The Intracellular Bacterium Wolbachia Uses Parasitoid Wasps as Phoretic Vectors for Efficient Horizontal Transmission

Abstract

Facultative bacterial endosymbionts are associated with many arthropods and are primarily transmitted vertically from mother to offspring. However, phylogenetic affiliations suggest that horizontal transmission must also occur. Such horizontal transfer can have important biological and agricultural consequences when endosymbionts increase host fitness. So far horizontal transmission is considered rare and has been difficult to document. Here, we use fluorescence in situ hybridization (FISH) and multi locus sequence typing (MLST) to reveal a potentially common pathway of horizontal transmission of endosymbionts via parasitoids of insects. We illustrate that the mouthparts and ovipositors of an aphelinid parasitoid become contaminated with Wolbachia when this wasp feeds on or probes Wolbachia-infected Bemisia tabaci AsiaII7, and non-lethal probing of uninfected B. tabaci AsiaII7 nymphs by parasitoids carrying Wolbachia resulted in newly and stably infected B. tabaci matrilines. After they were exposed to infected whitefly, the parasitoids were able to transmit Wolbachia efficiently for the following 48 h. Whitefly infected with Wolbachia by parasitoids had increased survival and reduced development times. Overall, our study provides evidence for the horizontal transmission of Wolbachia between insect hosts by parasitic wasps, and the enhanced survival and reproductive abilities of insect hosts may adversely affect biological control programs.

Plant–mediated horizontal transmission of Wolbachia between whiteflies

“…The vector-mediated interspecific transmission of intracellular bacterial endosymbionts was observed through shared food sources (in Wolbachia , Spiroplasma , Hamiltonella defensa ; Rigaud and Juchault, 1995; Oliver et al , 2010; Caspi-Fluger et al , 2012), ectoparasitic mites (Jaenike et al , 2007; Gehrer and Vorburger, 2012), host plants (in Rickettsia , Arsenophonus ; Caspi-Fluger et al , 2012; Bressan, 2014) and parasitoids (in Arsenophonus , Wolbachia ; Duron et al , 2010; Ahmed et al , 2015). The hypothesis that Wolbachia can be horizontally transmitted between two insect species has been supported by both phylogenetic and experimental analyses (Vavre et al , 1999; Huigens et al , 2000, 2004; Sintupachee et al , 2006; Ahmed et al , 2013; Yang et al , 2013).…”

“…We collected AsiaII7 adults 24–48 h after they emerged from the pupal stage, using a hand aspirator from the Wolbachia- positive subcolony. In AsiaII7, Wolbachia created the scattered infection pattern described by Ahmed et al (2015). Whiteflies were released into leaf cages (2 cm high, 3 cm diameter) covered on the undersurface of clean, healthy cotton leaves (as shown in Supplementary Figure S5).…”

“…Over the past two decades, there have been multiple phylogenetic and transinfection studies reporting evidence of Wolbachia transmission between both phylogenetically close and phylogenetically distant species (Boyle et al , 1993; Heath et al , 1999; Vavre et al , 1999). Thus, it is probable that Wolbachia horizontal transmission is occurring between some arthropod taxa (Ahmed et al , 2015). Although Wolbachia has been shown to undergo extensive horizontal transmission between several host taxa (Werren et al , 1995; Baldo et al , 2006; Chiel et al , 2009; Raychoudhury et al , 2009; Oliver et al , 2010; Ahmed et al , 2015), the mechanisms for this are poorly understood.…”

“…Thus, it is probable that Wolbachia horizontal transmission is occurring between some arthropod taxa (Ahmed et al , 2015). Although Wolbachia has been shown to undergo extensive horizontal transmission between several host taxa (Werren et al , 1995; Baldo et al , 2006; Chiel et al , 2009; Raychoudhury et al , 2009; Oliver et al , 2010; Ahmed et al , 2015), the mechanisms for this are poorly understood.…”

“…Recently, Wolbachia horizontal transmission through invertebrate predators and parasitoids has been revealed (Huigens et al , 2000, 2004; Le Clec'h et al , 2013; Ahmed et al , 2015). However, the presence of identical strains of Wolbachia among species that do not share predators and parasitoids but have similar habitats, such as shared host plants or food sources, suggests that plants or food may be involved in Wolbachia horizontal transmission (Sintupachee et al , 2006; Caspi-Fluger et al , 2012; Weinert et al , 2015).…”