Cool running: evolved reductions in body temperature and the metabolic costs of thermoregulation in deer mice native to high altitude

Abstract

The evolution of endothermy was instrumental to the diversification of birds and mammals, and enabled colonization of previously uninhabitable niches around the globe. However, in extreme environments such as high altitude, with extremely cold temperatures and limited O2 and food availability, the significant energetic demands of maintaining high body temperature (Tb) could offset the advantages of endothermy. We hypothesised that evolved reductions in Tb help overcome the metabolic challenges of cold hypoxia (CH) in deer mice native to high altitude. Deer mice with lowland or highland ancestry were held in warm normoxia (WN) or CH for 6 weeks, and then surgically instrumented with physiological telemeters. Mice in CH had significantly higher fH than mice in WN, underlain by reduced vagal tone and increased beta1-adrenergic tone on the heart, reflecting the metabolic challenges of CH. CH exposure led to marked reductions in Tb (~2˚C) in both lowlanders and highlanders. However, overlaid upon this plastic response to CH, highlanders had consistently lower Tb (~1˚C) than lowlanders. The combined effects of these plastic and evolved reductions in Tb were estimated to reduce metabolic demands by ~20%, based on theoretical expectations of Q10 effects and empirical measurements of the relationship between Tb and O2 consumption rate in these mice. Our results suggest that plastic and evolved reductions in Tb are important for overcoming the challenges at high altitudes, and provide a relatively rare example of evolved changes in Tb setpoint in a non-hibernating endotherm to cope with extreme environmental conditions.