Comparative mitogenomics of the eulipotyphlan species (Mammalia, Eulipotyphla) provides novel insights into the molecular evolution of hibernation

Hibernation is an elaborate response strategy employed by numerous mammals to survive in cold conditions that involves active suppression of metabolism. Despite the role of mitochondria as energy metabolism centers during hibernation, the adaptive and evolutionary mechanisms of mitochondrial genes in hibernating animals, like hedgehogs in eulipotyphlan species, are not yet fully understood. In this study, we sequenced and assembled mitochondrial genomes of the hibernating four-toed hedgehog (Atelerix albiventris) and the non-hibernating Asian house shrew (Suncus murinus). While no significant positive selection was detected, we identified unique amino acid substitutions and accelerated evolutionary rates of mitochondrial proteins and the encoding genes in hibernating hedgehogs. Moreover, the distinctive evolutionary patterns indicated a potential link among the adaptive evolution of mitochondrial genes (such as ATP6, CYTB, and ND6), the phenotypes of hibernation and longevity in eulipotyphlan species. These three genes evolved rapidly in hibernating Erinaceidae species and exhibited significant correlations with the two distinct phenotypes, indicating their pivotal roles in the evolution of hibernation and longevity. These findings provide insights into the genetic mechanisms responsible for metabolic plasticity and longevity in eulipotyphlan hibernators, with implications for other mammalian taxa.