The evolutionary history of vertebrate RNA viruses

Abstract

Our understanding of the diversity and evolution of vertebrate RNA viruses is largely limited to those found in mammalian and avian hosts and associated with overt disease. Here, using a large-scale meta-transcriptomic approach, we discover 214 vertebrate-associated viruses in reptiles, amphibians, lungfish, ray-finned fish, cartilaginous fish and jawless fish. The newly discovered viruses appear in every family or genus of RNA virus associated with vertebrate infection, including those containing human pathogens such as influenza virus, the Arenaviridae and Filoviridae families, and have branching orders that broadly reflected the phylogenetic history of their hosts. We establish a long evolutionary history for most groups of vertebrate RNA virus, and support this by evaluating evolutionary timescales using dated orthologous endogenous virus elements. We also identify new vertebrate-specific RNA viruses and genome architectures, and re-evaluate the evolution of vector-borne RNA viruses. In summary, this study reveals diverse virus-host associations across the entire evolutionary history of the vertebrates.

Expansion of the Metazoan Virosphere: Progress, Pitfalls, and Prospects

“…It has 'filled in' shallower parts of the tree, finding close relatives of iconic human pathogens, such as new influenzas in toads and eels (Shi et al 2018). It has also discovered new deep branches, such as clades of insectinfecting Partitiviruses (Webster et al 2015;Shi et al 2016a) and Luteo/Sobemo-like viruses (Tokarz et al 2014;Shi et al 2016a), and whole new families, such as the Chuviruses (Li et al 2015).…”

“…More importantly, metagenomics now contributes to our thinking on virus evolution. It has provided a better perspective on host-association and switching (Geoghegan et al 2017;Dolja and Koonin 2018;Shi et al 2018), found familiar virus lineages with unexpected genome sizes and structures (Li et al 2015;Shi et al 2016a;Shi et al 2016b), and uncovered an unexpectedly dynamic history of 'modular' protein swapping (Koonin et al 2015;Shi et al 2016a). Finally, merely having a PCR product from a metagenomic sample can provide an experimental route to the functional biology of an uncultured virus (van Mierlo et al 2014).…”

“…Tokarz et al 2018). The focus has subsequently expanded to include neglected animal lineages, identifying hundreds of new RNA viruses in arthropods and other invertebrates (Webster et al 2015;Shi et al 2016a;Roberts et al 2018;Waldron et al 2018), and recently in divergent and under-sampled chordates (Geoghegan et al 2018;Shi et al 2018).…”

Isolation of salmonid alphavirus subtype 6 from wild‐caught ballan wrasse, Labrus bergylta (Ascanius)

“…Nevertheless, the isolation of SAV6 from wild ballan wrasse would suggest that there is a greater diversity of alphavirus in the marine environment than previously thought, as suggested by Shi et al. () for RNA viruses in general.…”

“…Using a large‐scale meta‐transcriptomic approach, Shi et al. () reported the discovery of a number of previously undescribed RNA viruses, including alphaviruses, in fish, amphibians and reptiles. Thus, it would appear that the diversity of RNA viruses in the marine environment is greater than previously thought.…”