Abstract

Cytoplasmic incompatibility (CI) is the most common reproductive manipulation produced by Wolbachia, obligately intracellular alphaproteobacteria that infect roughly half of all insect species. Once infection frequencies within host populations approach 10%, intense CI can drive Wolbachia to near fixation within 10 generations. However, natural selection among Wolbachia variants within individual host populations does not favor enhanced CI. Indeed, variants that do not cause CI, but increase host fitness, are expected to spread –– if infected females remain protected from CI (Turelli 1994). Nevertheless, roughly half of analyzed Wolbachia infections cause detectable CI. Why? The frequency and persistence of CI is more plausibly explained by preferential spread to new host species rather than preferential spread within host populations (i.e., classical natural selection). CI-causing Wolbachia variants preferentially spread into new host species because: 1) CI increases equilibrium Wolbachia frequencies within populations, and 2) CI-causing variants can remain at high frequencies even when conditions change so that initially beneficial Wolbachia infections become harmful. In contrast, CI does little to help establish beneficial Wolbachia in new host species. An epidemiological model describing Wolbachia acquisition and loss by host species and the loss of CI-induction within Wolbachia lineages yields simple expressions for the incidence of Wolbachia infections and the fraction of those infections causing CI. Supporting a determinative role for differential interspecific spread in maintaining CI, many Wolbachia 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.