Abstract
Cytoplasmic incompatibility (CI) is induced by the endocellular bacterium Wolbachia. It results in an embryonic mortality occurring when infected males mate with uninfected females. The mechanism involved is currently unknown, but the mod resc model allows interpretation of all observations made so far. It postulates the existence of two bacterial functions: modification (mod) and rescue (resc). The mod function acts in the males' germline, before Wolbachia are shed from maturing sperm. If sperm is affected by mod, zygote development will fail unless resc is expressed in the egg. Interestingly, CI is also observed in crosses between infected males and infected females when the two partners bear different Wolbachia strains, demonstrating that mod and resc interact in a specific manner: Two Wolbachia strains are compatible with each other only if they harbor the same compatibility type. Here we focus on the evolutionary process involved in the emergence of new compatibility types from ancestral ones. We argue that new compatibility types are likely to evolve under a wider range of conditions than previously thought, through a two-step process. First, new mod variants can arise by mutation and spread by drift. This is possible because mod is expressed in males and Wolbachia is transmitted by females. Second, once such a mod variant achieves a certain frequency, it can create the conditions for the deterministic invasion of a new resc variant, allowing the invasion of a new mod resc pair. Furthermore, we show that a stable polymorphism might be maintained in natural populations, allowing the long-term existence of "suicidal" Wolbachia strains.
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Selected References
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- Bourtzis K., Dobson S. L., Braig H. R., O'Neill S. L. Rescuing Wolbachia have been overlooked. Nature. 1998 Feb 26;391(6670):852–853. doi: 10.1038/36017. [DOI] [PubMed] [Google Scholar]
- Callaini G., Dallai R., Riparbelli M. G. Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans. J Cell Sci. 1997 Jan;110(Pt 2):271–280. doi: 10.1242/jcs.110.2.271. [DOI] [PubMed] [Google Scholar]
- Fine P. E. On the dynamics of symbiote-dependent cytoplasmic incompatibility in culicine mosquitoes. J Invertebr Pathol. 1978 Jan;31(1):10–18. doi: 10.1016/0022-2011(78)90102-7. [DOI] [PubMed] [Google Scholar]
- Frank SA. Dynamics of Cytoplasmic Incompatability with Multiple Wolbachia Infections. J Theor Biol. 1998 May 21;192(2):213–218. doi: 10.1006/jtbi.1998.0652. [DOI] [PubMed] [Google Scholar]
- Hoffmann A. A., Turelli M., Harshman L. G. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics. 1990 Dec;126(4):933–948. doi: 10.1093/genetics/126.4.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jeyaprakash A., Hoy M. A. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol. 2000 Aug;9(4):393–405. doi: 10.1046/j.1365-2583.2000.00203.x. [DOI] [PubMed] [Google Scholar]
- Merçot H., Llorente B., Jacques M., Atlan A., Montchamp-Moreau C. Variability within the Seychelles cytoplasmic incompatibility system in Drosophila simulans. Genetics. 1995 Nov;141(3):1015–1023. doi: 10.1093/genetics/141.3.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Merçot H., Poinsot D. . . . and discovered on Mount Kilimanjaro. Nature. 1998 Feb 26;391(6670):853–853. doi: 10.1038/36021. [DOI] [PubMed] [Google Scholar]
- O'Neill S. L., Karr T. L. Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature. 1990 Nov 8;348(6297):178–180. doi: 10.1038/348178a0. [DOI] [PubMed] [Google Scholar]
- Poinsot D., Bourtzis K., Markakis G., Savakis C., Merçot H. Wolbachia transfer from Drosophila melanogaster into D. simulans: Host effect and cytoplasmic incompatibility relationships. Genetics. 1998 Sep;150(1):227–237. doi: 10.1093/genetics/150.1.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Poinsot D., Montchamp-Moreau C., Merçot H. Wolbachia segregation rate in Drosophila simulans naturally bi-infected cytoplasmic lineages. Heredity (Edinb) 2000 Aug;85(Pt 2):191–198. doi: 10.1046/j.1365-2540.2000.00736.x. [DOI] [PubMed] [Google Scholar]
- Rousset F., Solignac M. Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6389–6393. doi: 10.1073/pnas.92.14.6389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Steyerberg E. W., Kievit J., de Mol Van Otterloo J. C., van Bockel J. H., Eijkemans M. J., Habbema J. D. Perioperative mortality of elective abdominal aortic aneurysm surgery. A clinical prediction rule based on literature and individual patient data. Arch Intern Med. 1995 Oct 9;155(18):1998–2004. [PubMed] [Google Scholar]
- Turelli M., Hoffmann A. A. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics. 1995 Aug;140(4):1319–1338. doi: 10.1093/genetics/140.4.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Werren J. H. Biology of Wolbachia. Annu Rev Entomol. 1997;42:587–609. doi: 10.1146/annurev.ento.42.1.587. [DOI] [PubMed] [Google Scholar]