Abstract

The endosymbiotic bacterium Wolbachia is the most widespread bacteria in insects, yet the ecology of novel acquisitions in natural host populations is poorly understood. Using temporal data separated by 12 years, I tested the hypothesis that immigration of a parasitoid wasp led to transmission of its Wolbachia strain to its dipteran host, resulting in double‐strain infection, and I used geographic and community surveys to explore the history of transmission in fly and parasitoid. Double infection in the fly host was present before immigration of the parasitoid. Equal prevalence of double infection in males and females, constant prevalence before and after immigration in two regions, and increase in one region of immigration indicate little if no competition between strains. Double infection was present throughout the fly's distribution range, but proportions varied highly (0–0.71, mean = 0.26). Two fly‐specific MLST strains, observed in Eastern and Western Europe, respectively, differed at hcpA only. Flies with either fly‐strain could be double infected with the parasitoid's strain. The geographic distribution of double infection implies that it is older than the fly host's extent distribution range and that different proportions of double infection are caused by demographic fluctuations in the fly. The geographic data in combination with community surveys of infections and strains further suggest that the parasitoid strain was the fly's ancestral strain that was transmitted to the parasitoid, that is, the reverse transmission route as first hypothesized. Based on these findings together with a comparison of oviposition strategies of other hosts harboring related Wolbachia strains, I hypothesize that trans‐infection during an insect host's puparial metamorphosis might be important in promoting horizontal transmission among diverse holometabolic taxa.

Highlights

  • The maternally inherited intracellular bacterium Wolbachia pipientis Hertig 1936 is likely the most widely distributed endosymbiont in insects (Ahmed, Araujo-­Jnr, Welch, & Kawahara, 2015a; Hilgenboecker, Hammerstein, Schlattmann, Telschow, & Werren, 2008)

  • I studied Wolbachia infection at the community level to evaluate the alternative hypotheses that (1) Urophora cardui was the original host of the parasitoid strain and/or (2) double infection (DI) was related to other interacting species immediately associated with U. cardui’s life cycle

  • Fitness effects of Wolbachia on insects are experimentally well documented and diverse (Werren, 1997), yet elucidation of horizontal transmission between specific species in natural populations is often hampered by the difficulty of obtaining temporal or geographic data that relates environment to infection status, where the strongest support comes from immigrant species acquiring new, resident strains (e.g., Schuler et al, 2013)

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Summary

| INTRODUCTION

The maternally inherited intracellular bacterium Wolbachia pipientis Hertig 1936 is likely the most widely distributed endosymbiont in insects (Ahmed, Araujo-­Jnr, Welch, & Kawahara, 2015a; Hilgenboecker, Hammerstein, Schlattmann, Telschow, & Werren, 2008). Schuler et al (2013) surveyed the acquisition of a strain infecting European cherry fruit fly, Rhagoletis cerasi, in invasive Eastern American cherry fruit fly, Rhagoletis cingulata, in Europe Both species depend on cherries for oviposition and larval development. Confirmation of the hypothesis would represent evidence for recent horizontal transmission between interacting species and highlight how environmental change (i.e., parasitoid immigration) might influence both the spread and acquisition of new infections as well as promote genetic diversification between host populations. I studied Wolbachia infection at the community level to evaluate the alternative hypotheses that (1) Urophora cardui was the original host of the parasitoid strain and/or (2) DI was related to other interacting species immediately associated with U. cardui’s life cycle. The three levels infer the history of DI in U. cardui

| MATERIALS AND METHODS
| Procedure for testing mixed infections
Findings
| DISCUSSION
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