Abstract. According to the aerobic capacity model, endothermy in birds and mammals evolved as a correlated response to selection for an ability of sustained locomotor activity, rather than in a response to direct selection for thermoregulatory capabilities. A key assumption of the model is that aerobic capacity is functionally linked to basal metabolic rate (BMR). The assumption has been tested in several studies at the level of phenotypic variation among individuals or species, but none has provided a clear answer whether the traits are genetically correlated. Here we present results of a genetic analysis based on measurements of the basal and the maximum swim-and cold-induced oxygen consumption in about 1000 bank voles from six generations of a laboratory colony, reared from animals captured in the field. Narrow sense heritability (h 2 ) was about 0.5 for body mass, about 0.4 for mass-independent basal and maximum metabolic rates, and about 0.3 for factorial aerobic scopes. Dominance genetic and common environmental (ϭ maternal) effects were not significant. Additive genetic correlation between BMR and the swim-induced aerobic capacity was high and positive, whereas correlation resulting from specific-environmental effects was negative. However, BMR was not genetically correlated with the cold-induced aerobic capacity. The results are consistent with the aerobic capacity model of the evolution of endothermy in birds and mammals. Birds and mammals employ an extravagant economy of energy usage. They spend energy at a rate about 20 times higher than do reptiles (Nagy et al. 1999) and dissipate 20-50% of the energy as basal metabolism for maintenance of basic function (McNab 2002). How such a wasteful strategy of energy use evolved from an energetically frugal strategy is puzzling. This puzzle is the core of a nearly half-centurylong debate on selection forces behind the evolution of endothermy (i.e., the ability to maintain an elevated body temperature by means of metabolic heat production) in birds and mammals (see reviews: Hayes and Garland 1995;Ruben 1995;Farmer 2000Farmer , 2003 Koteja 2000Koteja , 2004McNab 2002;Angilletta and Sears 2003;Gomes et al. 2004).Although several hypotheses concerning the evolution of endothermy have been proposed, only one-the aerobic capacity model-has been subject to extensive empirical testing. According to the model, high basal metabolic rate (BMR) and consequently endothermic thermoregulation, evolved as a correlated response to selection for an ability of sustained locomotor activity, supported by aerobic metabolism (Bennett and Ruben 1979), rather than as a response to direct selection for thermoregulatory capability. A fundamental assumption of the hypothesis is that the aerobic capacity is functionally linked with BMR, which translates into a statistically tractable hypothesis of a positive correlation between BMR and the maximum rate of oxygen consumption (V O2max ), and therefore can be tested against empirical results obtained in extant species. The assumption has been...
SUMMARYAccording to life-history theory, investment in reproduction is associated with costs, which should appear as decreased survival to the next reproduction or lower future reproductive success. It has been suggested that oxidative stress may be the proximate mechanism of these trade-offs. Despite numerous studies of the defense against reactive oxygen species (ROS) during reproduction, very little is known about the damage caused by ROS to the tissues of wild breeding animals. We measured oxidative damage to lipids and proteins in breeding bank vole (Myodes glareolus) females after rearing one and two litters, and in non-breeding females. We used bank voles from lines selected for high maximum aerobic metabolic rates (which also had high resting metabolic rates and food intake) and non-selected control lines. The oxidative damage was determined in heart, kidneys and skeletal muscles by measuring the concentration of thiobarbituric acid-reactive substances, as markers of lipid peroxidation, and carbonyl groups in proteins, as markers of protein oxidation. Surprisingly, we found that the oxidative damage to lipids in kidneys and muscles was actually lower in breeding than in non-breeding voles, and it did not differ between animals from the selected and control lines. Thus, contrary to our predictions, females that bred suffered lower levels of oxidative stress than those that did not reproduce. Elevated production of antioxidant enzymes and the protective role of sex hormones may explain the results. The results of the present study do not support the hypothesis that oxidative damage to tissues is the proximate mechanism of reproduction costs.
In a laboratory colony of a wild rodent, the bank vole Myodes (=Clethrionomys) glareolus, a multiway artificial selection experiment was applied to mimic evolution toward high aerobic metabolism achieved during locomotor activity, predatory behavior, and ability to cope with herbivorous diet. Four lines for each of the selection directions and four unselected control lines have been maintained. After three generations of within-family selection, the maximum rate of oxygen consumption achieved during swimming was 15% higher in the selected than in the control lines (least square means, adjusted for body mass: 252.0 vs. 218.6 mL O(2)/h, P = 0.0001). When fed a low-quality diet made of dried grass, voles from the lines selected for ability to cope with herbivorous diet lost about 0.7 g less mass than voles from the control lines (-2.44 vs. -3.16 g/4 d, P = 0.008). In lines selected for predatory behavior toward crickets, proportion of "predatory" individuals was higher than in the control lines (43.6% vs. 24.9%; P = 0.045), but "time to capture" calculated for the successful trials did not differ between the lines. The experiment continues, and the selected lines of voles will provide a unique model for testing hypotheses concerning correlated evolution of complex traits.
Basal metabolic rate (BMR) is a fundamental energetic trait and has been measured in hundreds of birds and mammals. Nevertheless, little is known about the consistency of the population-average BMR or its repeatability at the level of individual variation. Here, we report that average mass-independent BMR did not differ between two generations of bank voles or between two trials separated by one month. Individual differences in BMR were highly repeatable across the one month interval: the coefficient of intraclass correlation was 0.70 for absolute log-transformed values and 0.56 for mass-independent values. Thus, BMR can be a meaningful measure of an individual physiological characteristic and can be used to test hypotheses concerning relationships between BMR and other traits. On the other hand, mass-independent BMR did not differ significantly across families, and the coefficient of intraclass correlation for full sibs did not differ from zero, which suggests that heritability of BMR in voles is not high.
According to the aerobic capacity model, endothermy in birds and mammals evolved as a correlated response to selection for an ability of sustained locomotor activity, rather than in a response to direct selection for thermoregulatory capabilities. A key assumption of the model is that aerobic capacity is functionally linked to basal metabolic rate (BMR). The assumption has been tested in several studies at the level of phenotypic variation among individuals or species, but none has provided a clear answer whether the traits are genetically correlated. Here we present results of a genetic analysis based on measurements of the basal and the maximum swim- and cold-induced oxygen consumption in about 1000 bank voles from six generations of a laboratory colony, reared from animals captured in the field. Narrow sense heritability (h2) was about 0.5 for body mass, about 0.4 for mass-independent basal and maximum metabolic rates, and about 0.3 for factorial aerobic scopes. Dominance genetic and common environmental (= maternal) effects were not significant. Additive genetic correlation between BMR and the swim-induced aerobic capacity was high and positive, whereas correlation resulting from specific-environmental effects was negative. However, BMR was not genetically correlated with the cold-induced aerobic capacity. The results are consistent with the aerobic capacity model of the evolution of endothermy in birds and mammals.
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 O 2 h 21 , respectively), and the values were intermediate in P lines (59.0 ml O 2 h 21 ). 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.
Basal metabolic rate (BMR), commonly used as a measure of the cost of living, is highly variable among species, and sources of the variation are subject to an enduring debate among comparative biologists. One of the hypotheses links the variation in BMR with diversity of food habits and life-history traits. We test this hypothesis by asking how BMR of a particular species, the bank vole The rate of energy metabolism varies at all possible levels of comparison: across large taxa, among species, individuals within a species, and also within individuals (McNab 2002). Explaining the sources of this variation remains one of the central issues in the ecological and evolutionary physiology of animals (e.g., Mueller and Diamond
Comparative studies have shown that diet, life history, and phylogeny interact to determine microbial community structure across mammalian hosts. However, these studies are often confounded by numerous factors. Selection experiments offer unique opportunities to validate conclusions and test hypotheses generated by comparative studies. We used a replicated, 15-generation selection experiment on bank voles (Myodes glareolus) that have been selected for high swim-induced aerobic metabolism, predatory behavior toward crickets, and the ability to maintain body mass on a high-fiber, herbivorous diet. We predicted that selection on host performance, mimicking adaptive radiation, would result in distinct microbial signatures. We collected foregut and cecum samples from animals that were all fed the same nutrient-rich diet and had not been subjected to any performance tests. We conducted microbial inventories of gut contents by sequencing the V4 region of the 16S rRNA gene. We found no differences in cecal microbial community structure or diversity between control lines and the aerobic or predatory lines. However, the cecal chambers of voles selected for herbivorous capability harbored distinct microbial communities that exhibited higher diversity than control lines. The foregut communities of herbivorous-selected voles were also distinct from control lines. Overall, this experiment suggests that differences in microbial communities across herbivorous mammals may be evolved, and not solely driven by current diet or other transient factors.
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