Agricultural crops around the world are attacked by approximately 3,000–10,000 species of pest insect. There is increasing interest in resolving this problem using environmentally friendly approaches. Wolbachia (Hertig), an insect endosymbiont, can modulate host reproduction and offspring sex through cytoplasmic incompatibility (CI). The incompatible insect technique (IIT) based on CI-Wolbachia is a promising biological control method. Previous studies have reported an association between CI and Wolbachia density, which may involve a quorum sensing (QS) mechanism. In this study, we investigated the effect of manipulating QS in Wolbachia using several chemicals including 3O-C12-HSL; C2HSL; spermidine (QS inducers), 4-phenylbutanoyl; and 4-NPO (QS inhibitors) on American serpentine leafminer (Liriomyza trifolii [Burgess]), an agricultural pest. The results showed that inducing QS with 3O-C12-HSL decreased the proportion of hatched eggs and increased Wolbachia density, whereas QS inhibition with 4-phenylbutanoyl had the opposite effects. Thus, manipulating QS in Wolbachia can alter cell density and the proportion of hatched eggs in the host L. trifolii, thereby reducing the number of insect progeny. These findings provide evidence supporting the potential efficacy of the IIT based on CI-Wolbachia for the environmentally friendly control of insect pest populations.
Introduction: The agricultural pests Liriomyza trifolii (Diptera: Agromyzidae) and Hercinothrips femoralis (Thysanoptera: Thripidae) harbor the endosymbiont Wolbachia, which induces cytoplasmic incompatibility and thelytokous parthenogenesis (asexual reproduction of female offspring without fertilization), respectively. The parasitoid Neochrysocharis formosa (Hymenoptera: Eulophidae), a natural enemy of leaf miners, is infected with Rickettsia, which also induces thelytokous parthenogenesis. Although symbionts can be eliminated in laboratory settings using antibiotics mixed with physical manipulation, the effects of agrochemical antibiotics designed for plant disease control on these insects and their symbionts remain unexplored. This study investigated the effects of MycoShield, a commercially available agrochemical containing 17% oxytetracycline, on symbiont-infected populations of these three insect species.Methods: MycoShield was applied to kidney bean plants or mixed into honey to expose L. trifolii, H. femoralis, and N. formosa to oxytetracycline. Offspring were screened for symbiont presence using PCR, and infection frequencies were compared across treatment concentrations. Additionally, H. femoralis populations were monitored in caged conditions under continuous exposure to treated plants.Results: At standard concentrations (1,000-fold dilution), MycoShield eliminated Wolbachia from L. trifolii and H. femoralis, resulting in L. trifolii producing uninfected offspring and H. femoralis producing only uninfected males. Similarly, Rickettsia was eliminated from N. formosa when adults ingested MycoShield-mixed honey. Additionally, N. formosa appeared to ingest the antibiotic indirectly by parasitizing L. trifolii larvae that had fed on treated leaves. Symbiont elimination was dose-dependent. Long-term exposure led to a substantial reduction in H. femoralis populations. Two out of eleven cages experienced complete extinction by day 100, likely due to genetic drift resulting from severe reproductive bottlenecks.Discussion: These findings demonstrate the potential of agrochemical antibiotics such as MycoShield as insecticidal agents targeting symbiont-mediated reproduction, with possible applications in sterile insect techniques. Further research is required to optimize efficacy and assess feasibility under field conditions.
Cytoplasmic incompatibility (CI) drives maternally transmitted endosymbionts such as Wolbachia through insect populations by inducing embryonic mortality when infected males fertilize uninfected females. CI is controlled by Wolbachia cif operons that are categorized into multiple phylogenetic types. CI strength is further shaped by poorly understood host factors, including development and genetic background. To study the strength of CI across different host species, we genotyped a Japanese field population of Liriomyza sativae . By uncovering paternal transmission of Wolbachia genic elements, we collected strong evidence of horizontal genome transfer, including Type I and Type V cif operons, from Wolbachia into the nuclear genome of L. sativae . We established a transinfection of w Ltri in L. sativae , a Wolbachia variant that induces strong CI in Liriomyza trifolii . No CI was observed in both intraspecific and interspecific reciprocal crosses with L. trifolii, suggesting that both uninfected females and infected males of L. sativae completely suppress w Ltri-mediated CI. Our results raise the appealing hypothesis that host suppression of Wolbachia- induced CI might evolve owing to horizontal transfer of cif operons into the host nuclear genome.