Keeping up with heat: skeletal muscle mitochondrial coupling efficiency under physiological hyperthermia

Birds and mammals are endotherms that maintain a high and relatively constant body temperature. During intense muscular activity, body temperature can rise significantly, reaching up to ∼44°C and ∼42°C in the skeletal muscle of birds and mammals, respectively. Locomotor skeletal muscles are therefore subject to substantial thermal fluctuations, which may affect numerous cellular processes, including mitochondrial oxidative phosphorylation. The present study investigated the thermal sensitivity of mitochondrial coupling efficiency in the skeletal muscles of pigeons (Columba livia) and rats (Rattus norvegicus). Mitochondrial function was assessed in vitro across specific resting temperatures (37°C for rats, 40°C for pigeons) and under a physiological hyperthermia condition mimicking exercise-induced muscle heating for both species (43°C). Our results reveal a greater temperature-dependent decline in maximum mitochondrial coupling efficiency in rats relative to pigeons, and further highlight distinct bioenergetics flexibility strategies between the two species. In rats, mitochondria adopt a more dissipative strategy, characterized by elevated proton leakage, sacrificing coupling efficiency in favour of a stable oxidative cost. In pigeon, mitochondria engage complex II as a compensatory mechanism, partially buffering coupling efficiency decline at the expense of a higher oxidative cost. Together, these results highlight the specific flexibility of mitochondrial responses to physiological hyperthermia in pigeon and rat. However, broader bioenergetics comparisons across a wider range of avian and mammal species will be necessary to uncover evolutionary patterns and discriminate mechanisms conserved in endotherms from those representing independent adaptations specific to each vertebrate group.