Wolbachiaendosymbionts responsible for various alterations of sexuality in arthropods

Abstract

Rickettsia-like maternally inherited bacteria have been shown to be involved in a variety of alterations of arthropod sexuality, such as female-biased sex ratios, parthenogenesis, and sterility of crosses either between infected males and uninfected females or between infected individuals (cytoplasmic incompatibility). We have characterized several of these microorganisms through partial sequences of the small (16S) and large (23S) subunit ribosomal DNA. All the symbionts identified, which include several cytoplasmic incompatibility microorganisms, several endosymbionts of terrestrial isopods, and symbionts of two thelytokous Trichogramma wasp species, belong to a monophyletic group of related symbionts, some of which have previously been detected in several insects exhibiting cytoplasmic incompatibility. Three molecular lineages can be identified on the basis of 16S as well as 23S sequences. Although they are only known as endocellular symbionts, Wolbachia spread by horizontal transfer across host lineages as evidenced by their diversification which occurred long after that of their hosts, and by the non-congruence of the phylogenetic relationships of symbionts and their hosts. Indeed, symbionts of two different lineages have been found in the same host species, whereas closely related endosymbionts are found in distinct insect orders. Isopod endosymbionts form a separate lineage, and they can determine feminization as well as cytoplasmic incompatibility. The ability to determine cytoplasmic incompatibility, found in all lineages, is probably ancestral to this group.

Hypervariable prophage WO sequences describe an unexpected high number of Wolbachia variants in the mosquito Culex pipiens

“…This notion was strengthened by the lack of congruence between Wolbachia and phage phylogenies established with the orf7 sequence (ORF Gp3 in our study), suggesting horizontal phage exchange between bacteria co-infecting the same intracellular environment (Bordenstein & Wernegreen 2004;Gavotte et al 2004;Sanogo & Dobson 2004). Since all polymorphic regions found so far in wPip DNA are mobile genetic elements (Sanogo & Dobson 2004;Duron et al 2005), the 'real' Wolbachia genes being monomorphic (Rousset et al 1992;Guillemaud et al 1997;Duron et al 2005), it was proposed that these mobile genetic elements could favour genome fluidity and enhance rapid adaptation, especially in the highly diversified CI system of C. pipiens. For all these reasons we decided to study WO prophage organization and variability in the wPip genome.…”

“…However, no polymorphism was observed in strains displaying incompatibilities using the ftsZ gene (Guillemaud et al 1997), driving the authors to conclude that factors other than Wolbachia variants were responsible for incompatibility in this species. Similarly, no polymorphism could be detected either in the 16S rRNA sequences of Wolbachia infecting different C. pipiens subspecies (Rousset et al 1992) or in the fastest Wolbachia evolving gene wsp of mosquitoes sampled worldwide (Duron et al 2005). Recent searches for polymorphism in wPip have produced a few markers, all affecting mobile genetic elements.…”

How many species are infected withWolbachia? Cryptic sex ratio distorters revealed to be common by intensive sampling

“…These manipulations fall into two classes. Sex-ratio-distorting strains increase the production of daughters at the expense of sons by killing males, feminizing genetic males or inducing parthenogenesis (Rousset et al 1992;Stouthamer et al 1993;Hurst et al 1999). Other strains induce cytoplasmic incompatibility, which (in singly infected diploid hosts) causes a reduction in the viability of o¡spring in crosses between infected males and uninfected females (O'Neill et al 1992).…”

A comparative analysis of Wolbachia‐induced host reproductive phenotypes reveals transition rate heterogeneity

“…As the ability to induce CI is found in different Wolbachia lineages, it has been suggested that this ability is ancestral (Rousset et al., 1992). Our analysis does not provide clear support for this hypothesis.…”

“…The host reproductive phenotype associated with this origin, that is the host reproductive phenotype ancestral to supergroups A and B, is unknown. It has been suggested that CI is ancestral to all Wolbachia lineages (Rousset, Bouchon, Pintureau, Juchault, & Solignac, 1992; Stouthamer, Breeuwer, & Hurst, 1999). However, to the best of our knowledge, this assertion has never been analyzed using comparative methods.…”