Why <i>Wolbachia</i>-induced cytoplasmic incompatibility is so common.

Cytoplasmic incompatibility (CI) is the most common reproductive manipulation produced by <i>Wolbachia</i>, obligately intracellular alphaproteobacteria that infect approximately half of all insect species. Once infection frequencies within host populations approach 10%, intense CI can drive <i>Wolbachia</i> to near fixation within 10 generations. However, natural selection among <i>Wolbachia</i> variants within individual host populations does not favor enhanced CI. Indeed, variants that do not cause CI but increase host fitness or are more reliably maternally transmitted are expected to spread if infected females remain protected from CI. Nevertheless, approximately half of analyzed <i>Wolbachia</i> infections cause detectable CI. Why? The frequency and persistence of CI are more plausibly explained by preferential spread to new host species (clade selection) rather than by natural selection among variants within host populations. CI-causing <i>Wolbachia</i> lineages preferentially spread into new host species because 1) CI increases equilibrium <i>Wolbachia</i> frequencies within host populations, and 2) CI-causing variants can remain at high frequencies within populations even when conditions change so that initially beneficial <i>Wolbachia</i> infections become harmful. An epidemiological model describing <i>Wolbachia</i> acquisition and loss by host species and the loss of CI-induction within <i>Wolbachia</i> lineages yields simple expressions for the incidence of <i>Wolbachia</i> infections and the fraction of those infections causing CI. Supporting a determinative role for differential interspecific spread in maintaining CI, many <i>Wolbachia</i> infections were recently acquired by their host species, many show evidence for contemporary spatial spread or retreat, and rapid evolution of CI-inducing loci, especially degradation, is common.