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 UCP1 in the Chacoan peccary (Catagonus wagneri), a member of the Tayassuid lineage that diverged from pigs during the late Eocene-mid Oligocene. Exons 1 and 2 have been deleted in peccary UCP1 and the remaining exons display additional inactivating mutations. A common nonsense mutation in exon 6 revealed that UCP1 was pseudogenized in a shared ancestor of pigs and peccaries. Our selection pressure analyses indicate that the inactivation occurred 36.2-44.3 MYA during the mid-late Eocene, which is much earlier than previously thought. Importantly, pseudogenized UCP1 provides the molecular rationale for cold sensitivity and current tropical biogeography of extant peccaries.