Comparative Genomics Reveals Factors Associated with Phenotypic Expression of Wolbachia

Abstract

Wolbachia is awidespread, vertically transmitted bacterial endosymbiont known for manipulating arthropod reproduction. Its most common form of reproductive manipulation is cytoplasmic incompatibility (CI), observed when a modification in the male sperm leads to embryonic lethality unless a compatible rescue factor is present in the female egg. CI attracts scientific attention due to its implications for host speciation and in the use ofWolbachia for controlling vector-borne diseases.However, our understanding ofCI is complicated by the complexity of the phenotype, whose expression depends on both symbiont and host factors. In the present study,we performa comparative analysis of nine completeWolbachia genomeswith known CI properties in the same genetic host background, Drosophila simulans STC.We describe genetic differences between closely related strains and uncover evidence that phages and othermobile elements contribute to the rapid evolution of both genomes and phenotypes of Wolbachia. Additionally, we identify both known and novel genes associatedwith themodification and rescue functions ofCI.We combine our observations with published phenotypic information and discuss howvariability in cif genes, novelCI-associated genes, andWolbachia titermight contribute topoorlyunderstoodaspectsofCI suchas strengthandbidirectional incompatibility.We speculate thathigh titerCI strains could be better at invading newhosts already infectedwith a CI Wolbachia, due to a higher rescue potential, and suggest that titer might thus be a relevant parameter to consider for future strategies using CI Wolbachia in biological control.