Advertisement

Applied Entomology and Zoology

, Volume 53, Issue 3, pp 403–409 | Cite as

Artificial transfer of a thelytoky-inducing Wolbachia endosymbiont between strains of the endoparasitoid wasp Asobara japonica (Hymenoptera: Braconidae)

  • Shinpei Yamashita
  • Kazuo H. Takahashi
Original Research Paper
  • 101 Downloads

Abstract

Infection with Wolbachia is known to induce diploidization of haploid eggs and enables the production of females from unfertilized eggs. Although there have been several attempts to achieve the artificial horizontal transfer of thelytoky-inducing Wolbachia in parasitoid wasps, the artificial induction of thelytoky has generally been unsuccessful. In this study, we used two strains of Asobara japonica as study materials—one infected with thelytoky-inducing Wolbachia and the other not. We investigated methods of artificially inducing thelytoky by transferring thelytoky-inducing Wolbachia from wasps of the infected strain (the donor wasps) to wasps that had been cured of Wolbachia and to wasps of the uninfected strain (the recipient wasps). To examine the efficiencies of various methods of transfection, we compared the survival and infection rates of recipient wasps that received microinjections at the pupal and adult stages and in different body parts. We also examined the infection rate of the recipients due to cannibalism of Wolbachia-infected pupae. Among those methods, only microinjection at the adult stage resulted in the successful artificial horizontal transfer of Wolbachia, and some of the Wolbachia-infected wasps showed incomplete thelytoky. A low Wolbachia titer in the artificially infected wasps may explain why the thelytoky was incomplete.

Keywords

Cannibalism Endoparasitoid Microinjection Parthenogenesis Quantitative PCR 

Notes

Acknowledgements

We thank Dr. Masahito Kimura for supplying us with A. japonica strains and Dr. Kenji Tomioka for giving us valuble advices and helping us to develop microinjection methods. This study was financially supported by the Japan Prize Foundation.

References

  1. Allemand R, Lematre C, Frey F, Bouletreau M, Vavre F, Nordlander G, van Alphen J, Carton Y (2002) Phylogeny of six African Leptopilina species (Hymenoptera: Cynipoidea, Figitidae), parasitoids of Drosophila, with description of three new species. Ann Soc Entomol Fr 38:319–332CrossRefGoogle Scholar
  2. Asplen MK, Anfora G, Biondi A, Choi DS, Chu D, Daane KM, Gibert P, Gutierrez AP, Hoelmer KA, Hutchison WD, Isaacs R, Jiang ZL, Kárpáti Z, Kimura MT, Pascual M, Philips CR, Plantamp C, Ponti L, Vétek G, Vogt H, Walton VM, Yu Y, Zappála L, Desneux N (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494CrossRefGoogle Scholar
  3. Calabria G, Máca J, Bächli G, Serra L, Pascual M (2010) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147CrossRefGoogle Scholar
  4. Cordaux R, Michel-Salzat A, Bouchon D (2001) Wolbachia infection in crustaceans: novel hosts and potential routes for horizontal transmission. J Evol Biol 14:237–243CrossRefGoogle Scholar
  5. Daane KM, Wang XG, Biondi A, Miller JC, Miller B, Miller JC, Reidl H, Shearer PW, Guerrieri E, Giorgini M, Buffington M, van Achterberg K, Song Y, Kang T, Yi H, Jung C, Lee DW, Chung B-K, Hoelmer KA, Walton VM (2016) First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J Pest Sci 89:823–835CrossRefGoogle Scholar
  6. Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98:6247–6252CrossRefPubMedGoogle Scholar
  7. Grenier S, Pintureau B, Heddi A, Lassabliére F, Jager C, Louis C, Khatchadourian C (1998) Successful horizontal transfer of Wolbachia symbionts between Trichogramma wasps. Proc R Soc Lond B 265:1441–1445CrossRefGoogle Scholar
  8. Hauser M, Gaimari S, Damus M (2009) Drosophila suzukii new to North America. Fly Times 43:12–15Google Scholar
  9. Heath BD, Butcher RD, Whitfield WG, Hubbard SF (1999) Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 9:313–316CrossRefPubMedGoogle Scholar
  10. Ideo S, Watada M, Mitsui H, Kimura MT (2008) Host range of Asobara japonica (Hymenoptera: Braconidae), a larval parasitoid of drosophilid flies. Entomol Sci 11:1–6CrossRefGoogle Scholar
  11. Kremer N, Charif D, Henri H, Bataille M, Prevost G, Kraaijeveld K, Vavre F (2009) A new case of Wolbachia dependence in the genus Asobara: evidence for parthenogenesis induction in Asobara japonica. Heredity 103:248–256CrossRefPubMedGoogle Scholar
  12. Kubota M, Morii T, Miura K (2005) In vitro cultivation of parthenogenesis-inducing Wolbachia in an Aedes albopictus cell line. Entomol Exp Appl 117:83–87CrossRefGoogle Scholar
  13. Le Clec’h W, Chevalier FD, Genty L, Bertaux J, Bouchon D, Sicard M (2013) Cannibalism and predation as paths for horizontal passage of Wolbachia between terrestrial isopods. PLoS One 8:e60232CrossRefPubMedPubMedCentralGoogle Scholar
  14. Memmott J, Martinez ND, Cohen JE (2000) Predators, parasitoids and pathogens: species richness, trophic generality and body sizes in a natural food web. J Anim Ecol 69:1–15CrossRefGoogle Scholar
  15. Mitsui H, Achterberg KV, Nordlander G, Kimura MT (2007) Geographical distributions and host associations of larval parasitoids of frugivorous Drosophilidae in Japan. J Nat Hist 41:25–28CrossRefGoogle Scholar
  16. Mouton L, Dedeine F, Henri H, Bouletreau M, Profizi N, Vavre F (2004) Virulence, multiple infections and regulation of symbiotic population in the WolbachiaAsobara tabida symbiosis. Genetics 168:181–189CrossRefPubMedPubMedCentralGoogle Scholar
  17. Pannebakker BA, Pijnacker LP, Zwaan BJ, Beukeboom LW (2004) Cytology of Wolbachia-induced parthenogenesis in Leptopilina clavipes (Hymenoptera: Figitidae). Genome 47:299–303CrossRefPubMedGoogle Scholar
  18. Ruang-areerate T, Kittayapong P (2006) Wolbachia transinfection in Aedes aegypti: a potential gene driver of dengue vectors. Proc Natl Acad Sci USA 103:12534–12539CrossRefPubMedGoogle Scholar
  19. Serbus LR, Casper-Lindley C, Landmann F, Sullivan W (2008) The genetics and cell biology of Wolbachia–host interactions. Annu Rev Genet 42:683–707Google Scholar
  20. Stouthamer R (1993) The use of sexual versus asexual wasps in biological control. Entomophaga 38:3–6CrossRefGoogle Scholar
  21. Stouthamer R, Kazmer DJ (1994) Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 7:317–327CrossRefGoogle Scholar
  22. Strand MR, Vinson SB (1985) In vitro culture of Trichogramma pretiosum on an artificial medium. Entomol Exp Appl 39:203–209CrossRefGoogle Scholar
  23. Watanabe M, Kageyama D, Miura K (2013) Transfer of a parthenogenesis-inducing Wolbachia endosymbiont derived from Trichogramma dendrolimi into Trichogramma evanescens. J Invertebr Pathol 112:83–87CrossRefPubMedGoogle Scholar
  24. Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42:587–609CrossRefPubMedGoogle Scholar
  25. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751CrossRefPubMedGoogle Scholar
  26. Xi Z, Dean JL, Khoo C, Dobson SL (2005) Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection. Insect Biochem Mol Biol 35:903–910CrossRefPubMedPubMedCentralGoogle Scholar
  27. Xi ZY, Khoo CCH, Dobson SL (2006) Interspecific transfer of Wolbachia into the mosquito disease vector Aedes albopictus. Proc R Soc Lond Ser B 273:1317–1322CrossRefGoogle Scholar

Copyright information

© The Japanese Society of Applied Entomology and Zoology 2018

Authors and Affiliations

  1. 1.Graduate School of Environmental ScienceOkayama UniversityOkayamaJapan

Personalised recommendations