Neofunctionalization of the UCP1 mediated the non-shivering thermogenesis in the evolution of small-sized placental mammals

Abstract

The acquisition of UCP1-mediated non-shivering thermogenesis (NST) was an important event during the evolution of mammals. Here, we assessed the thermogenic neofunctionalization that occurred in the mammalian UCP1, by performing detailed comparative evolutionary genomics analyses (including phylogenetic and selection analyses) of the UCP family members across all major vertebrate classes. Heterogeneously distributed positive selection signatures were found in several UCPs, being preferably located in the mitochondrial matrix domains. Additionally, comparisons with non-mammalian orthologs showed increased evolutionary rates of the mammalian UCP1, not observable in the phylogenetically related UCP2 and UCP3 paralogs. Also, parallel signatures of episodic positive selection (ω > 1) were found in the ancestral branches of both Glires (rodents and lagomorphs) and Afroinsectivores (afrosoricids and macroscelids), underlining the importance of the UCP1 thermogenic activity in these mammalian groups. Finally, we hypothesize that the independent positive selection events that occurred in these two lineages resulted in two UCP1-mediated NST approaches, namely the cold acute response in the Glires and the reproduction success enhancement in the Afroinsectivores.