Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-23T21:46:41.389Z Has data issue: false hasContentIssue false

Phylogenetic placement and evidence for horizontal transfer of Wolbachia in Plutella xylostella (Lepidoptera: Plutellidae) and its parasitoid, Diadegma insulare (Hymenoptera: Ichneumonidae)

Published online by Cambridge University Press:  02 April 2012

Philip D. Batista*
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Building, University of Alberta, Edmonton, Alberta, Canada T6E 2E9
B. Andrew Keddie
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Building, University of Alberta, Edmonton, Alberta, Canada T6E 2E9
Lloyd M. Dosdall
Affiliation:
Department of Agricultural, Food and Nutritional Science, 4–10 Agriculture/Forestry Centre, University of Alberta, Edmonton, Alberta, Canada T6G 2P5
Harriet L. Harris
Affiliation:
Department of Biological Sciences, University of Alberta, Department of Biological Sciences, CW405 Biological Sciences Building, University of Alberta, Edmonton, Alberta, Canada T6E 2E9, and Department of Biology and Environmental Sciences, Concordia University College of Alberta, Edmonton, Alberta, Canada T5B 4E4
*
1 Corresponding author (e-mail: [email protected]).

Abstract

The diamondback moth, Plutella xylostella (L.), is a global pest of cruciferous crops (Brassicaceae). It has developed resistance to virtually all known insecticides, and biological control has become an important management tool. In North America the parasitoid Diadegma insulare (Cresson) has been used successfully to reduce diamondback moth populations. We document the presence of the α-proteobacterial endosymbiont Wolbachia and its associated bacteriophage WO in P. xylostella and D. insulare and examine the phylogenetic relationships of Wolbachia and WO in both host species. Our results suggest that Wolbachia and WO have been horizontally transferred in this insect–parasitoid system in recent evolutionary history. Knowledge of the dynamics of Wolbachia in P. xylostella and D. insulare may be an important factor in future control of this pest in the field.

Résumé

La fausse teigne des crucifères, Plutella xylostella (L.), est un ravageur des récoltes de crucifères (Brassicaceae) à l'échelle de la planète. Elle a développé une résistance à presque tous les insecticides connus et la lutte biologique est un outil important pour sa gestion. En Amérique du Nord, le parasitoïde Diadegma insulare (Cresson) a servi à réduire avec succès les populations de la fausse teigne des crucifères. Nous démontrons la présence d'un Wolbachia endosymbionte α-protéobactérien et de son bactériophage WO chez P. xylostella et D. insulare et nous examinons les relations phylogénétiques de Wolbachia et de WO chez les deux espèces d'hôtes. Nos résultats indiquent que Wolbachia et WO ont subi un transfert horizontal dans ce système insecte-parasitoïde durant l'histoire évolutive récente. La connaissance de la dynamique de Wolbachia chez P. xylostella et D. insulare pourrait être un facteur important dans le contrôle de ce ravageur en nature dans le futur.

[Traduit par la Rédaction]

Type
Articles
Copyright
Copyright © Entomological Society of Canada 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baldo, L., Lo, N., and Werren, J.H. 2005. Mosaic nature of the wolbachia surface protein. Journal of Bacteriology, 187(15): 54065418. PMID:16030235 doi:10.1128/JB.187.15.5406-5418.2005.CrossRefGoogle ScholarPubMed
Baldo, L., Bordenstein, S., Wernegreen, J.J., and Werren, J.H. 2006. Widespread recombination throughout Wolbachia genomes. Molecular Biology and Evolution, 23(2): 437449. PMID:16267140 doi:10.1093/molbev/msj049.CrossRefGoogle ScholarPubMed
Bordenstein, S.R., and Wernegreen, J.J. 2004. Bacteriophage flux in endosymbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates. Molecular Biology and Evolution, 21(10): 19811991. PMID:15254259 doi:10.1093/molbev/msh211.CrossRefGoogle ScholarPubMed
Braig, H.R., Zhou, W., Dobson, S.L., and O'Neill, S.L. 1998. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. Journal of Bacteriology, 180(9): 23732378. PMID:9573188.CrossRefGoogle ScholarPubMed
Canchaya, C., Proux, C., Fournous, G., Bruttin, A., and Brüssow, H. 2003. Prophage genomics. Microbiology and Molecular Biology Reviews, 67(2): 238276. PMID:12794192 doi:10.1128/MMBR.67.2.238-276.2003.CrossRefGoogle ScholarPubMed
Casiraghi, M., Bordenstein, S.R., Baldo, L., Lo, N., Beninati, T., Wernegreen, J.J., et al. 2005. Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiology, 151(12): 40154022. PMID:16339946 doi:10.1099/mic. 0.28313-0.CrossRefGoogle Scholar
Delgado, A.M., and Cook, J.M. 2009. Effects of a sex-ratio distorting endosymbiont on mtDNA variation in a global insect pest. BMC Evolutionary Biology, 9: 49. doi:10.1186/1471-2148-9-49CrossRefGoogle Scholar
Dosdall, L.M., Mason, P.G., Olfert, O., Kaminski, L., and Keddie, B.A. 2004. The origins of infestations of diamondback moth, Plutella xylostella (L.), in canola in western Canada. In The Management of Diamondback Moth and Other Crucifer Pests: Proceedings of the Fourth International Workshop, 26–29 November 2001, Melbourne, Australia. Edited by Endersby, N.M. and Ridland, P.M.. Department of Natural Resources and Environment, Melbourne, Victoria, Australia. pp. 95100.Google Scholar
Floate, K.D., Kyei-Poku, G.K., and Coghlin, P.C. 2006. Overview and relevance of Wolbachia bacteria in biocontrol research. Biocontrol Science and Technology, 16(8): 767788. doi:10.1080/09583150600699606.CrossRefGoogle Scholar
Fytrou, A., Schofield, P.G., Kraaijeveld, A.R., and Hubbard, S.F. 2006. Wolbachia infection suppresses both host defence and parasitoid counterdefence. Proceedings of the Royal Society of London B Biological Sciences, 273: 791796.CrossRefGoogle ScholarPubMed
Gavotte, L., Henri, H., Stouthamer, R., Charif, D., Charlat, S., Boulétreau, M., and Vavre, F. 2007. A survey of the bacteriophage WO in the endosymbiotic bacteria Wolbachia. Molecular Biology and Evolution, 24(2): 427435. PMID:17095536 doi:10.1093/molbev/ms1171.CrossRefGoogle ScholarPubMed
Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 9598.Google Scholar
Hedges, L.M., Brownlie, J.C., O'Neill, S.L., and Johnson, K.N. 2008. Wolbachia and virus protection in insects. Science (Washington, D.C.), 322(5902): 702. PMID:18974344 doi:10.1126/science.1162418CrossRefGoogle ScholarPubMed
Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A., and Werren, J.H. 2008. How many species are infected with Wolbachia? — a statistical analysis of current data. FEMS Microbiology Letters, 281(2): 215220. PMID:18312577 doi:10.1111/j.1574-6968.2008.01110.x.CrossRefGoogle Scholar
Holden, P.R., Brookfield, J.F., and Jones, P. 1993. Cloning and characterization of an ftsZ homologue from a bacterial symbiont of Drosophila melanogaster. Molecular and General Genetics, 240(2): 213220. PMID:7689140 doi:10.1007/BF00277059.CrossRefGoogle ScholarPubMed
Hsiao, T.H. 1996. Studies of interactions between alfalfa weevil strains, Wolbachia endosymbionts and parasitoids. In The ecology of agricultural pests: biochemical approaches. Edited by Symondson, W.O.C. and Liddell, J.E.. Chapman and Hall, London, United Kingdom. pp. 5171.Google Scholar
Jeyaprakash, A., and Hoy, M.A. 2000. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Molecular Biology, 9(4): 393405. PMID:10971717 doi:10.1046/j.1365-2583.2000.00203.x.CrossRefGoogle ScholarPubMed
Koch, M., Al-Shehbaz, I.A., and Mummenhoff, K. 2003. Molecular systematics, evolution, and population biology in the mustard family (Brassicaceae). Annals of the Missouri Botanical Garden, 90(2): 151171. doi:10.2307/3298580.CrossRefGoogle Scholar
Lamb, R.J. 1989. Entomology of oilseed Brassica crops. Annual Review of Entomology, 34(1): 211229. doi:10.1146/annurev.en.34.010189.001235.CrossRefGoogle Scholar
Lo, N., Casiraghi, M., Salati, E., Bazzocchi, C., and Bandi, C. 2002. How many wolbachia supergroups exist? Molecular Biology and Evolution, 19(3): 341346. PMID:11861893.CrossRefGoogle ScholarPubMed
Masui, S., Sasaki, T., and Ishikawa, H. 1997. groEhomologous operon of Wolbachia, an intracellular symbiont of arthropods: a new approach for their phylogeny. Zoological Science (Tokyo), 14: 701706.CrossRefGoogle ScholarPubMed
Masui, S., Kamoda, S., Sasaki, T., and Ishikawa, H. 2000. Distribution and evolution of bacteriophage WO in Wolbachia, the endosymbiont causing sexual alterations in arthropods. Journal of Molecular Evolution, 51(5): 491497. PMID:11080372.CrossRefGoogle ScholarPubMed
Posada, D., and Crandall, K.A. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics, 14(9): 817818. PMID:9918953 doi:10.1093/bioinformatics/14.9.817.CrossRefGoogle ScholarPubMed
Putnam, L.G. 1978. Diapause and cold hardiness in Microplitis plutellae, a parasite of the larvae of the diamondback moth. Canadian Journal of Plant Science, 58: 911913.CrossRefGoogle Scholar
Rigaud, T., and Juchault, P. 1995. Success and failure of horizontal transfers of feminizing Wolbachia endosymbionts in woodlice. Journal of Evolutionary Biology, 8(2): 249255. doi:10.1046/j.1420-9101.1995.8020249.x.CrossRefGoogle Scholar
Ros, V.I., Fleming, V.M., Feil, E.J., and Breeuwer, J.A. 2009. How diverse is the genus Wolbachia? Multiple-gene sequencing reveals a putatively new Wolbachia supergroup recovered from spider mites (Acari: Tetranychidae). Applied and Environmental Microbiology, 75(4): 10361043. PMID:19098217 doi:10.1128/AEM.01109-08.CrossRefGoogle Scholar
Sarfraz, M., and Keddie, B.A. 2005. Conserving the efficacy of insecticides against Plutella xylostella (L.) (Lep.: Plutellidae). Journal of Appled Entomology, 129(3): 149157. doi:10.1111/j.1439-0418.2005.00930.x.CrossRefGoogle Scholar
Sarfraz, M., Keddie, A.B., and Dosdall, L.M. 2005. Biological control of the diamondback moth, Plutella xylostella: a review. Biocontrol Science and Technology, 15(8): 763789. doi:10.1080/09583150500136956.CrossRefGoogle Scholar
Sarfraz, M., Dosdall, L.M., and Keddie, B.A. 2006. Diamondback moth – host plant interactions: implications for pest management. Crop Protection, 25(7): 625639. doi:10.1016/j.cropro.2005.09.011.CrossRefGoogle Scholar
Sinkins, S.P., Walker, T., Lynd, A.R., Steven, A.R., Makepeace, B.L., Godfray, H.C., and Parkhill, J. 2005. Wolbachia variability and host effects on crossing type in Culex mosquitoes. Nature (London), 436(7048): 257260. PMID:16015330 doi:10.1038/nature03629.CrossRefGoogle ScholarPubMed
Sintupachee, S., Milne, J.R., Poonchaisri, S., Baimai, V., and Kittayapong, P. 2006. Closely related Wolbachia strains within the pumpkin arthropod community and the potential for horizontal transmission via the plant. Microbial Ecology, 51(3): 294301. PMID:16598632 doi:10.1007/s00248-006-9036-x.CrossRefGoogle ScholarPubMed
Smith, D.B., and Sears, M.K. 1982. Evidence for dispersal of diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae), into southern Ontario. Proceedings of the Entomological Society of Ontario, 113: 2127.Google Scholar
Stouthamer, R., Breeuwer, J.A., and Hurst, G.D. 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual Review of Microbiology, 53(1): 71102. PMID:10547686 doi:10.1146/annurev.micro.53.1.71.CrossRefGoogle ScholarPubMed
Swofford, D.L. 2000. PAUP*: phylogenetic analysis using parsimony (and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
Teixeira, L., Ferreira, A., Ashburner, M., and Keller, L. 2008. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biology, 6(12): 27532763. doi:10.1371/journal.pbio.1000002.CrossRefGoogle ScholarPubMed
Van Meer, M.M., Witteveldt, J., and Stouthamer, R. 1999. Phylogeny of the arthropod endosymbiont Wolbachia based on the wsp gene. Insect Molecular Biology, 8(3): 399408. PMID:10469257 doi:10.1046/j.1365-2583.1999.83129.x.CrossRefGoogle ScholarPubMed
Vavre, F., Fleury, F., Lepetit, D., Fouillet, P., and Boulétreau, M. 1999. Phylogenetic evidence for horizontal transmission of Wolbachia in host–parasitoid associations. Molecular Biology and Evolution, 16(12): 17111723. PMID:10605113.CrossRefGoogle ScholarPubMed
Werren, J.H. 1997. Biology of Wolbachia. Annual Review of Entomology, 42(1): 587609. PMID:15012323 doi:10.1146/annurev.ento.42.1.587.CrossRefGoogle ScholarPubMed
Werren, J.H., and Windsor, D.M. 2000. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proceedings of the Royal Society of London B Biological Sciences, 267: 12771285.CrossRefGoogle ScholarPubMed
Werren, J.H., Zhang, W., and Guo, L.R. 1995. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proceedings of the Royal Society B: Biological Sciences, 261: 5563.Google ScholarPubMed
West, S.A., Cook, J.M., Werren, J.H., and Godfray, H.C. 1998. Wolbachia in two insect host–parasitoid communities. Molecular Ecology, 7(11): 14571465. PMID:9819901 doi:10.1046/j.1365-294x.1998.00467.x.CrossRefGoogle ScholarPubMed
Zhao, J.Z., Collins, H.L., Li, Y.X., Mau, R.F.L., Thompson, G.D., Hertlein, M., et al. 2006. Monitoring of diamondback moth (Lepidoptera: Plutellidae) resistance to spinosad, indoxacarb, and emamectin benzoate. Journal of Economic Entomology, 99(1): 176181. PMID:16573338 doi:10.1603/0022-0493(2006)099[0176: MODMLP]2.0.CO;2.CrossRefGoogle ScholarPubMed
Zhou, W., Rousset, F., and O'Neil, S. 1998. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society of London B Biological Sciences, 265: 509515.CrossRefGoogle ScholarPubMed