The Study On Molecular Mechanisms Of Leptopilina Wasps Manipulating Host Behavior To Avoid Superparasitism

Parasitoid wasps have been widely used in biological control pest insects.Among parasitic species,the most fundamental and intriguing competition behaviours are superparasitism and superparasitism avoidance;however,the underlying mechanisms and ecological contexts of these phenomena are largely unknown.Here,we apply the Drosophila parasite Leptopilina as a study system and find that this solitary endoparasitic wasp provokes a host escape response for superparasitism avoidance.This behavior modification depends on the induction of reactive oxygen species(ROS)in the host central nervous system(CNS).We further find that ROS induction and escape behavior require both inputs of venom and the parasitoid-derived odors.1.Venom is required to induce the escape behaviour of hosts.We firstly find that the parasitoid venom is the main factor to trigger the escape behavior of the parasitized hosts.Then we have combined multi-omics and in vivo functional studies to characterize a small set of RhoGAP domain-containing genes that confer the manipulation of host escape by inducting ROS in the host CNS.We further uncover the underlying evolutionary scenario,showing that the neofunctionalization and specialization gave rise to the novel role of RhoGAP domain in avoiding superparasitism,with multiple duplication events in the genomes of Leptopilina wasps.2.Parasitoid-derived odorants are necessary for host escape behavior.We have identified two wasp-derived odorants,isoiridomyrmecin and actinidine,which can induce ROS levels in the CNS of parasitized host larvae,are important for host escape behavior.We also discover that isoiridomyrmecin is the ligand of Drosophila Or49 a and that actinidine is the ligand for two different Drosophila odor receptors,Or49 a and Or67 b.Overall,parasitoid odorants contribute together with venom to the induction of ROS levels in the host CNS and to promote parasitized-host escape behavior.3.Parasitoids utilize host escape behavior to avoid superparasitism.After dissecting the escapes and non-escaped hosts,we find extra number of eggs are laid in the non-escaped hosts.These results suggest that the Leptopilina wasps can take advantage of this host escape behavior to avoid superparasitism and avoid the intraspecific competition.Thus,we find a strategy by which venom protein and ordorants emitted by parasitoids induce a behavior in the host that can be recognized by the wasp to limit superparasitism.Our study demonstrates that superparasitism avoidance is adaptive and provides key empirical evidence to show the long-term effect of intraspecific competition in driving niche expansion and speciation.These findings provide the detailed molecular insights into a mechanism by which parasites alter host behavior and the possible function to increase the reproductive efficiency of agriculturally and ecologically important parasitic wasp species.