Assessment of fitness and vector competence of a New Caledonia wMel Aedes aegypti strain before field-release

Abstract

Background: Biological control programs involving Wolbachia-infected Aedes aegypti are currently deployed in different epidemiological settings. New Caledonia (NC) is an ideal location for the implementation and evaluation of such a strategy as the only proven vector for dengue virus (DENV) is Ae. aegypti and dengue outbreaks frequency and severity are increasing. We report the generation of a NC Wolbachia-infected Ae. aegypti strain and the results of experiments to assess the vector competence and fitness of this strain for future implementation as a disease control strategy in Noumea, NC.

Methods/principal findings: The NC Wolbachia strain (NC-wMel) was obtained by backcrossing Australian AUS-wMel females with New Caledonian Wild-Type (NC-WT) males. Blocking of DENV, chikungunya (CHIKV), and Zika (ZIKV) viruses were evaluated via mosquito oral feeding experiments and intrathoracic DENV challenge. Significant reduction in infection rates were observed for NC-wMel Ae. aegypti compared to WT Ae. aegypti. No transmission was observed for NC-wMel Ae. aegypti. Maternal transmission, cytoplasmic incompatibility, fertility, fecundity, wing length, and insecticide resistance were also assessed in laboratory experiments. Ae. aegypti NC-wMel showed complete cytoplasmic incompatibility and a strong maternal transmission. Ae. aegypti NC-wMel fitness seemed to be reduced compared to NC-WT Ae. aegypti and AUS-wMel Ae. aegypti regarding fertility and fecundity. However further experiments are required to assess it accurately.

Conclusions/significance: Our results demonstrated that the NC-wMel Ae. aegypti strain is a strong inhibitor of DENV, CHIKV, and ZIKV infection and prevents transmission of infectious viral particles in mosquito saliva. Furthermore, our NC-wMel Ae. aegypti strain induces reproductive cytoplasmic incompatibility with minimal apparent fitness costs and high maternal transmission, supporting field-releases in Noumea, NC.

Fig 1. Infection rates and transmission efficiencies for NC-WT and NC-wMel Aedes aegypti strains orally challenged with DENV-2, CHIKV or ZIKV.

(A, B, C) Infection rates and (D, E, F) transmission efficiencies obtained for DENV-2, CHIKV, and ZIKV respectively at different days post-challenge. Errors bars indicate Confidence Interval at 95%. Statistically significant differences are shown in the figures (Fisher’s exact test; *: p-value <0.05; **: p-value <0.01; ***: p-value <0.001; NS: not significant).

Fig 2. NC-WT, NC-wMel, AUS-Tet and AUS-wMel Aedes aegypti strains intrathoracically injected with the four DENV serotypes.

(A, B, C, D) Infection rates obtained for DENV-1, DENV-2, DENV-3, and DENV-4 respectively at 7 days post-injection. Errors bars indicate Confidence Interval at 95%. (E, F, G, H) Viral titers obtained from infected mosquitoes at 7 days post-injection, for DENV-1, DENV-2, DENV-3, and DENV-4 respectively. Median is shown for each mosquito strain. Statistically significant differences are shown in the figures (Fisher’s exact test for infection rates; Wilcoxon test for viral titers; *: p-value <0.05; **: p-value <0.01; ***: p-value <0.001; NS: not significant).

Fig 3. Mean wing lengths for males and females of NC-wMel, AUS-wMel, and NC-WT strains.

Wing lengths were calculated as the distance from the wing base to the wing tip, on 30 to 40 specimens of each sex and strain. Each point represents the length of a mosquito’s wing. The black bars represent the mean of wing lengths per group.

Fig 4. Dose-mortality to deltamethrin for NC-wMel, NC-WT, and Bora strains.

For each strain and each dose tested, 70 to 100 females (2–5 days old) were exposed for 1 h, and mortality was recorded at 24 h. The yellow dots (Bora), the blue triangles (NC-wMel) and the gray crosses (NC-WT) represent mortalities recorded for each dose. Dotted lines indicate the Confidence Interval at 95%.