A shift in the thermoregulatory curve as a result of selection for high activity-related aerobic metabolism

According to the “aerobic capacity model,” endothermy in birds and mammals evolved as a result of natural selection favoring increased persistent locomotor activity, fuelled by aerobic metabolism. However, this also increased energy expenditure even during rest, with the lowest metabolic rates occurring in the thermoneutral zone (TNZ) and increasing at ambient temperatures (Ta) below and above this range, depicted by the thermoregulatory curve. In our experimental evolution system, four lines of bank voles (Myodes glareolus) have been selected for high swim-induced aerobic metabolism and four unselected lines have been maintained as a control. In addition to a 50% higher rate of oxygen consumption during swimming, the selected lines have also evolved a 7.3% higher mass-adjusted basal metabolic rate. Therefore, we asked whether voles from selected lines would also display a shift in the thermoregulatory curve and an increased body temperature (Tb) during exposure to high Ta. To test these hypotheses we measured the RMR and Tb of selected and control voles at Ta from 10 to 34°C. As expected, RMR within and around the TNZ was higher in selected lines. Further, the Tb of selected lines within the TNZ was greater than the Tb of control lines, particularly at the maximum measured Ta of 34°C, suggesting that selected voles are more prone to hyperthermia. Interestingly, our results revealed that while the slope of the thermoregulatory curve below the lower critical temperature (LCT) is significantly lower in the selected lines, the LCT (26.1°C) does not differ. Importantly, selected voles also evolved a higher maximum thermogenesis, but thermal conductance did not increase. As a consequence, the minimum tolerated temperature, calculated from an extrapolation of the thermoregulatory curve, is 8.4°C lower in selected (−28.6°C) than in control lines (−20.2°C). Thus, selection for high aerobic exercise performance, even though operating under thermally neutral conditions, has resulted in the evolution of increased cold tolerance, which, under natural conditions, could allow voles to inhabit colder environments. Further, the results of the current experiment support the assumptions of the aerobic capacity model of the evolution of endothermy

Evolution of basal metabolic rate in bank voles from a multidirectional selection experiment

A major theme in evolutionary and ecological physiology of terrestrial vertebrates encompasses the factors underlying the evolution of endothermy in birds and mammals and interspecific variation of basal metabolic rate (BMR). Here, we applied the experimental evolution approach and compared BMR in lines of a wild rodent, the bank vole (Myodes glareolus), selected for 11 generations for: high swim-induced aerobic metabolism (A), ability to maintain body mass on a low-quality herbivorous diet (H) and intensity of predatory behaviour towards crickets (P). Four replicate lines were maintained for each of the selection directions and an unselected control (C). In comparison to C lines, A lines achieved a 49% higher maximum rate of oxygen consumption during swimming, H lines lost 1.3 g less mass in the test with low-quality diet and P lines attacked crickets five times more frequently. BMR was significantly higher in A lines than in C or H lines (60.8, 56.6 and 54.4 ml O2/h, respectively), and the values were intermediate in P lines (59.0 ml O2/h). Results of the selection experiment provide support for the hypothesis of a positive association between BMR and aerobic exercise performance, but not for the association of adaptation to herbivorous diet with either a high or low BMR

Phoenix from the Ashes: Fire, Torpor, and the Evolution of Mammalian Endothermy

The evolution of endothermy in mammals and birds has been widely debated. Endothermy is characterized by high endogenous heat production via combustion of metabolic fuels. This differs from ectothermy in most living organisms, which generally do not produce substantial amounts of internal heat for thermoregulation (Tattersall et al., 2012; Withers et al., 2016). Endogenous heat production is energetically very costly. In comparison to ectothermic terrestrial vertebrates, namely the amphibians and reptiles, the minimum metabolic rate (MR) of normothermic or homeothermic (high constant body temperature, Tb) animals at rest is about 4–8-fold higher in the endotherms. This difference is even more pronounced at low ambient temperatures (Ta) at which the Tb of ectotherms follows Ta, and the MR decreases to even lower levels. In contrast, the Tb of homeothermic endotherms remains high and constant over a wide range of Ta. Therefore, to compensate for increased heat loss at low Ta, MR of especially small mammals and birds must increase substantially and can be 100-fold or more of that in ectotherms (Bartholomew, 1982). Of course this high MR requires a substantial uptake of food and in endotherms much of this chemical energy is simply converted into heat for thermoregulation rather than growth or reproduction as in ectotherms

Responding to the weather: energy budgeting by a small mammal in the wild

Energy conservation is paramount for small mammals because of their small size, large surface area to volume ratio, and the resultant high heat loss to the environment. To survive on limited food resources and to fuel their expensive metabolism during activity, many small mammals employ daily torpor to reduce energy expenditure during the rest phase. We hypothesized that a small terrestrial semelparous marsupial, the brown antechinus Antechinus stuartii, would maximize activity when foraging conditions were favorable to gain fat reserves before their intense breeding period, but would increase torpor use when conditions were poor to conserve these fat reserves. Female antechinus were trapped and implanted with small temperature-sensitive radio transmitters to record body temperature and to quantify torpor expression and activity patterns in the wild. Most antechinus used torpor at least once per day over the entire study period. Total daily torpor use increased and mean daily body temperature decreased significantly with a reduction in minimum ambient temperature. Interestingly, antechinus employed less torpor on days with more rain and decreasing barometric pressure. In contrast to torpor expression, activity was directly related to ambient temperature and inversely related to barometric pressure. Our results reveal that antechinus use a flexible combination of physiology and behavior that can be adjusted to manage their energy budget according to weather variables

State dependence of arousal from torpor in brown long-eared bats (Plecotus auritus)

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Post-fire recovery of torpor and activity patterns of a small mammal

To cope with the post-fire challenges of decreased availability of food and shelter, brown antechinus (Antechinus stuartii), a small marsupial mammal, increase the use of energy conserving torpor and reduce activity. However, it is not known how long it takes for animals to resume pre-fire torpor and activity patterns during the recovery of burnt habitat. Therefore, we tested the hypothesis that antechinus will adjust torpor use and activity after a fire depending on vegetation recovery. We simultaneously quantified torpor and activity patterns for female antechinus from three adjacent areas: (i) the area of a management burn one year post-fire, (ii) an area that was burned two years prior and (iii) a control area. In comparison to shortly after the management burn, antechinus in all three groups displayed less frequent and less pronounced torpor while being more active. We provide the first evidence that only one year post-fire antechinus resume pre-fire torpor and activity patterns, likely in response to the return of herbaceous ground cover and foraging opportunities

Can hibernators sense and evade fires? Olfactory acuity and locomotor performance during deep torpor.

Increased habitat fragmentation, global warming and other human activities have caused a rise in the frequency of wildfires worldwide. To reduce the risks of uncontrollable fires, prescribed burns are generally conducted during the colder months of the year, a time when in many mammals torpor is expressed regularly. Torpor is crucial for energy conservation, but the low body temperatures (T b) are associated with a decreased responsiveness and torpid animals might therefore face an increased mortality risk during fires. We tested whether hibernators in deep torpor (a) can respond to the smell of smoke and (b) can climb to avoid fires at T bs below normothermic levels. Our data show that torpid eastern pygmy-possums (Cercartetus nanus) are able to detect smoke and also can climb. All males aroused from torpor when the smoke stimulus was presented at an ambient temperature (T a) of 15 °C (T b ∼18 °C), whereas females only raised their heads. The responses were less pronounced at T a 10 °C. The first coordinated movement of possums along a branch was observed at a mean T b of 15.6 °C, and animals were even able to climb their prehensile tail when they reached a mean T b of 24.4 °C. Our study shows that hibernators can sense smoke and move at low T b. However, our data also illustrate that at T b ≤13 °C, C. nanus show decreased responsiveness and locomotor performance and highlight that prescribed burns during winter should be avoided on very cold days to allow torpid animals enough time to respond