Abstract

There is currently considerable interest and practical progress in using the endosymbiotic bacteria Wolbachia as a vector control agent for human vector-borne diseases. Such vector control strategies may require the introduction of multiple, different Wolbachia strains into target vector populations, necessitating the identification and characterization of appropriate endosymbiont variants. Here, we report preliminary characterization of wFlu, a native Wolbachia from the neotropical mosquito Aedes fluviatilis, and evaluate its potential as a vector control agent by confirming its ability to cause cytoplasmic incompatibility, and measuring its effect on three parameters determining host fitness (survival, fecundity and fertility), as well as vector competence (susceptibility) for pathogen infection. Using an aposymbiotic strain of Ae. fluviatilis cured of its native Wolbachia by antibiotic treatment, we show that in its natural host wFlu causes incomplete, but high levels of, unidirectional cytoplasmic incompatibility, has high rates of maternal transmission, and no detectable fitness costs, indicating a high capacity to rapidly spread through host populations. However, wFlu does not inhibit, and even enhances, oocyst infection with the avian malaria parasite Plasmodium gallinaceum. The stage- and sex-specific density of wFlu was relatively low, and with limited tissue distribution, consistent with the lack of virulence and pathogen interference/symbiont-mediated protection observed. Unexpectedly, the density of wFlu was also shown to be specifically-reduced in the ovaries after bloodfeeding Ae. fluviatilis. Overall, our observations indicate that the Wolbachia strain wFlu has the potential to be used as a vector control agent, and suggests that appreciable mutualistic coevolution has occurred between this endosymbiont and its natural host. Future work will be needed to determine whether wFlu has virulent host effects and/or exhibits pathogen interference when artificially-transfected to the novel mosquito hosts that are the vectors of human pathogens.

Highlights

  • There is currently both considerable interest and practical progress in using artificial infections of the endosymbiotic bacteria Wolbachia to reduce the capacity of wild mosquito populations to transmit human pathogens [1,2,3]

  • Cytoplasmic incompatibility is a form of reproductive parasitism that increases the proportion of individuals in a host population infected with a given Wolbachia variant by suppressing the reproduction of those females that are either uninfected or infected with different Wolbachia variants

  • Using an aposymbiotic strain of Ae. fluviatilis cured of its Wolbachia by antibiotic treatment, we show that wFlu causes incomplete, but high levels of, unidirectional cytoplasmic incompatibility, has high rates of transmission from mother to offspring, and no apparent fitness costs, indicating that this strain of Wolbachia has the capacity to effectively and rapidly disseminate through host populations

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Summary

Introduction

There is currently both considerable interest and practical progress in using artificial infections of the endosymbiotic bacteria Wolbachia to reduce the capacity of wild mosquito populations to transmit human pathogens [1,2,3]. In the last 15 years, interest in the use of Wolbachia as a vector control agent has intensified [2] with the development of techniques to artificially-transfect mosquitoes with Wolbachia [21,22,23,24,25], and the discovery that such infections can inhibit the development of vector-borne pathogens [26,27,28,29,30,31,32,33], decrease the survival of adult female mosquitoes [25,30,34], and reduce their vector biting rate [35,36], thereby lowering the vectorial capacity of mosquito populations to transmit pathogens between human hosts [37,38,39,40]. Recent field trials have further demonstrated the proof-of-principle that release of relatively small seed populations of laboratory-reared mosquitoes artificially-infected with Wolbachia are sufficient to introduce and rapidly spread Wolbachia through wild uninfected mosquito populations [41], and a global effort is being made to implement a Wolbachia-based dengue control strategy (http://eliminatedengue.com) [2]

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