Evolutionary Ecology of Wolbachia Releases for Disease Control

Abstract

Wolbachia is an endosymbiotic Alphaproteobacteria that can suppress insect-borne diseases through decreasing host virus transmission (population replacement) or through decreasing host population density (population suppression). We contrast natural Wolbachia infections in insect populations with Wolbachia transinfections in mosquitoes to gain insights into factors potentially affecting the long-term success of Wolbachia releases. Natural Wolbachia infections can spread rapidly, whereas the slow spread of transinfections is governed by deleterious effects on host fitness and demographic factors. Cytoplasmic incompatibility (CI) generated by Wolbachia is central to both population replacement and suppression programs, but CI in nature can be variable and evolve, as can Wolbachia fitness effects and virus blocking. Wolbachia spread is also influenced by environmental factors that decrease Wolbachia titer and reduce maternal Wolbachia transmission frequency. More information is needed on the interactions between Wolbachia and host nuclear/mitochondrial genomes, the interaction between invasion success and local ecological factors, and the long-term stability of Wolbachia-mediated virus blocking.

Keywords: biocontrol; dengue; fitness costs; transinfections; vector replacement; vector suppression.

Figure 1

Factors influencing the success of Wolbachia releases during and after the releases. Wolbachia population replacement and suppression are influenced by features of the Wolbachia variant, mosquito host factors, production issues, and environmental factors. Long-term disease suppression may be affected by evolutionary changes in the mosquito host, virus, or Wolbachia and by a public commitment to maintain surveillance and perform additional releases as required. Abbreviation: CI, cytoplasmic incompatibility.

Figure 2

Effects of Wolbachia infections on mosquito fitness traits. Data were extracted from 75 studies that compared the fitness of Wolbachia-infected mosquitoes with that of uninfected mosquitoes. Shaded bars represent the proportion of traits on which Wolbachia infections had a negative (red), positive (blue), or no statistically significant (P > 0.05) effect (gray) on fitness according to statistical tests by the authors. Magnitudes of fitness effects are expressed in terms of effect sizes (Hedges’ g), where dots and error bars represent medians and 95% confidence intervals, respectively. Numbers to the right of the colored bars indicate the number of fitness estimates reported by the authors in each category. Numbers to the right of the effect-size chart are the number of estimated effects, often smaller than the number of fitness estimates because data needed to estimate effect sizes were not provided with all fitness estimates (an exception is fecundity for natural Wolbachia infections, where we were able to calculate some effect sizes, even when authors did not report statistical analyses of effects). Supplemental Data Set 1 provides the data and describes how they were compiled. Effects are shown separately for natural Wolbachia infections (black error bars) and Wolbachia transinfections (purple error bars). (a) Effects are separated by mosquito species and Wolbachia infection type (natural or transinfection). For Aedes aegypti, for which more data were available, effects are shown separately for three of the most-studied Wolbachia variants. (b) Fitness effects are separated into different trait types for natural Wolbachia infections and transinfections.