Role of Delayed Nuclear Envelope Breakdown and Mitosis in Wolbachia -Induced Cytoplasmic Incompatibility

Abstract

The bacterium Wolbachia manipulates reproduction in millions of insects worldwide; the most common effect is cytoplasmic incompatibility (CI). We found that CI resulted from delayed nuclear envelope breakdown of the male pronucleus in Nasonia vitripennis. This caused asynchrony between the male and female pronuclei and, ultimately, loss of paternal chromosomes at the first mitosis. When Wolbachia were present in the egg, synchrony was restored, which explains suppression of CI in these crosses. These results suggest that Wolbachia target cell cycle regulatory proteins. A striking consequence of CI is that it alters the normal pattern of reciprocal centrosome inheritance in Nasonia.

Bidirectional incompatibility among divergent Wolbachia and incompatibility level differences among closely related Wolbachia in Nasonia

“…Sperms that are 'modified' by Wolbachia in the testes show abnormal processing after fertilization of the egg, if the appropriate Wolbachia are not present in the egg to 'rescue' the modification (Werren, 1997). In particular, breakdown of the nuclear envelope of the male pronucleus is delayed (Tram and Sullivan, 2002) and the paternal chromatin undergoes improper condensation during early mitotic divisions (O'Neill and Karr, 1990;Reed and Werren, 1995;Callaini et al, 1997;Tram et al, 2006). As a result, most embryos usually die, but in some haplodiploid species haploidization of the embryo results in male development (Reed and Werren, 1995;Tram et al, 2006).…”

Differential fitness of mitochondrial DNA in perturbation cage studies correlates with global abundance and population history inDrosophila simulans

“…Two of these cause high levels of cytoplasmic incompatibility (James & Ballard 2000). In its simplest form, unidirectional incompatibility is expressed when a sperm from an infected male fertilizes an ovum from an uninfected female, resulting in embryonic death due to abortive karyogamy (Tram & Sullivan 2002). If the reproductive advantage of Wolbachia-infected females outweighs the cost of infection, theory predicts that the infection frequency will increase once a critical threshold is reached (Caspari & Watson 1959;Turelli & Hoffmann 1995).…”

Fitness advantage and cytoplasmic incompatibility in Wolbachia single- and superinfected Aedes albopictus

“…Cytoplasmic incompatibility (CI) results in karyogamy failure and arrested development of early embryos in diploid insects (Tram and Sullivan, 2002). Unidirectional CI occurs in matings between Wolbachia-infected males and uninfected females (Figure 1).…”