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

Abstract

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 (V̇O 2,swim), achieved a 64% higher V̇O 2,swim than those from unselected, control lines. The temporal pattern of exercise during the swimming trial also evolved, and the A-line voles achieved V̇O 2,swim later in the course of the trial, which indicates a modification of the stress response characteristics. Both V̇O 2,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.

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

“…1). This finding is similar to what was observed in brown lemmings (Fauteux et al, 2017), California mice (Dlugosz et al, 2012) and our earlier study on bank voles (Lipowska et al, 2019). The variation may be associated with the pulsatile character of corticosterone release in non-challenged animals: as found in rats, plasma corticosterone levels fluctuate by one or more orders of magnitude in the course of less than an hour (Carnes et al, 1989;Sarabdjitsingh et al, 2012;Windle et al, 1998).…”

“…The selection was applied mostly within families, but if more than 16 families were available, families in which all individuals scored below the line mean were excluded. Details of the colony origin, the selection protocol, animal husbandry and results of selection in successive generations are presented in our earlier work (Chrza scik et al, 2014;Sadowska et al, 2015Sadowska et al, , 2008Lipowska et al, 2019;Maiti et al, 2019).…”

“…The samples were analyzed in two batches representing parts of the experiment performed on animals from the two generations of selection, but within each generation the order in which the samples were analyzed was randomized. In generation 23, the samples were analyzed alongside samples from another experiment (Lipowska et al, 2019); therefore, in this generation the analyses spanned more (37) assays than in generation 22 (24 assays). The intra-assay variation equaled 9.29% in generation 22 and 9.80% in generation 23, and the inter-assay coefficient of variation equaled 11.3% and 13.8%, respectively.…”

“…This is reflected, for instance, by increased glucocorticoid levels observed during breeding (Kenagy and Place, 2000;Romero, 2002), at low ambient temperatures (de Bruijn and Romero, 2018) or following intense physical activity (Coleman et al, 1998;Duclos and Tabarin, 2016;Hill et al, 2008). However, a strong glucocorticoid response to metabolically demanding situations may hinder rather than promote an animal's performance (Breuner et al, 1998;Lipowska et al, 2019;Munck and Náray-Fejes-Tóth, 1992;Wingfield and Ramenofsky, 1999). Moreover, prolonged elevation of glucocorticoids can compromise an organism's health (Cohen et al, 2007;Sapolsky et al, 2000).…”

“…Importantly, voles do not have to swim vigorously to stay on the water surface. Thus, the selection favored both the eagerness to work and a high metabolic performance per se, both of which increased in the aerobic lines (Jaromin et al, 2016(Jaromin et al, , 2018(Jaromin et al, , 2019Lipowska et al, 2019); the Aerobic voles spent more time actively swimming and also swam more regularly, and in only about 5% cases, compared with about 15% in control lines, the swimming trial had to be interrupted to prevent drowning. The Aerobic voles were also more active in their home cages and in open field tests (Maiti et al, 2019), and have increased basal metabolic rate (Sadowska et al, 2015), daily food consumption and thermogenic capacity (Dheyongera et al, 2016).…”