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Hibernation is a period of metabolic suppression utilized by many small and large mammal species to survive during winter periods. As the underlying cellular and molecular mechanisms remain incompletely understood, our study aimed to determine whether skeletal muscle myosin and its metabolic efficiency undergo alterations during hibernation to optimize energy utilization. We isolated muscle fibers from small hibernators, Ictidomys tridecemlineatus and Eliomys quercinus and larger hibernators, Ursus arctos and Ursus americanus. We then conducted loaded Mant-ATP chase experiments alongside X-ray diffraction to measure resting myosin dynamics and its ATP demand. In parallel, we performed multiple proteomics analyses. Our results showed a preservation of myosin structure in U. arctos and U. americanus during hibernation, whilst in I. tridecemlineatus and E. quercinus, changes in myosin metabolic states during torpor unexpectedly led to higher levels in energy expenditure of type II, fast-twitch muscle fibers at ambient lab temperatures (20 °C). Upon repeating loaded Mant-ATP chase experiments at 8 °C (near the body temperature of torpid animals), we found that myosin ATP consumption in type II muscle fibers was reduced by 77-107% during torpor compared to active periods. Additionally, we observed Myh2 hyper-phosphorylation during torpor in I. tridecemilineatus, which was predicted to stabilize the myosin molecule. This may act as a potential molecular mechanism mitigating myosin-associated increases in skeletal muscle energy expenditure during periods of torpor in response to cold exposure. Altogether, we demonstrate that resting myosin is altered in hibernating mammals, contributing to significant changes to the ATP consumption of skeletal muscle. Additionally, we observe that it is further altered in response to cold exposure and highlight myosin as a potentially contributor to skeletal muscle non-shivering thermogenesis.
Many animals use hibernation as a tactic to survive harsh winters. During this dormant, inactive state, animals reduce or limit body processes, such as heart rate and body temperature, to minimise their energy use. To conserve energy during hibernation, animals can use different approaches. For example, garden dormice undergo periodic states of extremely low core temperatures (down to 48oC); whereas Eurasian brown bears see milder temperature drops (down to 2325oC). An important organ that changes during hibernation is skeletal muscle. Skeletal muscle typically uses large amounts of energy, making up around 50% of body mass. To survive, hibernating animals must change how their skeletal muscle uses energy. Traditionally, active myosin a protein found in muscles that helps muscles to contract was thought to be responsible for most of the energy use by skeletal muscle. But, more recently, resting myosin has also been found to use energy when muscles are relaxed. Lewis et al. studied myosin and skeletal muscle energy use changes during hibernation and whether they could impact the metabolism of hibernating animals. Lewis et al. assessed myosin changes in muscle samples from squirrels, dormice and bears during hibernation and during activity. Experiments showed changes in resting myosin in squirrels and dormice (whose temperature drops to 48oC during hibernation) but not in bears. Further analysis revealed that cooling samples from non-hibernating muscle to 48oC increased energy use in resting myosin, thereby generating heat. However, no increase in energy use was found after cooling hibernating muscle samples to 48oC. This suggest that resting myosin generates heat at cool temperatures a mechanism that is switched off in hibernating animals to allow them to cool their body temperature. These findings reveal key insights into how animals conserve energy during hibernation. In addition, the results show that myosin regulates energy use in skeletal muscles, which indicates myosin may be a potential drug target in metabolic diseases, such as obesity.
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Hibernación , Animales , Hibernación/fisiología , Metabolismo Energético , Miosinas del Músculo Esquelético/metabolismo , Ursidae/metabolismo , Ursidae/fisiología , Adenosina Trifosfato/metabolismo , Músculo Esquelético/metabolismo , Músculo Esquelético/fisiología , Fibras Musculares Esqueléticas/metabolismo , ProteómicaRESUMEN
Hibernation is a period of metabolic suppression utilized by many small and large mammal species to survive during winter periods. As the underlying cellular and molecular mechanisms remain incompletely understood, our study aimed to determine whether skeletal muscle myosin and its metabolic efficiency undergo alterations during hibernation to optimize energy utilization. We isolated muscle fibers from small hibernators, Ictidomys tridecemlineatus and Eliomys quercinus and larger hibernators, Ursus arctos and Ursus americanus. We then conducted loaded Mant-ATP chase experiments alongside X-ray diffraction to measure resting myosin dynamics and its ATP demand. In parallel, we performed multiple proteomics analyses. Our results showed a preservation of myosin structure in U. arctos and U. americanus during hibernation, whilst in I. tridecemlineatus and E. quercinus, changes in myosin metabolic states during torpor unexpectedly led to higher levels in energy expenditure of type II, fast-twitch muscle fibers at ambient lab temperatures (20°C). Upon repeating loaded Mant-ATP chase experiments at 8°C (near the body temperature of torpid animals), we found that myosin ATP consumption in type II muscle fibers was reduced by 77-107% during torpor compared to active periods. Additionally, we observed Myh2 hyper-phosphorylation during torpor in I. tridecemilineatus, which was predicted to stabilize the myosin molecule. This may act as a potential molecular mechanism mitigating myosin-associated increases in skeletal muscle energy expenditure during periods of torpor in response to cold exposure. Altogether, we demonstrate that resting myosin is altered in hibernating mammals, contributing to significant changes to the ATP consumption of skeletal muscle. Additionally, we observe that it is further altered in response to cold exposure and highlight myosin as a potentially contributor to skeletal muscle non-shivering thermogenesis.
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BACKGROUND: Ancient DNA studies suggest that Late Pleistocene climatic changes had a significant effect on population dynamics in Arctic species. The Eurasian collared lemming (Dicrostonyx torquatus) is a keystone species in the Arctic ecosystem. Earlier studies have indicated that past climatic fluctuations were important drivers of past population dynamics in this species. RESULTS: Here, we analysed 59 ancient and 54 modern mitogenomes from across Eurasia, along with one modern nuclear genome. Our results suggest population growth and genetic diversification during the early Late Pleistocene, implying that collared lemmings may have experienced a genetic bottleneck during the warm Eemian interglacial. Furthermore, we find multiple temporally structured mitogenome clades during the Late Pleistocene, consistent with earlier results suggesting a dynamic late glacial population history. Finally, we identify a population in northeastern Siberia that maintained genetic diversity and a constant population size at the end of the Pleistocene, suggesting suitable conditions for collared lemmings in this region during the increasing temperatures associated with the onset of the Holocene. CONCLUSIONS: This study highlights an influence of past warming, in particular the Eemian interglacial, on the evolutionary history of the collared lemming, along with spatiotemporal population structuring throughout the Late Pleistocene.
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Arvicolinae , Ecosistema , Animales , Dinámica Poblacional , Regiones Árticas , ADN AntiguoRESUMEN
Collared lemmings (Dicrostonyx) are cold adapted rodents, keystone animals in the tundra communities and the model taxa in studies of Arctic genetic diversity and Quaternary paleontology. We examined mitochondrial and nuclear genomic variation to reconstruct phylogenetic relationships among the Eurasian D. torquatus and North American D. groenlandicus, D. hudsonius and evaluate biogeographic hypothesis of the two colonization events of North America from Eurasia based on morphological variation in dental traits. The nuclear and mitogenome phylogenies support reciprocal monophyly of each species but reveal conflicting relationships among species. The mitogenome tree likely reflects ancient mitochondrial replacement between currently isolated D. groenlandicus and D. hudsonius. The nuclear genome phylogeny reveals species cladogenesis and supports the hypothesis that D. hudsonius with primitive and distinct molar morphology represents a relic of the first migration event from Eurasia to North America. Species widely distributed in the North American Arctic, D. groenlandicus, with advanced dental morphology originated from a later colonization event across the Bering Land Bridge. This study shows ancient mitochondrial capture between two Arctic species and emphasizes the importance of multilocus approaches for phylogenetic inference.
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Genoma Mitocondrial , Animales , Arvicolinae , ADN Mitocondrial/genética , Especiación Genética , Genómica , FilogeniaRESUMEN
Physical inactivity leads to losses of bone mass and strength in most mammalian species. In contrast, hibernating bears show no bone loss over the prolonged periods (4-6 months) of immobility during winter, which suggests that they have adaptive mechanisms to preserve bone mass. To identify transcriptional changes that underlie molecular mechanisms preventing disuse osteoporosis, we conducted a large-scale gene expression screening in the trabecular bone and bone marrow, comparing hibernating and summer active bears through sequencing of the transcriptome. Gene set enrichment analysis showed a coordinated down-regulation of genes involved in bone resorption, osteoclast differentiation and signaling, and apoptosis during hibernation. These findings are consistent with previous histological findings and likely contribute to the preservation of bone during the immobility of hibernation. In contrast, no significant enrichment indicating directional changes in gene expression was detected in the gene sets of bone formation and osteoblast signaling in hibernating bears. Additionally, we revealed significant and coordinated transcriptional induction of gene sets involved in aerobic energy production including fatty acid beta oxidation, tricarboxylic acid cycle, oxidative phosphorylation, and mitochondrial metabolism. Mitochondrial oxidation was likely up-regulated by transcriptionally induced AMPK/PGC1α pathway, an upstream stimulator of mitochondrial function.
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Densidad Ósea/genética , Resorción Ósea/genética , Huesos/metabolismo , Hibernación/fisiología , Osteogénesis/genética , Transcripción Genética/genética , Ursidae/genética , Ursidae/metabolismo , Adenilato Quinasa/metabolismo , Animales , Apoptosis/genética , Diferenciación Celular/genética , Expresión Génica , Mitocondrias/genética , Mitocondrias/metabolismo , Osteoclastos/fisiología , Oxidación-Reducción , Coactivador 1-alfa del Receptor Activado por Proliferadores de Peroxisomas gamma/metabolismo , Transducción de Señal/genética , Transducción de Señal/fisiología , Transcriptoma/genéticaRESUMEN
Physical inactivity generates muscle atrophy in most mammalian species. In contrast, hibernating mammals demonstrate limited muscle loss over the prolonged intervals of immobility during winter, which suggests that they have adaptive mechanisms to reduce disuse muscle atrophy. To identify transcriptional programs that underlie molecular mechanisms attenuating muscle loss, we conducted a large-scale gene expression profiling in quadriceps muscle of arctic ground squirrels, comparing hibernating (late in a torpor and during torpor re-entry after arousal) and summer active animals using next generation sequencing of the transcriptome. Gene set enrichment analysis showed a coordinated up-regulation of genes involved in all stages of protein biosynthesis and ribosome biogenesis during both stages of hibernation that suggests induction of translation during interbout arousals. Elevated proportion of down-regulated genes involved in apoptosis, NFKB signaling as well as significant under expression of atrogenes, upstream regulators (FOXO1, FOXO3, NFKB1A), key components of the ubiquitin proteasome pathway (FBXO32, TRIM63, CBLB), and overexpression of PPARGC1B inhibiting proteolysis imply suppression of protein degradation in muscle during arousals. The induction of protein biosynthesis and decrease in protein catabolism likely contribute to the attenuation of disuse muscle atrophy through prolonged periods of immobility of hibernation.
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Perfilación de la Expresión Génica , Músculo Esquelético/fisiología , Atrofia Muscular/genética , Sciuridae/fisiología , Alaska , Animales , Temperatura Corporal , Ácidos Grasos/genética , Ácidos Grasos/metabolismo , Femenino , Hibernación , Secuenciación de Nucleótidos de Alto Rendimiento , Masculino , LetargoRESUMEN
The Arctic climate was warmer than today at the last interglacial and the Holocene thermal optimum. To reveal the impact of past climate-warming events on the demographic history of an Arctic specialist, we examined both mitochondrial and nuclear genomic variation in the collared lemming (Dicrostonyx torquatus, Pallas), a keystone species in tundra communities, across its entire distribution in northern Eurasia. The ancestral phylogenetic position of the West Beringian group and divergence time estimates support the hypothesis of continental range contraction to a single refugial area located in West Beringia during high-magnitude warming of the last interglacial, followed by westward recolonization of northern Eurasia in the last glacial period. The West Beringian group harbors the highest mitogenome diversity and its inferred demography indicates a constantly large effective population size over the Late Pleistocene to Holocene. This suggests that northward forest expansion during recent warming of the Holocene thermal optimum did not affect the gene pool of the collared lemming in West Beringia but reduced genomic diversity and effective population size in all other regions of the Eurasian Arctic. Demographic inference from genomic diversity was corroborated by species distribution modeling showing reduction in species distribution during past climate warming. These conclusions are supported by recent paleoecological evidence suggesting smaller temperature increases and moderate northward forest advances in the extreme northeast of Eurasia during the Late Pleistocene-to-Holocene warming events. This study emphasizes the importance of West Beringia as a potential refugium for cold-adapted Arctic species under ongoing climate warming.
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Arvicolinae/genética , Variación Genética/genética , Calentamiento Global/historia , Animales , Regiones Árticas , Asia , Europa (Continente) , Genoma/genética , Genoma Mitocondrial/genética , Genómica , Historia Antigua , Refugio de Fauna , TundraRESUMEN
The complete mitochondrial genomes of two species of the North American collared lemmings were obtained by using PCR amplification and capillary sequencing (GenBank accession nos. KX712239 and KX683880). The collared lemming mitochondrial genomes are 16,341 and 16,338 base pairs long and show the gene order, contents and gene strand asymmetry typical for mammals. The mitogenome sequences provide an important genomic resource for the collared lemmings, which are model study species in Arctic genetic diversity and biogeographic history.
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The complete mitochondrial genome the Eurasian collared lemming was obtained by using PCR amplification and capillary sequencing (GenBank accession no. KX066190). The collared lemming mitochondrial genome is 16,340 base pairs long and shows the gene order, contents and gene strand asymmetry typical for mammals. The mitogenome sequence provides an important new genomic resource for the collared lemming, which is a model study species in Arctic phylogeography and biotic history.
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Recent studies suggest that alpine and arctic organisms may have distinctly different phylogeographic histories from temperate or tropical taxa, with recent range contraction into interglacial refugia as opposed to post-glacial expansion out of refugia. We use a combination of phylogeographic inference, demographic reconstructions, and hierarchical Approximate Bayesian Computation to test for phylodemographic concordance among five species of alpine-adapted small mammals in eastern Beringia. These species (Collared Pikas, Hoary Marmots, Brown Lemmings, Arctic Ground Squirrels, and Singing Voles) vary in specificity to alpine and boreal-tundra habitat but share commonalities (e.g., cold tolerance and nunatak survival) that might result in concordant responses to Pleistocene glaciations. All five species contain a similar phylogeographic disjunction separating eastern and Beringian lineages, which we show to be the result of simultaneous divergence. Genetic diversity is similar within each haplogroup for each species, and there is no support for a post-Pleistocene population expansion in eastern lineages relative to those from Beringia. Bayesian skyline plots for four of the five species do not support Pleistocene population contraction. Brown Lemmings show evidence of late Quaternary demographic expansion without subsequent population decline. The Wrangell-St. Elias region of eastern Alaska appears to be an important zone of recent secondary contact for nearctic alpine mammals. Despite differences in natural history and ecology, similar phylogeographic histories are supported for all species, suggesting that these, and likely other, alpine- and arctic-adapted taxa are already experiencing population and/or range declines that are likely to synergistically accelerate in the face of rapid climate change. Climate change may therefore be acting as a double-edged sword that erodes genetic diversity within populations but promotes divergence and the generation of biodiversity.
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Adaptación Fisiológica , Cambio Climático , Mamíferos/fisiología , Filogeografía , Animales , Regiones Árticas , Teorema de Bayes , Ecosistema , Variación GenéticaRESUMEN
Hibernation is an energy-saving adaptation that involves a profound suppression of physical activity that can continue for 6-8 months in highly seasonal environments. While immobility and disuse generate muscle loss in most mammalian species, in contrast, hibernating bears and ground squirrels demonstrate limited muscle atrophy over the prolonged periods of physical inactivity during winter, suggesting that hibernating mammals have adaptive mechanisms to prevent disuse muscle atrophy. To identify common transcriptional programmes that underlie molecular mechanisms preventing muscle loss, we conducted a large-scale gene expression screen in hind limb muscles comparing hibernating and summer-active black bears and arctic ground squirrels using custom 9600 probe cDNA microarrays. A molecular pathway analysis showed an elevated proportion of overexpressed genes involved in all stages of protein biosynthesis and ribosome biogenesis in muscle of both species during torpor of hibernation that suggests induction of translation at different hibernation states. The induction of protein biosynthesis probably contributes to attenuation of disuse muscle atrophy through the prolonged periods of immobility of hibernation. The lack of directional changes in genes of protein catabolic pathways does not support the importance of metabolic suppression for preserving muscle mass during winter. Coordinated reduction in multiple genes involved in oxidation-reduction and glucose metabolism detected in both species is consistent with metabolic suppression and lower energy demand in skeletal muscle during inactivity of hibernation.
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Adaptación Fisiológica/genética , Hibridación Genómica Comparativa , Hibernación , Atrofia Muscular/genética , Sciuridae/genética , Ursidae/genética , Animales , Masculino , Análisis de Secuencia por Matrices de Oligonucleótidos , Biosíntesis de Proteínas , TranscriptomaRESUMEN
BACKGROUND: Mammalian hibernators display phenotypes similar to physiological responses to calorie restriction and fasting, sleep, cold exposure, and ischemia-reperfusion in non-hibernating species. Whether biochemical changes evident during hibernation have parallels in non-hibernating systems on molecular and genetic levels is unclear. RESULTS: We identified the molecular signatures of torpor and arousal episodes during hibernation using a custom-designed microarray for the Arctic ground squirrel (Urocitellus parryii) and compared them with molecular signatures of selected mouse phenotypes. Our results indicate that differential gene expression related to metabolism during hibernation is associated with that during calorie restriction and that the nuclear receptor protein PPARα is potentially crucial for metabolic remodeling in torpor. Sleep-wake cycle-related and temperature response genes follow the same expression changes as during the torpor-arousal cycle. Increased fatty acid metabolism occurs during hibernation but not during ischemia-reperfusion injury in mice and, thus, might contribute to protection against ischemia-reperfusion during hibernation. CONCLUSIONS: In this study, we systematically compared hibernation with alternative phenotypes to reveal novel mechanisms that might be used therapeutically in human pathological conditions.
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Perfilación de la Expresión Génica , Hibernación/genética , Fenotipo , Sciuridae/genética , Sciuridae/fisiología , Animales , Restricción Calórica , Relojes Circadianos/genética , Frío , Femenino , Técnicas de Inactivación de Genes , Humanos , Ratones , Análisis de Secuencia por Matrices de Oligonucleótidos , PPAR alfa/deficiencia , PPAR alfa/genética , Daño por Reperfusión/genética , Privación de Sueño/genéticaRESUMEN
According to the IPCC, the global average temperature is likely to increase by 1.4-5.8 °C over the period from 1990 to 2100. In Polar regions, the magnitude of such climatic changes is even larger than in temperate and tropical biomes. This amplified response is particularly worrisome given that the so-far moderate warming is already impacting Arctic ecosystems. Predicting species responses to rapid warming in the near future can be informed by investigating past responses, as, like the rest of the planet, the Arctic experienced recurrent cycles of temperature increase and decrease (glacial-interglacial changes) in the past. In this study, we compare the response of two important prey species of the Arctic ecosystem, the collared lemming and the narrow-skulled vole, to Late Quaternary climate change. Using ancient DNA and Ecological Niche Modeling (ENM), we show that the two species, which occupy similar, but not identical ecological niches, show markedly different responses to climatic and environmental changes within broadly similar habitats. We empirically demonstrate, utilizing coalescent model-testing approaches, that collared lemming populations decreased substantially after the Last Glacial Maximum; a result consistent with distributional loss over the same period based on ENM results. Given this strong association, we projected the current niche onto future climate conditions based on IPCC 4.0 scenarios, and forecast accelerating loss of habitat along southern range boundaries with likely associated demographic consequences. Narrow-skulled vole distribution and demography, by contrast, was only moderately impacted by past climatic changes, but predicted future changes may begin to affect their current western range boundaries. Our work, founded on multiple lines of evidence suggests a future of rapidly geographically shifting Arctic small mammal prey communities, some of whom are on the edge of existence, and whose fate may have ramifications for the whole Arctic food web and ecosystem.
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Cambio Climático , Mamíferos/fisiología , Animales , Regiones Árticas , Modelos TeóricosRESUMEN
Ants of genus Formica demonstrate variation in social organization and represent model species for ecological, behavioral, evolutionary studies and testing theoretical implications of the kin selection theory. Subgeneric division of the Formica ants based on morphology has been questioned and remained unclear after an allozyme study on genetic differentiation between 13 species representing all subgenera was conducted. In the present study, the phylogenetic relationships within the genus were examined using mitochondrial DNA sequences of the cytochrome b and a part of the NADH dehydrogenase subunit 6. All 23 Formica species sampled in the Palaearctic clustered according to the subgeneric affiliation except F. uralensis that formed a separate phylogenetic group. Unlike Coptoformica and Formica s. str., the subgenus Serviformica did not form a tight cluster but more likely consisted of a few small clades. The genetic distances between the subgenera were around 10%, implying approximate divergence time of 5 Myr if we used the conventional insect divergence rate of 2% per Myr. Within-subgenus divergence estimates were 6.69% in Serviformica, 3.61% in Coptoformica, 1.18% in Formica s. str., which supported our previous results on relatively rapid speciation in the latter subgenus. The phylogeny inferred from DNA sequences provides a necessary framework against which the evolution of social traits can be compared. We discuss implications of inferred phylogeny for the evolution of social traits.
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Hormigas/genética , Citocromos b/genética , ADN Mitocondrial/genética , Paleontología , Filogenia , Animales , Secuencia de Bases , Evolución Molecular , Variación Genética , Haplotipos/genética , Funciones de Verosimilitud , Datos de Secuencia Molecular , Especificidad de la EspecieRESUMEN
Physical inactivity reduces mechanical load on the skeleton, which leads to losses of bone mass and strength in non-hibernating mammalian species. Although bears are largely inactive during hibernation, they show no loss in bone mass and strength. To obtain insight into molecular mechanisms preventing disuse bone loss, we conducted a large-scale screen of transcriptional changes in trabecular bone comparing winter hibernating and summer non-hibernating black bears using a custom 12,800 probe cDNA microarray. A total of 241 genes were differentially expressed (P < 0.01 and fold change >1.4) in the ilium bone of bears between winter and summer. The Gene Ontology and Gene Set Enrichment Analysis showed an elevated proportion in hibernating bears of overexpressed genes in six functional sets of genes involved in anabolic processes of tissue morphogenesis and development including skeletal development, cartilage development, and bone biosynthesis. Apoptosis genes demonstrated a tendency for downregulation during hibernation. No coordinated directional changes were detected for genes involved in bone resorption, although some genes responsible for osteoclast formation and differentiation (Ostf1, Rab9a, and c-Fos) were significantly underexpressed in bone of hibernating bears. Elevated expression of multiple anabolic genes without induction of bone resorption genes, and the down regulation of apoptosis-related genes, likely contribute to the adaptive mechanism that preserves bone mass and structure through prolonged periods of immobility during hibernation.
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Hibernación/genética , Ilion/anatomía & histología , Ilion/fisiología , Regulación hacia Arriba , Ursidae/fisiología , Animales , Apoptosis/genética , Vías Biosintéticas/genética , Resorción Ósea/genética , Expresión Génica , Perfilación de la Expresión Génica , Regulación de la Expresión Génica , Genes , Ilion/metabolismo , Masculino , Análisis de Secuencia por Matrices de Oligonucleótidos , Tamaño de los Órganos , Osteogénesis/genética , Ursidae/genética , Ursidae/metabolismoRESUMEN
Environmental processes govern demography, species movements, community turnover and diversification and yet in many respects these dynamics are still poorly understood at high latitudes. We investigate the combined effects of climate change and geography through time for a widespread Holarctic shrew, Sorex tundrensis. We include a comprehensive suite of closely related outgroup taxa and three independent loci to explore phylogeographic structure and historical demography. We then explore the implications of these findings for other members of boreal communities. The tundra shrew and its sister species, the Tien Shan shrew (Sorex asper), exhibit strong geographic population structure across Siberia and into Beringia illustrating local centres of endemism that correspond to Late Pleistocene refugia. Ecological niche predictions for both current and historical distributions indicate a model of persistence through time despite dramatic climate change. Species tree estimation under a coalescent process suggests that isolation between populations has been maintained across timeframes deeper than the periodicity of Pleistocene glacial cycling. That some species such as the tundra shrew have a history of persistence largely independent of changing climate, whereas other boreal species shifted their ranges in response to climate change, highlights the dynamic processes of community assembly at high latitudes.
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ADN Mitocondrial/genética , Evolución Molecular , Filogeografía , Musarañas/genética , Animales , Cambio Climático , Ecosistema , Variación Genética , Análisis de Secuencia de ADN , SiberiaRESUMEN
BACKGROUND: Hibernation is an adaptive strategy to survive in highly seasonal or unpredictable environments. The molecular and genetic basis of hibernation physiology in mammals has only recently been studied using large scale genomic approaches. We analyzed gene expression in the American black bear, Ursus americanus, using a custom 12,800 cDNA probe microarray to detect differences in expression that occur in heart and liver during winter hibernation in comparison to summer active animals. RESULTS: We identified 245 genes in heart and 319 genes in liver that were differentially expressed between winter and summer. The expression of 24 genes was significantly elevated during hibernation in both heart and liver. These genes are mostly involved in lipid catabolism and protein biosynthesis and include RNA binding protein motif 3 (Rbm3), which enhances protein synthesis at mildly hypothermic temperatures. Elevated expression of protein biosynthesis genes suggests induction of translation that may be related to adaptive mechanisms reducing cardiac and muscle atrophies over extended periods of low metabolism and immobility during hibernation in bears. Coordinated reduction of transcription of genes involved in amino acid catabolism suggests redirection of amino acids from catabolic pathways to protein biosynthesis. We identify common for black bears and small mammalian hibernators transcriptional changes in the liver that include induction of genes responsible for fatty acid ß oxidation and carbohydrate synthesis and depression of genes involved in lipid biosynthesis, carbohydrate catabolism, cellular respiration and detoxification pathways. CONCLUSIONS: Our findings show that modulation of gene expression during winter hibernation represents molecular mechanism of adaptation to extreme environments.
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Corazón/fisiología , Hibernación/fisiología , Hígado/fisiología , Ursidae/genética , Adaptación Fisiológica , Animales , ADN Complementario/genética , Perfilación de la Expresión Génica , Regulación de la Expresión Génica , Hibernación/genética , Masculino , Análisis de Secuencia por Matrices de Oligonucleótidos , Estaciones del Año , Ursidae/fisiologíaRESUMEN
Hibernating arctic ground squirrels (Urocitellus parryii), overwintering in frozen soils, maintain large gradients between ambient temperature (T(a)) and body temperature (T(b)) by substantially increasing metabolic rate during torpor while maintaining a subzero T(b). We used quantitative reverse-transcription PCR (qRT-PCR) to determine how the expression of 56 metabolic genes was affected by season (active in summer vs hibernating), metabolic load during torpor (imposed by differences in T(a): +2 vs -10°C) and hibernation state (torpid vs after arousal). Compared with active ground squirrels sampled in summer, liver from hibernators showed increased expression of genes associated with fatty acid catabolism (CPT1A, FABP1 and ACAT1), ketogenesis (HMGCS2) and gluconeogenesis (PCK1) and decreased expression of genes associated with fatty acid synthesis (ACACB, SCD and ELOVL6), amino acid metabolism, the urea cycle (PAH, BCKDHA and OTC), glycolysis (PDK1 and PFKM) and lipid metabolism (ACAT2). Stage of hibernation (torpid vs aroused) had a much smaller effect, with only one gene associated with glycogen synthesis (GSY1) in liver showing consistent differences in expression levels between temperature treatments. Despite the more than eightfold increase in energetic demand associated with defending T(b) during torpor at a T(a) of -10 vs +2°C, transcript levels in liver and brown adipose tissue differed little. Our results are inconsistent with a hypothesized switch to use of non-lipid fuels when ambient temperatures drop below freezing.
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Tejido Adiposo Pardo/fisiología , Metabolismo Energético/genética , Hibernación/genética , Hígado/fisiología , Sciuridae , Estaciones del Año , Temperatura , Animales , Regiones Árticas , Temperatura Corporal , Regulación de la Expresión Génica , Análisis de Componente Principal , Reacción en Cadena de la Polimerasa de Transcriptasa Inversa , Sciuridae/genética , Sciuridae/metabolismoRESUMEN
BACKGROUND: Global temperature increased by approximately half a degree (Celsius) within the last 150 years. Even this moderate warming had major impacts on Earth's ecological and biological systems, especially in the Arctic where the magnitude of abiotic changes even exceeds those in temperate and tropical biomes. Therefore, understanding the biological consequences of climate change on high latitudes is of critical importance for future conservation of the species living in this habitat. The past 25,000 years can be used as a model for such changes, as they were marked by prominent climatic changes that influenced geographical distribution, demographic history and pattern of genetic variation of many extant species. We sequenced ancient and modern DNA of the collared lemming (Dicrostonyx torquatus), which is a key species of the arctic biota, from a single site (Pymva Shor, Northern Pre Urals, Russia) to see if climate warming events after the Last Glacial Maximum had detectable effects on the genetic variation of this arctic rodent species, which is strongly associated with a cold and dry climate. RESULTS: Using three dimensional network reconstructions we found a dramatic decline in genetic diversity following the LGM. Model-based approaches such as Approximate Bayesian Computation and Markov Chain Monte Carlo based Bayesian inference show that there is evidence for a population decline in the collared lemming following the LGM, with the population size dropping to a minimum during the Greenland Interstadial 1 (Bølling/Allerød) warming phase at 14.5 kyrs BP. CONCLUSION: Our results show that previous climate warming events had a strong influence on genetic diversity and population size of collared lemmings. Due to its already severely compromised genetic diversity a similar population reduction as a result of the predicted future climate change could completely abolish the remaining genetic diversity in this population. Local population extinctions of collared lemmings would have severe effects on the arctic ecosystem, as collared lemmings are a key species in the trophic interactions and ecosystem processes in the Arctic.
Asunto(s)
Arvicolinae/genética , Clima , ADN/genética , Calentamiento Global , Animales , Regiones Árticas , ADN Mitocondrial/genética , Demografía , Flujo Génico/genética , Haplotipos/genética , Cubierta de Hielo , Modelos Genéticos , Filogenia , Federación de Rusia , Factores de TiempoRESUMEN
BACKGROUND: Species of the bear family (Ursidae) are important organisms for research in molecular evolution, comparative physiology and conservation biology, but relatively little genetic sequence information is available for this group. Here we report the development and analyses of the first large scale Expressed Sequence Tag (EST) resource for the American black bear (Ursus americanus). RESULTS: Comprehensive analyses of molecular functions, alternative splicing, and tissue-specific expression of 38,757 black bear EST sequences were conducted using the dog genome as a reference. We identified 18 genes, involved in functions such as lipid catabolism, cell cycle, and vesicle-mediated transport, that are showing rapid evolution in the bear lineage Three genes, Phospholamban (PLN), cysteine glycine-rich protein 3 (CSRP3) and Troponin I type 3 (TNNI3), are related to heart contraction, and defects in these genes in humans lead to heart disease. Two genes, biphenyl hydrolase-like (BPHL) and CSRP3, contain positively selected sites in bear. Global analysis of evolution rates of hibernation-related genes in bear showed that they are largely conserved and slowly evolving genes, rather than novel and fast-evolving genes. CONCLUSION: We provide a genomic resource for an important mammalian organism and our study sheds new light on the possible functions and evolution of bear genes.