Tracing the history and ecological context of Wolbachia double infection in a specialist host (Urophora cardui)—parasitoid (Eurytoma serratulae) system

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.

Wolbachia prevalence patterns: horizontal transmission, recombination, and multiple infections in chestnut gall wasp‐parasitoid communities

“…Horizontal transmission is important for Wolbachia in extending their host range (Sudakaran et al, 2017). A common view is that horizontal transfer of Wolbachia requires intimate between‐species relationships (Johannesen, 2017). Transmission through the host‐parasitoid relationship is probably the main form of horizontal transmission and several reports have provided direct evidence (Heath et al, 1999; Vavre et al, 1999; Haine et al, 2005; Yang et al, 2013; Johannesen, 2017).…”

“…Transmission through the host‐parasitoid relationship is probably the main form of horizontal transmission. Several studies have found the host and the parasitoid to be infected by the same Wolbachia strain, e.g., in Drosophila ‐parasitoid communities (Vavre et al, 1999; Haine et al, 2005), in gall wasp‐parasitoid communities (Yang et al, 2013), and in tephritid fly‐parasitoid communities (Johannesen, 2017). Parasitoids may acquire infection while developing inside an infected host (Heath et al, 1999; Chiel et al, 2009) and may also serve as phoretic vectors, spreading Wolbachia from infected to uninfected hosts (Gehrer & Vorburger, 2012; Ahmed et al, 2015).…”

Wolbachia pipientisassociated to tephritid fruit fly pests: from basic research to applications

“…No direct evidence of Wolbachia transmission via parasitoids exists in tephritids, but sharing of Wolbachia strains between a parasitoid and several sympatric tephritids [144, 153] is consistent with parasitoid-mediated transmission, or transmission from tephritid host to parasitoid [176]. The potential for horizontal transfer of Wolbachia among tephritids via parasitoids is high, due to the multiple instances where a single parasitoid utilizes several different tephritid host species [177–179].…”

Unravelling Wolbachia global exchange: a contribution from the Bicyclus and Mylothris butterflies in the Afrotropics

“…Although host-Wolbachia codivergence is relatively common between Nematode hosts and their Wolbachia strains, similar examples of co-divergence between insect hosts and their Wolbachia strains remain scarce [2, 3, but see 4]. These patterns thus suggest that Wolbachia may have jump jumped horizontally between host species throughout the ~ 400 million years of the symbiont evolutionary history [3,[5][6][7][8]. Hybridization events, followed by introgression between closely related species have been shown to support the interspecies transfer of various genetic entities, including Wolbachia [9][10][11].…”