Why Wolbachia-induced cytoplasmic incompatibility is so common

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.

Keywords: epidemiology; levels of selection; mutualism; reproductive manipulation; spite.

Fig. 1.

Effects of CI on fixation probabilities for initially rare deleterious (A) and mutualistic (B) Wolbachia infections with perfect maternal transmission (μ = 0). Both panels assume that a single infected female is introduced and plot the probability of fixation, denoted P(fix), as a function of the level of CI, with s_h = 1 − H denoting the proportional decrease of embryo viability caused by CI. The dots are estimates based on computer simulations; the solid lines are diffusion approximations (Materials and Methods). The effective population size is assumed to be 100 in A, whereas it is assumed to be 1,000 (black) or 5,000 (red) in B. (A), F, the relative fecundity of Wolbachia-infected females, is either 0.99 (upper line) or 0.95 (lower). (B), F = 1.05 (upper) or 1.02 (lower). The dotted lines in B provide the Haldane (83) approximation P(fix) ∼ 2(F − 1).

Fig. 2.

Effect of CI on the expected persistence times of Wolbachia infections when fitness effects fluctuate. As expected, persistence times increase with higher median Wolbachia fitness effects (blue versus gold) and more intense CI (increasing s_h). The simulations assume that the relative fecundity, F, of infected females fluctuates across generations as independent, identically distributed log-normal random variables with CV_F = 0.4. This corresponds to extreme variation in F. With median(F) = 1.05, the 0.025 and 0.975 percentiles are 0.49 and 2.23, respectively; with median(F) = 1.021, the corresponding values are 0.48 and 2.17. The effective female population size is 1,000 and maternal Wolbachia transmission is imperfect with μ = 0.02, so that eventual loss is certain. The estimates presented are the average over 25 replicate simulations. Persistence times are approximately exponentially distributed, so the SE for each estimate is approximately one-fifth of the estimated mean.

Fig. 3.

Estimated Wolbachia frequencies from 41 host species with detectable Wolbachia infections in which at least 30 individuals were sampled within each of at least two populations. (A) The mean infection frequencies (arithmetic means over populations, not weighted by sample sizes) for the 21 species showing statistically significant (P < 0.05) spatial heterogeneity in frequencies. (B) For the 21 species from A, abbreviated species names are listed and the ranges of estimated intraspecific infection frequencies, ordered from largest to smallest ranges. The dark blue dots in B show the unweighted arithmetic mean frequencies across populations (i.e., the values plotted in A). (C) The mean infection frequencies from the 20 infected species displaying no statistically significant (P > 0.05) spatial heterogeneity in frequencies. (D) The names and ranges of intraspecific frequency estimates for the 20 species from C.