Identification of diverse viruses associated with grasshoppers unveils phylogenetic congruence between hosts and viruses

Locusts and grasshoppers are one of the most dangerous agricultural pests. Environmentally benign microbial pesticides are increasingly desirable for controlling locust outbreaks in fragile ecosystems. Here we use metagenomic sequencing to profile the rich viral communities in 34 grasshopper species and report 322 viruses, including 202 novel species. Most of the identified viruses are related to other insect viruses and some are targeted by antiviral RNAi pathway, indicating they infect grasshoppers. Some plant/fungi/vertebrate associated viruses are also abundant in our samples. Our analysis of relationships between host and virus phylogenies suggests that the composition of viromes is closely allied with host evolution, and there is significant phylogenetic relatedness between grasshoppers and viruses from Lispiviridae, Partitiviridae, Orthomyxoviridae, Virgaviridae and Flaviviridae. Overall, this study is a thorough exploration of viruses in grasshoppers and provide an essential evolutionary and ecological context for host-virus interaction in Acridoidea. Author SummaryLocusts are the most destructive migratory pest in the world and continue to cause massive damages that endanger food security and threaten millions of people in 21st century. While chemical pesticides are still heavily relied on, biological pesticides developed from natural pathogens offer a reliable, less harmful alternative for controlling locust outbreaks in fragile ecosystems. Unfortunately, little is known about natural pathogens infecting this pest. In this study, we profile the viral communities in 34 grasshopper species include some major swarming species. While we identified as many as 202 novel viral species associated with grasshoppers, some of them are of potential to be developed as biocontrol agents. Our analysis of relatedness of phylogenies of grasshoppers and associated viruses helps to shed light on the eco-evolutionary interactions between insects and viruses. This work provides a valuable dataset of both academic and applied interest.