Revisiting Orthotospovirus Phylogeny Using Whole Genomic Data and a Hypothesis for their Geographic Origin and Diversification

The family Tospoviridae, a member of the Bunyavirales order, is constituted of tri-segmented negative-sense single-stranded RNA viruses that infect plants and are also able of replicating in their insect vectors in a persistent manner. The family is composed of a single genus, the Orthotospovirus, whose type species is Tomato spotted wilt virus (TSWV). Previous studies assessing the phylogenetic relationships within this genus were based upon partial genomic sequences, thus resulting in unresolved clades and a poor assessment of the roles of recombination and genome shuffling during mixed infections. Complete genomic data for most Orthotospovirus species are now available at NCBI genome database. In this study we have used 62 complete genomes from 20 species. Our study confirms the existence of four phylogroups (A to D), grouped in two major clades (A-B and C-D), within the genus. We have estimated the split between the two major clades [~]3,100 years ago shortly followed by the split between the A and B phylogroups [~]2,860 years ago. The split between the C and D phylogroups happened more recently, [~]1,465 years ago. Segment reassortment has been shown to be important in the generation of novel viruses. Likewise, within-segment recombination events have been involved in the origin of new viral species. Finally, phylogeographic analyses of representative viruses suggests the Australasian ecozone as the possible origin of the genus, followed by complex patterns of migration, with rapid global spread and numerous reintroduction events. IMPORTANCEMembers of the Orthotospovirus genus infect a large number of plant families, including food crops and ornamentals, resulting in multimillionaire economical losses. Despite this importance, phylogenetic relationships within the genus were established years ago based in partial genomic sequences. A peculiarity of orthotospoviruses is their tri-segmented negative sense genomes, which makes segment reassortment and within-segment recombination, two forms of viral sex, potential evolutionary forces. Using full genomes from all described orthotospovirus species, we revisited their phylogeny and confirmed the existence of four major phylogroups with uneven geographic distribution. We have also shown a pervasive role of sex in the origin of new viral species. Finally, using Bayesian phylogeographic methods, we assessed the possible geographic origin and historical dispersal of representative viruses from the different phylogroups.