Multiple Infections with Cardinium and Two Strains of Wolbachia in The Spider Mite Tetranychus phaselus Ehara: Revealing New Forces Driving the Spread of Wolbachia

Abstract

Cytoplasmic incompatibility (CI) has been proposed as a major mechanism by which certain strains of Wolbachia to invade and persist in host populations. However, mechanisms that underlie the invasion and persistence of non-CI strains are less well understood. Here, we established a spider mite Tetranychus phaselus population multiply infected by Cardinium as well as two distinct lineages of Wolbachia, designated wCon and wOri, to study the forces driving the spread of the non-CI strain of Wolbachia wOri. Interestingly, we found that wOri provided a longevity advantage to its female hosts under ideal conditions, making wOri stay longer in this population, and then being transmitted to more offspring. Furthermore, the lifespan of uninfected females was reduced when mated with multiple-infected males. As a result, the uninfected population is attenuated by the multiple-infected males. Thus, we infer that the host age effects of multiple infection may represent sufficient forces driving the spread of wOri through the host population.

<p align="center"><strong>A review of prevalence and phylogeny of the bacterial symbiont <em>Cardinium</em> in mites (subclass: Acari)</strong></p>

“…For example, Cardinium was found associated with nonreciprocal reproductive incompatibility in M. occidentalis, a phytoseiid mite that is an important predator of spider mite pests of agricultural crops (Wu & Hoy 2012). Cardinium-induced CI was also revealed in six phytophagous mite species, Eotetranychus suginamensis (Gotoh et al 2007), Bryobia sarothamni (Ros & Breeuwer 2009), Tetranychus cinnabarinus , T. piercei (Zhu et al 2012b), Tetranychus phaselus (Zhao et al 2013a) and Tetranychus truncatus (Zhao et al 2013b). All these CI types were expressed as female mortality, which is the only CI type found for Cardinium so far.…”

“…Subsequently, many mite species were reported to harbor this symbiont (Duron et al 2008;Ros et al 2012;Kopecky et al 2013;Famah Sourassou et al 2014;Weinert et al 2015;Chaisiri et al 2015). There are several studies reporting Cardinium-induced reproductive alterations in mites (Weeks & Stouthamer 2004;Groot & Breeuwer 2006;Gotoh et al 2007;Ros & Breeuwer 2009;Liu et al 2010;Xie et al 2010;Wu & Hoy 2012;Zhu et al 2012b;Zhao et al 2013a;Zhao et al 2013b;Famah Sourassou et al 2014), and Cardinium seem to be essential for oviposition in the Ghana population of Neoseiulus paepalivorus (Famah Sourassou et al 2014). The number of publications on the association mitesCardinium has substantially increased, a comprehensive study is helpful for understanding the interactions of symbionts and hosts.…”

“…Thus, the detection of its presence in mites is done mainly using PCR-based techniques, sometimes aided by bioassays (crossing breeding studies). Available molecular markers for its detection in mites include, but not limited to, the 16S ribosomal RNA (16S rRNA) and the Gyrase B (gyrB) (Hoy & Jeyaprakash 2005;Chigira & Miura 2005;Liu et al 2006;Novelli et al 2007;Enigl & Schausberger 2007;Novelli et al 2008;Chen et al 2009;Moro et al 2009b;Jeong et al 2009;Ros et al 2012;Zhu et al 2012b;Zhao et al 2013a;Zhao et al 2013b;Hubert et al 2012;Famah Sourasson et al 2014). The other techniques used to determine the presence and distribution of Cardinium in mites are transmission electron microscopy (Kitajima et al 2007) and fluorescence in situ hybridization (Zhu et al 2012a).…”

“…An example of this is observed in Bryobia spider mites where Cardinium, which causes CI, sometimes co-occurs with Wolbachia (Ros & Breeuwer 2009). Similarly, either or both Wolbachia and Cardinium induce CI, as Wolbachia induces weak CI, whereas Cardinium induces strong CI and doubly-infected ones showed the strongest CI in T. piercei (Zhu et al 2012), T. phaselus (Zhao et al 2013a) and T. truncates (Zhao et al 2013b). In addition, and Zchori-Fein & Perlman (2004) reported mixed infections with Wolbachia and Cardinium in the predatory mite M. occidentalis.…”

Cytoplasmic incompatibility and fitness benefits in the two-spotted spider mite Tetranychus urticae (red form) doubly infected with Wolbachia and Cardinium

“…SYBR green was used to monitor the amplification reaction. The following primers (Table 2) were designed specifically to amplify the 133 bp region of the Cardinium 16S rDNA gene and the 112bp region of the Wolbachia wsp gene: CLOF, CLOR (Xie et al 2010); wConQ-F, wConQ-R (Zhao et al 2013a).…”