Does Basal Metabolism Set the Limit for Metabolic Downregulation during Torpor?

Abstract

The evolution of endothermic thermoregulation is rooted in the processes involving high metabolism, which allows the maintenance of high and stable body temperatures (Tb). In turn, selection for high endothermic metabolism correlates with increased size of metabolically active organs and thus with high basal metabolic rate (BMR). Endothermic animals are characterized by an MR several times that of similar-sized ectotherms. However, many small mammals are temporally heterothermic and are able to temporally decrease Tb and MR by entering daily torpor or hibernation. Both BMR and minimum MR during torpor (TMRmin) likely result from oxidative respiration in mitochondria of the same tissues. It should be expected that these two MRs are positively correlated, suggesting that the evolution of endothermy and higher BMR set the limit for the ability to reduce MR while entering torpor. Using published data for 96 mammal species, we tested the hypothesis that, among heterothermic mammals, the processes leading to the evolution of higher BMR limit the ability to downregulate metabolism during torpor. We found that body mass (mb)-adjusted BMR was positively correlated with mb- and Tb-adjusted TMRmin, in a phylogenetically corrected analysis. Phylogenetic path modeling indicated that the mechanisms underlying the evolutionary increase of BMR in endotherms most likely constrain their ability to reduce MR during torpor. Given that heterothermy is considered an ancestral state in mammals, these results suggest an increase in BMR during the evolution of endothermy in homeothermic animals, which leads to the loss of their ability to enter torpor.