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

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.

背景：细菌内共生体沃尔巴克氏体（Wolbachia）可阻断其媒介埃及伊蚊（Aedes aegypti）传播登革病毒，目前该菌正被评估用于登革热疫情防控。沃尔巴克氏体可诱导细胞质不相容（cytoplasmic incompatibility, CI）现象，即感染沃尔巴克氏体的雄蚊与未感染雌蚊交配时，子代发育会出现失败。该现象可提升种群中感染雌蚊的相对交配成功率，进而促进这种有益菌的扩散。然而，唯有在野外环境下感染雄蚊具备足够的交配竞争力时，通过CI实现沃尔巴克氏体扩散的策略才具备可行性。本研究在半野外条件下，探究了沃尔巴克氏体对埃及伊蚊雄蚊交配竞争力的影响。

方法/主要结果：在一系列实验中，我们将未感染的雌蚊同时暴露于感染沃尔巴克氏体与未感染的雄蚊环境中。我们以因不相容性产生不可育卵的雌蚊占比，作为感染雄蚊交配竞争力的评估指标。实验结果显示，在实验帐篷与半野外笼养环境中，感染雄蚊与未感染雄蚊的交配成功率并无显著差异。这一结果既适用于携带温和型wMel沃尔巴克氏体菌株的雄蚊，也适用于携带强毒型wMelPop（爆米花）菌株的雄蚊。通过调控雄蚊体型大小，我们发现半野外笼养环境中，体型更大的雄蚊相较于体型较小的营养不良雄蚊，交配成功率更高，且这一规律不受其感染状态影响。

结论与意义：本研究结果表明，沃尔巴克氏体感染并不会降低埃及伊蚊雄蚊的交配竞争力。此外，体型对交配成功率的影响提示，实验室饲养的沃尔巴克氏体感染雄蚊因营养状况更佳、体型更大，在野外释放时具备潜在的竞争优势。这一优势或可推动沃尔巴克氏体通过CI在野生蚊种群中扩散，进一步凸显了其在疾病防控领域的应用潜力。