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Geography has a greater effect than Wolbachia infection on population genetic structure in the spider mite, Tetranychus pueraricola

Published online by Cambridge University Press:  14 June 2016

Y.-T. Chen ,
Y.-K. Zhang ,
W.-X. Du ,
P.-Y. Jin  and
X.-Y. Hong
Y.-T. Chen
Affiliation:
Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China
Y.-K. Zhang
Affiliation:
Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China
W.-X. Du
Affiliation:
Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China
P.-Y. Jin
Affiliation:
Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China
X.-Y. Hong*
Affiliation:
Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China
*
*Author for correspondence Fax: +86 25 84395339 Phone: +86 25 84395339 E-mail: [email protected]
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Abstract

Wolbachia is an intracellular symbiotic bacterium that infects various spider mite species and is associated with alterations in host reproduction, which indicates the potential role in mite evolution. However, studies of Wolbachia infections in the spider mite Tetranychus pueraricola, a major agricultural pest, are limited. Here, we used multilocus sequence typing to determine Wolbachia infection status and examined the relationship between Wolbachia infection status and mitochondrial diversity in T. pueraricola from 12 populations in China. The prevalence of Wolbachia ranged from 2.8 to 50%, and three strains (wTpue1, wTpue2, and wTpue3) were identified. We also found double infections (wTpue1 + wTpue3) within the same individuals. Furthermore, the wTpue1 strain caused weak cytoplasmic incompatibility (CI) (egg hatchability ~55%), whereas another widespread strain, wTpue3, did not induce CI. There was no reduction in mitochondrial DNA (mtDNA) or nuclear DNA diversity among infected individuals, and mtDNA haplotypes did not correspond to specific Wolbachia strains. Phylogenetic analysis and analysis of molecular variance revealed that the distribution of mtDNA and nuclear DNA haplotypes were significantly associated with geography. These findings indicate that Wolbachia infection in T. pueraricola is complex, but T. pueraricola genetic differentiation likely resulted from substantial geographic isolation.

Keywords

WolbachiaTetranychus pueraricolamtDNA6-phosphofructokinasepopulation structure
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 5 , October 2016 , pp. 685 - 694
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Copyright © Cambridge University Press 2016 

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References

Ahmed, M.Z., De Barro, P.J., Ren, S.X., Greeff, J.M. & Qiu, B.L. (2013) Evidence for horizontal transmission of secondary endosymbionts in the Bemisia tabaci cryptic species complex. PLoS ONE 8, e53084.Google Scholar
Ahrens, M.E. & Shoemaker, D. (2005) Evolutionary history of Wolbachia infections in the fire ant Solenopsis invicta . BMC Evolutionary Biology 5, 1.CrossRefGoogle ScholarPubMed
Avise, J.C. (2000) Phylogeography: the History and Formation of Species. Cambridge, MA, Harvard University Press.Google Scholar
Bailly, X., Migeon, A. & Navajas, M. (2004) Analysis of microsatellite variation in the spider mite pest Tetranychus turkestani (Acari: Tetranychidae) reveals population genetic structure and raises questions about related ecological factors. Biological Journal of the Linnean Society 82, 69–78.Google Scholar
Baker, E.W. & Tuttle, D.M. (1994) A Guide to the Spider Mites (Tetranychidae) of the United States. West Bloomfield, USA, Indira Publishing House.Google Scholar
Baldo, L., Hotopp, J.C.D., Jolley, K.A., Bordenstein, S.R., Biber, S.A., Choudhury, R.R., Hayashi, C., Maiden, M.C.J., Tettelin, H. & Werren, J.H. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis . Applied and Environmental Microbiology 72, 7098–7110.Google Scholar
Bandelt, H.J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.Google Scholar
Bandi, C., Anderson, T.J., Genchi, C. & Blaxter, M.L. (1998) Phylogeny of Wolbachia in filarial nematodes. Proceedings of the Royal Society of London B: Biological Sciences 265, 2407–2413.Google Scholar
Baudry, E., Bartos, J., Emerson, K., Whitworth, T. & Werren, J.H. (2003) Wolbachia and genetic variability in the birdnest blowfly Protocalliphora sialia . Molecular Ecology 12, 1843–1854.Google Scholar
Bolland, H.R., Gutierrez, J. & Flechtmann, C.H. (1998) World Catalogue of the Spider Mite Family (Acari: Tetranychidae). Leiden, Netherlands, Brill.Google Scholar
Braig, H.R., Zhou, W., Dobson, S.L. & 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, 2373–2378.Google Scholar
Breeuwer, J.A. (1997) Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani. Heredity 79, 41–47.CrossRefGoogle Scholar
Breeuwer, J.A.J. & Jacobs, G. (1996) Wolbachia: intracellular manipulators of mite reproduction. Experimental & Applied Acarology 20, 421–434.CrossRefGoogle ScholarPubMed
Dean, M.D., Ballard, K.J., Glass, A., William, J. & Ballard, O. (2003) Influence of two Wolbachia strains on population structure of East African Drosophila simulans . Genetics 165, 1959–1969.Google Scholar
Ehara, S. & Gotoh, T. (1996) Two new species of spider mites occurring in Japan (Acari, Tetranychidae). Journal of the Acarological Society of Japan 5, 17–25.Google Scholar
Excoffier, L. & Lischer, H.E. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Fay, J.C. & Wu, C.I. (1999) A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Molecular Biology and Evolution 16, 1003–1005.Google Scholar
Fenn, K., Conlon, C., Jones, M., Quail, M.A., Holroyd, N.E., Parkhill, J. & Blaxter, M. (2006) Phylogenetic relationships of the Wolbachia of nematodes and arthropods. PLoS Pathogens 2, e94.Google Scholar
Goodacre, S.L., Martin, O.Y., Thomas, C.G. & Hewitt, G.M. (2006) Wolbachia and other endosymbiont infections in spiders. Molecular Ecology 15, 517–527.CrossRefGoogle ScholarPubMed
Gotoh, T., Noda, H. & Hong, X.Y. (2003) Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan. Heredity 91, 208–216.Google Scholar
Gotoh, T., Suwa, A., Kitashima, Y. & Rezk, H.A. (2004) Developmental and reproductive performance of Tetranychus pueraricola Ehara and Gotoh (Acari: Tetranychidae) at four constant temperatures. Applied Entomology and Zoology 39, 675–682.Google Scholar
Grafton-Cardwell, E.E., Granett, J. & Normington, S.M. (1991) Influence of dispersal from almonds on the population dynamics and acaricide resistance frequencies of spider mites infesting neighboring cotton. Experimental & Applied Acarology 10, 187–212.CrossRefGoogle Scholar
Graham, R.I. & Wilson, K. (2012) Male-killing Wolbachia and mitochondrial selective sweep in a migratory African insect. BMC Evolutionary Biology 12, 204.Google Scholar
Grbić, M., Van Leeuwen, T., Clark, R.M., Rombauts, S., Rouzé, P., Grbić, V. & Hernández-Crespo, P. (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479, 487–492.Google Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Helle, W. & Sabelis, M.W. (Eds). (1985) Spider Mites: Their Biology, Natural Enemies and Control. Vol. 1, p. 458. Amsterdam: Elsevier.Google Scholar
Hoffmann, A. & Turelli, M. (1997) Cytoplasmic incompatibility in insects. pp. 42–80 in O'Neill, S., Hoffman, A. & Werren, J. (Eds) Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford: Oxford University Press.Google Scholar
Hurst, G.D. & Jiggins, F.M. (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proceedings of the Royal Society of London B: Biological Sciences 272, 1525–1534.Google ScholarPubMed
James, A.C., Dean, M.D., McMahon, M.E. & Ballard, J.W.O. (2002) Dynamics of double and single Wolbachia infections in Drosophila simulans from New Caledonia. Heredity 88, 182–189.Google Scholar
Jiggins, F.M. (2003) Male-killing Wolbachia and mitochondrial DNA: selective sweeps, hybrid introgression and parasite population dynamics. Genetics 164, 5–12.Google Scholar
Keller, G.P., Windsor, D.M., Saucedo, J.M. & Werren, J.H. (2004) Reproductive effects and geographical distributions of two Wolbachia strains infecting the Neotropical beetle, Chelymorpha alternans Boh. (Chrysomelidae, Cassidinae). Molecular Ecology 13, 2405–2420.Google Scholar
Kikuchi, Y. & Fukatsu, T. (2003) Diversity of Wolbachia endosymbionts in heteropteran bugs. Applied and Environmental Microbiology 69, 6082–6090.Google Scholar
Kraaijeveld, K., Franco, P., Knijff, P.D., Stouthamer, R. & Alphen, J.J.M.V. (2011) Clonal genetic variation in a wolbachia-infected asexual wasp: horizontal transmission or historical sex? Molecular Ecology 20, 3644–3652.Google Scholar
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.Google Scholar
Marshall, J.L. (2004) The allonemobius-Wolbachia host-endosymbiont system: evidence for rapid speciation and against reproductive isolation driven by cytoplasmic incompatibility. Evolution 58, 2409–2425.Google Scholar
McGraw, E.A., Merritt, D.J., Droller, J.N. & O'Neill, S.L. (2001) Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila . Proceedings of the Royal Society of London B: Biological Sciences 268, 2565–2570.Google Scholar
Migeon, A., Nouguier, E. & Dorkeld, F. (2011) Spider mites web: a comprehensive database for the Tetranychidae. pp. 557–560 in Sabelis, N.W. & Bruin, J. (Eds) Trends in Acarology. Netherlands, Springer.Google Scholar
Mitchell, R. (1973) Growth and population dynamics of a spider mite (Tetranychus urticae K., Acarina: Tetranychidae). Ecology 54, 1349–1355.Google Scholar
Navajas, M., Perrot-Minnot, M.J., Lagnel, J., Migeon, A., Bourse, T. & Cornuet, J.M. (2002) Genetic structure of a greenhouse population of the spider mite Tetranychus urticae: spatio-temporal analysis with microsatellite markers. Insect Molecular Biology 11, 157–165.Google Scholar
Nunes, M.D., Nolte, V. & Schlötterer, C. (2008) Nonrandom Wolbachia infection status of Drosophila melanogaster strains with different mtDNA haplotypes. Molecular Biology and Evolution 25, 2493–2498.Google Scholar
Perrot-Minnot, M.J., Guo, L.R. & Werren, J.H. (1996) Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis effects on compatibility. Genetics 143, 961–972.Google Scholar
Perrot-Minnot, M.J., Cheval, B., Migeon, A. & Navajas, M. (2002) Contrasting effects of Wolbachia on cytoplasmic incompatibility and fecundity in the haplodiploid mite Tetranychus urticae . Journal of Evolutionary Biology 15, 808–817.Google Scholar
Posada, D. (2004) Collapse 1.2. Program free. Available online at http://darwin.uvigo.es/ Google Scholar
Rasgon, J.L., Cornel, A.J. & Scott, T.W. (2006) Evolutionary history of a mosquito endosymbiont revealed through mitochondrial hitchhiking. Proceedings of the Royal Society of London B: Biological Sciences 273, 1603–1611.Google Scholar
Raychoudhury, R., Grillenberger, B.K., Gadau, J., Bijlsma, R., van de Zande, L., Werren, J.H. & Beukeboom, L.W. (2010) Phylogeography of Nasonia vitripennis (Hymenoptera) indicates a mitochondrial–Wolbachia sweep in North America. Heredity 104, 318–326.CrossRefGoogle ScholarPubMed
Ros, V.I., Fleming, V.M., Feil, E.J. & Breeuwer, J.A. (2012) Diversity and recombination in Wolbachia and Cardinium from Bryobia spider mites. BMC Microbiology 12, 1.Google Scholar
Rowley, S.M., Raven, R.J. & McGraw, E.A. (2004) Wolbachia pipientis in Australian spiders. Current Microbiology 49, 208–214.Google Scholar
Sakamoto, Y., Hirai, N., Tanikawa, T., Yago, M. & Ishii, M. (2015) Population genetic structure and Wolbachia infection in an endangered butterfly, Zizina emelina (Lepidoptera, Lycaenidae), in Japan. Bulletin of Entomological Research 105, 152–165.Google Scholar
Shoemaker, D., Keller, G. & Ross, K.G. (2003) Effects of Wolbachia on mtDNA variation in two fire ant species. Molecular Ecology 12, 1757–1771.Google Scholar
Sinkins, S.P. (2004) Wolbachia and cytoplasmic incompatibility in mosquitoes. Insect Biochemistry and Molecular Biology 34, 723–729.Google Scholar
Solignac, M., Vautrin, D. & Rousset, F. (1994) Widespread occurence of the proteobacteria Wolbachia and partial cytoplasmic incompatibility in Drosophila melanogaster . Comptes rendus de l'Académie des sciences. Série 3, Sciences de la vie 317, 461–470.Google Scholar
Sun, J.T., Lian, C., Navajas, M. & Hong, X.Y. (2012) Microsatellites reveal a strong subdivision of genetic structure in Chinese populations of the mite Tetranychus urticae Koch (Acari: Tetranychidae). BMC Genetics 13, 8.Google Scholar
Suwa, A. & Gotoh, T. (2006) Geographic variation in diapause induction and mode of diapause inheritance in Tetranychus pueraricola . Journal of Applied Entomology 130, 329–335.Google Scholar
Symula, R.E., Alam, U., Brelsfoard, C., Wu, Y., Echodu, R., Okedi, L.M., Aksoy, S. & Caccone, A. (2013) Wolbachia association with the tsetse fly, Glossina fuscipes, reveals high levels of genetic diversity and complex evolutionary dynamics. BMC Evolutionary Biology 13, 31.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, doi: 10.1093/molbev/mst197.Google Scholar
Tsagkarakou, A., Gulllemaud, T., Rousset, F. & Navajas, M. (1996) Molecular identification of a Wolbachia endosymbiont in a Tetranychus urticae strain (Acari: Tetranychidae). Insect Molecular Biology 5, 217–221.Google Scholar
Turelli, M. (1994) Evolution of incompatibility-inducing microbes and their hosts. Evolution 48, 1500–1513.Google Scholar
Vala, F., Weeks, A., Claessen, D., Breeuwer, J.A.J. & Sabelis, M.W. (2002) Within-and between-population variation for Wolbachia-induced reproductive incompatibility in a haplodiploid mite. Evolution 56, 1331–1339.Google Scholar
Werren, J.H. (1997) Biology of Wolbachia . Annual Review of Entomology 42, 587–609.Google Scholar
Werren, J.H., Baldo, L. & Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6, 741–751.Google Scholar
Xiao, J.H., Wang, N.X., Murphy, R.W., Cook, J., Jia, L.Y. & Huang, D.W. (2012) Wolbachia infection and dramatic intraspecific mitochondrial DNA divergence in a fig wasp. Evolution 66, 1907–1916.CrossRefGoogle Scholar
Xie, R.R., Chen, X.L. & Hong, X.Y. (2011) Variable fitness and reproductive effects of Wolbachia infection in populations of the two-spotted spider mite Tetranychus urticae Koch in China. Applied Entomology and Zoology 46, 95–102.Google Scholar
Yu, M.Z., Zhang, K.J., Xue, X.F. & Hong, X.Y. (2011) Effects of Wolbachia on mtDNA variation and evolution in natural populations of Tetranychus urticae Koch. Insect Molecular Biology 20, 311–321.Google Scholar
Zhang, Z.Q. (2003) Mites of Greenhouses: Identification, Biology and Control. UK, CABI Publishing.Google Scholar
Zhang, Y.K., Ding, X.L., Zhang, K.J. & Hong, X.Y. (2013 a) Wolbachia play an important role in affecting mtDNA variation of Tetranychus truncatus (Trombidiformes: Tetranychidae). Environmental Entomology 42, 1240–1245.Google Scholar
Zhang, Y.K., Zhang, K.J., Sun, J.T., Yang, X.M., Ge, C. & Hong, X.Y. (2013 b) Diversity of Wolbachia in natural populations of spider mites (genus Tetranychus): evidence for complex infection history and disequilibrium distribution. Microbial Ecology 65, 731–739.Google Scholar
Zhao, D.X., Chen, D.S., Ge, C., Gotoh, T. & Hong, X.Y. (2013) Multiple infections with Cardinium and two strains of Wolbachia in the spider mite Tetranychus phaselus Ehara: revealing new forces driving the spread of Wolbachia . PLoS ONE 8, e54964.Google Scholar
Zhu, L.Y., Zhang, K.J., Zhang, Y.K., Ge, C., Gotoh, T. & Hong, X.Y. (2012) Wolbachia strengthens Cardinium-induced cytoplasmic incompatibility in the spider mite Tetranychus piercei McGregor. Current Microbiology 65, 516–523.Google Scholar
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