Why Wolbachia-induced cytoplasmic incompatibility is so common

Significance

Wolbachia are obligately intracellular alphaproteobacteria that infect approximately half of all insect species. Maternal inheritance of these endosymbionts produces selection to enhance female fitness. In addition to mutualistic phenotypes such as nutrient provisioning, Wolbachia produce various reproductive manipulations that favor infected females. Most common is cytoplasmic incompatibility, namely reduced embryo viability when Wolbachia-infected males fertilize Wolbachia-uninfected females. The regular loss of cytoplasmic incompatibility indicates this phenotype is not favored by natural selection among Wolbachia variants within host populations. Instead, we argue that cytoplasmic incompatibility is pervasive because it enhances interspecific transmission and intraspecific persistence. Specifically, cytoplasmic incompatibility produces high prevalence frequencies within host populations and allows Wolbachia to persist in host species even when their mutualist phenotypes wane or vanish.

Abstract

Cytoplasmic incompatibility (CI) is the most common reproductive manipulation produced by Wolbachia, obligately intracellular alphaproteobacteria that infect approximately 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 or are more reliably maternally transmitted are expected to spread if infected females remain protected from CI. Nevertheless, approximately half of analyzed Wolbachia 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 Wolbachia lineages preferentially spread into new host species because 1) CI increases equilibrium Wolbachia frequencies within host populations, and 2) CI-causing variants can remain at high frequencies within populations even when conditions change so that initially beneficial Wolbachia infections become harmful. 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.