The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni

Abstract

Many arthropods are infected with vertically transmitted, intracellular bacteria manipulating their host's reproduction. Cytoplasmic incompatibility (CI) is commonly observed and is expressed as a reduction in the number of offspring in crosses between infected males and uninfected females (or females infected with a different bacterial strain). CI is often related to the presence of Wolbachia, but recent findings indicate that a second reproductive parasite, Cardinium, is also capable of inducing CI. Although both Wolbachia and Cardinium occur in arthropods and may infect the same host species, little is known about their interactions. We observed Wolbachia and Cardinium in the sexual spider mite Bryobia sarothamni (Acari: Tetranychidae) and investigated the effects of both bacteria on reproduction. We performed all possible crossing combinations using naturally infected strains, and show that Cardinium induces strong CI, expressed as an almost complete female mortality. B. sarothamni is the third host species in which Cardiniuminduced CI is observed, and this study reveals the strongest CI effect found so far. Wolbachia, however, did not induce CI. Even so, CI was not induced by doubly infected males, and neither singly Wolbachia-infected nor doubly infected females could rescue CI induced by Cardinium-infected males. Possibly, this is related to the differences between Cardinium strains infecting singly and doubly infected individuals. We found a cost of infection in single infected individuals, but not in doubly infected individuals. We show that infection frequencies in field populations ranged from completely uninfected to a polymorphic state. In none of the populations infections were fixed.

Diversity and Phylogeny of Cardinium (Bacteroidetes) in Armored Scale Insects (Hemiptera: Diaspididae)

“…Co-infections with different strains of the same bacterium or different reproductive parasites are known to occur across arthropods (Weeks et al 2003;Goodacre et al 2006;Gotoh et al 2006;Duron et al 2008a;Skaljac et al 2010;Goodacre and Martin 2012). This problem has been the focus of theoretical (e.g., Engelstädter et al 2008;Vautrin et al 2008) and empirical study focusing specifically on interactions between Cardinium and the widespread Wolbachia (Gotoh et al 2006;Ros and Breeuwer 2009;White et al 2009;Sirviö and Pamilo 2010). …”

“…Cardinium is now known to cause three of the four classic phenotypes often associated with reproductive parasites: cytoplasmic incompatibility in the parasitoid wasp Encarsia pergendiella (Hunter et al 2003), the spider mite Bryobia sarothamni (Ros and Breeuwer 2009), and the tetranychid mites Eotetranychus suginamensis (Gotoh et al 2006) and Tetranychus cinnabarinus (Xie et al 2010); feminization in Brevipalpus mites (Weeks et al 2001); and parthenogenesis in the hemipteran Aspidiotus nerii (Provencher et al 2005) and in Encarsia species (Zchori-Fein et al 2001;2004). In contrast to the better-known symbionts Wolbachia and Spiroplasma, the parasite Cardinium has so far not been found to be associated with male-killing.…”

Morphological variation and reproductive incompatibility of three coconut-mite-associated populations of predatory mites identified as Neoseiulus paspalivorus (Acari: Phytoseiidae)

“…Only in the phytoseiid Galendromus occidentalis (Nesbitt) and in some spider mites, the endosymbionts Wolbachia and more recently Cardinium have been demonstrated to mediate unidirectional reproductive incompatibility (Hess and Hoy 1982;Gotoh et al 1995;Johanowicz and Hoy 1996;Breeuwer 1997;Vala et al 2000Vala et al , 2002Vala et al , 2003Gotoh et al 2006;Ros and Breeuwer 2009). Bidirectional incompatibility is assumed to be caused by either negative nuclear-nuclear genes interactions, as has been reported in the spider mite Panonychus mori Yokoyama (Gotoh et al 2005), or infection by different strains of Wolbachia, as is well documented for insects (Laven 1959(Laven , 1967Mercot et al 1995;O"Neill and Karr 1990;Clancy and Hoffmann 1996).…”

Population dynamics and rapid spread of Cardinium, a bacterial endosymbiont causing cytoplasmic incompatibility in Encarsia pergandiella (Hymenoptera: Aphelinidae)

“…Wolbachia has been shown to cause CI in all of the major insect orders, as well as in mites and isopods (Stouthamer et al, 1999). More recently, Cardinium, a member of the phylum Bacteroidetes, has been found to cause CI in three hosts: in the parasitoid wasp Encarsia pergandiella , and in the spider mites Eotetranychus suginamensis and Bryobia sarothamni (Gotoh et al, 2007;Ros and Breeuwer, 2009). Since its discovery, Cardinium has been found in four orders and approximately 6-7% of arthropods (Weeks et al, 2003;Zchori-Fein and Perlman, 2004;Duron et al, 2008).…”