Revealing the potential transmission route of Cnaphalocrocis medinalis granulovirus capable of persistently causing granulosis epidemics

As crucial regulators of insect populations in nature, baculoviruses are promising biopesticides. However, due to the scarcity of individuals with overt disease and the sporadic nature of the epidemic, our knowledge of baculovirus ecology is very limited, which impacts the effective utilization of these viruses in biocontrol. Cnaphalocrocis medinalis granulovirus (CnmeGV) specifically infects the rice leaffolder, which is the main pest of rice. In this study, we identified a population of CnmeGV that can cause a persistent epizootic in Dahuai town, Enping County, Guangdong Province, China. We sequenced the whole genomes of 138 CnmeGV isolates collected from Dahuai town for four years, reporting for the first time the genetic structure of a natural population of baculovirus. The results indicated that a long-term endemic population of CnmeGV displayed substantial genetic variation. The discriminant analysis of principal components revealed that the genetic structure of CnmeGV is clearly differentiated annually and seasonally (by the rice-growing season). CnmeGV epidemics typically occur in three waves (W1, W2, and W3) during each rice-growing season. Although the genetic structures of the CnmeGV isolates within the same rice-growing season were closely related, nucleotide diversity analysis revealed that the CnmeGV genomes exhibit higher heterozygosity levels in the initial epidemic wave compared to subsequent waves. We also found that host behaviour, virus distribution, plant structure, and weather are important factors in the recurrence of CnmeGV epizootics. Leveraging these ecological insights, we revealed the potential transmission route of CnmeGV, named 'From W1 in sheath to W2+ in fold', during continuous epidemics in natural environments. This study provides important insights into the ecology and evolution of host-pathogen interactions and the route helps develop more effective biocontrol strategies.