Back and forth Wolbachia transfers reveal efficient strains to control spotted wing drosophila populations

Abstract

Since its recent invasion of the European and American continents, the spotted wing Drosophila Drosophila suzukii has become a burden of the fruit industry. Armed with a highly sclerotized ovipositor, females can lay eggs in a wider variety of ripening and healthy fruits than other Drosophila species. Economic losses due to D. suzukii reach millions of dollars annually and methods to control natural populations in the field mainly rely on the use of chemical pesticides. We tested if Wolbachia bacteria represents a potential ally to control this pest. These symbionts are naturally present in many insects and often induce a form of conditional sterility called cytoplasmic incompatibility (CI): the offspring of infected males die, unless the eggs are rescued by the compatible infection, inherited from the mother that protects the embryo. A long‐recognized strategy called the incompatible insect technique (IIT) makes use of the CI phenotype to control insect populations through the mass release of infected males. To implement this technique in D. suzukii, we used back and forth Wolbachia transfers between D. suzukii and Drosophila simulans to identify Wolbachia strains that can sterilize D. suzukii females despite the presence of wSuz, a natural Wolbachia infection in this species. We identified two Wolbachia strains as potential candidates for developing IIT in D. suzukii. Both induce a very high level of CI in this pest which is not attenuated by the presence of wSuz in females. Moreover, the newly transferred Wolbachia do not affect the fitness or the mating competitiveness of the sterilizing males. Synthesis and applications. However, several critical steps still need to be tested and developed outside the laboratory to achieve the control of Drosophila suzukii using Incompatible Insect Technique. By an experimental approach in large population cages, we showed that releases of transinfected males limit population size. Thus, we provide in this study the proof of concept that this technique can be a very promising approach to control Drosophila suzukii populations.

Combining sterile and incompatible insect techniques for the population suppression of Drosophila suzukii

“…Through our single-pair crosses we determined the CI levels of wHa and wTei lines and showed that wHa induces strong CI in D. suzukii, but wTei CI levels are rather moderate. The wTei results are not in alignment with the study performed by Cattel et al (2018), in which a high level of CI was induced by the wTei-infected D. suzukii Fig. 4 Hatching rates of crosses between irradiated, Wolbachiainfected males and fertile, wSuz females.…”

“…Therefore, two Wolbachia strains (wHa and wTei) acquired by other Drosophila species were microinjected into D. suzukii embryos and stable trans-infected lines were established in the laboratory. In both lines, Wolbachia induced strong CI (95.57% and 96.46%, respectively) that was not rescued by the wSuz strain thus giving rise in two promising candidates for a combined SIT/IIT strategy in D. suzukii (Cattel et al 2018;Nikolouli et al 2018). The mechanism of this approach has been previously dissected against mosquito vectors (Bourtzis et al 2016;Lees et al 2015;Zhang et al 2015aZhang et al , b, 2016Zheng et al 2019), and it can bear promising results if a low radiation dose to ensure female sterility is applied in flies infected with a Wolbachia strain that induces CI.…”

“…In the present study, we aimed to develop a combined SIT/IIT protocol which could potentially be used for the population suppression of D. suzukii. The two Wolbachia candidate strains (wHa and wTei) suggested by Cattel et al (2018) were used and three low irradiation doses were evaluated. The effect of the Wolbachia infection and irradiation on the adult emergence, longevity and flight ability were also assessed.…”

“…Four lines harboring the same genetic background from France, but with different infection status were obtained in a previous study by Cattel and colleagues (2018) through microinjections of Wolbachia strains from other Drosophila species into D.suzukii; a Wolbachia-free line (un-Fr), a wSuz-infected line (wSuz-Fr) and two trans-infected lines (wHa-Fr and wTei-Fr). These two exogenous Wolbachia strains, wHa and wTei, were shown to induce high CI levels in D. suzukii trans-infected lines despite the presence of the natural Wolbachia infection wSuz (Cattel et al 2018). All these lines were kindly provided by the Laboratory of Biometry and Evolutionary Biology, University Lyon 1, France.…”

Loss of cytoplasmic incompatibility and minimal fecundity effects explain relatively lowWolbachiafrequencies inDrosophila mauritiana

“…Quantitative predictions, based on the idealized model of Hoffmann and Turelli (1997), are discussed below. The maintenance of wMau is potentially analogous to the persistence of other non-CI-causing Wolbachia, specifically wAu in some Australian populations of D. simulans (Hoffmann et al 1996;Kriesner et al 2013) and wSuz in D. suzukii and wSpc in Drosophila subpulchrella (Hamm et al 2014;Conner et al 2017;Turelli et al 2018; but see Cattel et al 2018).…”