Which Way to Manipulate Host Reproduction?WolbachiaThat Cause Cytoplasmic Incompatibility Are Easily Invaded by Sex Ratio–Distorting Mutants

Abstract

The bacterium Wolbachia manipulates its hosts by inducing cytoplasmic incompatibility (CI), where zygotes formed from crosses between uninfected mothers and infected fathers die. In addition, it distorts the host's sex ratio via male killing, parthenogenesis induction, or feminization. Here, we model transitions between these states, examining the evolution of mutants of CI strains that retain both the ability to induce and resist CI but, in addition, cause sex ratio distortion. The model shows that CI strains are highly susceptible to invasion and subsequent elimination by these mutants. For all three types of sex ratio distortion, there is some parameter space in which the strain showing sex ratio distortion becomes extinct following exclusion of the progenitor CI strain, leaving the population uninfected. Extinction of the new Wolbachia strain is common for the case of male killing but rarer for parthenogenesis induction and feminization. Our models predict that CI strains of Wolbachia will occur most commonly in hosts that are male heterogametic, where there is little interaction between siblings because these hosts are unlikely to favor the spread of male killing, feminization, or parthenogenesis induction. The models raise the question of why CI strains apparently predominate in nature, and it is suggested that this is a result of either fewer restrictions on CI strains spreading through novel host populations or restrictions to the mutability of Wolbachia strains.