Development of the Incompatible Insect Technique targeting Aedes albopictus: introgression of a wild nuclear background restores the performance of males artificially infected with Wolbachia.

Abstract

The bacterium Wolbachia pipientis is increasingly studied for its potential use in controlling insect vectors or pests due to its ability to induce Cytoplasmic Incompatibility (CI). CI can be exploited by establishing an opportunistic Wolbachia infection in a targeted insect species through trans-infection and then releasing the infected males into the environment as sterilizing agents. Several host life history traits (LHT) have been reported to be negatively affected by artificial Wolbachia infection. Wolbachia is often considered the causative agent of these detrimental effects, and the importance of the host's genetic origins in the outcome of trans-infection is generally overlooked. In this study, we investigated the impact of host genetic background using an Aedes albopictus line recently trans-infected with wPip from the Culex pipiens mosquito, which exhibited some fitness costs. We measured several LHTs including fecundity, egg hatch rate, and male mating competitiveness in the incompatible line after four rounds of introgression aiming at restoring genetic diversity in the nuclear genome. Our results show that introgression with a wild genetic background restored most fitness traits and conferred mating competitiveness comparable to that of wild males. Finally, we show that introgression leads to faster and stronger population suppression under laboratory conditions. Overall, our data support that the host genome plays a decisive role in determining the fitness of Wolbachia-infected incompatible males.IMPORTANCEThe bacterium Wolbachia pipientis is increasingly used to control insect vectors and pests through the Incompatible Insect Technique (IIT) inducing a form of conditional sterility when a Wolbachia-infected male mates with an uninfected or differently infected female. Wolbachia artificial trans-infection has been repeatedly reported to affect mosquitoes LHTs, which may in turn compromise the efficiency of IIT. Using a tiger mosquito (Aedes albopictus) line recently trans-infected with a Wolbachia strain from Culex pipiens and displaying reduced fitness, we show that restoring genetic diversity through introgression significantly mitigated the fitness costs associated with Wolbachia trans-infection. This was further demonstrated through experimental population suppression, showing that introgression is required to achieve mosquito population suppression under laboratory conditions. These findings are significant for the implementation of IIT programs, as an increase in female fecundity and male performance improves mass rearing productivity as well as the sterilizing capacity of released males.