Ancient mitochondrial pseudogenes reveal hybridization between distant lineages in the evolution of the Rupicapra genus

Abstract

Mitochondrial pseudogenes (numts) inserted in the nuclear genome are frequently found in population studies. Its presence is commonly connected with problems and errors when they are confounded with true mitochondrial sequences. In the opposite side, numts can provide valuable phylogenetic information when they are copies of ancient mitochondrial lineages. We show that Rupicapra individuals of different geographic origin from the Cantabrian Mountains to the Apennines and the Caucasus share a nuclear COI fragment. The numt copies are monophyletic, and their pattern of differentiation shows two outstanding features: a long evolution as differentiated true mitochondrial lineage, and a recent integration and spread through the chamois populations. The COI pseudogene is much older than the present day mitochondrial clades of Rupicapra and occupies a basal position within the Rupicapra-Ammotragus- Arabitragus node. Joint analysis of this numt and a cytb pseudogene with a similar pattern of evolution places the source mitochondrial lineage as a sister branch that separated from the Ammotragus-Arabitragus lineage 6 million years ago (Mya). The occurrence of this sequence in the nucleus of chamois suggests hybridization between highly divergent lineages. The integration event seems to be very recent, more recent than the split of the present day mtDNA lineages of Rupicapra (1.9 Mya). This observation invites to think of the spread across the genus by horizontal transfer through recent male-biased dispersal.