Abstract

Simple SummaryWolbachia is an endosymbiotic bacterium that infects numerous insects and crustaceans. Its ability to alter the reproduction of hosts results in incompatibilities of differentially infected individuals. Therefore, Wolbachia has been applied to suppress agricultural and medical insect pests. The European cherry fruit fly, Rhagoletis cerasi, is mainly distributed throughout Europe and Western Asia, and is infected with at least five different Wolbachia strains. The strain wCer2 causes incompatibilities between infected males and uninfected females, making it a potential candidate to control R. cerasi. Thus, the prediction of its spread is of practical importance. Like mitochondria, Wolbachia is inherited from mother to offspring, causing associations between mitochondrial DNA and endosymbiont infection. Misassociations, however, can be the result of imperfect maternal transmission, the loss of Wolbachia, or its horizontal transmission from infected to uninfected individuals. These are important parameters influencing the spread of infection. Here, we studied Wolbachia-mitochondrial haplotype associations in R. cerasi in two transition zones in the Czech Republic and Hungary, where wCer2 is currently spreading. Our results suggest imperfect maternal transmission only in the early phases of wCer2 invasion and no evidence of horizontal transmission of wCer2 in R. cerasi.The endosymbiont Wolbachia can manipulate arthropod host reproduction by inducing cytoplasmic incompatibility (CI), which results in embryonic mortality when infected males mate with uninfected females. A CI-driven invasion of Wolbachia can result in a selective sweep of associated mitochondrial haplotype. The co-inheritance of Wolbachia and host mitochondrial DNA can therefore provide significant information on the dynamics of an ongoing Wolbachia invasion. Therefore, transition zones (i.e., regions where a Wolbachia strain is currently spreading from infected to uninfected populations) represent an ideal area to investigate the relationship between Wolbachia and host mitochondrial haplotype. Here, we studied Wolbachia-mitochondrial haplotype associations in the European cherry fruit fly, Rhagoletis cerasi, in two transition zones in the Czech Republic and Hungary, where the CI-inducing strain wCer2 is currently spreading. The wCer2-infection status of 881 individuals was compared with the two known R. cerasi mitochondrial haplotypes, HT1 and HT2. In accordance with previous studies, wCer2-uninfected individuals were associated with HT1, and wCer2-infected individuals were mainly associated with HT2. We found misassociations only within the transition zones, where HT2 flies were wCer2-uninfected, suggesting the occurrence of imperfect maternal transmission. We did not find any HT1 flies that were wCer2-infected, suggesting that Wolbachia was not acquired horizontally. Our study provides new insights into the dynamics of the early phase of a Wolbachia invasion.

Highlights

  • Wolbachia are a group of maternally inherited Alphaproteobacteria that infect a wide range of nematode and arthropod species [1,2]

  • In the majority of cases, wCer2-infected R. cerasi flies were associated with mitochondrial haplotype HT2, while wCer2-uninfected flies were associated with mitochondrial haplotype HT1

  • Out of the 881 flies analyzed, we found seven HT2 flies that were wCer2-uninfected and no HT1 flies that were wCer2-infected. Six of these misassociations were found within transitional populations, that were wCer2-infected. Six of these misassociations were found within transitional populations, having both infected and uninfected individuals, whereas one individual of HT2 was found within a having both infected and uninfected individuals, whereas one individual of HT2 was found within a wCer2-uninfected population (CZ-15)

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Summary

Introduction

Wolbachia are a group of maternally inherited Alphaproteobacteria that infect a wide range of nematode and arthropod species [1,2]. These endosymbionts influence the reproduction of their hosts and enhance their own spread. Analogous to the sterile insect technique (SIT), where laboratory-reared males are sterilized prior to field releases [4], the incompatible insect technique (IIT) is based on the release of Wolbachia-infected incompatible males, which will lead to the suppression of natural pest populations. Models based on attributes of the strain and its host are necessary to predict the spread of the endosymbiont in field populations (e.g., [10,11])

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