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

Abstract

Tomato spotted wilt orthotospovirus (TSWV) is a harmful pathogen that causes severe disease in tomato, pepper, and other horticultural and agronomic crops. The genome comprises three linear ssRNA molecules (segments L, M, and S) unequally packed in nucleocapsids. Although the genome structure and molecular mechanism of infection are well understood, the evolutionary dynamics require further analysis to know what we seek in this study: to determine the most probable viral ancestor, the date of divergence, the ancestral geographical source of dispersal, and the demographic history of TSWV. We employed the Bayesian framework to analyze whole genome sequences of 136 isolates of TSWV obtained from different sites worldwide and with a sampling window of 35 years. In independent analyses, we performed phylodynamic estimations with segment L, M, and S sequence data. Our results showed that the clock rates of different genome segments ranged from 1.678x10-4 to 2.444x10-4 substitutions/site/year. Likewise, the time to the most recent common ancestor shows variations according to the dataset used for the inferences; however, the most probable date of TSWV divergence is around 1768 CE. Our phylogeographic exploration showed concordant results for the three genomic segments analyzed; that is, the TSWV population originated in South Korea and, from there, early 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 increase of the agricultural frontier and the emergence of new species of insect vectors.