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?

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.

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.

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.

Laboratory model of adaptive radiation: a selection experiment in the bank vole.

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.