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1.
J Exp Biol ; 2024 Sep 25.
Artigo em Inglês | MEDLINE | ID: mdl-39319364

RESUMO

Hummingbirds save energy by facultatively entering torpor, but the physiological mechanisms underlying this metabolic suppression are largely unknown. We compared whole-animal and pectoralis mitochondrial metabolism between torpid and normothermic ruby-throated hummingbirds (Archilochus colubris). When fasting, hummingbirds were exposed to 10℃ ambient temperature at night, they entered torpor; average body temperature decreased by nearly 25℃ (From ∼37 to ∼13℃), and whole-animal metabolic rate (VO2) decreased by 95% compared to normothermia, a much greater metabolic suppression compared with mammalian daily heterotherms. We then measured pectoralis mitochondrial oxidative phosphorylation (OXPHOS) fueled by either carbohydrate or fatty acid substrates at both 39℃ and 10℃ in torpid and normothermic hummingbirds. Aside from a 20% decrease in electron transport system complex I-supported respiration with pyruvate, the capacity for OXPHOS at a common in vivo temperature did not differ in isolated mitochondria between torpor and normothermia. Similarly, the activities of pectoralis pyruvate dehydrogenase and 3-hydroxyacyl-CoA dehydrogenase did not differ between the states. Unlike heterothermic mammals, hummingbirds do not suppress muscle mitochondrial metabolism in torpor by active, temperature-independent mechanisms. Other mechanisms that may underly this impressive whole-animal metabolic suppression include decreasing ATP demand or relying on rapid passive cooling facilitated by the very small body size of A. colubris.

2.
J Exp Biol ; 2024 Sep 25.
Artigo em Inglês | MEDLINE | ID: mdl-39319380

RESUMO

The Thrifty Female Hypothesis states that females preserve more of their energy reserves during winter than males because of the sex-specific time frame of energy allocation for reproduction. As males reactivate their reproductive axis before the mating period, while females mainly allocate energy during gestation and lactation, we hypothesized that males would have to use shorter torpor bouts and longer periods of normothermic activity to promote spermatogenesis during winter, a period of low food availability. Here, we applied an acute two-week 80% caloric restriction in male and female gray mouse lemurs shortly before the mating period. We found evidence of thriftier phenotypes in wintering females, which performed deeper and longer torpor bouts than males and ultimately lost less body mass. Our results thus support the thrifty female hypothesis in a seasonally breeding primate and reinforce the concept of a sex-biased trade-off in using torpor, which might ultimately benefit reproduction and survival.

3.
Biol Lett ; 20(9): 20240291, 2024 Sep.
Artigo em Inglês | MEDLINE | ID: mdl-39288816

RESUMO

Hibernators face an energetic dilemma in the autumn at northern latitudes; while temperatures and food availability decrease, hibernating species need to build fat deposits to survive the winter. During this critical fattening phase, insectivorous boreal bats use torpor to build and conserve their reserves. However, we still know little about temporal variability in torpor use employed by bats during the prehibernation fattening period and how decreasing temperatures and food availability in combination with increasing individual body mass impact this. Here, we present two general hypotheses for explaining temporal torpor patterns observed in a boreal bat (Eptesicus nilssonii), in which torpor use (i) facilitates rapid mass gain or (ii) conserves stored body mass. Although temporally separated in our dataset, data on temperature, insect abundance and body mass throughout the prehibernation period indicate that E. nilssonii reaches the majority of its overwintering mass before the onset of increasing daytime and night-time torpor use. In combination with low food availability by this point in time, these observations suggest torpor expression may be intended to conserve gained reserves rather than facilitate mass gain. Our study is intended as a first proof of concept for disentangling temporal drivers of torpor in bats during the prehibernation fattening phase.


Assuntos
Quirópteros , Hibernação , Torpor , Animais , Quirópteros/fisiologia , Torpor/fisiologia , Hibernação/fisiologia , Estações do Ano , Peso Corporal
4.
J Therm Biol ; 124: 103933, 2024 Aug.
Artigo em Inglês | MEDLINE | ID: mdl-39208468

RESUMO

To assess the vulnerability of birds and mammals to climate change recent studies have used the upper critical limit of thermoneutrality (TUC) as an indicator of thermal tolerance. But, the association between TUC and thermal tolerance is not straightforward and most studies describe TUC based solely on a deviation in metabolism from basal levels, without also considering the onset of evaporative cooling. It was argued recently that certain torpor-using bat species who survived prolonged exposure to high ambient temperatures (i.e. high thermal tolerance) experienced during extreme heat events did so by entering torpor and using facultative heterothermy to thermoconform and save on body water. Assuming that TUC is indicative of thermal tolerance, we expect TUC in torpor-using species to be higher than that of species which are obligate homeotherms, albeit that this distinction is based on confirmation of torpor use at low temperatures. To test this prediction, we performed a phylogenetically informed comparison of bat species known to use torpor (n = 48) and homeothermic (n = 16) bat species using published thermoregulatory datasets to compare the lower critical limit of thermoneutrality (TLC) and TUC in relation to body temperature. The influence of diet, biogeographical region, body mass and basal metabolic rate (BMR) was also considered. Body mass had a positive relationship with BMR, an inverse relationship with TLC and no relationship with TUC. Normothermic body temperature scaled positively with BMR, TLC and TUC. There was no relationship between diet or region and BMR, but both influenced thermal limits. Torpor-using bats had lower body mass and body temperatures than homeothermic bats, but there was no difference in BMR, TLC and TUC between them. Exceptional examples of physiological flexibility were observed in 34 torpor-using species and eight homeothermic species, which included 15 species of bats maintaining BMR-level metabolism at ambient temperatures as high as 40 °C (and corresponding body temperatures ∼39.2 °C). However, we argue that TUC based on metabolism alone is not an appropriate indicator of thermal tolerance as it disregards differences in the ability of animals to tolerate higher levels of hyperthermia, importance of hydration status and capacity for evaporative cooling. Also, the variability in TUC based on diet challenges the idea of evolutionary conservatism and warrants further consideration.


Assuntos
Quirópteros , Termotolerância , Quirópteros/fisiologia , Animais , Torpor/fisiologia , Metabolismo Basal , Regulação da Temperatura Corporal , Temperatura Corporal
5.
ACS Nano ; 18(35): 23991-24003, 2024 Sep 03.
Artigo em Inglês | MEDLINE | ID: mdl-39167921

RESUMO

Achieving a reversible decrease of metabolism and other physiological processes in the whole organism, as occurs in animals that experience torpor or hibernation, could contribute to increased survival after serious injury. Using a Bayesian network tool with transcriptomic data and chemical structure similarity assessments, we predicted that the Alzheimer's disease drug donepezil (DNP) could be a promising candidate for a small molecule drug that might induce a torpor-like state. This was confirmed in a screening study with Xenopus laevis tadpoles, a nonhibernator whole animal model. To improve the therapeutic performance of the drug and minimize its toxicity, we encapsulated DNP in a nanoemulsion formulated with low-toxicity materials. This formulation is composed of emulsified droplets <200 nm in diameter that contain 1.250 mM DNP, representing ≥95% encapsulation efficiency. The DNP nanoemulsion induced comparable torpor-like effects to those produced by the free drug in tadpoles, as indicated by reduced swimming motion, cardiac beating frequency, and oxygen consumption, but with an improved biodistribution. Use of the nanoemulsion resulted in a more controlled increase of DNP concentration in the whole organism compared to free DNP, and to a higher concentration in the brain, which reduced DNP toxicity and enabled induction of a longer torpor-like state that was fully reversible. These studies also demonstrate the potential use of Xenopus tadpoles as a high-throughput in vivo screen to assess the efficacy, biodistribution, and toxicity of drug-loaded nanocarriers.


Assuntos
Donepezila , Emulsões , Larva , Xenopus laevis , Animais , Emulsões/química , Larva/efeitos dos fármacos , Donepezila/farmacologia , Donepezila/química , Nanopartículas/química , Tamanho da Partícula
6.
Ann N Y Acad Sci ; 2024 Aug 13.
Artigo em Inglês | MEDLINE | ID: mdl-39137248

RESUMO

The dwarf lemurs (Cheirogaleus spp.) of Madagascar are the only obligate hibernators among primates. Despite century-old field accounts of seasonal lethargy, and more recent evidence of hibernation in the western fat-tailed dwarf lemur (Cheirogaleus medius), inducing hibernation in captivity remained elusive for decades. This included the Duke Lemur Center (DLC), which maintains fat-tailed dwarf lemurs and has produced sporadic research on reproduction and metabolism. With cumulative knowledge from the field, a newly robust colony, and better infrastructure, we recently induced hibernation in DLC dwarf lemurs. We describe two follow-up experiments in subsequent years. First, we show that dwarf lemurs under stable cold conditions (13°C) with available food continued to eat daily, expressed shallower and shorter torpor bouts, and had a modified gut microbiome compared to peers without food. Second, we demonstrate that dwarf lemurs under fluctuating temperatures (12-30°C) can passively rewarm daily, which was associated with altered patterns of fat depletion and reduced oxidative stress. Despite the limitations of working with endangered primates, we highlight the promise of studying hibernation in captive dwarf lemurs. Follow-up studies on genomics and epigenetics, metabolism, and endocrinology could have relevance across multidisciplinary fields, from biomedicine to evolutionary biology, and conservation.

7.
Proc Biol Sci ; 291(2026): 20240855, 2024 Jul.
Artigo em Inglês | MEDLINE | ID: mdl-38981523

RESUMO

Understanding how animals meet their daily energy requirements is critical in our rapidly changing world. Small organisms with high metabolic rates can conserve stored energy when food availability is low or increase energy intake when energetic requirements are high, but how they balance this in the wild remains largely unknown. Using miniaturized heart rate transmitters, we continuously quantified energy expenditure, torpor use and foraging behaviour of free-ranging male bats (Nyctalus noctula) in spring and summer. In spring, bats used torpor extensively, characterized by lowered heart rates and consequently low energy expenditures. In contrast, in summer, bats consistently avoided torpor, even though they could have used this low-energy mode. As a consequence, daytime heart rates in summer were three times as high compared with the heart rates in spring. Daily energy use increased by 42% during summer, despite lower thermogenesis costs at higher ambient temperatures. Likely, as a consequence, bats nearly doubled their foraging duration. Overall, our results indicate that summer torpor avoidance, beneficial for sperm production and self-maintenance, comes with a high energetic cost. The ability to identify and monitor such vulnerable energetic life-history stages is particularly important to predict how species will deal with increasing temperatures and changes in their resource landscapes.


Assuntos
Quirópteros , Metabolismo Energético , Frequência Cardíaca , Estações do Ano , Animais , Masculino , Quirópteros/fisiologia , Torpor/fisiologia
8.
Proc Biol Sci ; 291(2026): 20241137, 2024 Jul.
Artigo em Inglês | MEDLINE | ID: mdl-38981525

RESUMO

Torpor is widespread among bats presumably because most species are small, and torpor greatly reduces their high mass-specific resting energy expenditure, especially in the cold. Torpor has not been recorded in any bat species larger than 50 g, yet in theory could be beneficial even in the world's largest bats (flying-foxes; Pteropus spp.) that are exposed to adverse environmental conditions causing energy bottlenecks. We used temperature telemetry to measure body temperature in wild-living adult male grey-headed flying-foxes (P. poliocephalus; 799 g) during winter in southern Australia. We found that all individuals used torpor while day-roosting, with minimum body temperature reaching 27°C. Torpor was recorded following a period of cool, wet and windy weather, and on a day with the coldest maximum air temperature, suggesting it is an adaptation to reduce energy expenditure during periods of increased thermoregulatory costs and depleted body energy stores. A capacity for torpor among flying-foxes has implications for understanding their distribution, behavioural ecology and life history. Furthermore, our discovery increases the body mass of bats known to use torpor by more than tenfold and extends the documented use of this energy-saving strategy under wild conditions to all bat superfamilies, with implications for the evolutionary maintenance of torpor among bats and other mammals.


Assuntos
Quirópteros , Torpor , Animais , Quirópteros/fisiologia , Torpor/fisiologia , Masculino , Metabolismo Energético , Telemetria , Temperatura Corporal , Estações do Ano , Austrália do Sul
9.
Ecology ; 105(9): e4384, 2024 Sep.
Artigo em Inglês | MEDLINE | ID: mdl-39039740

RESUMO

Seasonal variation in animal activity influences fitness and the intensity of ecological interactions (e.g., competition, predation), yet aspects of global change in the Anthropocene may catalyze shifts in seasonal activity. Invasive plants are components of global change and can modify animal daily activity, but their influence on animal seasonal activity is less understood. We examined how invasive woody shrubs (Autumn olive [Elaeagnus umbellata] and Amur honeysuckle [Lonicera maackii]) affect seasonal activity of three common small-mammal species by coupling experimental shrub removal with autumnal camera trapping for two consecutive years at six paired forest sites (total 12 plots). Eastern chipmunks (Tamias striatus) foraged more, and foraging was observed at least 20 days longer, in shrub-invaded forests. White-footed mice (Peromyscus leucopus) foraged more in invaded than cleared plots in one study year, but P. leucopus autumn activity timing did not differ between shrub-removal treatments. Fox squirrel (Sciurus niger) activity displayed year-specific responses to shrub removal suggesting intraannual cues (e.g., temperature) structure S. niger autumnal activity. Our work highlights how plant invasions can have species-specific effects on seasonal animal activity, may modify the timing of physiological processes (e.g., torpor), and could generate variation in animal-mediated interactions such as seed dispersal or granivory.


Assuntos
Espécies Introduzidas , Lonicera , Estações do Ano , Animais , Lonicera/fisiologia , Sciuridae/fisiologia , Elaeagnaceae/fisiologia , Especificidade da Espécie , Comportamento Alimentar
10.
J Therm Biol ; 123: 103909, 2024 Jul.
Artigo em Inglês | MEDLINE | ID: mdl-39084175

RESUMO

Fine-scale variation in microclimates between habitats may impact energy consumption for the organisms that inhabit them. This may be particularly important for sedentary species or those unable to change habitats for long periods, such as hibernators. Low ambient temperatures were traditionally thought key to microclimatic selection for hibernation locations, but recent research suggests that other factors may contribute or exceed ambient temperature in importance. We aimed to characterise microclimates at hibernacula of wild hibernating hazel dormice Muscardinus avellanarius, and test how these microclimates differ to those at locations without hibernacula using a microclimatic modelling approach. Dormice hibernated in areas with warmer soil temperatures and lower variability in humidity and relative shortwave radiation. These results add to the growing body of evidence that low ambient temperatures may not be the primary driver of hibernation microclimate selection, although temperature is still likely to play an important role. We also found that ambient temperatures measured at the microclimatic level were substantially buffered compared to point samples taken at the nearest weather station (∼1.6 km away), highlighting the importance of considering microclimates in wildlife conservation in the face of future environmental change.


Assuntos
Hibernação , Microclima , Animais , Hibernação/fisiologia , Estações do Ano , Temperatura , Myoxidae/fisiologia , Comportamento de Nidação , Ecossistema
11.
J Mammal ; 105(4): 823-837, 2024 Aug.
Artigo em Inglês | MEDLINE | ID: mdl-39081265

RESUMO

Although Mexico holds the southernmost hibernating bats in North America, information on winter behavior and hibernacula microclimate use of temperate Mexican bats is limited. We studied hibernating bats at high altitudes (>1,000 m a.s.l.) in northern and central Mexico during 5 consecutive winters. Our aims were to document and describe the hibernacula, winter behavior (such as abundance and roost pattern), and microclimates (estimated as adjacent substrate temperature) of cave-hibernating bats in Mexico. We found 78 hibernacula and 6,089 torpid bats of 10 vespertilionid species, increasing by over 50% the number of cave-hibernating bat species and quadrupling the number of hibernacula for Mexico. Hibernacula were at altitudes between 1,049 and 3,633 m a.s.l., located in 3 mountain ranges, mainly in oak and conifer forests. Myotis velifer was the most common species, followed by Corynorhinus townsendii and C. mexicanus. We recorded the adjacent substrate temperatures from 9 species totaling 1,106 torpid bats and found differences in microclimate use among the 3 most common species. In general, abundance of torpid bats in our region of study was similar to those in the western United States, with aggregations of tens to a few hundred individuals per cave, and was lower than in the eastern United States where a cave may hold thousands of individuals. Knowledge of bat hibernation is crucial for developing conservation and management strategies on current conditions while accommodating environmental changes and other threats such as emerging diseases.


Aunque México tiene los murciélagos hibernantes más sureños en Norteamérica, la información sobre el comportamiento invernal y el uso de microclimas en los refugios de hibernación de los murciélagos templados mexicanos es limitada. Estudiamos a los murciélagos hibernantes en altitudes altas (>1000 msnm) en el norte y centro de México durante cinco inviernos consecutivos. Nuestros objetivos fueron documentar y describir las cuevas de hibernación, el comportamiento invernal (como la abundancia y patrón de percha), y el uso de microclimas (estimado como la temperatura del sustrato adyacente), de los murciélagos que hibernan en cuevas en México. Encontramos 78 cuevas de hibernación con 6089 murciélagos en torpor de 10 especies de vespertiliónidos, incrementando en más del 50% el número de especies de murciélagos que hibernan en cuevas y cuadriplicando el número de cuevas de hibernación para México. Las cuevas de hibernación estuvieron en elevaciones entre 1049 y 3633 msnm, localizadas en tres cadenas montañosas, principalmente en bosques de encinos y coníferas. Myotis velifer fue la especie más común, seguida por Corynorhinus townsendii y C. mexicanus. Reportamos las temperaturas del sustrato adyacente de 1106 murciélagos en torpor de nueve especies y encontramos diferencias en el uso de microclimas entre las tres especies más comunes. Aquí proveemos información relevante para especies de murciélagos templados en la ocurrencia más sureña de hibernación de murciélagos en Norteamérica. En general, la abundancia de murciélagos en torpor que encontramos fue similar a las del oeste de Estados Unidos, con agregaciones de decenas y algunos cientos de individuos por cueva; y fue menor que las del este de Estados Unidos, donde las cuevas pueden albergar miles de murciélagos. El conocimiento de la hibernación de murciélagos es crucial para el desarrollo de estrategias de conservación y manejo adecuadas en la actualidad y mientras se adaptan a los cambios ambientales y a otras amenazas tales como las enfermedades emergentes.

12.
Acta Neuropathol Commun ; 12(1): 86, 2024 06 04.
Artigo em Inglês | MEDLINE | ID: mdl-38835043

RESUMO

Tau protein hyperphosphorylation and aggregation are key pathological events in neurodegenerative tauopathies such as Alzheimer's disease. Interestingly, seasonal hibernators show extensive tau hyperphosphorylation during torpor, i.e., the hypothermic and hypometabolic state of hibernation, which is completely reversed during arousal. Torpor-associated mechanisms that reverse tau hyperphosphorylation may be of therapeutic relevance, however, it is currently not known to what extent they apply to human tau. Here we addressed this issue using daily torpor in wildtype mice that express mouse tau (mtau) and in mice that lack mtau expression and instead express human tau (htau). AT8, AT100 and Ser396 immunoblotting and immunohistochemistry were used to assess tau (hyper)phosphorylation at clinically relevant phosphorylation sites. We found that torpor robustly and reversibly increases the levels of phosphorylated tau in both mtau and htau mice. Immunohistochemistry revealed four brain areas that show prominent tau phosphorylation: the hippocampus, posterior parietal cortex, piriform cortex and cortical amygdala. Whereas wildtype mice primarily showed increased levels of diffusely organized hyperphosphorylated tau during torpor, htau mice contained clear somato-dendritic accumulations of AT8 reactivity resembling tau pre-tangles as observed in the Alzheimer brain. Interestingly, AT8-positive accumulations disappeared upon arousal, and tau phosphorylation levels at 24 h after arousal were lower than observed at baseline, suggesting a beneficial effect of torpor-arousal cycles on preexisting hyperphosphorylated tau. In conclusion, daily torpor in mice offers a quick and standardized method to study tau phosphorylation, accumulation and clearance in mouse models relevant for neurodegeneration, as well as opportunities to discover new targets for the treatment of human tauopathies.


Assuntos
Encéfalo , Camundongos Transgênicos , Torpor , Proteínas tau , Animais , Humanos , Masculino , Camundongos , Encéfalo/metabolismo , Camundongos Endogâmicos C57BL , Fosforilação , Proteínas tau/metabolismo , Proteínas tau/genética , Torpor/fisiologia
13.
J Physiol Sci ; 74(1): 33, 2024 Jun 12.
Artigo em Inglês | MEDLINE | ID: mdl-38867187

RESUMO

Hibernation and torpor are not passive responses caused by external temperature drops and fasting but are active brain functions that lower body temperature. A population of neurons in the preoptic area was recently identified as such active torpor-regulating neurons. We hypothesized that the other hypothermia-inducing maneuvers would also activate these neurons. To test our hypothesis, we first refined the previous observations, examined the brain regions explicitly activated during the falling phase of body temperature using c-Fos expression, and confirmed the preoptic area. Next, we observed long-lasting hypothermia by reactivating torpor-tagged Gq-expressing neurons using the activity tagging and DREADD systems. Finally, we found that about 40-60% of torpor-tagged neurons were activated by succeeding isoflurane anesthesia and by icv administration of an adenosine A1 agonist. Isoflurane-induced and central adenosine-induced hypothermia is, at least in part, an active process mediated by the torpor-regulating neurons in the preoptic area.


Assuntos
Adenosina , Isoflurano , Neurônios , Área Pré-Óptica , Animais , Área Pré-Óptica/efeitos dos fármacos , Área Pré-Óptica/metabolismo , Isoflurano/farmacologia , Isoflurano/administração & dosagem , Adenosina/administração & dosagem , Adenosina/farmacologia , Adenosina/metabolismo , Neurônios/efeitos dos fármacos , Neurônios/metabolismo , Neurônios/fisiologia , Masculino , Anestésicos Inalatórios/farmacologia , Anestésicos Inalatórios/administração & dosagem , Temperatura Corporal/efeitos dos fármacos , Temperatura Corporal/fisiologia , Hipotermia/induzido quimicamente , Hipotermia/metabolismo , Torpor/efeitos dos fármacos , Camundongos , Proteínas Proto-Oncogênicas c-fos/metabolismo
14.
Ecol Evol Physiol ; 97(3): 180-189, 2024.
Artigo em Inglês | MEDLINE | ID: mdl-38875137

RESUMO

AbstractDuring periods of torpor, hibernators can reduce metabolic rate (MR) and body temperature (Tb) substantially. However, to avoid physiological dysfunction at low temperatures, they defend Tb at a critical minimum, often between ~0°C and 10°C via an increase in MR. Because thermoregulation during torpor requires extra energy, individuals with lower Tb's and thus minimal MR during torpor should be selected in colder climates. Such inter- and intraspecific variations occur in some placental mammals, but for the evolutionary separate marsupials, available information is scarce. Marsupial eastern pygmy possums (Cercartetus nanus; ~22 g body mass), widely distributed along the Australian southeastern coast including subtropical to alpine areas, were used to test the hypothesis that the defended Tb of torpid individuals is related to the climate of their habitat. Possums were captured from five regions, 1,515 km apart, with midwinter (July) minimum environmental temperatures (min Tenv's) ranging from -3.9°C to 6.6°C. Captive possums in deep torpor were slowly cooled with ambient temperature (Ta), while their MR was measured to determine the minimum torpor metabolic rate (TMR), the Ta at which their MR increased for thermoregulation (min Ta), and the corresponding minimum Tb (min Tb). Partial least squares regression analysis revealed that Ta and Tenv were the strongest explanatory variables for the min Tb. The min Tb and Ta were also correlated with latitude but not elevation of the capture sites. However, the best correlations were observed between the min Tenv and the min Tb and Ta for individuals experiencing min Tenv>0°C; these individuals thermoconformed to min Ta's between -0.8°C and 3.7°C, and their min Tb ranged from 0.5°C to 6.0°C and was 0.5°C-2.6°C below the min Tenv at the capture site. In contrast, individuals experiencing a min Tenv of -3.9°C regulated Tb at 0.6°C±0.2°C or 4.5°C above the Tenv. The minimum TMR of all possums did not differ with Ta and thus did not differ among populations and was 2.6% of the basal MR. These data provide new evidence that thermal variables of marsupials are subject to regional intraspecific variation. It suggests that min Tb is a function of the min Tenv but only above 0°C, perhaps because the Tb-Ta differential for torpid possums in the wild, at a min Tenv of -3.9°C, remains small enough to be compensated by a small increase in MR and does not require the physiological capability for a reduction of Tb below 0°C.


Assuntos
Regulação da Temperatura Corporal , Animais , Regulação da Temperatura Corporal/fisiologia , Metabolismo Basal/fisiologia , Hibernação/fisiologia , Marsupiais/fisiologia , Austrália , Temperatura Corporal/fisiologia , Temperatura , Especificidade da Espécie , Feminino
15.
Ecol Evol ; 14(6): e11579, 2024 Jun.
Artigo em Inglês | MEDLINE | ID: mdl-38932950

RESUMO

Maintenance metabolism as the minimum energy expenditure needed to maintain homeothermy (a high and stable body temperature, T b), reflects the magnitude of metabolic machinery and the associated costs of self-maintenance in endotherms (organisms able to produce heat endogenously). Therefore, it can interact with most, if not all, organismal functions, including the behavior-fitness linkage. Many endothermic animals can avoid the costs of maintaining homeothermy and temporally reduce T b and metabolism by entering heterothermic states like torpor, the most effective energy-saving strategy. Variations in BMR, behavior, and torpor use are considered to be shaped by food resources, but those conclusions are based on research studying these traits in isolation. We tested the effect of ecological contexts (food availability and predation risk) on the interplay between the maintenance costs of homeothermy, heterothermy, and exploration in a wild mammal-the yellow-necked mouse. We measured maintenance metabolism as basal metabolic rate (BMR) using respirometry, distance moved (exploration) in the open-field test, and variation in T b (heterothermy) during short-term fasting in animals captured at different locations of known natural food availability and predator presence, and with or without supplementary food resources. We found that in winter, heterothermy and exploration (but not BMR) negatively correlated with natural food availability (determined in autumn). Supplementary feeding increased mouse density, predation risk and finally had a positive effect on heterothermy (but not on BMR or exploration). The path analysis testing plausible causal relationships between the studied traits indicated that elevated predation risk increased heterothermy, which in turn negatively affected exploration, which positively correlated with BMR. Our study indicates that adaptive heterothermy is a compensation strategy for balancing the energy budget in endothermic animals experiencing low natural food availability. This study also suggests that under environmental challenges like increased predation risk, the use of an effective energy-saving strategy predicts behavioral expression better than self-maintenance costs under homeothermy.

16.
Physiol Genomics ; 56(8): 555-566, 2024 Aug 01.
Artigo em Inglês | MEDLINE | ID: mdl-38881427

RESUMO

Thirteen-lined ground squirrels (TLGSs) are obligate hibernators that cycle between torpor (low metabolic rate and body temperature) and interbout euthermia (IBE; typical euthermic body temperature and metabolism) from late autumn to spring. Many physiological changes occur throughout hibernation, including a reduction in liver mitochondrial metabolism during torpor, which is reversed during arousal to interbout euthermia. Nuclear-encoded microRNA (miRNA, small posttranscriptional regulator molecules) differ in abundance throughout TLGS hibernation and have been shown to regulate mitochondrial gene expression in mammalian cell culture (where they are referred to as mitomiRs). This study characterized differences in mitomiR profiles from TLGS liver mitochondria isolated during summer, torpor, and IBE, and predicted their mitochondrial targets. Using small RNA sequencing, differentially abundant mitomiRs were identified between hibernation states, and using quantitative PCR analysis, we quantified the expression of predicted mitochondrial mRNA targets. Most differences in mitomiR abundances were seasonal (i.e., between summer and winter) with only one mitomiR differentially abundant between IBE and torpor. Multiple factor analysis (MFA) revealed three clusters divided by hibernation states, where clustering was predominantly driven by mitomiR abundances. Nine of these differentially abundant mitomiRs had predicted mitochondrial RNA targets, including subunits of electron transfer system complexes I and IV, 12S rRNA, and two tRNAs. Overall, mitomiRs were predicted to suppress the expression of their mitochondrial targets and may have some involvement in regulating protein translation in mitochondria. This study found differences in mitomiR abundances between seasons and hibernation states of TLGS and suggests potential mechanisms for regulating the mitochondrial electron transfer system.NEW & NOTEWORTHY During the hibernation season, thirteen-lined ground squirrels periodically increase metabolism remarkably between torpor and interbout euthermia (IBE). This process involves rapid reactivation of mitochondrial respiration. We predicted that mitochondrial microRNA (mitomiRs) might be altered during this response. We found that the abundance of 38 liver mitomiRs differs based on hibernation state (summer, IBE, and torpor). Small RNA sequencing identified mitomiR profiles, including some mitomiRs that are predicted to bind to mitochondrial RNAs.


Assuntos
Hibernação , MicroRNAs , Sciuridae , Animais , Sciuridae/genética , Hibernação/genética , MicroRNAs/genética , MicroRNAs/metabolismo , Estações do Ano , Torpor/genética , Mitocôndrias/genética , Mitocôndrias/metabolismo , Mitocôndrias Hepáticas/metabolismo , Mitocôndrias Hepáticas/genética
17.
Biochimie ; 225: 40-48, 2024 Oct.
Artigo em Inglês | MEDLINE | ID: mdl-38705508

RESUMO

During the hibernation season, the thirteen-lined ground squirrel undergoes cyclical torpor and arousal periods. The decrease and restoration of metabolic rate and oxygen delivery during torpor and arousal, respectively, may cause reperfusion-ischemia injury in the kidneys. In order to maintain the structural integrity of the kidneys necessary for renal function resumption during arousal, the thirteen-lined ground squirrel has developed adaptive methods to prevent and repair kidney injury. In this present study, computational methods were used to clean and analyze sequenced kidney RNA samples. Significantly differentially expressed microRNAs and enriched gene sets were also determined. From the gene set analysis, the results showed an increase in ubiquitin-related processes and p53 signaling pathways which suggested the occurrence of kidney damage during torpor. There was also an observed increase in cell cycle processes and the anchoring junction cellular compartment which may lend to the prevention of kidney injury. From the differentially expressed microRNAs, miR-27a (log2FC = 1.639; p-value = 0.023), miR-129 (log2FC = 2.516; p-value = 0.023), miR-let-7b (log2FC = 2.360; p-value = 0.025), miR-let-7c (log2FC = 2.291; p-value = 0.037) and miR-let-7i (log2FC = 1.564; p-value = 0.039) were found to be significantly upregulated. These biochemical adaptations may allow the thirteen-lined ground squirrel to maintain kidney structure and function during hibernation.


Assuntos
Rim , MicroRNAs , Traumatismo por Reperfusão , Sciuridae , Animais , MicroRNAs/genética , MicroRNAs/metabolismo , Traumatismo por Reperfusão/metabolismo , Traumatismo por Reperfusão/genética , Rim/metabolismo , Torpor , Regulação da Expressão Gênica , Hibernação
18.
Front Physiol ; 15: 1377986, 2024.
Artigo em Inglês | MEDLINE | ID: mdl-38725569

RESUMO

Most mammals adapt thermal physiology around 37°C and large deviations from their range, as observed in severe hypothermia and hyperthermia, resulting in organ dysfunction and individual death. A prominent exception is mammalian hibernation. Mammalian hibernators resist the long-term duration of severe low body temperature that is lethal to non-hibernators, including humans and mice. This cold resistance is supported, at least in part, by intrinsic cellular properties, since primary or immortalized cells from several hibernator species can survive longer than those from non-hibernators when cultured at cold temperatures. Recent studies have suggested that cold-induced cell death fulfills the hallmarks of ferroptosis, a type of necrotic cell death that accompanies extensive lipid peroxidation by iron-ion-mediated reactions. In this review, we summarize the current knowledge of cold resistance of mammalian hibernators at the cellular and molecular levels to organ and systemic levels and discuss key pathways that confer cold resistance in mammals.

19.
J Comp Physiol B ; 194(3): 383-401, 2024 Jun.
Artigo em Inglês | MEDLINE | ID: mdl-38733409

RESUMO

Vocalisations are increasingly being recognised as an important aspect of normal rodent behaviour yet little is known of how they interact with other spontaneous behaviours such as sleep and torpor, particularly in a social setting. We obtained chronic recordings of the vocal behaviour of adult male and female Djungarian hamsters (Phodopus sungorus) housed under short photoperiod (8 h light, 16 h dark, square wave transitions), in different social contexts. The animals were kept in isolation or in same-sex sibling pairs, separated by a grid which allowed non-physical social interaction. On approximately 20% of days hamsters spontaneously entered torpor, a state of metabolic depression that coincides with the rest phase of many small mammal species in response to actual or predicted energy shortages. Animals produced ultrasonic vocalisations (USVs) with a peak frequency of 57 kHz in both social and asocial conditions and there was a high degree of variability in vocalisation rate between subjects. Vocalisation rate was correlated with locomotor activity across the 24-h light cycle, occurring more frequently during the dark period when the hamsters were more active and peaking around light transitions. Solitary-housed animals did not vocalise whilst torpid and animals remained in torpor despite overlapping with vocalisations in social-housing. Besides a minor decrease in peak USV frequency when isolated hamsters were re-paired with their siblings, changing social contexts did not influence vocalisation behaviour or structure. In rare instances, temporally overlapping USVs occurred when animals were socially-housed and were grouped in such a way that could indicate coordination. We did not observe broadband calls (BBCs) contemporaneous with USVs in this paradigm, corroborating their correlation with physical aggression which was absent from our experiment. Overall, we find little evidence to suggest a direct social function of hamster USVs. We conclude that understanding the effects of vocalisations on spontaneous behaviours, such as sleep and torpor, will inform experimental design of future studies, especially where the role of social interactions is investigated.


Assuntos
Ritmo Circadiano , Phodopus , Fotoperíodo , Vocalização Animal , Animais , Vocalização Animal/fisiologia , Masculino , Phodopus/fisiologia , Feminino , Ritmo Circadiano/fisiologia , Cricetinae , Atividade Motora/fisiologia , Fenótipo , Torpor/fisiologia , Ultrassom , Estações do Ano , Comportamento Social
20.
Front Neuroanat ; 18: 1334206, 2024.
Artigo em Inglês | MEDLINE | ID: mdl-38686173

RESUMO

Hibernating animals demonstrate a remarkable ability to withstand extreme physiological brain changes without triggering adverse neuroinflammatory responses. While hibernators may offer valuable insights into the neuroprotective mechanisms inherent to hibernation, studies using such species are constrained by the limited availability of molecular tools. Laboratory mice may serve as an alternative, entering states of hypometabolism and hypothermia similar to the torpor observed in hibernation when faced with energy shortage. Notably, prolonged calorie restriction (CR) induces serial daily torpor patterns in mice, comparable to species that utilize daily hibernation. Here, we examined the neuroinflammatory response in the hippocampus of male C57BL/6 mice undergoing serial daily torpor induced by a 30% CR for 4 weeks. During daily torpor episodes, CR mice exhibited transient increases in TNF-α mRNA expression, which normalized upon arousal. Concurrently, the CA1 region of the hippocampus showed persistent morphological changes in microglia, characterized by reduced cell branching, decreased cell complexity and altered shape. Importantly, these morphological changes were not accompanied by evident signs of astrogliosis or oxidative stress, typically associated with detrimental neuroinflammation. Collectively, the adaptive nature of the brain's inflammatory response to CR-induced torpor in mice parallels observations in hibernators, highlighting its value for studying the mechanisms of brain resilience during torpor. Such insights could pave the way for novel therapeutic interventions in stroke and neurodegenerative disorders in humans.

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