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.
Highlights
Wolbachia is a maternally inherited and ubiquitous endosymbiont of insects
Witzenhausen showed differences in the infection status of R. cerasi deriving from different host plants: in Lonicera-infesting flies, wCer2 expanded from 14% in 1998 to 43.8% in 2008, while Prunus-infesting flies were already completely invaded by wCer2 in 2000 and 2014
We studied the infection dynamics of Wolbachia in R. cerasi in Europe and focussed on the invasion history of wCer2 over a time period of 15 years
Summary
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. The alphaproteobacterium Wolbachia infects a broad range of arthropods and filarial nematodes and is probably the most common endosymbiont (Werren et al 2008) It is mostly maternally inherited and spreads by increasing reproductive fitness of infected females (Engelst€adter & Hurst 2009). Maternal Wolbachia transmission is rarely perfect and can lead to a continuous emergence of uninfected females, hindering fixation of a Wolbachia strain (Kriesner et al 2013; Hamm et al 2014) This leakage may, on the other hand, be compensated by selective effects such as CI or beneficial effects of Wolbachia provided to its host, including the protection against pathogens (Hedges et al 2008; Fenton et al 2011)
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