Wolbachia Divergence and the Evolution of Cytoplasmic Incompatibility in Culex pipiens

Abstract

Many insect species harbor Wolbachia bacteria that induce cytoplasmic incompatibility (CI), i.e. embryonic lethality in crosses between infected males and uninfected females, or between males and females carrying incompatible Wolbachia strains. The molecular mechanism of CI remains unknown, but the available data are best interpreted under a modification–rescue model, where a mod function disables the reproductive success of infected males’ sperm, unless the eggs are infected and express a compatible resc function. Here we examine the evolution of CI in the mosquito Culex pipiens, harbouring a large number of closely related Wolbachia strains structured in five distinct phylogenetic groups. Specifically, we used a worldwide sample of mosquito lines to assess the hypothesis that genetic divergence should correlate with the divergence of CI properties on a low evolutionary scale. We observed a significant association of Wolbachia genetic divergence with CI patterns. Most Wolbachia strains from the same group were compatible whereas those from different groups were often incompatible. Consistently, we found a strong association between Wolbachia groups and their mod-resc properties. Finally, lines from the same geographical area were rarely incompatible, confirming the conjecture that the spatial distribution of Wolbachia compatibility types should be constrained by selection. This study indicates a clear correlation between Wolbachia genotypes and CI properties, paving the way toward the identification of the molecular basis of CI through comparative genomics.

Variation in Wolbachia cidB gene, but not cidA, is associated with cytoplasmic incompatibility mod phenotype diversity in Culex pipiens

“…CI is a form of conditional sterility resulting in embryonic lethality when infected males mate with uninfected females or with females infected with a different, incompatible Wolbachia strain (Atyame, Duron, et al, ; Bonneau, Landmann, et al, ; Bordenstein, O'Hara, & Werren, ; Breeuwer & Werren, ; Callaini, Riparbelli, Giordano, & Dallai, ; Duron et al, ; Laven, ; O'Neill & Karr, ). In C. pipiens where all males and females are infected, CI may be unidirectional (crossing is compatible in one direction but incompatible in the other) or bidirectional (crosses in both directions are incompatible; Atyame et al, ; Dumas et al, ; Laven, ; Rasgon & Scott, ; Sicard, Bonneau, & Weill, ). CI can be seen as a toxin‐antidote model or modification‐rescue model ( mod ‐ resc ) in which the Wolbachia present in the male produce a toxin ( mod factors) during spermatogenesis which induces CI through embryonic defects after fertilization unless the Wolbachia present in the eggs produce compatible antidotes ( resc factors) (Hurst, ; Poinsot, Charlat, & Merçot, ; Werren, ).…”

“…Cytoplasmic incompatibility in Culex pipiens mosquitoes is characterized by its unprecedented diversity of compatibility and incompatibility relationships that is based on the diversity of the Wolbachia strains infecting this species (Atyame et al, ; Duron et al, ; Laven, ). All the Wolbachia infecting C. pipiens belong to the monophyletic group w Pip inside the supergroup B and are closely related to w Bol, the Wolbachia strain infecting the butterfly Hypolimnas bolina (Atyame, Delsuc, Pasteur, Weill, & Duron, ; Bleidorn & Gerth, ).…”

First report of the endobacteriaWolbachiain natural populations ofCulex pipiensin Morocco

“…pipiens populations, facilitating the selective elimination of the other Wolbachia strains. It has been generally described that at a given site, there is only one group of Wolbachia , or Wolbachia belonging to different groups but that are compatible (Aytame et al ). In Marrakech, three groups of wPip were found (I, IV, and V).…”

Wolbachia endosymbionts and human disease control

“…Wolbachia transmission through the germ line to the next generation enables their survival, but also requires that any negative fitness effects, such as a biochemical cost for Wolbachia maintenance in the host, be balanced with positive effects for the host (Darwinian fitness). Thus, the fitness of infected hosts could be increased (mutualistic benefit) or the relative fitness of uninfected hosts could be decreased (cytoplasmic incompatibility, CI) [51,57,58]. The reproductive strategies used by Wolbachia in arthropods and nematodes provide a mechanism for their maintenance in populations, despite any negative effect on the fitness of their hosts.…”