Intra-lineage microevolution ofWolbachialeads to the emergence of new cytoplasmic incompatibility patterns

Abstract

AbstractMosquitoes of theCulex pipienscomplex are worldwide vectors of arbovirus, filarial nematode, and avian malaria agents. In these hosts, the endosymbiotic bacteriaWolbachiainduce cytoplasmic incompatibility (CI), that is, reduced embryo viability in so-called incompatible crosses.WolbachiainfectingCulex pipiens(wPip) cause CI patterns of unparalleled complexity, associated with the amplification and diversification ofcidAandcidBgenes, with up to six different gene copies described in a singlewPip genome. By repeating crosses betweenCulexisofemale lines over 17 years, we documented the emergence of a new compatibility type. Using a new sequencing method adapted to multigene families to acquirecidgenes, we showed that somewPip genomes lost specificcidAgene copies, thus giving rise to several sub-lineages segregating in the same cage. By linking phenotypic changes to their underlying genotypic bases, we showed that gene copies that are key for CI phenotypes originated from recombinations, not point mutations. We revealed how new CI patterns could emerge as part of a two-step process: first, local changes take place in the CI repertoires while maintaining compatibility with the surrounding mosquitoes, and then migration and secondary contact occur with the incompatible lines.