Evolutionary origin and demographic trajectory of tomato spotted wilt virus (Orthotospovirus tomatomaculae)

Tomato spotted wilt virus (TSWV) is a harmful pathogen that causes severe disease in tomato, pepper, and other horticultural and agronomic crops. Its genome comprises three linear single-stranded RNA molecules (segments L, M, and S), which are unequally packed in nucleocapsids. Although its genome structure and molecular mechanism of infection are well understood, the evolutionary dynamics of this virus require further analysis to determine the most probable viral ancestor, the date of divergence, the ancestral geographical source of dispersal, and the demographic history of TSWV. For this, we employed a Bayesian framework to analyze whole-genome sequences of 136 isolates of TSWV obtained from different sites worldwide with a sampling window of 35 years, and phylodynamic analysis was performed separately for segments L, M, and S. Our results showed that the mutation rates of the different genome segments ranged from 1.678 × 10^- 4 to 2.444 × 10^- 4 substitutions/site/year. Although the estimated time to the most recent common ancestor varied depending on the dataset used, the most probable date of TSWV divergence was around 1768 CE. Our phylogeographic analysis yielded concordant results for the three genome segments, indicating that the TSWV population originated in South Korea and, from there, first expanded to Europe and then to North America and other continents. Past population dynamics analysis showed that the virus experienced two major population expansions that coincided with the expansion of the agricultural frontier and the emergence of new species of insect vectors.