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Detection of Wolbachia in the tick Ixodes ricinus is due to the presence of the hymenoptera endoparasitoid Ixodiphagus hookeri.

Plantard O, Bouju-Albert A, Malard MA, Hermouet A, Capron G, Verheyden H - PLoS ONE (2012)

Bottom Line: Here we report that the endoparasitoid wasp Ixodiphagus hookeri (Hymenoptera, Chalcidoidea, Encyrtidae)--strictly associated with ticks for their development--infested at almost 100% prevalence by a W. pipientis strain belonging to a Wolbachia supergroup that has already been reported as associated with other hymenopteran parasitoids.We hypothesize that previous studies that have reported W. pipientis in ticks are due to the cryptic presence of the endoparasitoid wasp I. hookeri.This association has remained hidden until now because parasitoids within ticks cannot be detected until engorgement of the nymphs brings the wasp eggs out of diapause.

View Article: PubMed Central - PubMed

Affiliation: Biology, Epidemiology and Risk Analysis in Animal Health, (BioEpAR), INRA, UMR 1300, Nantes, France. olivier.plantard@oniris-nantes.fr

ABSTRACT
The identification of micro-organisms carried by ticks is an important issue for human and animal health. In addition to their role as pathogen vectors, ticks are also the hosts for symbiotic bacteria whose impact on tick biology is poorly known. Among these, the bacterium Wolbachia pipientis has already been reported associated with Ixodes ricinus and other tick species. However, the origins of Wolbachia in ticks and their consequences on tick biology (known to be very diverse in invertebrates, ranging from nutritional symbionts in nematodes to reproductive manipulators in insects) are unknown. Here we report that the endoparasitoid wasp Ixodiphagus hookeri (Hymenoptera, Chalcidoidea, Encyrtidae)--strictly associated with ticks for their development--infested at almost 100% prevalence by a W. pipientis strain belonging to a Wolbachia supergroup that has already been reported as associated with other hymenopteran parasitoids. In a natural population of I. ricinus that suffers high parasitism rates due to I. hookeri, we used specific PCR primers for both hymenopteran and W. pipientis gene fragments to show that all unfed tick nymphs parasitized by I. hookeri also harbored Wolbachia, while unparasitized ticks were Wolbachia-free. We demonstrated experimentally that unfed nymphs obtained from larvae exposed to I. hookeri while gorging on their vertebrate host also harbor Wolbachia. We hypothesize that previous studies that have reported W. pipientis in ticks are due to the cryptic presence of the endoparasitoid wasp I. hookeri. This association has remained hidden until now because parasitoids within ticks cannot be detected until engorgement of the nymphs brings the wasp eggs out of diapause. Finally, we discuss the consequences of this finding for our understanding of the tick microbiome, and their possible role in horizontal gene transfer among pathogenic and symbiotic bacteria.

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Ixodiphagus hookeri (Hymenoptera : Chalcidoidea, Encyrtidae).A Female habitus. B Female ovipositing in an engorged nymphs of Ixodes ricinus (ovipositor indicated by the arrow). C Adults of I. hookeri around the dead body of an engorged nymph of I. ricinus. D Emergence hole from which parasitoids exit the dead body of the engorged nymph.
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pone-0030692-g001: Ixodiphagus hookeri (Hymenoptera : Chalcidoidea, Encyrtidae).A Female habitus. B Female ovipositing in an engorged nymphs of Ixodes ricinus (ovipositor indicated by the arrow). C Adults of I. hookeri around the dead body of an engorged nymph of I. ricinus. D Emergence hole from which parasitoids exit the dead body of the engorged nymph.

Mentions: Based on both (i) engorged nymphs collected on roe-deer and (ii) host-seeking nymphs collected on vegetation that were subsequently engorged in the lab, a total of 54 ticks collected in 4 natural populations were found to be parasitized by I. hookeri (Table 2; Figure 1). Variation of parasitism rates among years and sites range from 3,2% to 12,5% in Chizé (tick nymphs collected on roe deer), and from 19,6% to 20% in Gardouch (tick nymphs collected on roe-deer and on vegetation respectively). Among the I. hookeri individuals obtained from those 54 ticks, a total of 121 I. hookeri individuals (74 females and 47 males) were screened for Wolbachia pipientis by PCR using Wsp primers. Wolbachia DNA was found in 120 (99,2%) of those individuals (a single wasp male from the Gardouch population was Wolbachia-free, even after a second PCR trial).


Detection of Wolbachia in the tick Ixodes ricinus is due to the presence of the hymenoptera endoparasitoid Ixodiphagus hookeri.

Plantard O, Bouju-Albert A, Malard MA, Hermouet A, Capron G, Verheyden H - PLoS ONE (2012)

Ixodiphagus hookeri (Hymenoptera : Chalcidoidea, Encyrtidae).A Female habitus. B Female ovipositing in an engorged nymphs of Ixodes ricinus (ovipositor indicated by the arrow). C Adults of I. hookeri around the dead body of an engorged nymph of I. ricinus. D Emergence hole from which parasitoids exit the dead body of the engorged nymph.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3266912&req=5

pone-0030692-g001: Ixodiphagus hookeri (Hymenoptera : Chalcidoidea, Encyrtidae).A Female habitus. B Female ovipositing in an engorged nymphs of Ixodes ricinus (ovipositor indicated by the arrow). C Adults of I. hookeri around the dead body of an engorged nymph of I. ricinus. D Emergence hole from which parasitoids exit the dead body of the engorged nymph.
Mentions: Based on both (i) engorged nymphs collected on roe-deer and (ii) host-seeking nymphs collected on vegetation that were subsequently engorged in the lab, a total of 54 ticks collected in 4 natural populations were found to be parasitized by I. hookeri (Table 2; Figure 1). Variation of parasitism rates among years and sites range from 3,2% to 12,5% in Chizé (tick nymphs collected on roe deer), and from 19,6% to 20% in Gardouch (tick nymphs collected on roe-deer and on vegetation respectively). Among the I. hookeri individuals obtained from those 54 ticks, a total of 121 I. hookeri individuals (74 females and 47 males) were screened for Wolbachia pipientis by PCR using Wsp primers. Wolbachia DNA was found in 120 (99,2%) of those individuals (a single wasp male from the Gardouch population was Wolbachia-free, even after a second PCR trial).

Bottom Line: Here we report that the endoparasitoid wasp Ixodiphagus hookeri (Hymenoptera, Chalcidoidea, Encyrtidae)--strictly associated with ticks for their development--infested at almost 100% prevalence by a W. pipientis strain belonging to a Wolbachia supergroup that has already been reported as associated with other hymenopteran parasitoids.We hypothesize that previous studies that have reported W. pipientis in ticks are due to the cryptic presence of the endoparasitoid wasp I. hookeri.This association has remained hidden until now because parasitoids within ticks cannot be detected until engorgement of the nymphs brings the wasp eggs out of diapause.

View Article: PubMed Central - PubMed

Affiliation: Biology, Epidemiology and Risk Analysis in Animal Health, (BioEpAR), INRA, UMR 1300, Nantes, France. olivier.plantard@oniris-nantes.fr

ABSTRACT
The identification of micro-organisms carried by ticks is an important issue for human and animal health. In addition to their role as pathogen vectors, ticks are also the hosts for symbiotic bacteria whose impact on tick biology is poorly known. Among these, the bacterium Wolbachia pipientis has already been reported associated with Ixodes ricinus and other tick species. However, the origins of Wolbachia in ticks and their consequences on tick biology (known to be very diverse in invertebrates, ranging from nutritional symbionts in nematodes to reproductive manipulators in insects) are unknown. Here we report that the endoparasitoid wasp Ixodiphagus hookeri (Hymenoptera, Chalcidoidea, Encyrtidae)--strictly associated with ticks for their development--infested at almost 100% prevalence by a W. pipientis strain belonging to a Wolbachia supergroup that has already been reported as associated with other hymenopteran parasitoids. In a natural population of I. ricinus that suffers high parasitism rates due to I. hookeri, we used specific PCR primers for both hymenopteran and W. pipientis gene fragments to show that all unfed tick nymphs parasitized by I. hookeri also harbored Wolbachia, while unparasitized ticks were Wolbachia-free. We demonstrated experimentally that unfed nymphs obtained from larvae exposed to I. hookeri while gorging on their vertebrate host also harbor Wolbachia. We hypothesize that previous studies that have reported W. pipientis in ticks are due to the cryptic presence of the endoparasitoid wasp I. hookeri. This association has remained hidden until now because parasitoids within ticks cannot be detected until engorgement of the nymphs brings the wasp eggs out of diapause. Finally, we discuss the consequences of this finding for our understanding of the tick microbiome, and their possible role in horizontal gene transfer among pathogenic and symbiotic bacteria.

Show MeSH
Related in: MedlinePlus