Disruption of thermogenic UCP1 predated the divergence of pigs and peccaries

Abstract

Uncoupling protein 1 (UCP1) governs non-shivering thermogenesis in brown adipose tissue. It has been estimated that pigs lost UCP1 ∼20 million years ago (MYA), dictating cold intolerance among piglets. Our current understanding of the root causes of UCP1 loss are, however, incomplete. Thus, examination of additional species can shed light on these fundamental evolutionary questions. Here, we investigated Chacoan peccary (Catagonus wagneri) UCP1, a member of the Tayassuid lineage that diverged from pigs during the Late Eocene-Mid Oligocene. Peccary UCP1 exons 1 and 2 have been deleted while the remaining exons display additional inactivating mutations. A common nonsense mutation in exon 6 reveals UCP1 was pseudogenized in a shared ancestor of pigs and peccaries. Our selection pressure analyses indicate the inactivation occurred much earlier, 36.2-44.3 MYA during the mid-late Eocene, than previously thought. Importantly, pseudogenized UCP1 provides the molecular basis for cold sensitivity and current tropical biogeography of extant peccaries.