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

Abstract

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.

Keywords: aerobic metabolism; endothermy; experimental evolution; food habits.

Figure 1.

Direct phenotypic responses to 11 generations of selecting bank voles towards (a) high swim-induced aerobic metabolism, (b) herbivorous capability measured as ability to maintain body mass in a test with low-quality diet, (c) predatory propensity measured as ranked time to attack a cricket, and (d) comparison of the cumulative effects of selection in the three directions expressed as a difference between the means of four selected (in each direction) and four control lines (expressed in units of phenotypic standard deviation). In generation 8, the food used in selection trial in the ‘herbivorous’ lines was different than in other generations, which resulted in the irregular pattern (marked with dashed lines and open symbols on graphs (b) and (d)). (Online version in colour.)

Figure 2.

Adjusted least-square means from mixed ANCOVA models (±95% CIs) of (a) body mass measured before BMR trials (g; all individuals) and (b) basal metabolic rate (ml O₂ h⁻¹), in male and female voles from lines selected in three directions (A, Aerobic; P, Predatory and H,Herbivorous) and unselected control (C) lines. The values are back-transformed from the analyses on log-transformed data. Lowercase letters (abc) indicate selection groups not statistically different at p = 0.05 (Tukey–Kramer post hoc pairwise comparisons). Open symbols denote males, and filled symbols females. (Online version in colour.)

Figure 3.

The relationship between BMR and body mass (note the log–log scale) in voles from all four selection directions. The slopes of the lines did not differ significantly (note that the values are not adjusted for any other effects used for calculation of the adjusted means presented on figure 2b; common slope from the ANCOVA model ± s.e. = 0.78 ± 0.04). (Online version in colour.)