Here and there, but not everywhere: Repeated loss of uncoupling protein 1 in amniotes

Abstract

Endothermy is an evolutionary innovation in eutherian mammals and birds. In eutherian mammals, UCP1 is a key protein in adaptive nonshivering thermogenesis (NST). Although ucp1 arose early in the vertebrate lineage, the loss of ucp1 was previously documented in several reptile species (including birds). Here we determine that ucp1 was lost at the base of the reptile lineage, as we fail to find ucp1 in every major reptile lineage. Furthermore, though UCP1 plays a key role in mammalian NST, we confirm that pig has lost several exons from ucp1 and conclude that pig is not a sole outlier as the only eutherian mammal lineage to do so. Through similarity searches and synteny analysis, we show that ucp1 has also been lost/pseudogenized in Delphinidae (dolphin, orca) and potentially Xenarthra (sloth, armadillo) and Afrotheria (hyrax). These lineages provide models for investigating alternate mechanisms of thermoregulation and energy metabolism in the absence of functional UCP1. Further, the repeated losses of a functional UCP1 suggest the pervasiveness of NST via UCP1 across the mammalian lineage needs re-evaluation.