BackgroundHuddling is highly evolved as a cooperative behavioral strategy for social mammals to maximize their fitness in harsh environments. Huddling behavior can change psychological and physiological responses. The coevolution of mammals with their microbial communities confers fitness benefits to both partners. The gut microbiome is a key regulator of host immune and metabolic functions. We hypothesized that huddling behavior altered energetics and thermoregulation by shaping caecal microbiota in small herbivores. Brandt’s voles (Lasiopodomys brandtii) were maintained in a group (huddling) or as individuals (separated) and were exposed to warm (23 ± 1 °C) and cold (4 ± 1 °C) air temperatures (Ta).ResultsVoles exposed to cold Ta had higher energy intake, resting metabolic rate (RMR) and nonshivering thermogenesis (NST) than voles exposed to warm Ta. Huddling voles had lower RMR and NST than separated voles in cold. In addition, huddling voles had a higher surface body temperature (Tsurface), but lower core body temperature (Tcore) than separated voles, suggesting a lower set-point of Tcore in huddling voles. Both cold and huddling induced a marked variation in caecal bacterial composition, which was associated with the lower Tcore. Huddling voles had a higher α and β-diversity, abundance of Lachnospiraceae and Veillonellaceae, but lower abundance of Cyanobacteria, Tenericutes, TM7, Comamonadaceae, and Sinobacteraceae than separated voles. Huddling or cold resulted in higher concentrations of short-chain fatty acids (SCFAs), particularly acetic acid and butyric acid when compared to their counterparts. Transplantation of caecal microbiota from cold-separated voles but not from cold-huddling voles induced significant increases in energy intake and RMR compared to that from warm-separated voles.ConclusionsThese findings demonstrate that the remodeling of gut microbiota, which is associated with a reduction in host Tcore, mediates cold- and huddling-induced energy intake and thermoregulation and therefore orchestrates host metabolic and thermal homeostasis. It highlights the coevolutionary mechanism of host huddling and gut microbiota in thermoregulation and energy saving for winter survival in endotherms.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0473-9) contains supplementary material, which is available to authorized users.
Stress-induced hyperglycemia is a fundamental adaptive response that mobilizes energy stores in response to threats. Here, our examination of the contributions of the central catecholaminergic (CA) neuronal system to this adaptive response revealed that CA neurons in the ventrolateral medulla (VLM) control stress-induced hyperglycemia. Ablation of VLM CA neurons abolished the hyperglycemic response to both physical and psychological stress, whereas chemogenetic activation of these neurons was sufficient to induce hyperglycemia. We further found that CA neurons in the rostral VLM, but not those in the caudal VLM, cause hyperglycemia via descending projections to the spinal cord. Monosynaptic tracing experiments showed that VLM CA neurons receive direct inputs from multiple stress-responsive brain areas. Optogenetic studies identified an excitatory PVN-VLM circuit that induces hyperglycemia. This study establishes the central role of VLM CA neurons in stress-induced hyperglycemia and substantially expands our understanding of the central mechanism that controls glucose metabolism.
The adjustments in thermal physiology and energetics were investigated in male desert hamsters (Phodopus roborovskii) which were acclimated to 5°C for 4 weeks. Mean core body temperature in cold acclimated animals decreased by 0.21°C compared with controls. Further analysis revealed that the decrease mainly occurred in the scotophase, while in the photophase core body temperature remained constant during the whole cold acclimation. Thermogenic capacity, represented by resting metabolic rate and nonshivering thermogenesis increased in cold acclimated hamsters from initial values of 1.38 ± 0.05 and 5.32 ± 0.30 to 1.77 ± 0.08 and 8.79 ± 0.31 mlO(2) g(-1) h(-1), respectively. After cold acclimation, desert hamsters maintained a relative stable body mass of 21.7 ± 0.1 g very similar to the controls kept at 23°C (21.8 ± 0.1 g). The mean values of food intake and digestible energy (metabolisable energy) in cold acclimated hamsters were 5.3 ± 0.1 g day(-1) and 76.3 ± 0.9 kJ day(-1) (74.8 ± 0.9), respectively, which were significantly elevated by 76.7 and 80.4% compared to that in control group. The apparent digestibility was 81.0 ± 0.3% in cold acclimated animals which was also higher than the 79.7 ± 0.2% observed in controls. This increase corresponded with adaptive adjustments in morphology of digestive tracts with 20.2 and 36.8% increases in total length and wet mass, respectively. Body fat mass and serum leptin levels in cold acclimated hamsters decreased by 40.7 and 67.1%, respectively. The wheel running turns and the onset of wheel running remained unchanged. Our study indicated that desert hamsters remained very active during cold acclimation and displayed adaptive changes in thermal physiology and energy metabolism, such as enhanced thermogenic and energy processing capacities.
The Qinghai-Tibetan Plateau, with low precipitation, low oxygen partial pressure, and temperatures routinely dropping below −30 °C in winter, presents several physiological challenges to its fauna. Yet it is home to many endemic mammalian species, including the plateau pika (Ochotona curzoniae). How these small animals that are incapable of hibernation survive the winter is an enigma. Measurements of daily energy expenditure (DEE) using the doubly labeled water method show that pikas suppress their DEE during winter. At the same body weight, pikas in winter expend 29.7% less than in summer, despite ambient temperatures being approximately 25 °C lower. Combined with resting metabolic rates (RMRs), this gives them an exceptionally low metabolic scope in winter (DEE/RMRt = 1.60 ± 0.30; RMRt is resting metabolic rate at thermoneutrality). Using implanted body temperature loggers and filming in the wild, we show that this is achieved by reducing body temperature and physical activity. Thyroid hormone (T3 and T4) measurements indicate this metabolic suppression is probably mediated via the thyroid axis. Winter activity was lower at sites where domestic yak (Bos grunniens) densities were higher. Pikas supplement their food intake at these sites by eating yak feces, demonstrated by direct observation, identification of yak DNA in pika stomach contents, and greater convergence in the yak/pika microbiotas in winter. This interspecific coprophagy allows pikas to thrive where yak are abundant and partially explains why pika densities are higher where domestic yak, their supposed direct competitors for food, are more abundant.
SUMMARY We evaluated factors limiting lactating Mongolian gerbils (Meriones unguiculatus) at three temperatures (10, 21 and 30°C−1 less energy as milk at peak lactation than those allocated to 10 or 21°C, with no difference between the latter groups. On day 14 of lactation, the litter masses at 10 and 30°C were 12.2 and 9.3g lower than those at 21°C, respectively. Lactating gerbils had higher thermal conductance of the fur and lower UCP-1 levels in brown adipose tissue than non-reproductive gerbils, independent of ambient temperature, suggesting that they were attempting to avoid heat stress. Thermal conductance of the fur was positively related to circulating prolactin levels. We implanted non-reproductive gerbils with mini-osmotic pumps that delivered either prolactin or saline. Prolactin did not influence thermal conductance of the fur, but did reduce physical activity and UCP-1 levels in brown adipose tissue. Transferring lactating gerbils from warm to hot conditions resulted in reduced milk production, consistent with the heat dissipation limit theory, but transferring them from warm to cold conditions did not elevate milk production, consistent with the peripheral limitation hypothesis, and placed constraints on pup growth. Supplementary material available online at
SUMMARYThe limitation on sustainable energy intake (SusEI) is important because it establishes the upper energetic limit on the ability of animals to disperse, survive and reproduce. However, there are still arguments about what factors impose that limitation. Thermoregulation in cold environments imposes great energy demands on small mammals. A cold-exposed animal has been suggested to be a model suitable for testing these factors. Here, we examined the changes in food intake and digestible energy intake (DEI) as measures of SusEI, thermogenic capacity and behavioral patterns in Swiss mice exposed to consecutively lower ambient temperatures from 23 to -15°C. Cold-exposed mice showed significant decreases in body mass, fat content of the carcass and body temperature, and increases in DEI compared with controls. The time spent on feeding significantly increased with decreasing temperatures, and time spent on general activity decreased following cold exposure. Resting metabolic rate, nonshivering thermogenesis and serum tri-iodothyronine levels significantly increased in mice exposed to lower temperatures in comparison with controls, whereas these thermogenic variables were not significantly different between 0 and -15°C. It might suggest that SusEI in cold exposed Swiss mice was constrained peripherally by the capacity to produce heat and also by the ability to dissipate body heat, but to a different extent. Moderate cold exposure might result in a relaxation of the heat dissipation limit (HDL), allowing the animals to increase food intake to meet cold stress. When animals are exposed to severe cold, the thermogenenic capacity might reach a ceiling, failing to compensate for the heat loss and which would finally result in lower body temperature and considerable weight loss. This might indicate that the HDL was set at a higher level than peripheral limits for Swiss mice exposed to a consecutive decrease in ambient temperatures.
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