Evolution of UCP1 Gene and Its Significance to Temperature Adaptation in Rodents

Adaptive thermogenesis comprises shivering thermogenesis dependent on skeletal muscles and non-shivering thermogenesis (NST) mediated by uncoupling protein 1 (UCP1). Although the thermogenic function of UCP1 was adopted early in some placental mammals, positive selection predominantly occurred in the ancestral branches of small-bodied species. Some previous studies have revealed that rodents living in northern or high mountain regions adapt to cold environments by increasing NST, whereas those living in tropical and subtropical regions that are not exposed to cold stress express low concentrations of UCP1, indicating that UCP1 may have evolved to adapt to ambient temperatures. In this study, we explored the evolution of UCP1 and its significance to temperature adaptation by performing detailed evolutionary and statistical analyses on 64 rodents with known genomes. As a result, a total of 71 UCP1 gene sequences were obtained, including 47 intact genes, 22 partial genes, and 2 pseudogenes. Further, 47 intact genes and 3 previously published intact UCP1 genes were incorporated into evolutionary analyses, and correlation analyses between evolutionary rate and ambient temperatures (including average annual temperature, maximum temperature, and minimum temperature) of the rodent survives were conducted. The results show that UCP1 is under purifying selection (omega = 0.11), and among rodents with intact UCP1 sequences, Urocitellus parryii and Dicrostonyx groenlandicus-the two species with the lowest ambient temperatures among the rodents used here-have higher evolutionary rates than others. In the statistical analyses, in addition to ambient temperatures, body weight and weight at birth were also taken into account since weight was previously proposed to be linked to UCP1 evolution. The results showed that after controlling for the phylogenetic effect, the maximum temperature was significantly negatively correlated with the evolutionary rate of UCP1, whereas weight did not have a relationship with UCP1 evolutionary rate. Consequently, it is suggested that ambient temperature can drive the evolution of rodent UCP1, thereby enhancing NST adaptation to cold stress.