Wolbachia association with the tsetse fly, Glossina fuscipes fuscipes, reveals high levels of genetic diversity and complex evolutionary dynamics

Abstract

BackgroundWolbachia pipientis, a diverse group of α-proteobacteria, can alter arthropod host reproduction and confer a reproductive advantage to Wolbachia-infected females (cytoplasmic incompatibility (CI)). This advantage can alter host population genetics because Wolbachia-infected females produce more offspring with their own mitochondrial DNA (mtDNA) haplotypes than uninfected females. Thus, these host haplotypes become common or fixed (selective sweep). Although simulations suggest that for a CI-mediated sweep to occur, there must be a transient phase with repeated initial infections of multiple individual hosts by different Wolbachia strains, this has not been observed empirically. Wolbachia has been found in the tsetse fly, Glossina fuscipes fuscipes, but it is not limited to a single host haplotype, suggesting that CI did not impact its population structure. However, host population genetic differentiation could have been generated if multiple Wolbachia strains interacted in some populations. Here, we investigated Wolbachia genetic variation in G. f. fuscipes populations of known host genetic composition in Uganda. We tested for the presence of multiple Wolbachia strains using Multi-Locus Sequence Typing (MLST) and for an association between geographic region and host mtDNA haplotype using Wolbachia DNA sequence from a variable locus, groEL (heat shock protein 60).ResultsMLST demonstrated that some G. f. fuscipes carry Wolbachia strains from two lineages. GroEL revealed high levels of sequence diversity within and between individuals (Haplotype diversity = 0.945). We found Wolbachia associated with 26 host mtDNA haplotypes, an unprecedented result. We observed a geographical association of one Wolbachia lineage with southern host mtDNA haplotypes, but it was non-significant (p = 0.16). Though most Wolbachia-infected host haplotypes were those found in the contact region between host mtDNA groups, this association was non-significant (p = 0.17).ConclusionsHigh Wolbachia sequence diversity and the association of Wolbachia with multiple host haplotypes suggest that different Wolbachia strains infected G. f. fuscipes multiple times independently. We suggest that these observations reflect a transient phase in Wolbachia evolution that is influenced by the long gestation and low reproductive output of tsetse. Although G. f. fuscipes is superinfected with Wolbachia, our data does not support that bidirectional CI has influenced host genetic diversity in Uganda.

Genetically DistinctGlossina fuscipes fuscipesPopulations in the Lake Kyoga Region of Uganda and Its Relevance for Human African Trypanosomiasis

“…It is also possible that Wolbachia -induced mating incompatibility is driving the differentiation between the population structure inferred from mitochondrial and nuclear DNA. Wolbachia mediated effects on host fitness and host population genetic can drive patterns of mtDNA variation regardless of the nuclear DNA background [36, 61, 62]. A finer scale analysis of Wolbachia infection prevalence and strain types present in flies in the contact zone is necessary to further clarify the role of Wolbachia mediated reproductive effects.…”

Tsetse fly microbiota: form and function

“…In field G. m. morsitans , Wolbachia infection prevalence ranges from 10 to 100% depending on their resident habitats (Doudoumis et al, 2012). Some G. fuscipes individuals also harbor infections with multiple Wolbachia strains (Symula et al, 2013). For example, Wolbachia strains detected in Ugandan G. fuscipes belong to two different lineages.…”

Glossina fuscipes populations provide insights for human African trypanosomiasis transmission in Uganda

“…Previous surveys using standard PCR assays could not detect Wolbachia infections in Gff in Uganda or Kenya [78,79]. When more stringent PCR assay conditions and qPCR analysis were used, low-density Wolbachia infections were detected in different Gff populations [80]. The infection prevalence in different host genetic populations ranged from zero to complete fixation, with the greatest prevalence observed in the southern genotypes, followed by northern and western genotypes (55%, 42%, and 26%, respectively) [80].…”

“…When more stringent PCR assay conditions and qPCR analysis were used, low-density Wolbachia infections were detected in different Gff populations [80]. The infection prevalence in different host genetic populations ranged from zero to complete fixation, with the greatest prevalence observed in the southern genotypes, followed by northern and western genotypes (55%, 42%, and 26%, respectively) [80]. To understand Wolbachia evolutionary dynamics and their relationship with host mtDNA, populations of known genetic background were screened for Wolbachia infection status, which showed that Wolbachia infections in Gff are not limited to a single host mtDNA haplotype [80].…”