Winter weather versus group thermoregulation: what determines survival in hibernating mammals?

For socially hibernating mammals, the effectiveness of huddling as a means of energy conservation should increase with group size. However, group size has only been linked to increased survival in a few hibernating species, and the relative importance of social structure versus winter conditions during hibernation remains uncertain. We studied the influence of winter weather conditions, social group composition, age-structure, and other environmental factors and individual attributes on the overwinter survival of hoary marmots (Marmota caligata) in the Yukon Territory, Canada. Juvenile hoary marmot survival was negatively correlated with the mean winter (November to May) Pacific Decadal Oscillation (PDO) index. Survival in older age-classes was negatively correlated with PDO lagged by 1 year. Social group size and structure were weakly correlated with survival in comparison to PDO. The relationship between winter PDO and survival was most likely due to the importance of snowpack as insulation during hibernation. The apparent response of hoary marmots to changing winter conditions contrasted sharply with those of other marmot species and other mammalian alpine herbivores. In conclusion, the severity of winter weather may constrain the effectiveness of group thermoregulation in socially hibernating mammals.     

Ectoparasite loads decrease the fitness of alpine marmots (Marmota marmota) but are not a cost of sociality

Parasites arc often considered an unavoidable cost of livingin groups. We examined this hypothesis by investigating theectoparasite fauna of a free-living alpine marmot population,a highly social sciurid species. Only a single important ectoparasitewas found, the mite Echinonyssus blanchardi. Heavy infestationwith this mite correlated with reproductive success of marmotsin two ways. Infant winter mortality increased with ectoparasiteload, probably because ectoparasites reduced the ability ofparents and alloparents to warm infants during hibernation.Litters produced by females exposed to a high number of mitesduring the preceding winter were weaned later. Late weanershad a lower chance of surviving hibernation. However, we foundno relationship between ectoparasite load and group size ormarmot density. Instead, the number of E. blanchardi per animalwas lower in areas where marmot groups were clumped, i.e., infavorable habitats. Although ectoparasites most likely decreasethe fitess of alpine marmots to some extent, they should notbe considered a cost of social life in this species.     

Climate Tolerances and Habitat Requirements Jointly Shape the Elevational Distribution of the American Pika (Ochotona princeps), with Implications for Climate Change Effects

Some of the most compelling examples of ecological responses to climate change are elevational range shifts of individual species, which have been observed throughout the world. A growing body of evidence, however, suggests substantial mediation of simple range shifts due to climate change by other limiting factors. Understanding limiting factors for a species within different contexts, therefore, is critical for predicting responses to climate change. The American pika (Ochotona princeps) is an ideal species for investigating distributions in relation to climate because of their unusual and well-understood natural history as well as observed shifts to higher elevation in parts of their range. We tested three hypotheses for the climatic or habitat characteristics that may limit pika presence and abundance: summer heat, winter snowpack, and forage availability. We performed these tests using an index of pika abundance gathered in a region where environmental influences on pika distribution have not been well-characterized. We estimated relative pika abundance via scat surveys and quantified climatic and habitat characteristics across two North-Central Rocky Mountain Ranges, the Wind River and Bighorn ranges in Wyoming, USA. Pika scat density was highest at mid-elevations and increased linearly with forage availability in both ranges. Scat density also increased with temperatures conducive to forage plant growth, and showed a unimodal relationship with the number of days below -5°C, which is modulated by insulating snowpack. Our results provide support for both the forage availability and winter snowpack hypotheses. Especially in montane systems, considering the context-dependent nature of climate effects across regions and elevations as well as interactions between climatic and other critical habitat characteristics, will be essential for predicting future species distributions.     

Quantum Speciation of <Emphasis Type="Italic">Yersinia pestis</Emphasis> Plague Microbe in a Heteroimmune Environment: In the Populations of Hibernating Tarbagan Marmots (<Emphasis Type="Italic">Marmota sibirica</Emphasis>)

This review is devoted to the ecological mechanism for the transformation of the population of the psychrophilic saprozoobiont pseudotuberculosis microbe Yersinia pseudotuberculosis O:1b into the population of the obligate blood plague microbe Yersinia pestis in the host–parasite system of the marmot flea (Marmota sibirica–Oropsylla silantiewi). The correspondence of this mechanism to the evolutionary principle of quantum speciation has been shown. The most significant population–genetic microbial transformations took place in the populations of hibernating marmots. The main factor of rapid speciation was the heterothermic and, accordingly, heteroimmune state of host marmots during hibernation. During winter awakenings, the body temperature of marmots increases in an S-shaped manner from 5 to 37°C within a short period of time (from dozens of minutes to several hours). A drastic acceleration of metabolic and immune processes occurs in the temperature range of 20–30°C. Rapid adaptation to the “explosive” increase in the immune activity of the primary host (tarbagan marmot) during its regular winter awakenings was the essence of the process of Y. pestis speciation.     

Ecological,Evolutionary and Social Constraints on Reproductive Effort: Are Hoary Marmots Really Biennial Breeders?

Biennial breeding is a rare life-history trait observed in animal species living in harsh, unproductive environments. This reproductive pattern is thought to occur in 10 of 14 species in the genus Marmota, making marmots useful model organisms for studying its ecological and evolutionary implications. Biennial breeding in marmots has been described as an obligate pattern which evolved as a mechanism to mitigate the energetic costs of reproduction (Evolved Constraint hypothesis). However, recent anecdotal evidence suggests that it is a facultative pattern controlled by annual variation in climate and food availability (Environmental Constraint hypothesis). Finally, in social animals like marmots, biennial breeding could result from reproductive competition between females within social groups (Social Constraint hypothesis). We evaluated these three hypotheses using mark-recapture data from an 8-year study of hoary marmot (Marmota caligata) population dynamics in the Yukon. Annual variation in breeding probability was modeled using multi-state mark-recapture models, while other reproductive life-history traits were modeled with generalized linear mixed models. Hoary marmots were neither obligate nor facultative biennial breeders, and breeding probability was insensitive to evolved, environmental, or social factors. However, newly mature females were significantly less likely to breed than older individuals. Annual breeding did not result in increased mortality. Female survival and, to a lesser extent, average fecundity were correlated with winter climate, as indexed by the Pacific Decadal Oscillation. Hoary marmots are less conservative breeders than previously believed, and the evidence for biennial breeding throughout Marmota, and in other arctic/alpine/antarctic animals, should be re-examined. Prediction of future population dynamics requires an accurate understanding of life history strategies, and of how life history traits allow animals to cope with changes in weather and other demographic influences.     

Diet of the snow leopard (Panthera uncia) in the Annapurna Conservation Area, Nepal

The diet of the snow leopard ( Panthera uncia ) was studied from 213 scats collected between April 1990 and February 1991 in the Annapurna Conservation Area. Nepal. Seven species of wild and five species of domestic mammals were taken, as well as an unidentified mammal and birds. Blue sheep ( Pseudois nayaur ) were the most frequently eaten prey. Himalayan marmots ( Marmota himalayana ) were also important, except in winter when they were hibernating. During winter, snow leopards ate more Royle's pika ( Odiotona royki ) and domestic livestock. Yaks were eaten more frequently than other livestock types.     

Habitat preferences in gray marmots (Marmota baibacina)

We examined habitat preferences of the Southern Altai subspecies of gray marmots (Marmota baibacina baibacina) both at the small and large scale. Considerable differences in habitat use among the gray marmot (sub)species complex have been described; Marmota kastschenkoi possibly represents the only forest-dwelling Palearctic marmot. Our results show that habitat use in Southern Altai marmots is determined mainly by vegetation type. The Altai marmots preferred grasslands and shrublands and their distribution was limited to the alpine zone above timberline. Marmots clearly avoided woodlands, even the forest edges and forest-steppe areas with a tree cover greater than 10 %. Gray marmots occur rarely in habitats occupied by alpine pikas, whereas presence of ground squirrels had no effect on marmot distribution. Altai marmots preferred mesic habitats with permeable subsoil layers. Livestock grazing and human disturbance did not affect marmot occurrence. Habitat requirements of examined Altai subspecies M. baibacina baibacina differ from the forest-steppe M. kastschenkoi; nevertheless, the ecological factors to which the forest-dwelling species responds remain to be analyzed. A recent speciation process in gray marmot complex was followed by the evolution of ecological requirements resulting in adaptation to forest dwelling.     

Weather conditions during hunting season affect the number of harvested roe deer (Capreolus capreolus)

Due to human‐induced climate and landscape changes, distribution and abundance of many ungulate species have increased worldwide. Especially in areas where natural predators are absent, hunting is the essential management tool for regulating ungulate populations. Therefore, understanding the factors associated with harvest rates is the first step toward an adaptive management approach. Weather influences hunter and ungulate behavior and thus presumably harvest, but how and which meteorological parameters are linked to harvest numbers have rarely been evaluated. We used nearly 65,000 “sit and wait” and driven hunt harvests of roe deer (Capreolus capreolus) in Bavaria, Germany, and weather data from 2008 to 2017 to test for factors affecting roe deer harvests (i.e., temperature, rain hours, wind speed, sunshine duration, snow depth, workdays vs. weekends, month) using zero‐inflated negative binomial mixed‐effect models. Our results reveal that, besides workdays, high temperatures and prolonged rain resulted in fewer harvested animals, whereas sunshine duration in summer and snow height in snow‐rich areas partially favored harvests during sitting hunts in summer and winter, respectively. The influence of wind speed varied over the course of the year. In summer and autumn, wind speed commonly had a negative effect, positively affecting harvests in winter in some regions. Daily harvest numbers decreased during the summer and autumn hunting periods (May till mid‐October), while they increased during the winter period (mid‐October till mid‐January). Interestingly, harvest success during driven hunts, which are planned well in advance and therefore take place largely independent of weather conditions, was similarly affected by the weather. This result suggests that the inferred weather influence is not only due to the hunters'' decisions but also due to deer behavior. Since many ungulate populations may further benefit from climate change, building an understanding of the relationship between hunting success and weather will aid adaptive ungulate management.     

Rewarming rates of two large hibernators: Comparison of a monotreme and a eutherian

We measured body temperatures in two large hibernating mammals, the eutherian alpine marmot (Marmota marmota) and the egg-laying echidna (Tachyglossus aculeatus) from unrestrained animals in their natural environment. In both species hibernation is broken every 13 days on average by rewarming to euthermic temperatures. We found that the time course of a rewarming could be closely fitted with a sigmoid curve, allowing calculation of peak rewarming rate and corresponding body temperature. Maximum rewarming rates were twice as high in marmots as in echidnas (12.1±1.3 °C h⁻¹, n=10 cf. 6.2±1.2 °C h⁻¹, n=10). Peak rewarming rates were positively correlated with body temperature in echidnas, but negatively correlated in marmots.     

Male-biased sex ratio in litters of Alpine marmots supports the helper repayment hypothesis

In a French population of Alpine marmots (Marmota marmota),the sex ratio at weaning was biased in favor of males. Thisbias also seemed to exist at birth. Under Fisher's equal allocationprinciple, this means that daughters should be more costlyto produce than sons. Because the Alpine marmot can be considereda cooperative breeding species, we investigated whether thedifferential cost between sons and daughters may be explainedby the helper repayment hypothesis. The Alpine marmot usessocial thermoregulation during hibernation, allowing juvenilesto better survive over winter. In the study population, juvenilesurvival during winter increased with group size. More precisely,juvenile survival during winter increased with the number andwith the proportion of subordinate males in the hibernatinggroup, but juvenile survival did not depend on the number of subordinate females. As our results did not support alternativehypotheses to explain the observed bias in sex ratio amongoffspring at emergence, we conclude that the helper repaymenthypothesis is the best candidate to explain the observed offspringsex ratio bias in Alpine marmots. By participating in socialthermoregulation, subordinate males may repay part of the investment they received from their parents and thus become less costlyto produce. We suggest that only subordinate males helped becausethey may gain direct fitness benefits, whereas subordinatefemales may only expect indirect fitness benefits from helping.Finally, the offspring sex ratio per individual parent wasmale biased, but mothers adjusted the size and the sex compositionof their litters according to their phenotypic condition asexpected from the Trivers-Willard hypothesis.     

Genetic characterization of four wild species of Chinese marmots using microsatellite markers

Marmots are large ground squirrels, and 14 species have been reported in the world, including four species of marmots (Himalayan marmot, Tarbagan marmot, gray marmot and long-tailed marmot) living in China. Although these biological resources are abundant in China, information regarding their genetic features is lacking, hampering further study regarding them. The aims of this research were to evaluate genetic variations of four species of Chinese wild marmots, and analyzed kinship of these marmot populations. In the current study, we collected samples of four species of Chinese wild marmot and analyzed the effective allele number, gene diversity, the Shannon index, and polymorphism information to evaluate genetic variations using 13 microsatellite loci. Based on Nei’s genetic distance using the unweighted pair group method, we constructed a dendrogram to analyze the population kinship. We determined that all four Chinese marmot species had high genetic polymorphisms and departure from Hardy-Weinberg equilibrium. The Chinese marmots to be divided into two large groups: Himalayan marmot was independent group. Tarbagan marmot, gray marmot and long-tailed marmot were others; Tarbagan marmot and gray marmot showed a close kinship with each other, but long-tailed marmot did not have a close relationship with the other species. The high polymorphisms and the kinship of Chinese marmot populations were correlated with geographical terrain of their habitat. Himalayan marmot was characterized as living in unique alpine meadows in Qinghai-Tibet plateau and was affected by terrain; however, Tarbagan marmot, gray marmot and long-tailed marmot were characterized as living in grassland or alpine grassland and were not affected by terrain. Genetic features of Chinese wild marmots were investigated in this study. This may give using information regarding protection of Chinese wild marmot resource and further application of biomedical research.     

Predation as a probable mechanism relating winter weather to population dynamics in a North American porcupine population

An abundance index of an eastern Quebec population of North American porcupines (Erethizon dorsatum) has cycled with superimposed periodicities of 11 and 22 years from 1868 to 2000. This cycle closely followed 11- and 22-year cycles in solar irradiance and local weather (e.g., winter precipitation and spring temperature), generating the hypothesis that solar activity may affect porcupine abundance through effects on local weather. We investigated the mechanisms linking porcupine abundance to local weather conditions using a 6-year study (2000–2005) involving individual mark-recapture, radio tracking, seasonal survival analyses and identification of mortality causes. Summer (May–August) survival was high and constant over the study period, whereas winter (August–May) survival was lower and varied during the duration of our study. Variations in local winter precipitation explained 89% of the variation in winter survival. Porcupine predation rates appeared strongly related to snow conditions; 95% of depredated porcupines were killed when snow was covering the ground, and predation rates were higher in years with increased winter precipitation. Our data thus support the hypothesis that changes in predation rates under different snow conditions were the mechanism relating climate to porcupine population dynamics, via modifications of the local predator–prey interactions and impacts on porcupine winter survival. Our study adds to the growing body of evidence supporting an effect of climate on predator–prey processes. Also, it identifies one possible mechanism involved in the relationship between solar irradiance and porcupine population cycles observed at this study site over a 130-year period.     

Nonlinear effects of climate on boreal rodent dynamics: mild winters do not negate high‐amplitude cycles

Small rodents are key species in many ecosystems. In boreal and subarctic environments, their importance is heightened by pronounced multiannual population cycles. Alarmingly, the previously regular rodent cycles appear to be collapsing simultaneously in many areas. Climate change, particularly decreasing snow quality or quantity in winter, is hypothesized as a causal factor, but the evidence is contradictory. Reliable analysis of population dynamics and the influence of climate thereon necessitate spatially and temporally extensive data. We combined data on vole abundances and climate, collected at 33 locations throughout Finland from 1970 to 2011, to test the hypothesis that warming winters are causing a disappearance of multiannual vole cycles. We predicted that vole population dynamics exhibit geographic and temporal variation associated with variation in climate; reduced cyclicity should be observed when and where winter weather has become milder. We found that the temporal patterns in cyclicity varied between climatically different regions: a transient reduction in cycle amplitude in the coldest region, low‐amplitude cycles or irregular dynamics in the climatically intermediate regions, and strengthening cyclicity in the warmest region. Our results did not support the hypothesis that mild winters are uniformly leading to irregular dynamics in boreal vole populations. Long and cold winters were neither a prerequisite for high‐amplitude multiannual cycles, nor were mild winters with reduced snow cover associated with reduced winter growth rates. Population dynamics correlated more strongly with growing season than with winter conditions. Cyclicity was weakened by increasing growing season temperatures in the cold, but strengthened in the warm regions. High‐amplitude multiannual vole cycles emerge in two climatic regimes: a winter‐driven cycle in cold, and a summer‐driven cycle in warm climates. Finally, we show that geographic climatic gradients alone may not reliably predict biological responses to climate change.     

Induction of summer hibernation in the 13-lined ground squirrel shown by comparative serum transfusions from arctic mammals.

A “trigger” substance was again indicated to be present in sera of hibernating animals. Sera from the hibernating 13-lined ground squirrel, hibernating woodchuck, hibernating Arctic ground squirrel, and hibernating Arctic marmot were all capable of inducing the 13-lined ground squirrel to hibernate in the summer, a season when that species would normally be active. The hibernation trigger is thus not species specific. It is effective whether drawn from these two Arctic species of hibernators or drawn from these two species of hibernators from the midwestern states. The normothermic Arctic marmot appears to have an “anti-trigger” substance in its serum in the summer, which impedes fall hibernation in the transfused 13-lined ground squirrel. This is similar to the anti-trigger observed in the summer serum of active 13-lined ground squirrels and active woodchucks. With respect to hypothermia, it was induced in Artic marmots and in Arctic foxes at Point Barrow, Alaska, in summer. Though in such cases body temperatures fell significantly (as in hibernation), no trigger was recovered from their hypothermic sera that could be shown to be capable of inducing summer hibernation in the ground squirrel. Neither was anti-trigger found in the serum of hypothermic experimentals. These latter experiments thus suggest that the release of trigger into the blood during hibernation is dependent on a mechanism more complex than simply lowering body temperature.     

Detecting snow-related signals in radial growth of Pinus uncinata mountain forests

Climate warming is responsible for observed reduction in snowpack depth and an earlier and faster melt-out in many mountains of the Northern Hemisphere. Such changes in mountain hydroclimate could negatively affect productivity and tree growth in high-elevation forests, but few studies have investigated how and where recent warming trends and changes in snow cover influence forest growth. A network comprising 36 high-elevation Pinus uncinata forests was sampled in the NE Iberian Peninsula, mainly across the Spanish Pyrenees, using dendrochronology to relate tree radial growth to a detailed air temperature and snow depth data. Radial growth was negatively influenced by a longer winter snow season and a higher late-spring snowpack depth. Notably, the effect of snow on tree growth was found regardless the widely reported positive effect of growing-season air temperatures on P. uncinata growth. No positive influence of moisture from spring snowmelt on annual growth of P. uncinata was detected in sampled forests. Tall trees showed a lower growth responsiveness to snow than small trees. Decreasing trends in winter and spring snow depths were detected at most Pyrenean forests, suggesting that the growth of high-elevation P. uncinata forests can beneficiate for a shallower and of shorter duration snowpack associated with warmer conditions. However, water-limited sites located on steep slopes or on rocky substrates, with poor soil-water holding capacity, could experience drought stress because of early depleted snow-related soil moisture.     

Snow cover and extreme winter warming events control flower abundance of some,but not all species in high arctic Svalbard

The High Arctic winter is expected to be altered through ongoing and future climate change. Winter precipitation and snow depth are projected to increase and melt out dates change accordingly. Also, snow cover and depth will play an important role in protecting plant canopy from increasingly more frequent extreme winter warming events. Flower production of many Arctic plants is dependent on melt out timing, since season length determines resource availability for flower preformation. We erected snow fences to increase snow depth and shorten growing season, and counted flowers of six species over 5 years, during which we experienced two extreme winter warming events. Most species were resistant to snow cover increase, but two species reduced flower abundance due to shortened growing seasons. Cassiope tetragona responded strongly with fewer flowers in deep snow regimes during years without extreme events, while Stellaria crassipes responded partly. Snow pack thickness determined whether winter warming events had an effect on flower abundance of some species. Warming events clearly reduced flower abundance in shallow but not in deep snow regimes of Cassiope tetragona, but only marginally for Dryas octopetala. However, the affected species were resilient and individuals did not experience any long term effects. In the case of short or cold summers, a subset of species suffered reduced reproductive success, which may affect future plant composition through possible cascading competition effects. Extreme winter warming events were shown to expose the canopy to cold winter air. The following summer most of the overwintering flower buds could not produce flowers. Thus reproductive success is reduced if this occurs in subsequent years. We conclude that snow depth influences flower abundance by altering season length and by protecting or exposing flower buds to cold winter air, but most species studied are resistant to changes.     

Alpine marmot (Marmota marmota) distribution evolution under climate change: The use of species distribution models at a local scale in the western Pyrenees massif (France)

The Alpine marmot (Marmota marmota) is a social mammal living in mountainous grassland areas and has the particularity to hibernate in winter. Recent studies on a population in the French Alps found that climate change is affecting Alpine marmot population dynamics and might impact their overall distribution in the future. Using Species Distribution Models (SDMs), the effect of climate change on Alpine marmot's future distribution was investigated at a local scale, in the western part of the Pyrenean massif (New-Aquitaine region, France). This scale was chosen as an appropriate action scale for the conservation strategy for the species. Three climatic scenarios were used (RCP 2.6, RCP 4.5, and RCP 8.5) over three future 30-year periods (2021–2050, 2040–2070, 2071–2100) to predict the short- to long-term potential distribution of the target species. The results are consistent with naturalistic knowledge of the species´ ecological needs in terms of variable importance and response type. Mean maximum temperature in winter, standard-deviation of daily temperature in winter, along with the median rainfall amount in summer were the three most important climatic variables. Predictions under the two most pessimistic climate scenarios showed potential large habitat loss. In the long term, for RCP 4.5, an estimated habitat loss of 18% was predicted. In the case of RCP 8.5, a higher impact was predicted, with a 54% habitat loss. Our results show that high impact due to climate change can be expected at a long term. In addition, if winter climatic conditions are important for marmot survival through hibernation, drought in summer might be one of the drivers of future population dynamic and distribution. Our findings can be applied for other species living in grassland mountainous environments and for which access to food resources in summer is essential, facilitating the conservation of target areas.     

Thermoregulatory responses to temperature manipulation of the spinal cord in the marmot

Yellow-bellied marmots (M. flaviventris) acclimated to T_a = 20 °C were implanted with U-shaped polyethylene thermodes in the peridural space of the spinal cord. Decreasing the temperature of the cervical, thoracic, or lumbar areas of the cord increased heart rate, electromyographic activity, and oxygen consumption in the animals. These responses differed qualitatively from those elicited by heating the same cord areas, indicating specificity of the response to the temperature change.Increases in heat production were proportional to the amount of cooling of the cord. The thoracic area was found to be more thermosensitive than the lumbar area. No behavioral or physical thermoregulation was apparent when the spinal cord temperature was changed in these animals.In addition to the conclusion that regulation of spinal cord temperature may be important in the euthermic marmot, it was postulated that the temperature receptors located in the thoracic cord of the marmot may be important in maintaining shivering thermogenesis during arousal from hibernation.     

Influence of experimental snow removal on root and canopy physiology of sugar maple trees in a northern hardwood forest

Due to projected increases in winter air temperatures in the northeastern USA over the next 100 years, the snowpack is expected to decrease in depth and duration, thereby increasing soil exposure to freezing air temperatures. To evaluate the potential physiological responses of sugar maple (Acer saccharum Marsh.) to a reduced snowpack, we measured root injury, foliar cation and carbohydrate concentrations, woody shoot carbohydrate levels, and terminal woody shoot lengths of trees in a snow manipulation experiment in New Hampshire, USA. Snow was removed from treatment plots for the first 6 weeks of winter for two consecutive years, resulting in lower soil temperatures to a depth of 50 cm for both winters compared to reference plots with an undisturbed snowpack. Visibly uninjured roots from trees in the snow removal plots had significantly higher (but sub-lethal) levels of relative electrolyte leakage than trees in the reference plots. Foliar calcium: aluminum (Al) molar ratios were significantly lower, and Al concentrations were significantly higher, in trees from snow removal plots than trees from reference plots. Snow removal also reduced terminal shoot growth and increased foliar starch concentrations. Our results are consistent with previous research implicating soil freezing as a cause of soil acidification that leads to soil cation imbalances, but are the first to show that this translates into altered foliar cation pools, and changes in soluble and structural carbon pools in trees. Increased soil freezing due to a reduced snowpack could exacerbate soil cation imbalances already caused by acidic deposition, and have widespread implications for forest health in the northeastern USA.     

Functional evolution of leptin of Ochotona curzoniae in adaptive thermogenesis driven by cold environmental stress

Background

Environmental stress can accelerate the directional selection and evolutionary rate of specific stress-response proteins to bring about new or altered functions, enhancing an organism''s fitness to challenging environments. Plateau pika (Ochotona curzoniae), an endemic and keystone species on Qinghai-Tibetan Plateau, is a high hypoxia and low temperature tolerant mammal with high resting metabolic rate and non-shivering thermogenesis to cope in this harsh plateau environment. Leptin is a key hormone related to how these animals regulate energy homeostasis. Previous molecular evolutionary analysis helped to generate the hypothesis that adaptive evolution of plateau pika leptin may be driven by cold stress.

Methodology/Principal Findings

To test the hypothesis, recombinant pika leptin was first purified. The thermogenic characteristics of C57BL/6J mice injected with pika leptin under warm (23±1°C) and cold (5±1°C) acclimation is investigated. Expression levels of genes regulating adaptive thermogenesis in brown adipose tissue and the hypothalamus are compared between pika leptin and human leptin treatment, suggesting that pika leptin has adaptively and functionally evolved. Our results show that pika leptin regulates energy homeostasis via reduced food intake and increased energy expenditure under both warm and cold conditions. Compared with human leptin, pika leptin demonstrates a superior induced capacity for adaptive thermogenesis, which is reflected in a more enhanced β-oxidation, mitochondrial biogenesis and heat production. Moreover, leptin treatment combined with cold stimulation has a significant synergistic effect on adaptive thermogenesis, more so than is observed with a single cold exposure or single leptin treatment.

Conclusions/Significance

These findings support the hypothesis that cold stress has driven the functional evolution of plateau pika leptin as an ecological adaptation to the Qinghai-Tibetan Plateau.