Wolbachia and invasion

Work financed by the Austrian Science Fund (FWF) projects (P30456-B29 and P30957-B29) awarded to Hannes Schuler

Globalization and climate disruption have allowed further long-range colonization events by invasive species than ever before. These facilitate interactions between invasive species with co-occurring native species. The Eastern cherry fruit fly, Rhagoletis cingulata, is a significant economic pest species in North America and has recently been introduced in Europe. Here, it co-infests cherries with the native European cherry fruit fly, R. cerasi. This shared habitat has resulted in two independent horizontal transfers of a native Wolbachia strain, wCer1, from R. cerasi to the invasive R. cingulata in Germany and Hungary. Although intraspecific horizontal Wolbachia transmissions have been documented in various insects on an evolutionary time scale, direct evidence for the horizontal transmission of Wolbachia on an ecological timescale in nature is rare. Our system provides a unique opportunity to resolve the spatial dynamics of directional horizontal Wolbachia transfers in natural populations. Our system also allows us to investigate the role of Wolbachia infection in invasiveness by comparing measured temporal infection dynamics to expected values under classical Wolbachia infection models. Using a combination of short-read (Illumina) and long-read (PacBio and Nanopore) sequencing, we first assembled a dozen Wolbachia genomes from individuals of the invasive (wCin2 strains) and the native fly species (wCer1 strains). We compared these strains and found that major structural inversions and duplications resulted in differences in cytoplasmic incompatibility factor genes between the two strains. These genes are essential as they determine the Wolbachia spread dynamics through the invasive R. cingulata populations. In addition to these two main Wolbachia strains, we also found and characterized three minor strains (wCer2, wCer4, and wCer5) in the native R. cerasi species. We hypothesize that these strains might interact and lead to complex dynamics within R. cerasi local populations due to multiple combinations of different cytoplasmic incompatibilities factors. After comparing the invasive R. cingulata regional German and Hungarian strains to North American strains, we found significantly more SNPs in Germany. These results strongly suggest that the German invasion route is older than the Hungarian route. This work paints a picture of a highly dynamic system where Wolbachia plays a significant role in the invasive potential of R. cingulata in Europe. It also highlights the role of horizontal Wolbachia transfers between species as a mechanism for biological novelty.