Does selection for behavioral and physiological performance traits alter glucocorticoid responsiveness in bank voles?

One of the key elements of an animal's Darwinian fitness is its ability to adequately respond to and cope with challenging situations. Glucocorticoid hormones, such as corticosterone, affect an organism's ability to overcome such challenges. We hypothesized that changes in the glucocorticoid response curve contribute to the evolution of increased performance during challenging conditions, and tested it on bank voles (Myodes glareolus) from a multidirectional artificial selection experiment, which involves lines selected for high aerobic exercise metabolism achieved during swimming (A - Aerobic), predatory behavior towards a cricket (P - Predatory) and ability to maintain body mass on a low-quality herbivorous diet (H - Herbivorous), as well as unselected control lines (C - Control). We elicited a glucocorticoid response either by restraining the animal or by maximum pharmacological stimulation, and measured plasma corticosterone levels at baseline, during the response and during the recovery phase. Response-level corticosterone was higher in females, and recovery from maximal level was faster than that of males. Selection did not affect baseline or stress-induced corticosterone levels, but it decreased the maximum corticosterone level in Aerobic and Predatory lines, reducing the difference between stress-induced and maximum levels. Recovery from restraint-induced corticosterone level tended to be slower in the Herbivorous than in the other lines, an effect that was stronger in females than in males. In conclusion, successful selection for increased performance in challenging conditions was not associated with changes in absolute values of the glucocorticoid response to stress, but can affect other characteristics of the glucocorticoid response curve.

Stress coping and evolution of aerobic exercise performance: corticosterone levels in voles from a selection experiment.

The locomotor performance achieved in a challenging situation depends not only on physiological limitations, such as the aerobic exercise capacity, but also on behavioral characteristics, such as adequate coping with stress. The stress response is mediated largely by the hypothalamic-pituitary-adrenal (HPA) axis, through modulated release of glucocorticoids. We used a unique experimental evolution model system to test the hypothesis that the evolution of an increased aerobic exercise performance can be facilitated by modification of the glucocorticoid-related stress-coping mechanisms. Bank voles (Myodes glareolus) from 'aerobic' (A) lines, selected for 22 generations for high maximum swim-induced rate of oxygen consumption (V̇O2,swim), achieved a 64% higher V̇O2,swim than those from unselected, control lines. The temporal pattern of exercise during the swimming trial also evolved, and the A-line voles achieved V̇O2,swim later in the course of the trial, which indicates a modification of the stress response characteristics. Both V̇O2,swim and the average metabolic rate measured during the trial tended to increase with baseline corticosterone level, and decreased with the post-exercise corticosterone level. Thus, increased baseline corticosterone level promotes high metabolic performance, but a high corticosterone response to swimming acts as an inhibitor rather than stimulator of intense activity. However, neither of the corticosterone traits differed between the A-selected and control lines. Thus, the experiment did not provide evidence that evolution of increased aerobic performance is facilitated by the modification of glucocorticoid levels. The results, however, do not exclude the possibility that other aspects of the HPA axis function evolved in response to the selection.

Experimental evolution of aerobic exercise performance and hematological traits in bank voles.

The maximum rate of aerobic exercise metabolism (VO2max) is a trait informative from both medical and evolutionary perspective, and both the physiological mechanisms limiting its level and its evolution are subject to vivid debate. Both comparative analyses and studies on the effects of training or acclimation to aerobically-demanding conditions suggest a role of oxygen transport-related properties of blood in limiting VO2max. Here we used a unique experimental evolution model - lines of bank voles selected for high rate of swim-induced aerobic metabolism (VO2swim; A lines), which evolved a 60% higher VO2swim than that observed in unselected control lines (C) - and asked how the hematological parameters evolved in response to the selection. Voles from the A lines had a decreased hemoglobin concentration in cardiac blood samples (adjusted means ±â€¯SE, A: 14.7 ±â€¯1.1, C: 15.3 ±â€¯1.1 g/dl; p = .008), hematocrit (A: 51.7 ±â€¯4.5, C: 53.8 ±â€¯4.2%; p = .042) and tended to have less erythrocytes per microliter of blood (A: 11.5 ±â€¯1.4, C: 12.7 ±â€¯1.3 mln/µl; p = .083). The effect of selection was more pronounced in males than in females. Thus, selection for high aerobic-exercise performance resulted in a paradoxical decrease in traits positively associated with oxygen-carrying capacity per unit of blood volume, and the effect was sex-dependent. However, as a decreased blood viscosity associated with the lowered hematocrit reduces the costs of blood circulation, it can be hypothesized that the change can actually boost the oxygen supply to peripheral tissues.

Evolution of an increased performance under acute challenge does not exacerbate vulnerability to chronic stress.

An adequate stress response plays a vital role in coping with challenges. However, if selection for improved coping with an acute challenge affects the entire stress response system, susceptibility to adverse effects of chronic stressors can be deepened. Here, we used bank voles from lines selected for high swim-induced aerobic metabolism (A) and unselected control (C), and asked if the selection affected sensitivity to chronic mild stress (CMS). The voles were first habituated to daily weighing and feces collection for three weeks, and then for two weeks were exposed to CMS or remained undisturbed. The habituation itself resulted in an increased swim-induced oxygen consumption in both line types, and a decreased body mass. The CMS treatment caused reduction of food consumption in the second week of the experiment, and, in males, a decline in the metabolic rate. Paradoxically, fecal corticosterone metabolites decreased in the CMS-treated group. The response to CMS did not differ between the line types. Thus, the selection for increased performance was not traded off by increased vulnerability to chronic stress. The counter-intuitive results may even lead to a speculation that bank voles-and perhaps also other animals-prefer experiencing unpredictable, unpleasant stressors over the monotony of standard laboratory housing.