Contrasting Evolutionary Dynamics and Global Dissemination of the DNA-A and DNA-B Components of Watermelon Chlorotic Stunt Virus.

Watermelon chlorotic stunt virus (WmCSV), a bipartite begomovirus, poses a severe and expanding threat to global cucurbit and watermelon production, driving an urgent need to unravel its genetic diversity indices and evolutionary complexities. To elucidate its evolutionary history, this study investigated the genetic diversity, evolutionary dynamics, and global dispersal of its genomic components, DNA-A (WmA) and DNA-B (WmB). The analyses uncovered striking contrasts between the components. WmB exhibited markedly greater genetic diversity (π = 0.0508 vs. 0.0119 for WmA), a slightly faster evolutionary rate (1.26 × 10-4 vs. 1.44 × 10-3 substitutions/site/year), and a far more complex recombination profile, with 34 events detected compared to only one in WmA. The abundance of recombination breakpoints in WmB underscores its central role in shaping genomic variability and adaptive potential. Phylogenetic analyses of both components unveil eight robustly supported clades per segment, predominantly shaped by geographical boundaries, hinting at localized evolutionary trajectories with constrained long-distance gene flow, with the exception of Oman. Bayesian time-scaled phylogenies and phylogeographic reconstructions further illuminate distinct dissemination pathways, suggesting an intriguing origin, with WmA likely emerging from the United States and WmB tracing back to Saudi Arabia, while the Middle East emerges as a dynamic epicenter for regional spread and subsequent incursions into the Americas. Together, these findings reveal contrasting evolutionary forces driving WmCSV diversification and provide critical insights into its origins and ongoing global emergence.