Evolutionary history of Wolbachia infections in the fire ant Solenopsis invicta

Abstract

BackgroundWolbachia are endosymbiotic bacteria that commonly infect numerous arthropods. Despite their broad taxonomic distribution, the transmission patterns of these bacteria within and among host species are not well understood. We sequenced a portion of the wsp gene from the Wolbachia genome infecting 138 individuals from eleven geographically distributed native populations of the fire ant Solenopsis invicta. We then compared these wsp sequence data to patterns of mitochondrial DNA (mtDNA) variation of both infected and uninfected host individuals to infer the transmission patterns of Wolbachia in S. invicta.ResultsThree different Wolbachia (wsp) variants occur within S. invicta, all of which are identical to previously described strains in fire ants. A comparison of the distribution of Wolbachia variants within S. invicta to a phylogeny of mtDNA haplotypes suggests S. invicta has acquired Wolbachia infections on at least three independent occasions. One common Wolbachia variant in S. invicta (wSinvictaB) is associated with two divergent mtDNA haplotype clades. Further, within each of these clades, Wolbachia-infected and uninfected individuals possess virtually identical subsets of mtDNA haplotypes, including both putative derived and ancestral mtDNA haplotypes. The same pattern also holds for wSinvictaA, where at least one and as many as three invasions into S. invicta have occurred. These data suggest that the initial invasions of Wolbachia into host ant populations may be relatively ancient and have been followed by multiple secondary losses of Wolbachia in different infected lineages over time. Finally, our data also provide additional insights into the factors responsible for previously reported variation in Wolbachia prevalence among S. invicta populations.ConclusionThe history of Wolbachia infections in S. invicta is rather complex and involves multiple invasions or horizontal transmission events of Wolbachia into this species. Although these Wolbachia infections apparently have been present for relatively long time periods, these data clearly indicate that Wolbachia infections frequently have been secondarily lost within different lineages. Importantly, the uncoupled transmission of the Wolbachia and mtDNA genomes suggests that the presumed effects of Wolbachia on mtDNA evolution within S. invicta are less severe than originally predicted. Thus, the common concern that use of mtDNA markers for studying the evolutionary history of insects is confounded by maternally inherited endosymbionts such as Wolbachia may be somewhat unwarranted in the case of S. invicta.

Loss of microbial (pathogen) infections associated with recent invasions of the red imported fire ant Solenopsis invicta

“…We sequenced each PCR amplicon to further verify the PCR products that were amplified from a given PCR assay actually represented the targeted pathogen species. The general methods can be found in Ahrens and Shoemaker (2005). Briefly, PCR amplicons were gel purified, ligated into PCR4-TOPO vector, and transformed into TOP10 competent Escherichia coli cells (Invitrogen, USA).…”

Analysis of the Hypervariable Regions (HVRs) of the wsp Gene of Wolbachia from Solenopsis invicta Ants in Southeastern Brazil

“…However, other mechanisms such as vertical transmission, loss and reintroduction of infection, populations structure, distinct behaviors and the spreading and radiation of populations [7] may also be important in the phylogenetic grouping we report here for Wolbachia A groups.…”

“…We estimated 50% infection rate in the sampled S. invicta mounds which is probably due to Wolbachia-infected and uninfected S. invicta queens invading new areas, generating infected and uninfected nests [7] [8] [24] [25]. A previous study [24], found 10% to 90% prevalence of Wolbachia infection in native populations of S. invicta.…”

“…Several factors influence Wolbachia infection of ant nests including microgeographic variation, environmental factors or intrinsic characteristics of the hosts [7]. We estimated 50% infection rate in the sampled S. invicta mounds which is probably due to Wolbachia-infected and uninfected S. invicta queens invading new areas, generating infected and uninfected nests [7] [8] [24] [25].…”

“…Wolbachia infection of S. invicta populations has occurred six different times via horizontal transmission [7], but there have been multiple infections and independent loses. These researchers also noted that significant variation in the prevalence of the Wolbachia infection can be caused by regional limits, environment factors and loss of infection by hosts.…”