Rapid turnover of pathogen-blocking Wolbachia and their incompatibility loci

Shropshire JD, Conner WR, Vanderpool D, Hoffmann AA, Turelli M, Cooper BS.,  bioRxiv,  2023.

At least half of all insect species carry maternally inherited Wolbachia alphaproteobacteria, making Wolbachia the most common endosymbionts in nature. Wolbachia spread to high frequencies is often due to cytoplasmic incompatibility (CI), a Wolbachia -induced sperm modification that kills embryos without Wolbachia . Several CI-causing Wolbachia variants, including w Mel from Drosophila melanogaster , also block viruses. Establishing pathogen-blocking w Mel in natural Aedes aegypti mosquito populations has reduced dengue disease incidence, with one study reporting about 85% reduction when w Mel frequency is high. However, w Mel transinfection establishment is challenging in many environments, highlighting the importance of identifying CI-causing Wolbachia variants that stably persist in diverse hosts and habitats. We demonstrate that w Mel-like variants have naturally established in widely distributed holometabolous dipteran and hymenopteran insects that diverged approximately 350 million years ago, with w Mel variants spreading rapidly among these hosts over only the last 100,000 years. Wolbachia genomes contain prophages that encode CI-causing operons ( cifs ). These cifs move among Wolbachia genomes – with and without prophages – even more rapidly than Wolbachia move among insect hosts. Our results shed light on how rapid host switching and horizontal gene transfer contribute to Wolbachia and cif diversity in nature. The diverse w Mel variants we report here from hosts present in different climates offer many new options for broadening Wolbachia -based biocontrol of diseases and pests.

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