The spread of incompatibility-inducing parasites in sub-divided host populations

Background: Maternally transmitted symbionts have evolved a variety of ways to promote their spread through host populations. One strategy is to hamper the reproduction of uninfected females by a mechanism called cytoplasmic incompatibility (CI). CI occurs in crosses between infected males and uninfected females and leads to partial to near-complete infertility. CI-infections are under positive frequency-dependent selection and require genetic drift to overcome the range of low frequencies where they are counter-selected. Given the importance of drift, population subdivision would be expected to facilitate the spread of CI. Nevertheless, a previous model concluded that variance in infection between competing groups of breeding individuals impedes the spread of CI. Results: In this paper we derive a model on the spread of CI-infections in populations composed of demes linked by restricted migration. Our model shows that population sub-division facilitates the invasion of CI. While host philopatry (low migration) favours the spread of infection, deme size has a non-monotonous effect, with CI-invasion being most likely at intermediate deme size. Individual-based simulations confirm these predictions and show that high levels of local drift speed up invasion but prevent high levels of prevalence across the entire population. Additional simulations with sex-specific migration rates further show that low migration rates of both sexes are required to facilitate the spread of CI. Conclusion: Our analyses show that population structure facilitates the invasion of CI-infections. Since some level of sub-division is likely to occur in most natural populations, our results help to explain the high incidence of CI-infections across species of arthropods. Furthermore, our work has important implications for the use of CI-systems in order to genetically modify natural populations of disease vectors.