Mate choice for neutral and MHC genetic characteristics in Alpine marmots: different targets in different contexts?

Sexual selection through female mate choice for genetic characteristics has been suggested to be an important evolutionary force maintaining genetic variation in animal populations. However, the genetic targets of female mate choice are not clearly identified and whether female mate choice is based on neutral genetic characteristics or on particular functional loci remains an open question. Here, we investigated the genetic targets of female mate choice in Alpine marmots (Marmota marmota), a socially monogamous mammal where extra‐pair paternity (EPP) occurs. We used 16 microsatellites to describe neutral genetic characteristics and two MHC loci belonging to MHC class I and II as functional genetic characteristics. Our results reveal that (1) neutral and MHC genetic characteristics convey different information in this species, (2) social pairs show a higher MHC class II dissimilarity than expected under random mate choice, and (3) the occurrence of EPP increases when social pairs present a high neutral genetic similarity or dissimilarity but also when they present low MHC class II dissimilarity. Thus, female mate choice is based on both neutral and MHC genetic characteristics, and the genetic characteristics targeted seem to be context dependent (i.e., the genes involved in social mate choice and genetic mate choice differ). We emphasize the need for empirical studies of mate choice in the wild using both neutral and MHC genetic characteristics because whether neutral and functional genetic characteristics convey similar information is not universal.

Differential plasticity of size and mass to environmental change in a hibernating mammal.

Morphological changes following changes in species' distribution and phenology have been suggested to be the third universal response to global environmental change. Although structural size and body mass result from different genetic, physiological, and ecological mechanisms, they are used interchangeably in studies evaluating population responses to environmental change. Using a 22-year (1991-2013) dataset including 1768 individuals, we investigated the coupled dynamics of size and mass in a hibernating mammal, the Alpine marmot (Marmota marmota), in response to local environmental conditions. We (i) quantified temporal trends in both traits, (ii) determined the environmental drivers of trait dynamics, and (iii) identified the life-history processes underlying the observed changes. Both phenotypic traits were followed through life: we focused on the initial trait value (juvenile size and mass) and later-life development (annual change in size [Δsize] and mass [Δmass]). First, we demonstrated contrasting dynamics between size and mass over the study period. Juvenile size and subsequent Δsize showed significant declines, whereas juvenile mass and subsequent Δmass remained constant. As a consequence of smaller size associated with a similar mass, individuals were in better condition in recent years. Second, size and mass showed different sensitivities to environmental variables. Both traits benefited from early access to resources in spring, whereas Δmass, particularly in early life, also responded to summer and winter conditions. Third, the interannual variation in both traits was caused by changes in early life development. Our study supports the importance of considering the differences between size and mass responses to the environment when evaluating the mechanisms underlying population dynamics. The current practice of focusing on only one trait in population modeling can lead to misleading conclusions when evaluating species' resilience to contemporary climate change.

Multiple geographic origins and high genetic differentiation of the Alpine marmots reintroduced in the Pyrenees

Reintroductions inherently involve a small number of founders leading reintroduced populations to be prone to genetic drift and, consequently, to inbreeding depression. Assessing the origins as the genetic diversity and structure of reintroduced populations compared to native populations are thus crucial to foresee their future. Here, we aim to clarify the origins of the Alpine marmots reintroduced in the Pyrenees and to evaluate the genetic consequences of this reintroduction after almost 30 years without monitoring. We search for the origins and compare the genetic structure and the genetic variability of three reintroduced Pyrenean and eight native Alpine populations using pairwise genetic distances, Bayesian clustering method and multivariate analyses. Our results reveal that the Alpine marmots reintroduced in the Pyrenees originated both from the Northern and the Southern Alps, and that, despite these multiple origins, none of the current Pyrenean marmots are admixed. The reintroduction led to a strong genetic differentiation and to a decrease in genetic diversity. This pattern likely results from the small number of founders and the low dispersal capacities of Alpine marmots and thus, highlight the necessity to consider both genetic characteristics and natural history when reintroducing a species.

Socially mediated effects of climate change decrease survival of hibernating Alpine marmots.

In the context of global change, an increasing challenge is to understand the interaction between weather variables and life histories. Species-specific life histories should condition the way climate influences population dynamics, particularly those that are associated with environmental constraints, such as lifestyles like hibernation and sociality. However, the influence of lifestyle in the response of organisms to climate change remains poorly understood. Based on a 23-year longitudinal study on Alpine marmots, we investigated how their lifestyle, characterized by a long hibernation and a high degree of sociality, interacts with the ongoing climate change to shape temporal variation in age-specific survival. As generally reported in other hibernating species, we expected survival of Alpine marmots to be affected by the continuous lengthening of the growing season of plants more than by changes in winter conditions. We found, however, that Alpine marmots displayed lower juvenile survival over time. Colder winters associated with a thinner snow layer lowered juvenile survival, which in turn was associated with a decrease in the relative number of helpers in groups the following years, and therefore lowered the chances of over-winter survival of juveniles born in the most recent years. Our results provide evidence that constraints on life-history traits associated with hibernation and sociality caused juvenile survival to decrease over time, which might prevent Alpine marmots coping successfully with climate change.

Age-specific survival in the socially monogamous alpine marmot (Marmota marmota): evidence of senescence

We investigated age-specific variation in survival of dominant individuals in a long-lived and monogamous mammal, the alpine marmot ( Marmota marmota ), from a large dataset collected during a 24-year intensive monitoring of a free-ranging population. We found evidence of actuarial senescence in dominant individuals for both sexes. Survivorship was constant with age until dominant marmots were between 6 and 8 years of age and declined markedly thereafter. No between sex differences occurred in the intensity of actuarial senescence, which might be related to the weak intensity of sexual selection in this socially monogamous mammal. More investigations are needed to know whether cooperative breeding, hibernation, and monogamy, which are key features of the alpine marmot life history, could have shaped the patterns of actuarial senescence we report.

Factors influencing the discovery and use of wildlife passages for small fauna

Summary While many studies have looked at how large mammals respond to road mitigation measures, few have examined the effects on smaller mammals. We investigated the effectiveness of three different types of wildlife passages along Highway 175 in Quebec, Canada, for small‐ and medium‐sized mammals (<30 kg) using infrared cameras. Wildlife passages (n = 17) were monitored 24 h a day 7 days a week from 2012 to 2015. Two research questions were addressed: (i) What influences passage discovery and use? and (ii) does it differ between species? Global and species‐specific models were produced for both discovery and use. A linear mixed‐effects model was used for the discovery data (log‐transformed counts), and a generalized linear mixed model was used for the crossing data (binary response). Species' responded to the passages differently, with discoveries increasing overall and in particular for marmots Marmota monax as latitude increased. Pipe culverts were significantly more likely to be discovered by micromammals and wooden ledge culverts by red squirrels Tamiasciurus hudsonicus. Older passages were discovered less in general, with the exception of marmots. Marmots were also the only species to show a difference in crossings by passage type, favouring pipe culverts. Passage use was less likely with a median present for all models, except squirrels. More open passages had higher use overall and particularly for marmots and weasels Mustela spp. Synthesis and applications. By separating animal responses to wildlife passages into two types (discovery and use), we have shown it is possible to incorporate multiple dimensions into post‐mitigation evaluation. This study highlights how transportation agencies can engineer more effective wildlife passages by minimizing the barrier effect of the structures themselves and constructing more passages better suited to the needs of the species they are targeting. To benefit the most species, it is recommended that future projects contain a diversity of open, single segment passages requiring long‐term monitoring.

Insights into the evolution of pathogenicity of Escherichia coli from genomic analysis of intestinal E. coli of Marmota himalayana in Qinghai–Tibet plateau of China

Escherichia coli is both of a widespread harmless gut commensal and a versatile pathogen of humans. Domestic animals are a well-known reservoir for pathogenic E. coli. However, studies of E. coli populations from wild animals that have been separated from human activities had been very limited. Here we obtained 580 isolates from intestinal contents of 116 wild Marmot Marmota himalayana from Qinghai–Tibet plateau, China, with five isolates per animal. We selected 125 (hereinafter referred to as strains) from the 580 isolates for genome sequencing, based on unique pulse field gel electrophoresis patterns and at least one isolate per animal. Whole genome sequence analysis revealed that all 125 strains carried at least one and the majority (79.2%) carried multiple virulence genes based on the analysis of 22 selected virulence genes. In particular, the majority of the strains carried virulence genes from different pathovars as potential 'hybrid pathogens'. The alleles of eight virulence genes from the Marmot E. coli were found to have diverged earlier than all known alleles from human and other animal E. coli. Phylogenetic analysis of the 125 Marmot E. coli genomes and 355 genomes selected from 1622 human and other E. coli strains identified two new phylogroups, G and H, both of which diverged earlier than the other phylogroups. Eight of the 12 well-known pathogenic E. coli lineages were found to share a most recent common ancestor with one or more Marmot E. coli strains. Our results suggested that the intestinal E. coli of the Marmots contained a diverse virulence gene pool and is potentially pathogenic to humans. These findings provided a new understanding of the evolutionary origin of pathogenic E. coli.Emerging Microbes & Infections (2016) 5, e122; doi:10.1038/emi.2016.122; published online 7 December 2016

Sex-specific determinants of fitness in a social mammal.

Sociality should evolve when the fitness benefits of group living outweigh the costs. Theoretical models predict an optimal group size maximizing individual fitness. However, beyond the number of individuals present in a group, the characteristics of these individuals, like their sex, are likely to affect the fitness payoffs of group living. Using 20 years of individually based data on a social mammal, the Alpine marmot (Marmota marmota), we tested for the occurrence of an optimal group size and composition, and for sex-specific effects of group characteristics on fitness. Based on lifetime data of 52 males and 39 females, our findings support the existence of an optimal group size maximizing male fitness and an optimal group composition maximizing fitness of males and females. Additionally, although group characteristics (i.e., size, composition and instability) affecting male and female fitness differed, fitness depended strongly on the number of same-sex subordinates within the social group in the two sexes. By comparing multiple measures of social group characteristics and of fitness in both sexes, we highlighted the sex-specific determinants of fitness in the two sexes and revealed the crucial role of intrasexual competition in shaping social group composition.

Early and adult social environments have independent effects on individual fitness in a social vertebrate.

Evidence that the social environment at critical stages of life-history shapes individual trajectories is accumulating. Previous studies have identified either current or delayed effects of social environments on fitness components, but no study has yet analysed fitness consequences of social environments at different life stages simultaneously. To fill the gap, we use an extensive dataset collected during a 24-year intensive monitoring of a population of Alpine marmots (Marmota marmota), a long-lived social rodent. We test whether the number of helpers in early life and over the dominance tenure length has an impact on litter size at weaning, juvenile survival, longevity and lifetime reproductive success (LRS) of dominant females. Dominant females, who were born into a group containing many helpers and experiencing a high number of accumulated helpers over dominance tenure length showed an increased LRS through an increased longevity. We provide evidence that in a wild vertebrate, both early and adult social environments influence individual fitness, acting additionally and independently. These findings demonstrate that helpers have both short- and long-term effects on dominant female Alpine marmots and that the social environment at the time of birth can play a key role in shaping individual fitness in social vertebrates.

Litter sex composition influences dominance status of Alpine marmots (Marmota marmota).

In social species, the hierarchical status of an individual has important consequences for its fitness. While many studies have focused on individual condition to explain access to dominance, very few have investigated the influence of the social environment, especially during early life. Yet it is known that environmental conditions early in life may influence several traits at adulthood. Here, we examine the influence of early social environment on accession to dominance by investigating the influence of litter size and sex composition on survival and the probability of ascending to dominance later in life using a 20-year dataset from a wild population of Alpine marmots (Marmota marmota). Although litter size had no effect on the fate of individuals, litter sex composition affected male juvenile survival and both male and female probabilities of reaching dominant status when adult. Male juveniles incur lower survival when the number of male juveniles in the litter increases, and individuals of both sexes from male-biased litters are more likely to become dominant than individuals from female-biased litters. However, the absolute number of sisters in the litter, rather than the sex ratio, seems to be an important predictor of the probability of acquiring dominant status: pups having more sisters are less likely to become dominant. Several potential mechanisms to explain these results are discussed.

Large-scale genotyping of highly polymorphic loci by next-generation sequencing: how to overcome the challenges to reliably genotype individuals?

Studying the different roles of adaptive genes is still a challenge in evolutionary ecology and requires reliable genotyping of large numbers of individuals. Next-generation sequencing (NGS) techniques enable such large-scale sequencing, but stringent data processing is required. Here, we develop an easy to use methodology to process amplicon-based NGS data and we apply this methodology to reliably genotype four major histocompatibility complex (MHC) loci belonging to MHC class I and II of Alpine marmots (Marmota marmota). Our post-processing methodology allowed us to increase the number of retained reads. The quality of genotype assignment was further assessed using three independent validation procedures. A total of 3069 high-quality MHC genotypes were obtained at four MHC loci for 863 Alpine marmots with a genotype assignment error rate estimated as 0.21%. The proposed methodology could be applied to any genetic system and any organism, except when extensive copy-number variation occurs (that is, genes with a variable number of copies in the genotype of an individual). Our results highlight the potential of amplicon-based NGS techniques combined with adequate post-processing to obtain the large-scale highly reliable genotypes needed to understand the evolution of highly polymorphic functional genes.

Microhabitat Utilization of the Tatra Marmot (Marmota marmota latirostris) in the Western Carpathian Mountains, Europe

The function of Alpine marmot subspecies burrows and factors influencing their distribution were investigated at 17 sites in the Tatra Mountains in Slovakia, Europe. Topographic variables and habitat types expected to influence the location of the Tatra marmot burrows were observed and examined. In the various locations of the studied home ranges (summer, winter and grazing areas, marmot trails) and outside the family territories, we recorded 36 vegetation samples including several reliefs. The collected data were analyzed using multivariate analysis.The summer areas of the marmot home ranges in the Tatra Mountains are often located within the alpine zone in communities of the Braun-Blanquet alliance Juncion trifidi (siliceous short stem grasslands) and in chionophilous communities on stable scree slopes of the alliance Festucion picturatae (tall stem grasslands). Marmots usually avoid habitats that have the lowest trophic benefits and the most extreme sites with low-stems or mat-grass communities in the alliance Nardion strictae, dense stands of dwarf pine in the alliance Pinion mugo (krummholz), and dwarf-shrub and lichen communities in the alliance Loiseleurio-Vaccinion. Marmot habitats in summer have suitable grazing areas. The most preferred habitats for foraging are grasslands and tall herb plant communities dominated by Calamagrostis villosa, Trisetum fuscum, and similar tall grass species.The most important factor influencing the locations of different parts of home ranges is the gradient of the relief structure. According to their functional differentiation, the location of a marmot burrow is most significantly influenced by the presence of convex geomorphic features and reinforced rock forms.

Helpers influence on territory use and maintenance in Alpine marmot groups

In social mammals, territory size and shape vary according to the number and strength of neighbour individuals competing for resources. Two main theories have been proposed to explain this variability: the Group Augmentation (GA) and the realized Resource Holding Potential (rRHP) hypotheses. The first states that the outcome of the interactions among groups depends on the total number of individuals in the group while the second states that only the number of animals directly involved in intergroup competition determines this outcome. We collected data on space use of individually tagged Alpine marmots (Marmota marmota), a cooperative breeding species that overlaps part of its territory with neighbouring groups. In accordance with the rRHP hypothesis, we found that groups having higher proportion of helpers, rather than higher total number of individuals, had lower percentage of the territory overlapping with neighbouring groups and a larger area available for individual exclusive use.

Plague Persistence in Western Europe: A Hypothesis

Historical sources documenting recurrent plagues of the “Second Pandemic” usually focus on urban epidemic mortality. Instead, plague persists in remote, rural hinterlands: areas less visible in the written sources of late medieval Europe. Plague spreads as fleas move from relatively resistant rodents, which serve as “maintenance hosts,” to an array of more susceptible rural mammals, now called “amplifying hosts.” Using sources relevant to plague in thinly populated Central and Western Alpine regions, this paper postulates that Alpine Europe could have been a region of plague persistence via its population of wild rodents, particularly the Alpine marmot.

How do animals optimize the size–number trade‐off when aging? Insights from reproductive senescence patterns in marmots

We investigated the influence of female age on five reproductive traits and on the offspring size-number trade-off from an extensive data set spanning 20 years of study on free-ranging Alpine marmots. Offspring mass increased with female age, whereas litter size and reproductive allocation remained constant in females up to 10 years of age and declined thereafter. Although reproductive allocation declined, post-weaning juvenile survival and the size-number trade-off did not change markedly throughout a female's lifetime. Senescence of annual reproductive success (i.e., the number of offspring surviving their first hibernation within a given litter) only resulted from senescence of litter size. The data were insufficient to determine whether the decrease in litter size with age was caused by declining litter size at birth, offspring pre-weaning survival, or both. Regardless, our findings demonstrate that marmot females display a size-number trade-off invariant with age, and that their reproductive tactic involves increasing offspring size at the cost of decreasing litter size with increasing age. As a result, reproductive performance remains constant throughout a female's lifetime, despite the deleterious effects of senescence in litter size.

Изменения структуры семейных участков сурка (Marmota bobak) в условиях резерватных сукцессий

Изменения структуры семейных участков сурка (Marmota bobak) в условиях резерватных сукцессий

Credal model averaging for classification: representing prior ignorance and expert opinions

Bayesian model averaging (BMA) is the state of the art approach for overcoming model uncertainty. Yet, especially on small data sets, the results yielded by BMA might be sensitive to the prior over the models. Credal model averaging (CMA) addresses this problem by substituting the single prior over the models by a set of priors (credal set). Such approach solves the problem of how to choose the prior over the models and automates sensitivity analysis. We discuss various CMA algorithms for building an ensemble of logistic regressors characterized by different sets of covariates. We show how CMA can be appropriately tuned to the case in which one is prior-ignorant and to the case in which instead domain knowledge is available. CMA detects prior-dependent instances, namely instances in which a different class is more probable depending on the prior over the models. On such instances CMA suspends the judgment, returning multiple classes. We thoroughly compare different BMA and CMA variants on a real case study, predicting presence of Alpine marmot burrows in an Alpine valley. We find that BMA is almost a random guesser on the instances recognized as prior-dependent by CMA.

Ecological aspects of the origin of Yersinia pestis, causative agent of the plague: Concept of intermediate environment

Modern phylogenies of Yersinia pestis (Logh.), causative agent of the plague, constructed using molecular-genetic methods, do not receive a satisfactory functional and adaptive interpretation and are far from being ecologically valid. We have presented an ecological scenario of the origin of the causative agent of the plague through the transition of the initial pseudotuberculosis microbe Yersinia pseudotuberculosis O:1b to a free hostal ecological niche (and a new adaptive zone) under ultracontinental climatic conditions of the Late Pleistocene (Sartan time, 22000–15000 years ago) in southern Siberia and Central Asia. An intermediate environment, i.e., the “Mongolian marmot Marmota sibirica-flea Oropsylla silatiewi” parasitic system, where the process of adaptation development of the plague microbe took place, has been characterized. A scenario based on the major principles of the modern synthetic theory of evolution opens the way to an ecological-genetic synthesis of the problem of plague origin and is an appropriate model for developing a theory of molecular evolution of pathogenic (plaguelike) microorganisms.

The effect of anthelmintic treatment on coccidia oocyst shedding in a wild mammal host with intermittent cestode infection.

While hosts are routinely exploited by a community of parasite species, the principles governing host responses towards parasites are unclear. Identifying the health outcomes of coinfections involving helminth macroparasites and microparasites is one area of importance for public and domestic animal health. For instance, it is controversial how deworming programmes affect incidence and severity of such important microparasite diseases as malaria. One problem is that most study systems involve domestic and laboratory animals with conditions hardly comparable to those of free-living animals. Here, we study the effect of anthelmintic treatment on coccidia infection intensity in wild Alpine marmots, M. marmota. Our results lend support to the hypothesis that helminth infection has a positive effect on concurrent microparasite infection. However, our work also points to the fact that within-host interactions between helminths and microparasites are context-dependent and can turn to negative ones once helminth burdens increase. Our study suggests that coccidia benefit from intermittent helminth infection in marmots due to the protective effects of helminth infection only during the early phase of the host's active season. Also, the marmot's response towards coccidia infection appears optimal only under no helminth infection when the host immune response towards coccidia would not be compromised, thereby pointing to the importance of regular intestinal helminth elimination by marmots just before hibernation.