Wolbachia Infection in Populations of Ostrinia furnacalis: Diversity, Prevalence, Phylogeny and Evidence for Horizontal Transmission

doi:10.1016/S2095-3119(13)60227-0

Journal of Integrative Agriculture ›› 2013, Vol. 12 ›› Issue (2): 283-295.DOI: 10.1016/S2095-3119(13)60227-0

Wolbachia Infection in Populations of Ostrinia furnacalis: Diversity, Prevalence, Phylogeny and Evidence for Horizontal Transmission

LI Jing, WANG Zhen-ying, Denis Bourguet , HE Kang-lai

1.State Key Laboratory for the Biology of the Plant Diseases and Insect Pests/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
2.Centre de Biologie pour la Gestion des Populations (CBGP), UMR INRA-IRD-CIRAD-Montpellier SupAgro, Campus International de Baillarguet, Montferrier/Lez 34988, France

收稿日期:2012-03-13 出版日期:2013-02-01 发布日期:2013-02-06
通讯作者: Correspondence WANG Zhen-ying, Tel: +86-10-62815945, Fax: +86-10-62896114, E-mail: zywang@ippcaas.cn
基金资助:
This work was funded by China Agriculture Research System (CARS-02).

Wolbachia Infection in Populations of Ostrinia furnacalis: Diversity, Prevalence, Phylogeny and Evidence for Horizontal Transmission

LI Jing, WANG Zhen-ying, Denis Bourguet , HE Kang-lai

1.State Key Laboratory for the Biology of the Plant Diseases and Insect Pests/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
2.Centre de Biologie pour la Gestion des Populations (CBGP), UMR INRA-IRD-CIRAD-Montpellier SupAgro, Campus International de Baillarguet, Montferrier/Lez 34988, France

Received:2012-03-13 Online:2013-02-01 Published:2013-02-06
Contact: Correspondence WANG Zhen-ying, Tel: +86-10-62815945, Fax: +86-10-62896114, E-mail: zywang@ippcaas.cn
Supported by:
This work was funded by China Agriculture Research System (CARS-02).

摘要/Abstract

摘要： Wolbachia are maternally inherited endosymbiotic bacteria infecting a wide range of arthropods and filarial nematodes. They can induce various reproduction alterations in their hosts, including thelytokous parthenogenesis, cytoplasmic incompatibility (CI), feminization of genetic males and male killing. Here we investigated diversity and prevalence patterns of Wolbachia infection in 43 geographical populations of the Asian corn borer, Ostrinia furnacalis, in China and one population in North Korea. Based on Wolbachia surface protein gene (wsp) sequences, nine strains of Wolbachia (wFur1-wFur9), belonging to supergroups A and B, were identified in populations of O. furnacalis with an average infection rate of 10.5%. Superinfection commonly appeared in individuals of O. furnacalis and coinfection patterns were very complex. There was no specific pattern for the prevalence and distribution of the nine Wolbachia strains suggesting an intricate evolutionary history of Wolbachia infection in this species. The genetic similarity of the wFur1-wFur9 strains with those detected in two parasitoids of O. furnacalis, Macrocentrus cingulum and Lydella grisescens, strongly suggests host-parasitoid horizontal transmission.

关键词: Wolbachia , Ostrinia furnacalis , infection diversity , prevalence pattern , horizontal transmission

Abstract: Wolbachia are maternally inherited endosymbiotic bacteria infecting a wide range of arthropods and filarial nematodes. They can induce various reproduction alterations in their hosts, including thelytokous parthenogenesis, cytoplasmic incompatibility (CI), feminization of genetic males and male killing. Here we investigated diversity and prevalence patterns of Wolbachia infection in 43 geographical populations of the Asian corn borer, Ostrinia furnacalis, in China and one population in North Korea. Based on Wolbachia surface protein gene (wsp) sequences, nine strains of Wolbachia (wFur1-wFur9), belonging to supergroups A and B, were identified in populations of O. furnacalis with an average infection rate of 10.5%. Superinfection commonly appeared in individuals of O. furnacalis and coinfection patterns were very complex. There was no specific pattern for the prevalence and distribution of the nine Wolbachia strains suggesting an intricate evolutionary history of Wolbachia infection in this species. The genetic similarity of the wFur1-wFur9 strains with those detected in two parasitoids of O. furnacalis, Macrocentrus cingulum and Lydella grisescens, strongly suggests host-parasitoid horizontal transmission.

Key words: Wolbachia , Ostrinia furnacalis , infection diversity , prevalence pattern , horizontal transmission

LI Jing, WANG Zhen-ying, Denis Bourguet , HE Kang-lai. Wolbachia Infection in Populations of Ostrinia furnacalis: Diversity, Prevalence, Phylogeny and Evidence for Horizontal Transmission[J]. Journal of Integrative Agriculture, 2013, 12(2): 283-295.

参考文献

[1]Ahrens M E, Shoemaker D. 2005. Evolutionary history ofWolbachia infections in the fire ant Solenopsis invicta.BMC Evolutionary Biology, 5, 35.

[2]Baldo L, Bordenstein S, Wernegreen J J, Werren J H. 2006a.Widespread recombination throughout Wolbachiagenomes. Molecular Biology and Evolution, 23, 437-449

[3]Baldo L, Dunning Hotopp J C, Jolley K A, Bordenstein S R,Biber S A, Choudhury R R, Hayashi C, Maiden M C J,Tettelin H, Werren J H. 2006b. Multilocus sequencetyping system for the endosymbiont Wolbachiapipientis. Applied and Environmental Microbiology,72, 7098-7110

[4]Baldo L, Lo N, Werren J H. 2005. Mosaic nature of wsp(Wolbachia surface protein). Journal of Bacteriology, 187, 5406-5418

[5]Baldo L, Werren J H. 2007. Revisiting Wolbachia supergrouptyping based on wsp: spurious lineages anddiscordance with MLST. Current Microbiology, 55,81-87

[6]Bordenstein S R, O’Hara F P, Werren J H. 2001. Wolbachiainducedincompatibility precedes other hybridincompatibilities in Nasonia. Nature, 409, 707-710

[7]Braig H R, Zhou W, Dobson S L, O’Neill S L. 1998. Cloningand characterization of a gene encoding the majorsurface protein of the bacterial endosymbiontWolbachia. Journal of Bacteriology, 180, 2373-2378

[8]Breeuwer J A J, Werren J H. 1990. Microorganismsassociated with chromosome destruction andreproductive isolation between two insect species.Nature, 346, 558-560

[9]Cordaux R, Michel-Salzat A, Bouchon D. 2001. Wolbachiainfection in crustaceans: novel hosts and potentialroutes for horizontal transmission. Journal ofEvolutionary Biology, 14, 237-243

[10]Godfray H C J. 1994. Parasitoids, Behavioral andEvolutionary Ecology. Princeton University Press,Princeton.Heath B D, Butcher R D J, Whitfield W G F, Hubbard S F.1999. Horizontal transfer of Wolbachia betweenphylogenetically distant insect species by a naturallyoccurring mechanism. Current Biology, 9, 313-316

[11]Hilgenboecker K, Hammerstein P, Schlattmann P, TelschowA, Werren J H. 2008. How many species are infectedwith Wolbachia? - a statistical analysis of current data.FEMS Microbiology Letters, 281, 215-220

[12]Huigens M E, DeAlmeida R P, Boons P A H, Luck R F,Stouthamer R. 2004. Natural interspecific andintraspecific horizontal transfer of parthenogensisinducingWolbachia in Trichogramma wasps.Proceedings of the Royal Society of London (B:Biological Sciences), 271, 509-515

[13]Jeyaprakash A, Hoy M A. 2000. Long PCR improvesWolbachia DNA amplification: wsp sequences foundin 76% of sixty-three arthropod species. InsectMolecular Biology, 9, 393-405

[14]Jiggins F M, Hurst G D, Yang Z. 2002. Host-symbiontconflicts: positive selection on an outer membraneprotein of parasitic but not mutualistic Rickettsiaceae.Molecular Biology and Evolution, 19, 1341-1349

[15]Kageyama D, Hoshizaki S, Ishikawa Y. 1998. Female-biasedsex ratio in the Asian corn borer, Ostrinia furnacalis:evidence for the occurrence of feminizing bacteria in aninsect. Heredity, 81, 311-316

[16]Kageyama D, Nishimura G, Hoshizaki S, Ishikawa Y. 2002.Feminizing Wolbachia in an insect, Ostrinia furnacalis(Lepidoptera: Crambidae). Heredity, 88, 444-449

[17]Kageyama D, Nishimura G, Hoshizaki S, Ishikawa Y. 2003a.Two kinds of sex ratio distorters in a moth, Ostriniascapulalis. Genome, 46, 974-982

[18]Kageyama D, Nishimura G, Ohno S, Takanashi T. 2004.Wolbachia infection and an all-female trait in Ostriniaorientalis and Ostrinia zaguliaevi. EntomologiaExperimentalis et Applicata, 111, 79-83

[19]Kageyama D, Ohno S, Hoshizaki S, Ishikawa Y. 2003b.Sexual mosaics induced by tetracycline treatment inthe Wolbachia-infected adzuki bean borer, Ostriniascapulalis. Genome, 46, 983-989

[20]Kikuchi Y, Fukatsu T. 2003. Diversity of Wolbachiaendosymbionts in heteropteran bugs. Applied andEnvironmental Microbiology, 69, 6082-6090

[21]Malloch G, Fenton B. 2005. Super-infections of Wolbachiain byturid beetles and evidence for genetic transferbetween A and B super-groups of Wolbachia.Molecular Ecology, 14, 627-637

[22]McGraw E A, O’Neill S L. 1999. Evolution of Wolbachiapipientis transmission dynamics in insects. Trends inMicrobiology, 7, 297-302

[23]van Meer M M M, Witteveldt J, Stouthamer R. 1999.Phylogeny of the arthropod endosymbiont Wolbachiabased on the wsp gene. Insect Molecular Biology, 8,399-408

[24]Moran N A, Munson M A, Baumann P, Ishikawa H. 1993. Amolecular clock in endosymbiotic bacteria is calibratedusing the insect hosts. Proceedings of the RoyalSociety of London (B: Biological Sciences), 253, 167-171

[25]Nafus D M, Schreiner I. 1991. Review of the biology andcontrol of the Asian corn borer, Ostrinia furnacalis(Lepidoptera: Pyralidae). Tropical Pest Management,37, 41-56

[26]Noda H, Miyoshi T, Zhang Q, Watanabe K, Deng K,Hoshizaki S. 2001. Wolbachia infection shared amongplanthoppers (Homoptera: Delphacidae) and theirendoparasite (Strepsiptera: Elenchidae): a probable caseof interspecies transmission. Molecular Ecology, 10,2101-2106

[27]O’Neill S L, Giordano R, Colbert A M E, Karr T L, RobertsonH M. 1992. 16S rRNA phylogenetic analysis of thebacterial endosymbionts associated with cytoplasmicincompatibility in insects. Proceedings of the NationalAcademy of Sciences of the United States of Ameica,89, 2699-2702

[28]O’Neill S L, Hoffman A A, Werren J H. 1997. InfluentialPassengers: Inherited Microorganisms and ArthropodReproduction. Oxford University Press, New York.Paraskevopoulos C, Bordenstein S R, Wernegreen J J,Werren J H, Bourtzis K. 2006. Toward a Wolbachiamultilocus sequence typing system: discrimination ofWolbachia strains present in Drosophila species.Current Microbiology, 53, 388-395

[29]Rigaud T, Juchault P. 1995. Success and failure of horizontaltransfers of feminizing Wolbachia endosymbionts inwoodlice. Journal of Evolutionary Biology, 8, 249-255

[30]Rousset F, Bouchon D, Pintureau B, Juchault P, SolignacM. 1992. Wolbachia endosymbionts responsible forvarious alterations of sexuality in arthropods. Proceedings of the Royal Society of London (B:Biological Sciences), 250, 91-98

[31]Sakamoto H, Kageyama D, Hoshizaki S, Ishikawa Y. 2007.Sex-specific death in the Asian corn borer moth(Ostrinia furnacalis) infected with Wolbachia occursacross larval development. Genome, 50, 645-652

[32]Schilthuizen M, Stouthamer R. 1997. Horizontaltransmission of parthenogenesis inducing microbes inTrichogramma wasps. Proceedings of the RoyalSociety of London (B: Biological Sciences), 264, 361-366

[33]Shoemaker D D, Katju V, Jaenike J J. 1999. Wolbachia andthe evolution of reproductive isolation betweenDrosophilla recens and Drosophila subquinaria.Evolution, 53, 1157-1164

[34]Shoemaker D D, Keller G, Ross K G. 2003. Effects ofWolbachia on mtDNA variation in two fire ant species.Molecular Ecology, 12, 1757-1771

[35]Sintupachee S, Milne J R, Poonchaisri S, Baimai V,Kittayapong P. 2006. Closely related Wolbachia strainswithin the pumpkin arthropod community and thepotential for horizontal transmission via the plant.Microbial Ecology, 51, 294-301

[36]Stouthammer R, Breeuwer J A J, Hurst G D D. 1999.Wolbachia pipientis: microbial manipulator ofarthropod reproduction. Annual Review ofMicrobiology, 53, 71-102

[37]Telschow A, Flor M, Kobayashi Y, Hammerstein P, WerrenJ H. 2007. Wolbachia-induced unidirectionalcytoplasmic incompatibility and speciation: mainlandislandmodel. PLoS ONE, 2, e701.Telschow A, Hammerstein P, Werren J H. 2002a. The effectof Wolbachia on genetic divergence betweenpopulations: mainland-island model. Integrative andComparative Biology, 42, 340-351

[38]Telschow A, Hammerstein P, Werren J H. 2002b. The effectof Wolbachia on genetic divergence betweenpopulations: models with two-way migration. AmericanNaturalist, 160, 54-66

[39]Thompson J D, Gibson T J, Plewniak F, Jeanmougin F,Higgins D G. 1997. The ClustalX windows interface:flexible strategies for multiple sequence alignment aidedby quality analysis tools. Nucleic Acids Research, 24,4876-4882

[40]Tsutsui N D, Kauppinen S N, Oyafuso A F, Grosberg R K.2003. The distribution and evolutionary history ofWolbachia infection in native and introducedpopulations of the invasive argentine ant (Linepithemahumile). Molecular Ecology, 12, 3057-3068

[41]Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4:molecular evolutionary genetics analysis (MEGA)software version 4.0. Molecular Biology andEvolution, 24, 1596-1599

[42]Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M. 1999.Phylogenetic evidence for horizontal transmission ofWolbachia in host-parasitoid associations. MolecularBiology and Evolution, 16, 1711-1723

[43]Wang Z Y, Lu X, He K L, Zhou D R. 2000. Review of history,present situation and prospect of the Asian maize borerresearch in China. Journal of Shenyang AgriculturalUniversity, 31, 402-412(in Chinese)

[44]Wang Z Y, Zhou D R, Song Y Y, Li B X, Zhang G Y, Gao SL, Liu Y, Zheng L, Wang Y S, Xie W M, et al. 1994.Studies on behavior of dispersal and possibility ofmigration on adult overwintering generation Asian cornborer by using release-and-recapture technique. ActaPhytophylacica Sinica, 21, 25-31(in Chinese)

[45]Werren J H. 1997. Biology of Wolbachia. Annual Review ofEntomology, 42, 587-609

[46]Werren J H. 1998. Wolbachia and speciation. In: HowardD, Berlocher S, eds., Endless Forms: Species andSpeciation. Oxford University Press, UK. pp. 245-260

[47]Werren J H, Bartos J D. 2001. Recombination in Wolbachia.Current Biology, 11, 431-435

[48]Werren J H, Windsor D M. 2000. Wolbachia infectionfrequencies in insects: evidence of a global equilibrium?Proceedings of the Royal Society of London (B:Biological Sciences), 267, 1277-1285

[49]Werren J H, Zhang W, Guo L. 1995. Evolution andphylogeny of Wolbachia: reproductive parasites ofarthropods. Proceedings of the Royal Society ofLondon (B: Biological Sciences), 261, 55-71

[50]Zhou D R, Wang Y S, Li W D. 1988. Studies on theidentification of the dominant corn borer species inChina. Acta Phytophylacica Sinica, 15, 145-152(in Chinese)

[51]Zhou W, Rousset F, O’Neill S. 1998. Phylogeny and PCRbasedclassification of Wolbachia strains using wspgene sequences. Proceedings of the Royal Society ofLondon (B: Biological Sciences), 265, 509-515

Wolbachia Infection in Populations of Ostrinia furnacalis: Diversity, Prevalence, Phylogeny and Evidence for Horizontal Transmission

Wolbachia Infection in Populations of Ostrinia furnacalis: Diversity, Prevalence, Phylogeny and Evidence for Horizontal Transmission

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