Abstract

The common endosymbiotic Wolbachia bacteria influence arthropod hosts in multiple ways. They are mostly recognized for their manipulations of host reproduction, yet, more recent studies demonstrate that Wolbachia also impact host behavior, metabolic pathways and immunity. Besides their biological and evolutionary roles, Wolbachia are new potential biological control agents for pest and vector management. Importantly, Wolbachia-based control strategies require controlled symbiont transfer between host species and predictable outcomes of novel Wolbachia-host associations. Theoretically, this artificial horizontal transfer could inflict genetic changes within transferred Wolbachia populations. This could be facilitated through de novo mutations in the novel recipient host or changes of haplotype frequencies of polymorphic Wolbachia populations when transferred from donor to recipient hosts. Here we show that Wolbachia resident in the European cherry fruit fly, Rhagoletis cerasi, exhibit ancestral and cryptic sequence polymorphism in three symbiont genes, which are exposed upon microinjection into the new hosts Drosophila simulans and Ceratitis capitata. Our analyses of Wolbachia in microinjected D. simulans over 150 generations after microinjection uncovered infections with multiple Wolbachia strains in trans-infected lines that had previously been typed as single infections. This confirms the persistence of low-titer Wolbachia strains in microinjection experiments that had previously escaped standard detection techniques. Our study demonstrates that infections by multiple Wolbachia strains can shift in prevalence after artificial host transfer driven by either stochastic or selective processes. Trans-infection of Wolbachia can claim fitness costs in new hosts and we speculate that these costs may have driven the shifts of Wolbachia strains that we saw in our model system.

Highlights

  • The ubiquitous intracellular a-proteobacterium Wolbachia pipientis manipulates reproductive biology of many arthropod species in order to warrant its own transmission in host populations

  • Insertion Sequence elements (IS) and Variable Number of Tandem Repeats (VNTRs) had earlier been reported as hypervariable entities of Wolbachia genomes, we did not detect any structural re-arrangements for the five tested loci in wCer2 of the novel hosts (Figure S2 and Data S1)

  • Instead of tracing new mutations upon transfer in the recipients, we discovered ancestral polymorphic sites in symbiont genes deriving from the donor, pinpointing that both wCer1 and wCer2 exhibit ancestral and cryptic sequence polymorphism in its original host R. cerasi

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Summary

Introduction

The ubiquitous intracellular a-proteobacterium Wolbachia pipientis manipulates reproductive biology of many arthropod species in order to warrant its own transmission in host populations (reviewed by [1,2]). Wolbachia could be used in combination with the widely used SIT ([24]) that has encountered some problems with male fitness, mating performance, sperm size and number due to gamma irradiation of individuals ([25,26]) All of these Wolbachia applications require that (i) Wolbachia strains are transferable between diverse host systems and insect genera, (ii) the transferred strains are capable of inducing the expected phenotype such as CI, life shortening or resistance against pathogens, and (iii) transferred infection and their expected phenotypes persist stably in the novel host. Re-introduction of the Aedes-cell line adapted Wolbachia from cell lines into their native host D. melanogaster, resulted in fluctuations of maternal transmission efficiency, lower titers, and a reduced life shortening effect ([36]) These findings implicate that both host and symbiont interact dynamically and co-evolve rapidly within relatively short time periods

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