The effect of virus-blocking Wolbachia on male competitiveness of the dengue vector mosquito, Aedes aegypti

Abstract

Background: The bacterial endosymbiont Wolbachia blocks the transmission of dengue virus by its vector mosquito Aedes aegypti, and is currently being evaluated for control of dengue outbreaks. Wolbachia induces cytoplasmic incompatibility (CI) that results in the developmental failure of offspring in the cross between Wolbachia-infected males and uninfected females. This increases the relative success of infected females in the population, thereby enhancing the spread of the beneficial bacterium. However, Wolbachia spread via CI will only be feasible if infected males are sufficiently competitive in obtaining a mate under field conditions. We tested the effect of Wolbachia on the competitiveness of A. aegypti males under semi-field conditions.

Methodology/principal findings: In a series of experiments we exposed uninfected females to Wolbachia-infected and uninfected males simultaneously. We scored the competitiveness of infected males according to the proportion of females producing non-viable eggs due to incompatibility. We found that infected males were equally successful to uninfected males in securing a mate within experimental tents and semi-field cages. This was true for males infected by the benign wMel Wolbachia strain, but also for males infected by the virulent wMelPop (popcorn) strain. By manipulating male size we found that larger males had a higher success than smaller underfed males in the semi-field cages, regardless of their infection status.

Conclusions/significance: The results indicate that Wolbachia infection does not reduce the competitiveness of A. aegypti males. Moreover, the body size effect suggests a potential advantage for lab-reared Wolbachia-males during a field release episode, due to their better nutrition and larger size. This may promote Wolbachia spread via CI in wild mosquito populations and underscores its potential use for disease control.

Figure 1. Experiment 1: Competitiveness of wMel infected vs. uninfected males.

Data pooled for all females of a certain treatment a) Percentage of viable eggs for females of compatible controls (n = 60 females), incompatible controls (n = 48 females), experimental tents (n = 161 females) and semi-field cages (n = 57 females). Numbers on bottom and top of figure represent the number of overlapping data points with extreme values (0% and 100% respectively) The dashed line represent the threshold for scoring females as viable (≥50%) or non-viable (<50%). b) Percentage of viable and non-viable females in each of the above treatments. Asterisks represent significance level for deviation from 1∶1 using observed vs. expected chi square test with each tent/cage as a repetition (see text).

Figure 2. Experiment 2: Competitiveness of wMelPop infected vs. uninfected males.

Data pooled for all females of a certain treatment. a) Percentage of viable eggs for females of compatible controls (n = 55 females), incompatible controls (n = 48 females), experimental tents (n = 158 females), experimental tents with older males (n = 48 female), and experimental semi-field cages (n = 31 females). Numbers on bottom and top of figure represent the number of overlapping data points with extreme values (0% and 100% respectively). The dashed line represent the threshold for scoring females as viable (≥50%) or non-viable (<50%). b) Percentage of viable and non-viable females in each of the above treatments. Asterisks represent significance level for deviation from 1∶1 using observed vs. expected chi square test with each tent/cage as a repetition (see text).

Figure 3. Male body size in the different rearing groups.

Distribution male body size (estimated as wing length) for a sample of large lab reared males (fed ad libitum, n = 119), small lab reared males (fed 1/4 the amount of food, n = 117) and males trapped from the field during Nov-Dec 2012 (n =  males).

Figure 4. Experiment 3: Competitiveness of wMel infected vs. uninfected males of different sizes.

Data pooled for all females of a certain treatment. a) Percentage of viable eggs for females of tents with larger uninfected males (n = 86 females), tents with larger infected males (n = 93 females), semi-field cages with larger uninfected males (n =  females) and semi-field cages with larger infected males (n =  females). Numbers on bottom and top of figure represent the number of overlapping data points with extreme values (0% and 100% respectively). The dashed line represent the threshold for scoring females as viable (≥50%) or non-viable (<50%). b) Percentage of viable and non-viable females in each of the above treatments. Asterisks represent significance level for deviation from 1∶1 using observed vs. expected chi square test with each tent/cage as a repetition (see text).