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

The effect of monoamines reuptake inhibitors on aerobic exercise performance in bank voles from a selection experiment

Exercise performance depends on both physiological abilities (e.g., muscle strength) and behavioral characteristics (e.g., motivation). We tested the hypothesis that evolution of increased aerobic exercise performance can be facilitated by evolution of neuropsychological mechanisms responsible for motivation to undertake physical activity. We used a unique model system: lines of bank voles Myodes glareolus selected for high swim-induced aerobic metabolism ("aerobic" A lines). In generation 21, voles from the 4 A lines achieved a 57% higher "voluntary maximum" swim-induced aerobic metabolism (VO_{2}swim) than voles from 4 unselected, "control" C lines. In C lines, VO_{2}swim was 9% lower than the maximum forced-exercise aerobic metabolism (VO_{2}run; P=0.007), while in A lines it was even higher than VO_{2}run, although not significantly (4%, P=0.15). Thus, we hypothesized that selection changed both the aerobic capacity and the neuronal mechanisms behind motivation to undertake activity. We investigated the influence of reuptake inhibitors of dopamine (DARI), serotonin (SSRI), and norepinephrine (NERI) on VO_{2}swim. The drugs decreased VO_{2}swim both in C and A lines (% decrease compared with saline: DARI 8%, P<0.001; SSRI 6%, P<0.001; NERI 8%, P<0.001), but the proportional response differed between selection directions only for NERI (stronger effect in C lines: P=0.008) and the difference was marginally non-significant for SSRI (P=0.07) and DARI (P=0.06). Thus, the results suggest that all the 3 monoamines are involved in signaling pathways controlling the motivation to be active and that norepinephrine could have played a role in the evolution of increased aerobic exercise performance in our animal model

Experimental evolution of personality traits : open-field exploration in bank voles from a multidirectional selection experiment

Evolution of complex physiological adaptations could be driven by natural selection acting on behavioral traits. Consequently, animal personality traits and their correlation with physiological traits have become an engaging research area. Here, we applied a unique experimental evolution model - lines of bank voles selected for (A) high exercise-induced aerobic metabolism, (H) ability to cope with low-quality herbivorous diet, and (P) intensity of predatory behavior, that is, traits shaping evolutionary path and diversity of mammals - and asked how the selection affected the voles’ personality traits, assessed in an open field test. The A- and P-line voles were more active, whereas the H-line voles were less active, compared those from unselected control lines (C). H-line voles moved slower but on more meandering trajectories, which indicated a more thorough exploration, whereas the A- and P-line voles moved faster and on straighter trajectories. A-line voles showed also an increased escape propensity, whereas P-line voles tended to be bolder. The remarkable correlated responses to the selection indicate a common genetic underlying mechanism of behavioral and physiological traits, and support the paradigm of evolutionary physiology built around the concept of correlated evolution of behavior and physiology

Limits to sustained energy intake. XXIII. Does heat dissipation capacity limit the energy budget of lactating bank voles?

Acknowledgements We are grateful to our technicians and several students for their help during this study and for animal care. We thank Catherine Hambly and Peter Thompson for technical assistance for the isotope analysis for the DLW measurements. We thank Ulf Bauchinger for stimulating discussion and his comments, and two anonymous referees for comments on the manuscript. Funding This project was supported by grants from the Polish Ministry of Science and Higher Education [0595/B/P01/2011/40 to E.T.S. and 8167/B/P01/2011/40 to P.K.], and Jagiellonian University [DS/WBINOZ/INOS/757 to P.K.].Peer reviewedPublisher PD

Age-related changes of physiological performance and survivorship of bank voles selected for high aerobic capacity

Variation in lifespans is an intriguing phenomenon, but how metabolic rate influence this variation remains unclear. High aerobic capacity can result in health benefits, but also in increased oxidative damage and accelerated ageing. We tested these contradictory predictions using bank voles (Myodes=Clethrionomys glareolus) from lines selected for high swim-induced aerobic metabolism (A), which had about 50% higher maximum metabolic rate and a higher basal and routine metabolic rates, than those from unselected control lines (C). We measured sprint speed (VSmax), forced-running maximum metabolic rate (VO_{2}run), maximum long-distance running speed (VLmax), running speed at VO_{2}run (VVO_{2}), and respiratory quotient at VO_{2}run (RQ) at three age classes (I: 3-5, II: 12-14, III: 17-19 months), and analysed survivorship. We asked if ageing, understood as the age-related decline of the performance traits, differs between the A and C lines. At age class I, voles from A lines had 19% higher VO_{2}run, and 12% higher VLmax, but tended to have 19% lower VSmax, than those from C lines. RQ was nearly 1.0 for both A and C lines. The pattern of age-related changes differed between the lines mainly between age classes I and II, but not in older animals. VSmax increased by 27% in A lines and by 10% in C lines between age class I and II, but between classes II and III, it increased by 16% in both selection directions. VO_{2}run decreased by 7% between age class I and II in A lines only, but in C lines it remained constant across all age classes. VLmax decreased by 8% and VVO_{2} by 12% between age classes II and III, but similarly in both selection directions. Mortality was higher in A than in C lines only between the age of 1 and 4 months. The only trait for which the changes in old animals differed between the lines was RQ. In A lines, RQ increased between age classes II and III, whereas in C lines such an increase occurred between age classes I and II. Thus, we did not find obvious effects of selection on the pattern of ageing. However, the physiological performance and mortality of bank voles remained surprisingly robust to ageing, at least until the age of 17-19 months, similar to the maximum lifespan under natural conditions. Therefore, it is possible that the selection could affect the pattern of ageing in even older individuals when symptoms of senility might be more profound

Genetic variation in bank vole populations in natural and metal-contaminated areas

The effects of isolation and heavy-metal pollution on genetic diversity in Myodes (=Clethrionomys) glareolus populations were studied. Isolation and pollution are considered to have important effects on biodiversity. Animals were collected from ten populations in isolated (island), mainland, and metal-polluted areas. Three populations were in areas near zinc and lead smelters; four were on islands in the relatively unpolluted Mazurian Lake District and in the Bieszczady Mountains; and three were in clean-mainland areas in the Mazurian Lake District, the Niepołomice Forest, and the Bieszczady Mountains. Cadmium and lead concentrations in liver and kidney were measured to assess the animals’ exposure to metals. The metal concentrations were greater in animals from areas classed as polluted than in animals from the clean-mainland areas and islands. The genetic diversity of each population was analyzed using eight microsatellite markers. The results confirmed that isolation adversely affects genetic diversity in M. glareolus populations (giving low heterozygosity and poor allelic richness), but the effect of metal exposure on genetic diversity was not strong. Of the samples from polluted areas, only the Katowice population, which is exposed to high levels of metal pollution and is also isolated because of human activity, showed genetic variation parameters that were similar to those for the island populations. Nei’s genetic distances indicated that the island populations were genetically distant from each other and from the other populations, and there were noticeable inbreeding effects that would have been caused by the isolation of these populations