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. 2018 Jul 18;12(7):e0006626.
doi: 10.1371/journal.pntd.0006626. eCollection 2018 Jul.

Combining Wolbachia-induced sterility and virus protection to fight Aedes albopictus-borne viruses

Riccardo Moretti  1 , Pei-Shi Yen  2 , Vincent Houé  2 , Elena Lampazzi  1 , Angiola Desiderio  1 , Anna-Bella Failloux  2 , Maurizio Calvitti  1
Affiliations

Combining Wolbachia-induced sterility and virus protection to fight Aedes albopictus-borne viruses

Riccardo Moretti et al. PLoS Negl Trop Dis. .

Abstract

Among the strategies targeting vector control, the exploitation of the endosymbiont Wolbachia to produce sterile males and/or invasive females with reduced vector competence seems to be promising. A new Aedes albopictus transinfection (ARwP-M) was generated by introducing wMel Wolbachia in the ARwP line which had been established previously by replacing wAlbA and wAlbB Wolbachia with the wPip strain. Various infection and fitness parameters were studied by comparing ARwP-M, ARwP and wild-type (SANG population) Ae. albopictus sharing the same genetic background. Moreover, the vector competence of ARwP-M related to chikungunya, dengue and zika viruses was evaluated in comparison with ARwP. ARwP-M showed a 100% rate of maternal inheritance of wMel and wPip Wolbachia. Survival, female fecundity and egg fertility did not show to differ between the three Ae. albopictus lines. Crosses between ARwP-M males and SANG females were fully unfertile regardless of male age while egg hatch in reverse crosses increased from 0 to about 17% with SANG males aging from 3 to 17 days. When competing with SANG males for SANG females, ARwP-M males induced a level of sterility significantly higher than that expected for an equal mating competitiveness (mean Fried index of 1.71 instead of 1). The overall Wolbachia density in ARwP-M females was about 15 fold higher than in ARwP, mostly due to the wMel infection. This feature corresponded to a strongly reduced vector competence for chikungunya and dengue viruses (in both cases, 5 and 0% rates of transmission at 14 and 21 days post infection) with respect to ARwP females. Results regarding Zika virus did not highlight significant differences between ARwP-M and ARwP. However, none of the tested ARwP-M females was capable at transmitting ZIKV. These findings are expected to promote the exploitation of Wolbachia to suppress the wild-type Ae. albopictus populations.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1
Survival of ARwP-M females (left) and males (right) in comparison with recipient ARwP and wild-type Ae. albopictus. S = SANG wild-type Ae. albopictus; ARwP = wPip infected Ae. albopictus; ARwP-M wPip + wMel infected Ae. albopictus. Error bars show the SEM of three biological replicates, each containing 50:50 females:males. In both cases, survival curves did not show to significantly differ by Kaplan-Meier method and log-rank (Mantel-Cox) test.
Fig 2
Fig 2
Female fecundity (left) and hatch rate (right) in ARwP-M Ae. albopictus in comparison with recipient ARwP and wild-type Ae. albopictus. S = SANG wild-type Ae. albopictus; ARwP = wPip infected Ae. albopictus; ARwP-M wPip + wMel infected Ae. albopictus. Error bars show the SEM of three biological replicates, each containing 17–20 fed females. In both cases, values are not significantly different by ANOVA-Bonferroni (P > 0.05).
Fig 3
Fig 3. wMel and wPip Wolbachia density in ARwP and ARwP-M females and males measured by using Ae. albopictus actin gene as reference.
Fig 4
Fig 4. Rates of infection, dissemination efficiency and transmission efficiency for CHIKV, DENV and ZIKV in ARwP and ARwP-M Ae. Albopictus.
IR = Infection rate; DE = Dissemination rate; TE = transmission rate; A: the differences between Ae. albopictus lines are significant with respect to all of the three parameters and at both time intervals (7, 14 dpi) post the infection (Fisher exact test, P < 0.05); B: ARwP and ARwP-M significantly differed with regard to IR and DE at 14 dpi (Fisher exact test, P < 0.05); C: ARwP and ARwP-M did not significantly differ with regard to any of the evaluated parameters.
Fig 5
Fig 5. Titration of the viral particles of CHIKV, DENV and ZIKV in body and saliva of ARwP and ARwP-M Ae. Albopictus.
The number of viral particles in the body and saliva of both mosquito lines were titrated for evaluating the viral load in each mosquito line. A: the number of CHIKV viral particles in the body and saliva of ARwP and ARwP-M at 7 and 14 dpi; B and C: the number of DENV-1 (B) and ZIKV (C) viral particles in the body and saliva of ARwP and ARwP-M at 14 and 21 dpi. Differences between Ae. albopictus lines were not statistically significant (Kruskal–Wallis test: P > 0.05).
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This project has received resources funded by the European Union’s Horizon 2020 research and innovation programme under grant agreement No 731060 (Infravec2, Research Infrastructures for the control of vector-borne diseases; http://infravec2.eu/). Funding followed the positive evaluation of a formal request describing the research project which was prepared and submitted to Infravec2 by RM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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