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

Segoli M, Hoffmann AA, Lloyd J, Omodei GJ, Ritchie SA - PLoS Negl Trop Dis (2014)

Bottom Line: We found that infected males were equally successful to uninfected males in securing a mate within experimental tents and semi-field cages.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.

View Article: PubMed Central - PubMed

Affiliation: Mitrani Department of Desert Ecology, The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel; School of Public Health and Tropical Medicine and Rehabilitative Sciences, James Cook University, Cairns, Queensland, Australia.

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.

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Related in: MedlinePlus

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).
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pntd-0003294-g003: 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).

Mentions: Males reared on a low nutrition diet were within the lower range of the size distribution for wild males, while males fed ad libitum were within the higher range (Fig. 3). Male size differed significantly among the groups (two-way ANOVA, F2,429 = 81.41, p<0.001; means ± SD (n) were 1.83±0.12 mm (117) for small males, 2.14±.09 mm (119) for large males, 2.04±.19 (199) for wild males), but this was not affected by infection status (F1,429 = 0.91, p = 0.34) or by the interaction between rearing condition and infection status (F2,429 = 0.57, p = 0.57). The results from the experimental tents were not consistent: while most of the females from tents with larger uninfected males produced viable eggs, suggesting an advantage to larger males (Fig. 4, χ2 = 11.30, df = 5, p = 0.05, n = 6 tents, 86 females), in the tents with larger infected males the percentage of females producing viable eggs did not deviate from 50% (Fig. 4, χ2 = 6.31, df = 5, p = 0.28, n = 6 tents, 93 females) and the proportion of viable vs. non-viable females did not differ significantly between these treatments (Fisher exact test, p = 0.09). In contrast, the results from the semi-field cages were consistent, with higher competitiveness for larger males of either infection status: the majority of females produced viable eggs when uninfected males were larger (Fig. 4, χ2  = 19.72, df = 4, p<0.001, n = 5 cages, 118 females) and the majority of females produced non-viable eggs when infected males were larger (Fig. 4, χ2 = 20.09, df = 4, p = 0.005, n = 5 cages, 101 females). As expected, the proportion of females mating with uninfected (viable eggs) and infected (non-viable eggs) males differed significantly between these treatments (Fisher exact test, p<0.001).


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

Segoli M, Hoffmann AA, Lloyd J, Omodei GJ, Ritchie SA - PLoS Negl Trop Dis (2014)

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).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263406&req=5

pntd-0003294-g003: 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).
Mentions: Males reared on a low nutrition diet were within the lower range of the size distribution for wild males, while males fed ad libitum were within the higher range (Fig. 3). Male size differed significantly among the groups (two-way ANOVA, F2,429 = 81.41, p<0.001; means ± SD (n) were 1.83±0.12 mm (117) for small males, 2.14±.09 mm (119) for large males, 2.04±.19 (199) for wild males), but this was not affected by infection status (F1,429 = 0.91, p = 0.34) or by the interaction between rearing condition and infection status (F2,429 = 0.57, p = 0.57). The results from the experimental tents were not consistent: while most of the females from tents with larger uninfected males produced viable eggs, suggesting an advantage to larger males (Fig. 4, χ2 = 11.30, df = 5, p = 0.05, n = 6 tents, 86 females), in the tents with larger infected males the percentage of females producing viable eggs did not deviate from 50% (Fig. 4, χ2 = 6.31, df = 5, p = 0.28, n = 6 tents, 93 females) and the proportion of viable vs. non-viable females did not differ significantly between these treatments (Fisher exact test, p = 0.09). In contrast, the results from the semi-field cages were consistent, with higher competitiveness for larger males of either infection status: the majority of females produced viable eggs when uninfected males were larger (Fig. 4, χ2  = 19.72, df = 4, p<0.001, n = 5 cages, 118 females) and the majority of females produced non-viable eggs when infected males were larger (Fig. 4, χ2 = 20.09, df = 4, p = 0.005, n = 5 cages, 101 females). As expected, the proportion of females mating with uninfected (viable eggs) and infected (non-viable eggs) males differed significantly between these treatments (Fisher exact test, p<0.001).

Bottom Line: We found that infected males were equally successful to uninfected males in securing a mate within experimental tents and semi-field cages.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.

View Article: PubMed Central - PubMed

Affiliation: Mitrani Department of Desert Ecology, The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel; School of Public Health and Tropical Medicine and Rehabilitative Sciences, James Cook University, Cairns, Queensland, Australia.

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.

Show MeSH
Related in: MedlinePlus