BMC Genomics | 2021
Genome analyses of four Wolbachia strains and associated mitochondria of Rhagoletis cerasi expose cumulative modularity of cytoplasmic incompatibility factors and cytoplasmic hitchhiking across host populations
Abstract
Background The endosymbiont Wolbachia can manipulate arthropod reproduction and invade host populations by inducing cytoplasmic incompatibility (CI). Some host species are coinfected with multiple Wolbachia strains which may have sequentially invaded host populations by expressing different types of modular CI factor ( cif ) genes. The tephritid fruit fly Rhagoletis cerasi is a model for CI and Wolbachia population dynamics. It is associated with at least four Wolbachia strains in various combinations, with demonstrated ( w Cer2, w Cer4), predicted ( w Cer1) or unknown ( w Cer5) CI phenotypes. Results We sequenced and assembled the draft genomes of the Wolbachia strains w Cer1, w Cer4 and w Cer5, and compared these with the previously sequenced genome of w Cer2 which currently invades R. cerasi populations. We found complete cif gene pairs in all strains: four pairs in w Cer2 (three Type I; one Type V), two pairs in w Cer1 (both Type I) and w Cer4 (one Type I; one Type V), and one pair in w Cer5 (Type IV). Wolbachia genome variant analyses across geographically and genetically distant host populations revealed the largest diversity of single nucleotide polymorphisms (SNPs) in w Cer5, followed by w Cer1 and then w Cer2, indicative of their different lengths of host associations. Furthermore, mitogenome analyses of the Wolbachia genome-sequenced individuals in combination with SNP data from six European countries revealed polymorphic mitogenome sites that displayed reduced diversity in individuals infected with w Cer2 compared to those without. Conclusions Coinfections with Wolbachia are common in arthropods and affect options for Wolbachia -based management strategies of pest and vector species already infected by Wolbachia . Our analyses of Wolbachia genomes of a host naturally coinfected\xa0by several strains unravelled signatures of the evolutionary dynamics in both Wolbachia and host mitochondrial genomes as a consequence of repeated invasions. Invasion of already infected populations by new Wolbachia strains requires new sets of functionally different cif genes and thereby may select for a cumulative modularity of cif gene diversity in invading strains. Furthermore, we demonstrated at the mitogenomic scale that repeated CI-driven Wolbachia invasions of hosts result in reduced mitochondrial diversity and hitchhiking effects. Already resident Wolbachia strains may experience similar cytoplasmic hitchhiking effects caused by the invading Wolbachia strain.