Tunicate metatranscriptomes reveal evidence of ancient co-divergence between viruses and their hosts.

Abstract

Tunicates are a key transitional taxon in animal evolution as the closest extant invertebrate relatives of the vertebrates. Their RNA viruses may also reflect this transitional state, but this has not been tested. In particular, it is not known whether tunicate RNA viruses form a sister group to those found in vertebrates, indicative of virus-host co-divergence throughout the entire evolutionary history of the chordates. To address this key question in RNA virus evolution, we analyzed primary and publicly available RNA libraries to identify tunicate-associated RNA viruses and determine their phylogenetic relationships. Although the majority of the tunicate viruses identified were most closely related to those found in invertebrates or were not animal associated, others shared common ancestry with vertebrate influenza viruses, alphaviruses, and mononegaviruses, thereby extending the evolutionary timescales of these groups. We also showed that the recombination of glycoproteins between different orders of RNA viruses, including between positive- and negative-sense viruses, may have shaped the evolution of multiple lineages. Overall, our study reveals that some disease-causing RNA virus lineages have ancestries that date to the early chordates and highlights that the evolution of structural genes may be incongruent with that of the highly conserved RNA-dependent RNA polymerase.