The hitchhiker's guide to Europe: the infection dynamics of an ongoing Wolbachia invasion and mitochondrial selective sweep in Rhagoletis cerasi

Abstract

Wolbachia is a maternally inherited and ubiquitous endosymbiont of insects. It can hijack host reproduction by manipulations such as cytoplasmic incompatibility (CI) to enhance vertical transmission. Horizontal transmission of Wolbachia can also result in the colonization of new mitochondrial lineages. In this study, we present a 15‐year‐long survey of Wolbachia in the cherry fruit fly Rhagoletis cerasi across Europe and the spatiotemporal distribution of two prevalent strains, wCer1 and wCer2, and associated mitochondrial haplotypes in Germany. Across most of Europe, populations consisted of either 100% singly (wCer1) infected individuals with haplotype HT1, or 100% doubly (wCer1&2) infected individuals with haplotype HT2, differentiated only by a single nucleotide polymorphism. In central Germany, singly infected populations were surrounded by transitional populations, consisting of both singly and doubly infected individuals, sandwiched between populations fixed for wCer1&2. Populations with fixed infection status showed perfect association of infection and mitochondria, suggesting a recent CI‐driven selective sweep of wCer2 linked with HT2. Spatial analysis revealed a range expansion for wCer2 and a large transition zone in which wCer2 splashes appeared to coalesce into doubly infected populations. Unexpectedly, the transition zone contained a large proportion (22%) of wCer1&2 individuals with HT1, suggesting frequent intraspecific horizontal transmission. However, this horizontal transmission did not break the strict association between infection types and haplotypes in populations outside the transition zone, suggesting that this horizontally acquired Wolbachia infection may be transient. Our study provides new insights into the rarely studied Wolbachia invasion dynamics in field populations.

Wolbachia endosymbionts in haplodiploid and diploid scolytine beetles (Coleoptera: Curculionidae: Scolytinae)

“…The incongruence of the Wolbachia phylogeny with that of its hosts suggests that haplodiploid scolytine beetles have acquired different Wolbachia strains horizontally from independent sources. Previous studies have shown that the ecological overlap of different species by sharing the same host provides the opportunity for Wolbachia exchange between different species (Stahlhut et al, 2010;Schuler et al, 2013;2016). Different factors, such as shared parasitoids (Heath et al, 1999;Vavre et al, 1999;Ahmed et al, 2015), cannibalism (Le Clec'h et al, 2013) and the host plant itself (Sintupachee et al, 2006), can facilitate the switch between different species boundaries.…”

“…In addition, incongruence between the phylogeny of Wolbachia and its host shows that these bacteria can switch species boundaries and move horizontally between species Watanabe et al, 2012). The close ecological relationship between different species, such as shared habitats or shared parasitoids, can facilitate the horizontal transmission of Wolbachia (Heath et al, 1999;Stahlhut et al, 2010;Schuler et al, 2013;2016;Ahmed et al, 2015).…”

Cuticular hydrocarbons as potential mediators of cryptic species divergence in a mutualistic ant association

“…In insects, this is often found in the context of an infection with the endosymbiont Wolbachia that can manipulate its hosts reproduction (through e.g., mate-discrimination, cytoplasmic incompatibilities;Hoffmann, Turelli, & Simmons, 1986;Schuler et al, 2016). femoratus PS and Ca.…”

Host plant‐related genomic differentiation in the European cherry fruit fly, Rhagoletis cerasi

“…Finally, it is also possible that endosymbionts could restrict gene flow between the Prunus and Lonicera host races. If the endosymbiont, Wolbachia, infects Prunus flies at higher levels than it does Lonicera flies, which appears to be the case (Schuler et al, ), it will establish a form of unidirectional incompatibility between infected Prunus males and uninfected Lonicera females, strengthening RI between the host races (Telschow, Flor, Kobayashi, Hammerstein, & Werren, ). As such, unidirectional CI can also help account for the pattern of geographic and host‐associated genomic differentiation in R. cerasi , as based on our current knowledge of the system, unidirectional CI is expected to reduce gene flow but not stop it entirely (Boller & Bush, ).…”

“…In addition, the timing of endosymbiont acquisition differs between Prunus and Lonicera flies. Wolbachia , a maternally inherited endosymbiont, which causes unidirectional incompatibilities between infected males and uninfected females of R. cerasi , reached fixation in Prunus flies, while only infecting 17% of Lonicera flies in German populations (Schuler et al, ). These results provide some evidence of phenotypic differentiation among host‐associated flies and suggest that mating may not be entirely random.…”