Evidence for Female Mortality in Wolbachia-Mediated Cytoplasmic Incompatibility in Haplodiploid Insects: Epidemiologic and Evolutionary Consequences

Abstract

Until now, only two Wolbachia-mediated cytoplasmic incompatibility (CI) types have been described in haplodiploid species, the first in Nasonia (Insect) and the second in Tetranychus (Acari). They both induce a malebiased sex ratio in the incompatible cross. In Nasonia, CI does not reduce fertility since incompatible eggs develop as haploid males, whereas in Tetranychus CI leads to a partial mortality of incompatible eggs, thus reducing the fertility of females. Here, we study Wolbachia infection in a Drosophila parasitoid, Leptopilina heterotoma (Hymenoptera: Figitidae). A survey of Wolbachia infection shows that all natural populations tested are totally infected. Crosses between infected males and cured females show complete incompatibility: almost no females are produced. Moreover, incompatible eggs die early during their development, unlike Nasonia. This early death allows the parasitized Drosophila larva to achieve its development and to emerge. Thus, uninfected females crossed with infected males have reduced offspring production consisting only of males. Evidence of this CI type in insects demonstrates that the difference in CI types of Nasonia and Tetranychus is not due to specific factors of insects or acari. Using theoretical models, we compare the invasion processes of different strategies of Wolbachia: CI in diploid species, the two CI types in haplodiploid species, and parthenogenesis (the classical effect in haplodiploid species). Models show that CI in haplodiploid species is less efficient than in diploid ones. However, the Leptopilina type is advantageous compared to the Nasonia type. Parthenogenesis may be more or less advantageous, depending on the infection cost and on the proportion of fertilized eggs. Finally, we can propose different processes of Wolbachia strategy evolution in haplodiploid species from Nasonia CI type to Leptopilina CI type or parthenogenesis.

Intra-Individual Coexistence of a Wolbachia Strain Required for Host Oogenesis With Two Strains Inducing Cytoplasmic Incompatibility in the Wasp Asobara Tabida

“…To determine whether strains wAtab1 and wAtab2 are able to induce CI, we performed a series of crosses in which males harbored one or two Wolbachia strains that the females lacked (Table 3). For these crosses, we observed that offspring sex ratios were highly male biased compared to the intraline control crosses (F ϭ 80.790; df ϭ 1, 9; P Ͻ 0.0001), a pattern similar to other studies in haplodiploids where CI occurs (Breeuwer and Werren 1990;Breeuwer 1997;Vavre et al 2000Vavre et al , 2001Bordenstein et al 2003). These results showed that both the strains wAtab1 and wAtab2 are able to induce CI.…”

“…CI is a sperm-egg incompatibility that results when a male infected with a certain Wolbachia strain(s) mates with either an uninfected female or an infected female harboring a different bacterial strain(s) (reviewed in Bourtzis et al 2003). These crosses result in mortality in diploids and either increased male production or female mortality in haplodiploids (Breeuwer and Werren 1990;Breeuwer 1997;Vavre et al 2000Vavre et al , 2001Bordenstein et al 2003). Consequently, multiply infected females simultaneously harboring several Wolbachia strains have a reproductive advantage over uninfected females or females infected with only a subset of Wolbachia strains (Frank 1998).…”

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

“…Female mortality is the only CI type found for Cardinium so far (Hunter et al, 2003;Gotoh et al, 2006). It is also the most common type of CI expression observed for Wolbachia in haplodiploid species (Breeuwer, 1997;Vala et al, 2000;Vavre et al, 2000;Mouton et al, 2005). The second CI type that has been observed in haplodiploid species is the male development type, which is expressed as an increased male production due to the conversion of fertilized diploid eggs into haploid eggs in early development (Breeuwer and Werren, 1993;Breeuwer, 1997;Vavre et al, 2000;Bordenstein et al, 2003;Mouton et al, 2005).…”

“…Usually, the embryos die before hatching, and therefore an increased number of unhatched eggs is observed (Hoffmann and Turelli, 1997). In haplodiploid host species, two types of CI effectsincreased female mortality (the hybrid sex in haplodiploids) and increased male production-have been described (Breeuwer and Werren, 1993;Breeuwer, 1997;Vavre et al, 2000;Bordenstein et al, 2003;Mouton et al, 2005). In the latter case, fertilized eggs develop as normal, haploid, males after complete elimination of the paternal chromosomes.…”

No variation for Wolbachia-induced hybrid breakdown in two populations of a spider mite

“…Mortality of aneuploid embryos may explain why, in most haplodiploid species, CI is expressed as a bias of F1 sex ratio towards males associated with an increase in mortality (cf. Breeuwer (1997) and Vala et al (2000), Vavre et al (2000)). …”