Suppression of cytoplasmic incompatibility in the leaf-mining fly Liriomyza sativae with a nuclear Wolbachia insert

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 wLtri 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 wLtri-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.