The aerobic capacity model postulates that high basal metabolic rates (BMR) associated with endothermy evolved as a correlated response to the selection on maximum, peak metabolic rate Vo2max. Furthermore, the model assumes that BMR and Vo2max are causally linked, and therefore, evolutionary changes in their levels cannot occur independently. To test this, we compared metabolic and anatomical correlates of selection for high and low body mass-corrected BMR in males of laboratory mice of F18 and F19 selected generations. Divergent selection resulted in between-line difference in BMR equivalent to 2.3 phenotypic standard deviation units. Vo2max elicited by forced swimming in 20 degrees C water was higher in the low BMR than high BMR line and did not differ between the lines when elicited by exposure to heliox at -2.5 degrees C. Moreover, the magnitude of swim- and heliox-induced hypothermia was significantly smaller in low BMR mice, whereas their interscapular brown adipose tissue was larger than in high BMR mice. Our results are therefore at variance with the predictions of aerobic capacity model. The selection also resulted in correlated response in food consumption (C) and masses of metabolically active internal organs: kidneys, liver, small intestine, and heart, which fuel maximum, sustained metabolic rate (SusMR) rather than Vo2max. These correlated responses were strong enough to claim the existence of positive, genetic correlations between BMR and the mass of viscera as well as C. Thus, our findings support the suggestion that BMR evolved as a correlated response to selection for SusMR, not Vo2max. In functional terms BMR should therefore be interpreted as a measure of energetic costs of maintenance of metabolic machinery necessary to sustain high levels of energy assimilation rate.

Basal metabolic rate (BMR) provides a widely accepted benchmark of metabolic expenditure for endotherms under laboratory and natural conditions. While most studies examining BMR have concentrated on inter-specific variation, relatively less attention has been paid to the determinants of within-species variation. Even fewer studies have analysed the determinants of within-species BMR variation corrected for the strong influence of body mass by appropriate means (e.g. ANCOVA). Here, we review recent advancements in studies on the quantitative genetics of BMR and organ mass variation, along with their molecular genetics. Next, we decompose BMR variation at the organ, tissue and molecular level. We conclude that within-species variation in BMR and its components have a clear genetic signature, and are functionally linked to key metabolic process at all levels of biological organization. We highlight the need to integrate molecular genetics with conventional metabolic field studies to reveal the adaptive significance of metabolic variation. Since comparing gene expressions inter-specifically is problematic, within-species studies are more likely to inform us about the genetic underpinnings of BMR. We also urge for better integration of animal and medical research on BMR; the latter is quickly advancing thanks to the application of imaging technologies and ‘omics’ studies. We also suggest that much insight on the biochemical and molecular underpinnings of BMR variation can be gained from integrating studies on the mammalian target of rapamycin (mTOR), which appears to be the major regulatory pathway influencing the key molecular components of BMR.

Artificial selection experiments are potentially powerful, yet under-utilized tool of evolutionary and physiological ecology. Here we analyze and review three important aspects of such experiments. First, we consider the effects of instrumental measurement errors and random fluctuations of body mass on the total phenotypic variation. We illustrate this with the analysis of measurements of oxygen consumption in an open-flow respirometry set-ups. We conclude that measurement errors and fluctuations of body mass are likely to reduce the repeatability of oxygen consumption by about one third. Using published estimates of repeatability of metabolic rates we also showed that it does not tend to decline with increasing time between measurements. Second, we review data on narrow sense heritability (h(2)) of metabolic rates in mammals. The results are equivocal: many studies report very low (∼0.1) h(2), whereas some recent studies (including our own estimates of h(2) in laboratory mice, obtained by means of parent-offspring regression) report significant h(2) ≥ 0.4. Finally, we discuss consequences of the lack of replicated lines in artificial selection experiments. We focus on the confounding effect of genetic drift on statistical inferences related to primary (selected) and secondary (correlated) traits, in the absence of replications. We review literature data and analyze them following the guidelines formulated by Henderson (1989, 1997). We conclude that most results obtained in unreplicated experiments are probably robust enough to ascribe them to the effect of selection, rather than genetic drift. However, Henderson's guidelines by no means should be treated as a legitimate substitute of the analysis of variance, based on replicated lines.

Summary1. It has been hypothesized that the induction of silicon (Si)-based plant defence in response to herbivore damage may engender rodent population cycles. Many studies have also considered accumulation of Si as a process controlled by geo-hydrological factors. 2. To test these ideas, we investigated the relationship between concentration of Si in fibrous tussock sedge (Carex appropinquata) and the population density of a major sedge consumer, the root vole (Microtus oeconomus), in field enclosures in natural habitat under a variety of natural water regimes and weather conditions. 3. We found that a high density of voles at the end of summer resulted in the immediate accumulation of Si by rhizomes, followed by accumulation of Si in leaves with a 1-year lag time. The level of river flooding in the same year had an additional impact on Si concentration in rhizomes but did not affect silicification of leaves. 4. Overwinter changes in concentration of Si in sedges were influenced by fluctuations in ambient temperature and the depth of snow cover (multiple freeze-thaw cycles), thus affecting the quality of winter food available for voles. 5. Smaller voles had lower mortality during early winter than large voles, which seemed to be connected with changes in the quality of the autumn rather than the winter food base. Winter survival of voles was not associated with Si concentration in their faeces, however. 6. Our results suggest that changes in Si concentration in fibrous tussock sedge can be induced by changes in vole population density and are also additionally affected by the amount of flooding and weather conditions.

Proximal mechanisms describing the evolution of high levels of basal metabolic rate (BMR) in endotherms are one of the most intriguing problems of evolutionary physiology. Because BMR mostly reflects metabolic activity of internal organs, evolutionary increase in BMR could have been realized by an increase in relative organ size and/or mass-specific cellular metabolic rate. According to the "membrane pacemaker" theory of metabolism, the latter is mediated by an increase in the average number of double bonds (unsaturation index) in cell membrane fatty acids. To test this, we investigated the effect of divergent artificial selection for body-mass-corrected BMR on the mass of internal organs and the fatty acid composition of cell membranes in laboratory mice (Mus musculus). Mice from the high-BMR line had considerably larger liver, kidneys, heart, and intestines. In contrast, the unsaturation index of liver cell membranes was significantly higher in low-BMR mice, mainly because of the significantly higher content of highly polyunsaturated 22 : 6 docosahexanoic fatty acid. Thus, divergent selection for BMR did not affect fatty acyl composition of liver and kidney phospholipids in the direction predicted by the membrane pacemaker theory. We conclude that an intraspecific increase in BMR may rapidly evolve mainly as a result of the changes in size of internal organs, without simultaneous increase of the unsaturation index in cell membrane lipids.