Agata M. Rudolf

The optimal combination of standard metabolic rate and aerobic scope for somatic growth depends on food availability

Summary Metabolic rates can vary as much as threefold among individuals of the same size and age in a population, but why such variation persists is unclear given that they determine the energetic cost of living. Relationships between standard metabolic rate (SMR), growth and survival can vary with environmental conditions, suggesting that the fitness consequences of a given metabolic phenotype may be context-dependent. Less attention has focused on the link between absolute aerobic scope (AS, the difference between standard and maximum metabolic rate) and fitness under different environmental conditions, despite the importance of aerobic scope to an organisms total energetic capacity. We examined the links between individual variation in both SMR and AS and somatic growth rates of brown trout (Salmo trutta) under different levels of food availability. Standard metabolic rate and AS were uncorrelated across individuals. However, SMR and AS not only had interactive effects on growth, but these interactions depended on food level: at ad libitum food levels, AS had a positive effect on growth whose magnitude depended on SMR; at intermediate food levels, AS and SMR had interactive effects on growth, but at the low food level, there was no effect of either AS or SMR on growth. As a result, there was no metabolic phenotype that performed best or worst across all food levels. These results demonstrate the importance of aerobic scope in explaining somatic growth rates and support the hypothesis that links between individual variation in metabolism and fitness are context-dependent. The larger metabolic phenotype and the environmental context in which performance is evaluated both need to be considered in order to better understand the link between metabolic rates and fitness and thereby the persistence of individual variation in metabolic rates.

Individuals with higher metabolic rates have lower levels of reactive oxygen species in vivo

There is increasing interest in the effect of energy metabolism on oxidative stress, but much ambiguity over the relationship between the rate of oxygen consumption and the generation of reactive oxygen species (ROS). Production of ROS (such as hydrogen peroxide, H2O2) in the mitochondria is primarily inferred indirectly from measurements in vitro, which may not reflect actual ROS production in living animals. Here, we measured in vivo H2O2 content using the recently developed MitoB probe that becomes concentrated in the mitochondria of living organisms, where it is converted by H2O2 into an alternative form termed MitoP; the ratio of MitoP/MitoB indicates the level of mitochondrial H2O2 in vivo. Using the brown trout Salmo trutta, we tested whether this measurement of in vivo H2O2 content over a 24 h-period was related to interindividual variation in standard metabolic rate (SMR). We showed that the H2O2 content varied up to 26-fold among fish of the same age and under identical environmental conditions and nutritional states. Interindividual variation in H2O2 content was unrelated to mitochondrial density but was significantly associated with SMR: fish with a higher mass-independent SMR had a lower level of H2O2. The mechanism underlying this observed relationship between SMR and in vivo H2O2 content requires further investigation, but may implicate mitochondrial uncoupling which can simultaneously increase SMR but reduce ROS production. To our knowledge, this is the first study in living organisms to show that individuals with higher oxygen consumption rates can actually have lower levels of H2O2.

Flexibility in metabolic rate confers a growth advantage under changing food availability

Phenotypic flexibility in physiological, morphological and behavioural traits can allow organisms to cope with environmental challenges. Given recent climate change and the degree of habitat modification currently experienced by many organisms, it is therefore critical to quantify the degree of phenotypic variation present within populations, individual capacities to change and what their consequences are for fitness. Flexibility in standard metabolic rate (SMR) may be particularly important since SMR reflects the minimal energetic cost of living and is one of the primary traits underlying organismal performance. SMR can increase or decrease in response to food availability, but the consequences of these changes for growth rates and other fitness components are not well known. We examined individual variation in metabolic flexibility in response to changing food levels and its consequences for somatic growth in juvenile brown trout (Salmo trutta). SMR increased when individuals were switched to a high food ration and decreased when they were switched to a low food regime. These shifts in SMR, in turn, were linked with individual differences in somatic growth; those individuals that increased their SMR more in response to elevated food levels grew fastest, while growth at the low food level was fastest in those individuals that depressed their SMR most. Flexibility in energy metabolism is therefore a key mechanism to maximize growth rates under the challenges imposed by variability in food availability and is likely to be an important determinant of species’ resilience in the face of global change.

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−1, respectively), and the values were intermediate in P lines (59.0 ml O2 h−1). 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.

Experimental Evolution on a Wild Mammal Species Results in Modifications of Gut Microbial Communities

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.

Learning ability in bank voles selected for high aerobic metabolism, predatory behaviour and herbivorous capability

Although great progress has been made in understanding neurological mechanisms of cognitive processes, the questions concerning interrelation between evolution of cognitive abilities and evolution of diverse life histories and adaptive strategies remains largely open. We approached the problem using a unique experimental evolution model system: lines of bank voles selected for high swim-induced aerobic metabolism, intensity of predatory behaviour towards crickets, and ability to grow on a low-quality herbivorous diet. To test a hypothesis that selection for these traits resulted in correlated changes in spatial learning and memory, voles from generation 13 of the selected and unselected control lines were examined in Morris water maze. Most of the individuals successfully learned the position of the platform hidden under water surface, but the spatial learning scores did not differ significantly between selection directions. The results are not consistent with either the hypothesis of a functional trade-off between high cognitive abilities and capability to cope with adverse nutritional conditions, or the hypothesis of a positive link between evolution of cognitive abilities and high aerobic exercise performance.

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

ABSTRACT Understanding factors limiting sustained metabolic rate (SusMR) is a central issue in ecological physiology. According to the heat dissipation limit (HDL) theory, the SusMR at peak lactation is constrained by the maternal capacity to dissipate body heat. To test that theory, we shaved lactating bank voles (Myodes glareolus) to experimentally elevate their capacity for heat dissipation. The voles were sampled from lines selected for high aerobic exercise metabolism (A; characterized also by increased basal metabolic rate) and unselected control lines (C). Fur removal significantly increased the peak-lactation food intake (mass-adjusted least square means±s.e.; shaved: 16.3±0.3 g day−1, unshaved: 14.4±0.2 g day−1; P<0.0001), average daily metabolic rate (shaved: 109±2 kJ day−1, unshaved: 97±2 kJ day−1; P<0.0001) and metabolisable energy intake (shaved: 215±4 kJ day−1, unshaved: 185±4 kJ day−1; P<0.0001), as well as the milk energy output (shaved: 104±4 kJ day−1; unshaved: 93±4 kJ day−1; P=0.021) and litter growth rate (shaved: 9.4±0.7 g 4 days−1, unshaved: 7.7±0.7 g 4 days−1; P=0.028). Thus, fur removal increased both the total energy budget and reproductive output at the most demanding period of lactation, which supports the HDL theory. However, digestive efficiency was lower in shaved voles (76.0±0.3%) than in unshaved ones (78.5±0.2%; P<0.0001), which may indicate that a limit imposed by the capacity of the alimentary system was also approached. Shaving similarly affected the metabolic and reproductive traits in voles from the A and C lines. Thus, the experimental evolution model did not reveal a difference in the limiting mechanism between animals with inherently different metabolic rates. Summary: Fur removal increases both energy budget and reproductive output at peak lactation in a non-laboratory rodent, the bank vole, supporting the heat dissipation limit theory.

Variation in Metabolic Rate among Individuals Is Related to Tissue-Specific Differences in Mitochondrial Leak Respiration

Standard metabolic rate (SMR) and maximum metabolic rate (MMR) typically vary two- or threefold among conspecifics, with both traits assumed to significantly impact fitness. However, the underlying mechanisms that determine such intraspecific variation are not well understood. We examined the influence of mitochondrial properties on intraspecific variation in SMR and MMR and hypothesized that if SMR supports the cost of maintaining the metabolic machinery required for MMR, then the mitochondrial properties underlying these traits should be shared. Mitochondrial respiratory capacity (leak and phosphorylating respiration) and mitochondrial content (cytochrome c oxidase activity) were determined in the liver and white muscle of brown trout Salmo trutta of similar age and maintenance conditions. SMR and MMR were uncorrelated across individuals and were not associated with the same mitochondrial properties, suggesting that they are under the control of separate physiological processes. Moreover, tissue-specific relationships between mitochondrial properties and whole-organism metabolic traits were observed. Specifically, SMR was positively associated with leak respiration in liver mitochondria, while MMR was positively associated with muscle mitochondrial leak respiration and mitochondrial content. These results suggest that a high SMR or MMR, rather than signaling a higher ability for respiration-driven ATP synthesis, may actually reflect greater dissipation of energy, driven by proton leak across the mitochondrial inner membrane. Knowledge of these links should aid interpretation of the potential fitness consequences of such variation in metabolism, given the importance of mitochondria in the utilization of resources and their allocation to performance.

Differential effects of food availability on minimum and maximum rates of metabolism

Metabolic rates reflect the energetic cost of living but exhibit remarkable variation among conspecifics, partly as a result of the constraints imposed by environmental conditions. Metabolic rates are sensitive to changes in temperature and oxygen availability, but effects of food availability, particularly on maximum metabolic rates, are not well understood. Here, we show in brown trout (Salmo trutta) that maximum metabolic rates are immutable but minimum metabolic rates increase as a positive function of food availability. As a result, aerobic scope (i.e. the capacity to elevate metabolism above baseline requirements) declines as food availability increases. These differential changes in metabolic rates likely have important consequences for how organisms partition available metabolic power to different functions under the constraints imposed by food availability.

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

ABSTRACT 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 (VO2run), maximum long‐distance running speed (VLmax), running speed at VO2run (VVO2), and respiratory quotient at VO2run (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 VO2run, 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. VO2run 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 VVO2 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. HighlightsBank voles selected for high swim‐induced metabolism had increased aerobic capacity.Several other physiological performance traits were increased in selected voles.Age‐related detrimental changes were observed only in some of the performance traits.For most of the traits the deteriorations were similar in selected and control voles.The selection did not cause clear and strong changes in the rate of ageing process.