Diversity and distribution of Wolbachia in relation to geography, host plant affiliation and life cycle of a heterogonic gall wasp

Abstract

BackgroundThe maternally inherited endosymbiont Wolbachia is widespread in arthropods and nematodes and can play an important role in the ecology and evolution of its host through reproductive manipulation. Here, we survey Wolbachia in Belonocnema treatae, a widely distributed North American cynipid gall forming wasp that exhibits regional host specialization on three species of oaks and alternation of sexually and asexually reproducing generations. We investigated whether patterns of Wolbachia infection and diversity in B. treatae are associated with the insect’s geographic distribution, host plant association, life cycle, and mitochondrial evolutionary history.ResultsScreening of 463 individuals from 23 populations including sexual and asexual generations from all three host plants across the southern U.S. showed an average infection rate of 56% with three common Wolbachia strains: wTre1–3 and an additional rare variant wTre4. Phylogenetic analysis based on wsp showed that these strains are unrelated and likely independently inherited. We found no difference in Wolbachia infection frequency among host plant associated populations or between the asexual and sexual generations, or between males and females of the sexual generation. Partially incomplete Wolbachia transmission rates might explain the occurrence of uninfected individuals. A parallel analysis of the mitochondrial cytochrome oxidase I gene in B. treatae showed high mtDNA haplotype diversity in both infected and uninfected populations suggesting an ancestral infection by Wolbachia as well as a clear split between eastern and western B. treatae mtDNA clades with a sequence divergence of > 6%. The strain wTre1 was present almost exclusively in the western clade while wTre2 and wTre3 occur almost exclusively in eastern populations. In contrast, the same strains co-occur as double-infections in Georgia and triple-infections in two populations in central Florida.ConclusionsThe diversity of Wolbachia across geographically and genetically distinct populations of B. treatae and the co-occurrence of the same strains within three populations highlights the complex infection dynamics in this system. Moreover, the association of distinct Wolbachia strains with mitochondrial haplotypes of its host in populations infected by different Wolbachia strains suggests a potential role of the endosymbiont in reproductive isolation in B. treatae.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1151-z) contains supplementary material, which is available to authorized users.

Host plant associations and geography interact to shape diversification in a specialist insect herbivore

“…As hypothesized by Anderson () and Remington (), this region likely reflects the midpoint between refugia and the union of allopatric populations upon postglacial expansions. Our results conform to predictions based on the geographic distribution of mitochondrial haplotypes of B. treatae previously sampled from 23 sites distributed across the geographic ranges of Qf, Qv and Qg (including many of the sites investigated here) (Schuler et al, ). However, mtDNA haplotype data can be misleading with respect to population history particularly when secondary contact scenarios seem likely (Linnen & Farrell, ; Zakharov, Lobo, Nowak, & Hellmann, ).…”

“…For example, B. treatae , the focal species of this study, develops within galls induced on only American live oaks, ( Quercus subsection Virentes Nixon), a clade of seven species distributed throughout portions of North and Central America and Cuba (Cavender‐Bares et al, ; Hipp et al, ; Muller, ). Within the United States, B. treatae exhibits regional specialization on Quercus fusiformis ( Qf ), Q. virginiana ( Qv ) and Q. geminata ( Qg ) (Lund, Ott, & Lyon, ; Schuler et al, ). The geographic range of B. treatae largely parallels the geographic ranges of these hosts, which are distributed across the southern and southeastern United States with varying degrees of overlap spanning sympatry to parapatry to allopatry (Cavender‐Bares et al, ; Manos, Doyle, & Nixon, ; Nixon, ; Figure ).…”

“…A prior study of one nuclear and two mitochondrial loci described limited genetic divergence among parapatric populations of B. treatae developing on Qv and Qg in Florida, suggesting that these host‐associated lineages are in the early stages of divergence (Egan, Hood, Feder, et al, ). Subsequently, Schuler et al () examined mitochondrial haplotypes of a single gene across the geographic and host plant range of B. treatae and identified two deeply diverged clades with B. treatae from Qg and eastern Qv constituting one lineage and B. treatae from Qf and western Qv constituting the other. These studies suggest that populations of B. treatae distributed in sympatry or parapatry on their respective host plants in Florida do not represent highly diverged lineages and implicate a larger role for geography than host plant in structuring genetic variation at larger spatial scales, thus forming the basis of the hypotheses tested herein.…”

Combined effects of elevated CO2 concentration and Wolbachia on Hylyphantes graminicola (Araneae: Linyphiidae)

“…However, the number of eggs laid by H. armigera did not differ between ambient and high CO 2 concentrations (Chen et al, 2005). (Schuler et al, 2018).…”

“…They belong to α-subdivision of the Proteobacteria (Weisburg et al, 1989), and Wolbachia have attracted a considerable recent interest (Schuler et al, 2018). They belong to α-subdivision of the Proteobacteria (Weisburg et al, 1989), and Wolbachia have attracted a considerable recent interest (Schuler et al, 2018).…”