Dataset Information

Wolbachia Horizontal Transmission Events in Ants: What Do We Know and What Can We Learn?

ABSTRACT: While strict vertical transmission insures the durability of intracellular symbioses, phylogenetic incongruences between hosts and endosymbionts suggest horizontal transmission must also occur. These horizontal acquisitions can have important implications for the biology of the host. Wolbachia is one of the most ecologically successful prokaryotes in arthropods, infecting an estimated 50-70% of all insect species. Much of this success is likely due to the fact that, in arthropods, Wolbachia is notorious for manipulating host reproduction to favor transmission through the female germline. However, its natural potential for horizontal transmission remains poorly understood. Here we evaluate the fundamental prerequisites for successful horizontal transfer, including necessary environmental conditions, genetic potential of bacterial strains, and means of mediating transfers. Furthermore, we revisit the relatedness of Wolbachia strains infecting the Panamanian leaf-cutting ant, Acromyrmex echinatior, and its inquiline social parasite, Acromyrmex insinuator, and compare our results to a study published more than 15 years ago by Van Borm et al. (2003). The results of this pilot study prompt us to reevaluate previous notions that obligate social parasitism reliably facilitates horizontal transfer and suggest that not all Wolbachia strains associated with ants have the same genetic potential for horizontal transmission.

SUBMITTER: Tolley SJA

PROVIDER: S-EPMC6414450 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Wolbachia Horizontal Transmission Events in Ants: What Do We Know and What Can We Learn?

Tolley Sarah J A SJA Nonacs Peter P Sapountzis Panagiotis P

Frontiers in microbiology 20190306

While strict vertical transmission insures the durability of intracellular symbioses, phylogenetic incongruences between hosts and endosymbionts suggest horizontal transmission must also occur. These horizontal acquisitions can have important implications for the biology of the host. Wolbachia is one of the most ecologically successful prokaryotes in arthropods, infecting an estimated 50-70% of all insect species. Much of this success is likely due to the fact that, in arthropods, Wolb ...[more]

PMID: 30894837

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Project description:BACKGROUND: The role of Wolbachia endosymbionts in shaping the mitochondrial diversity of their arthropod host depends on the effects they have on host reproduction and on the mode of transmission of the bacteria. We have compared the sequence diversity of wsp (Wolbachia surface protein gene) and the host mtDNA in a group of Formica ant species that have diverged approximately 0.5 million years ago (MYA). The aim was to study the relationship of Wolbachia and its ant hosts in terms of vertical and horizontal transmission of the bacteria. RESULTS: All studied ant species were doubly infected with two Wolbachia strains (wFex1 and wFex4) all over their geographical distribution area in Eurasia. The most common haplotypes of these strains were identical with strains previously described from a more distantly related Formica ant, with an estimated divergence time of 3.5 - 4 MYA. Some strain haplotypes were associated to the same or closely related mtDNA haplotypes as expected under vertical transmission. However, in several cases the wsp haplotypes coexisted with distant mtDNA haplotypes, a pattern which is more compatible with horizontal transmission of the bacteria. CONCLUSION: Two lines of evidence suggest that the sharing of Wolbachia strains by all F. rufa species is rather due to horizontal than vertical transmission. First, the fact that endosymbiont strains identical to those of F. rufa ants have been found in another species that diverged 3.5-4 MYA strongly suggests that horizontal transfer can and does occur between Formica ants. Second, the frequent sharing of identical Wolbachia strains by distant mitochondrial lineages within the F. rufa group further shows that horizontal transmission has occurred repeatedly. Nevertheless, our dataset also provides some evidence for longer-term persistence of infection, indicating that Wolbachia infection within this host clade has been shaped by both horizontal and vertical transmission of symbionts. The fact that all the ants were infected irrespective of the family structure of their societies gives no support to the proposed hypotheses that the spreading of Wolbachia in ants might be associated to the types of their societies.

Project description:Horizontal transmission of the endosymbiont, Wolbachia, may occur during superparasitism when parasitoid females deposit a second clutch of eggs on a host. Wolbachia may increase the superparasitism tendency of Trichogramma wasps by depriving their memory. To test this hypothesis, we investigated the effects of conditioning experience and memory inhibitors (actinomycin D [ACD] and anisomycin [ANI]) on memory capacity, and expressions of memory-related genes (CREB1 and PKA), and superparasitism frequency of Wolbachia-infected (TDW) and uninfected (TD) lines of Trichogramma dendrolimi after conditioning with lemon or peppermint odor. We detected the presence of Wolbachia in eggs, larvae, pre-pupae, pupae, and adults of Trichogramma by using fluorescence in situ hybridization. The results showed that TDW females had a more reduced memory capacity than TD females after conditioning. Compared with TD females, TDW females showed a higher proportion of superparasitism and a downregulation of CREB1 and PKA genes after conditioning. TD females fed ACD or ANI showed a higher tendency for superparasitism and a downregulation of CREB1 and PKA, along with memory loss after conditioning than TD females fed honey solution only. The presence of Wolbachia was detected in the anterior region of the larva, pre-pupa, and pupa, but was not found in the head of the adult. The results provide evidence of host behavioral manipulation of Wolbachia by depriving memory of host Trichogramma wasps based on Poulin' s criteria. These host behavioral changes led by Wolbachia may be caused by the virulence of Wolbachia on the nervous system of the host. IMPORTANCE The endosymbiotic bacteria, Wolbachia, live widely within cells of arthropods. Wolbachia are not only transmitted vertically from host mother to offspring, but are also transmitted horizontally among host individuals. Horizontal transmission is expected to occur during superparasitism when host parasitoid females deposit a clutch of eggs on a host previously parasitized by the same parasitoid species. Thus, a question is proposed regarding whether superparasitism behavior is a behavior modification induced by the symbiont to favor symbiont transmission. This study highlights behavioral mechanisms of Wolbachia-induced superparasitism in Trichogramma wasps and the manipulation of symbionts on host parasitoids.

Project description:Wolbachia are maternally inherited endosymbiotic bacteria of arthropods and nematodes. In arthropods, they manipulate the reproduction of their hosts to facilitate their own spread in host populations, causing cytoplasmic incompatibility, parthenogenesis induction, feminization of genetic males and male-killing. In this study, we investigated Wolbachia infection and studied wsp (Wolbachia surface protein) sequences in three wasp species associated with the unisexual galls of A. mukaigawae with the aim of determining the transmission mode and the reason for multiple infections of Wolbachia. Frequency of Wolbachia infected populations for A. mukaigawae, Synergus japonicus (inquiline), and Torymus sp. (parasitoid) was 75%, 100%, and 100%, respectively. Multiple Wolbachia infections were detected in A. mukaigawae and S. japonicus, with 5 and 8 Wolbachia strains, respectively. The two host species shared 5 Wolbachia strains and were infected by identical strains in several locations, indicating horizontal transmission of Wolbachia. The transmission potentially takes place through gall tissues, which the larvae of both wasps feed on. Furthermore, three recombination events of Wolbachia were observed: the strains W8, W2 and W6 apparently have derived from W3 and W5a, W6 and W7, W4 and W9, respectively. W8 and W2 and their respective parental strains were detected in S. japonicus. W6 was detected with only one parent (W4) in S. japonicus; W9 was detected in Torymus sp., suggesting horizontal transmission between hosts and parasitoids. In conclusion, our research supports earlier studies that horizontal transmission of Wolbachia, a symbiont of the Rickettsiales order, may be plant-mediated or take place between hosts and parasitoids. Our research provides novel molecular evidence for multiple recombination events of Wolbachia in gall wasp communities. We suggest that genomic recombination and potential plant-mediated horizontal transmission may be attributable to the high levels of multiple Wolbachia infections observed in A. mukaigawae and S. japonicus.

Dataset Information

Wolbachia Horizontal Transmission Events in Ants: What Do We Know and What Can We Learn?

Publications

<i>Wolbachia</i> Horizontal Transmission Events in Ants: What Do We Know and What Can We Learn?

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