Social control is associated with increased reproductive skew in a wild mammal.

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.

Comparison of hematologic and serum biochemical variables in Brucella-infected and Brucella-free adult Himalayan marmots (Marmota himalayana).

BACKGROUND: The Himalayan marmot (Marmota himalayana) plays a reservoir role in the epidemiology of brucellosis. However, the changes in blood biochemical parameters are still unclear in Brucella-seropositive marmots. OBJECTIVES: The present study was designed to explore the hematologic and biochemical variable changes in Brucella-seropositive marmots. METHODS: Blood samples were collected from the dorsalis pedis vein of Himalayan marmots (24 Brucella-seropositive marmots and 24 Brucella-free marmots). Ten hematologic and 10 serum biochemical variable examinations were performed and analyzed. RESULTS: Our results showed that leukocyte, platelet, neutrophil, and lymphocyte counts significantly increased, while the level of carbon dioxide combining power decreased in Brucella-infected marmots. These findings indicate that Brucella triggers an immune response in Himalayan marmots. CONCLUSIONS: This study provides a preliminary investigation of the changes in blood biochemical analytes in Brucella-infected marmots. The interaction between Brucella infection and blood biochemical indices in Himalayan marmots should be further explored.

Energy expenditure and body composition in a hibernator, the alpine marmot.

Visceral organs and tissues of 89 free-living alpine marmots (Marmota marmota) shot during a population control program in Switzerland, were collected. Between emergence from hibernation in April to July, the gastrointestinal tract (stomach to colon) gained 51% of mass and the liver mass increased by 24%. At the same time, the basal metabolic rate (BMR), determined with a portable oxygen analyzer, increased by 18%. The organ masses of the digestive system (stomach, small intestine, caecum, large intestine) were all significantly correlated with BMR. Interestingly, the mass of abdominal white adipose tissue (WAT) and of the remaining carcass (mainly skin and bones) were also significantly correlated with BMR. These results indicate that the gastrointestinal tract and organs involved in digestive function are metabolically expensive. They also show that it is costly to maintain even tissues with low metabolic rate such as WAT, especially if they are large. Heart and kidneys and especially brain and lungs did not explain a large proportion of the variance in BMR. Marmots increased the uptake of fat prior to hibernation, both by selective feeding and enhanced gastrointestinal capacity. Large fat reserves enable marmots to hibernate without food intake and to reproduce in spring, but at the cost of an elevated BMR. We predict that climate changes that disturb energy accumulation in summer, increase energy expenditure in winter, or delay the emergence from hibernation in spring, such as the occurrence of storms with increasing frequency, will increase mortality in alpine marmots.

Retrospective analysis of hibernation parameters and breeding success in captive Vancouver Island marmots (Marmota vancouverensis): 1997-2018.

Vancouver Island marmots (Marmota vancouverensis) have been managed in a captive-breeding program since 1997, as in situ conservation efforts were insufficient in raising the numbers of this critically endangered species. The success of captive-breeding programs centers on sustainable reproduction and survival of individuals once released into the wild. Captive-born Vancouver Island marmots released to the wild have lower survival rates than their wild-born counterparts; this difference may arise from compromised hibernation patterns or behaviors. Hibernation duration, body weight over the hibernation season, and reproductive success of captive Vancouver Island marmots were reviewed to assess the effect of these variables on each other. Data from a total of 1782 hibernations and 456 breeding attempts were compiled from 1997 to 2018. The number of winters spent in captivity, the origin of the marmot (captive-born or wild-born), the facility at which hibernation occurred, and the body weight all had a significant effect on hibernation length (all p < .001). Increased weight was associated with increased hibernation length by 0.4 ± 0.1 day/kg on average (p = .0015). Captive, wild-born marmots hibernated for significantly longer than their captive-born counterparts by about 21 ± 2 days (p < .001). The odds of successful breeding were significantly increased with increasing hibernation length by approximatively 20% for every 10 additional days of hibernation. This study provides information on the intrinsic relationship between body weight, reproduction, and hibernation in captive Vancouver Island marmots.

How social behaviour and life-history traits change with age and in the year prior to death in female yellow-bellied marmots.

Studies in natural populations are essential to understand the evolutionary ecology of senescence and terminal allocation. While there are an increasing number of studies investigating late-life variation in different life-history traits of wild populations, little is known about these patterns in social behaviour. We used long-term individual based data on yellow-bellied marmots (Marmota flaviventer) to quantify how affiliative social behaviours and different life-history traits vary with age and in the last year of life, and how patterns compare between the two. We found that some social behaviours and all life-history traits varied with age, whereas terminal last year of life effects were only observed in life-history traits. Our results imply that affiliative social behaviours do not act as a mechanism to adjust allocation among traits when close to death, and highlight the importance of adopting an integrative approach, studying late-life variation and senescence across multiple different traits, to allow the identification of potential trade-offs. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

Destruction of Sound Signal Structure in a Peripheral Population (as Exemplified by the Gray Marmot Marmota baibacina).

The variability of the alarm call of the gray marmot (Marmota baibacina) in the peripheral population in the valley of the Arpa River (Kyrgyzstan) is described. It was earlier reported that this population lived together with the red marmot (M. caudata). The authors did not find the red marmot there. Two forms of aberrations were found in the edge population of the gray marmot: amplitude modulation and no pause between the components. The destruction of the signal structure that is typical of the species is probably associated with the disruption of gene flow and does not contain clear signs of hybridization. The material was collected under the field conditions.

Characterization of Seasonal Pharmacokinetic Variability in Woodchucks.

The eastern woodchuck (Marmota monax) is a hibernating species extensively used as an in vivo efficacy model for chronic human hepatitis B virus infection. Under laboratory conditions, woodchucks develop a pseudohibernation condition; thus, the pharmacokinetics (PK) of small-molecule therapeutics may be affected by the seasonal change. The seasonal PK of four probe compounds were characterized over 12 months in seven male and nine female laboratory-maintained woodchucks. These compounds were selected to study changes in oxidative metabolism [antipyrine (AP)], glucuronidation [raltegravir (RTG)], renal clearance [lamivudine (3TC)], and hepatic function [indocyanine green (ICG)]. Seasonal changes in physiologic parameters and PK were determined. Seasonal body weight increases were ≥30%. Seasonal changes in body temperature and heart rate were <10%. The mean AP exposure remained unchanged from April to August 2017, followed by a significant increase (≥1.0-fold) from August to December and subsequent decrease to baseline at the end of study. A similar trend was observed in RTG and 3TC exposures. The ICG exposure remained unchanged. No significant sex difference in PK was observed, although female woodchucks appeared to be less susceptible to seasonal PK and body weight changes. Significant seasonal PK changes for AP, RTG, and 3TC indicate decreases in oxidative metabolism, phase II glucuronidation, and renal clearance during pseudohibernation. The lack of seasonal change in ICG exposure suggests there are no significant changes in hepatic function. This information can be used to optimize the scheduling of woodchuck studies to avoid seasonally driven variation in drug PK. SIGNIFICANCE STATEMENT: Woodchuck is a hibernating species and is commonly used as a nonclinical model of hepatitis B infection. Investigation of seasonal PK changes is perhaps of greater interest to pharmaceutical industry scientists, who use the woodchuck model to optimize the scheduling of woodchuck studies to avoid seasonally driven variation in drug PK and/or toxicity. This information is also valuable to drug metabolism and veterinary scientists in understanding woodchuck's seasonal metabolism and behavior under the pseudohibernation condition.

Older mothers produce more successful daughters.

Annual reproductive success and senescence patterns vary substantially among individuals in the wild. However, it is still seldom considered that senescence may not only affect an individual but also affect age-specific reproductive success in its offspring, generating transgenerational reproductive senescence. We used long-term data from wild yellow-bellied marmots (Marmota flaviventer) living in two different elevational environments to quantify age-specific reproductive success of daughters born to mothers differing in age. Contrary to prediction, daughters born to older mothers had greater annual reproductive success on average than daughters born to younger mothers, and this translated into greater lifetime reproductive success. However, in the favorable lower elevation environment, daughters born to older mothers also had greater age-specific decreases in annual reproductive success. In the harsher higher elevation environment on the other hand, daughters born to older mothers tended to die before reaching ages at which such senescent decreases could be observed. Our study highlights the importance of incorporating environment-specific transgenerational parent age effects on adult offspring age-specific life-history traits to fully understand the substantial variation observed in senescence patterns in wild populations.

The effects of neurectomy and hibernation on bone properties and the endocannabinoid system in marmots (Marmota flaviventris).

Hibernators have adapted a physiological mechanism allowing them to undergo long periods of inactivity without experiencing bone loss. However, the biological mechanisms that prevent bone loss are unknown. Previous studies found meaningful changes, between active and hibernating marmots, in the endocannabinoid system of many tissues, including bone. Cannabinoid receptors (CB1 and CB2) have divergent localization in bone. CB1 is predominately found on sympathetic nerve terminals, while CB2 is more abundant on bone cells and their progenitors. This study aimed to determine the contribution of innervation on endocannabinoid regulation of bone properties in hibernating (during torpor) and non-hibernating yellow-bellied marmots. Neurectomy, a model for disuse osteoporosis, was performed unilaterally in both hibernating and active marmots. Endocannabinoid concentrations were measured in bone marrow, cortical, and trabecular regions from fourth metatarsals of both hindlimbs using microflow chromatography-tandem quadrupole mass spectrometry. Trabecular bone architectural properties of fifth metatarsals were evaluated using micro-computed tomography. There were ligand-specific increases with neurectomy in active, but not hibernating, marmots. Trabecular bone architectural properties were not affected by neurectomy during hibernation, but did show some minor negative changes in active marmots. These findings suggest protection from bone loss in hibernating rodents is peripherally rather than centrally regulated. Furthermore, findings suggest even active marmots with normal metabolism are partially protected from disuse induced bone loss compared to laboratory rodents. Understanding the mechanism hibernators use to maintain bone density may guide development for novel bone loss prevention therapies.

Marmots.

Walter Arnold introduces the biology of marmots.

Correlates of maternal glucocorticoid levels in a socially flexible rodent.

While it is generally accepted that social isolation has detrimental effects on social species, little is known about the importance of social interactions in less social species-particularly for wild reproductive females. We studied socially-flexible yellow-bellied marmots (Marmota flaviventer) and asked whether features of the social environment are associated with maternal fecal glucocorticoid metabolite (FGM) concentrations. Since changes in maternal baseline glucocorticoids may have positive or negative consequences for offspring fitness, we were also interested in estimating their relationship with measures of reproductive success. We fitted generalized linear mixed effects models to a dataset including maternal FGM measurements, social network metrics, maternal/alloparental care, and pup FGM and survival. Agonistic interactions were positively associated with maternal FGM levels, while mothers that engaged in relatively more affiliative interactions had reduced FGM levels when living in environments with low predator pressure. Pups associated with mothers exhibiting high FGM levels had low annual survival rates, received less maternal/alloparental care and had higher FGM levels. Interestingly, offspring from mothers with high FGM levels were more likely to survive the summer when born in small litters. In sum, social interactions likely influence and are influenced by glucocorticoid levels of facultatively social females. Potential benefits of social bonds may be context-specific, and agonistic interactions may be tightly correlated with fitness. Female marmots exhibiting high FGM levels had overall low reproductive success, which is predicted by the cort-fitness hypothesis. However, under adverse conditions, offspring summer survival can be maximized if pups are born in small litters.

Responses of snow leopards, wolves and wild ungulates to livestock grazing in the Zorkul Strictly Protected Area, Tajikistan.

Long recognized as a threat to wildlife, livestock grazing in protected areas has the potential to undermine conservation goals, via competition, habitat degradation, human-carnivore conflict and disruption of predator-prey relationships. In the Strictly Protected Area Zorkul in Tajikistan (Zorkul Reserve), grazing is commonplace despite official prohibition, with potentially detrimental effects on local fauna, in particular, snow leopard Panthera uncia, wolf Canis lupus, brown bear Ursus arctos, argali sheep Ovis ammon, Asiatic ibex Capra sibirica, and long-tailed marmot Marmota caudata. To understand the impacts of grazing and associated human pastoralism on the large mammal community in Zorkul Reserve we used data from camera traps to build models of ungulate and carnivore site use intensity, and we investigated carnivore summer diets using microscopic scat analysis. While sample sizes limited our inference for several species, we found that site use of the most common ungulate, argali, decreased with proximity to herder's camps, indicating possible displacement into sub-optimal habitats. However, no such pattern was present in carnivore site use. For wolf and snow leopard, the most frequently encountered prey items were argali and marmot, while bear depended almost exclusively on marmot. While current pastoralist practices in the reserve may not be incompatible with wildlife presence, our findings suggest that pastoralism may negatively impact ungulates by displacing them from otherwise suitable habitats, with unknown fitness consequences for ungulates or the predators that depend upon them. Managing Zorkul Reserve and other actively grazed protected areas to meet potentially competing demands of local pastoralist communities and conservation will require careful consideration of such interactions to minimize the risk of cascading negative impacts on wildlife.

Extrinsic and intrinsic constraints interact to drive extra-pair paternities in the Alpine marmot.

To reproduce, animals have to form pairs and large variations in the degree of mate switching are observed. Extrinsic and intrinsic factors can constrain individual's mate switching. Among intrinsic factors, genes involved in pair-bonding, such as Avpr-1a, receive increasing attention. The length of microsatellites present in the regulatory region of Avpr-1a determines the neural densities and distributions of the vasopressin receptors known to impact pair-bonding behaviours. For the first time, we investigated whether and how the genetic makeup at Avpr-1a, an intrinsic factor, and the social context, an extrinsic factor, experienced by wild Alpine marmot (Marmota marmota) females affect the proportion of extra-pair young. This proportion was positively correlated with the length of their Avpr-1a regulatory region but only when the social constraints were relaxed, that is when mature male subordinates were present. When ignoring the interactive effect between the length of their Avpr-1a regulatory region and the social constraints, the genetic makeup at Avpr-1a was not associated with the proportion of extra-pair young. Under natural conditions, the genetic regulation of pair-bonding could be hidden by extrinsic factors constraining mate choice.

Early and Adult Social Environments Shape Sex-Specific Actuarial Senescence Patterns in a Cooperative Breeder.

Sociality modulates life-history traits through changes in resource allocation to fitness-related traits. However, how social factors at different stages of the life cycle modulate senescence remains poorly understood. To address this question, we assessed the influence of social environment in both early life and adulthood on actuarial senescence in the Alpine marmot, a cooperative breeder. The influence of helpers on actuarial senescence strongly differed depending on when help was provided and on the sex of the dominant. Being helped when adult slowed down senescence in both sexes. However, the effect of the presence of helpers during the year of birth of a dominant was sex specific. Among dominants helped during adulthood, females born in the presence of helpers senesced slower, whereas males senesced faster. Among dominants without helpers during adulthood, females with helpers at birth senesced faster. Social environment modulates senescence but acts differently between sexes and life stages.

Seasonal Changes in Endocannabinoid Concentrations between Active and Hibernating Marmots (Marmota flaviventris).

Hibernation is a naturally occurring model for studying diseases such as obesity and osteoporosis. Hibernators, marmots (Marmota flaviventris) among them, are able to nearly double their body mass by increasing fat stores prior to hibernation without the negative consequences of obesity. They are also physically inactive for extended periods of time without experiencing negative effects on the skeleton. The endocannabinoid system is involved in modulating neural signaling, circannual rhythms, behavior, appetite, thermogenesis, and bone and energy metabolism. These systems are also altered to maintain homeostasis during hibernation. This study aims to better understand the involvement of the endocannabinoid system in the regulation of physiological processes during hibernation by quantifying the seasonal variation of endocannabinoids and endocannabinoid-like ligands in both active and hibernating marmots. We hypothesized that there would be significant changes in endocannabinoid concentrations at the tissue level in marmots between active and hibernating states. Concentrations were measured in brain, serum, brown adipose tissue, white adipose tissue, bone marrow, cortical bone, and trabecular bone using microflow chromatography coupled with tandem quadrupole mass spectrometry. Significant changes were found, such as a 30-fold decrease in 2-arachidonoyl glycerol (2-AG) in cortical bone during hibernation. Many endocannabinoid and endocannabinoid-like ligands decreased in brown adipose tissue, white adipose tissue, and cortical bone, while several ligands increased in bone marrow. This result supports our hypothesis and suggests the possibility of a peripherally controlled shift in energy metabolism, reduction in bone metabolism, and suppression of the immune system during hibernation.

Strong social relationships are associated with decreased longevity in a facultatively social mammal.

Humans in strong social relationships are more likely to live longer because social relationships may buffer stressors and thus have protective effects. However, a shortcoming of human studies is that they often rely on self-reporting of these relationships. By contrast, observational studies of non-human animals permit detailed analyses of the specific nature of social relationships. Thus, discoveries that some social animals live longer and healthier lives if they are involved in social grooming, forage together or have more affiliative associates emphasizes the potential importance of social relationships on health and longevity. Previous studies have focused on the impact of social metrics on longevity in obligately social species. However, if sociality indeed has a key role in longevity, we might expect that affiliative relationships should also influence longevity in less social species. We focused on socially flexible yellow-bellied marmots (Marmota flaviventer) and asked whether female longevity covaries with the specific nature of social relationships. We quantified social relationships with social network statistics that were based on affiliative interactions, and then estimated the correlation between longevity and sociality using bivariate models. We found a significant negative phenotypic correlation between affiliative social relationship strength and longevity; marmots with greater degree, closeness and those with a greater negative average shortest path length died at younger ages. We conclude that sociality plays an important role in longevity, but how it does so may depend on whether a species is obligately or facultatively social.

The effect of maternal glucocorticoid levels on juvenile docility in yellow-bellied marmots.

Maternal effects can have significant and long-term consequences on offspring behavior and survival, while consistent individual differences (i.e., personality) can have profound impacts on individual fitness. Thus, both can influence population dynamics. However, the underlying mechanisms that determine variation in personality traits are poorly understood. Maternal effects are one potential mechanism that may explain personality variation. We capitalized on a long-term study of yellow-bellied marmots (Marmota flaviventris) to identify maternal effects on juvenile docility. To do so, we partitioned the variance in juvenile docility using a quantitative genetic modeling approach to isolate potential maternal effects. We also directly tested whether maternal stress, measured through fecal glucocorticoid metabolite levels during lactation of 82 mothers, was associated with offspring docility. Docility scores were estimated for 645 juveniles trapped between 2002 and 2012. We found an interaction between maternal glucocorticoid levels and dam age on juvenile docility. We also found significant maternal, litter, permanent environment, and year effects. These results suggest that a mother's life history stage interacts with stress to influence offspring personality. This early life influence can have long lasting effects on an individual's docility throughout life.

Faithful or not: direct and indirect effects of climate on extra-pair paternities in a population of Alpine marmots.

Despite being identified an area that is poorly understood regarding the effects of climate change, behavioural responses to climatic variability are seldom explored. Climatic variability is likely to cause large inter-annual variation in the frequency of extra-pair litters produced, a widespread alternative mating tactic to help prevent, correct or minimize the negative consequences of sub-optimal mate choice. In this study, we investigated how climatic variability affects the inter-annual variation in the proportion of extra-pair litters in a wild population of Alpine marmots. During 22 years of monitoring, the annual proportion of extra-pair litters directly increased with the onset of earlier springs and indirectly with increased snow in winters. Snowier winters resulted in a higher proportion of families with sexually mature male subordinates and thus, created a social context within which extra-pair paternity was favoured. Earlier spring snowmelt could create this pattern by relaxing energetic, movement and time constraints. Further, deeper snow in winter could also contribute by increasing litter size and juvenile survival. Optimal mate choice is particularly relevant to generate adaptive genetic diversity. Understanding the influence of environmental conditions and the capacity of the individuals to cope with them is crucial within the context of rapid climate change.

Exploring the Bone Proteome to Help Explain Altered Bone Remodeling and Preservation of Bone Architecture and Strength in Hibernating Marmots.

Periods of physical inactivity increase bone resorption and cause bone loss and increased fracture risk. However, hibernating bears, marmots, and woodchucks maintain bone structure and strength, despite being physically inactive for prolonged periods annually. We tested the hypothesis that bone turnover rates would decrease and bone structural and mechanical properties would be preserved in hibernating marmots (Marmota flaviventris). Femurs and tibias were collected from marmots during hibernation and in the summer following hibernation. Bone remodeling was significantly altered in cortical and trabecular bone during hibernation with suppressed formation and no change in resorption, unlike the increased bone resorption that occurs during disuse in humans and other animals. Trabecular bone architecture and cortical bone geometrical and mechanical properties were not different between hibernating and active marmots, but bone marrow adiposity was significantly greater in hibernators. Of the 506 proteins identified in marmot bone, 40 were significantly different in abundance between active and hibernating marmots. Monoaglycerol lipase, which plays an important role in fatty acid metabolism and the endocannabinoid system, was 98-fold higher in hibernating marmots compared with summer marmots and may play a role in regulating the changes in bone and fat metabolism that occur during hibernation.

[Sympatric Speciation of the Plague Microbe Yersinia pestis: Monohostal Specialization in the Host-Parasite Marmot-Flea (Marmota sibirica-Oropsylla silantiewi) System].

An ecological scenario of the origin of the plague microbe that is interpreted in the light of modern Darwinism (synthetic theory of evolution) is presented. It is shown that the plague microbe emerged from a clone of the psychrophilic saprozoonotic pseudotuberculosis microbe Yersinia pseudotuberculosis O:1b in the mountain steppe landscapes of Central Asia in the Sartan time, 22000-15000 years ago, in the monohostal Mongolian marmot (Marmota sibirica)-flea (Oropsylla silantiewi) host-parasite system. It was noted that the evolutionary process described corresponds to the sympatric form of speciation by transition ofthe clone of migrant founders to a new, already-existing ecological niche. It was established that monohostal specialization of the plague microbe was made possible due to heterothermia (5-37 degrees C) of marmots in the hibernation period. The factors of the speciation process--isolation, the struggle for existence, and natural selection--were analyzed.