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Diversity of Wolbachia in Natural Populations of Spider Mites (genus Tetranychus): Evidence for Complex Infection History and Disequilibrium Distribution

  • Invertebrate Microbiology
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Abstract

Wolbachia are endosymbiotic bacteria that commonly infect arthropods and cause reproductive disorders in host. Within several Tetranychus species, Wolbachia have been detected and shown to affect their reproduction. However, little is known about their transmission and distribution patterns in natural populations of Tetranychus species. Here, we used multilocus sequence typing to confirm Wolbachia infection status and examined the relationship between Wolbachia infection status and host phylogeny, mitochondrial diversity, and geographical range in five Tetranychus species (Tetranychus truncatus, Tetranychus urticae, Tetranychus pueraricola, Tetranychus phaselus, and Tetranychus kanzawai) from 21 populations in China. The prevalence of Wolbachia within the five Tetranychus species ranged from 31.4 to 100 %, and the strains were remarkably diverse. Together, these observations indicate that Wolbachia was introduced to these populations on multiple separate occasions. As in other arthropods, the same Tetranychus species can accommodate very different strains, and identical Wolbachia occasionally infect different species. These observations suggest that Wolbachia are transmitted both vertically and horizontally. Horizontally, transmission is probably mediated by the host plants. The distribution patterns of Wolbachia were quite different among populations of the same species, suggesting that the dynamics of Wolbachia in nature may be affected by ecological and other factors.

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References

  1. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia?—a statistical analysis of current data. FEMS Microbiol Lett 281:215–220

    Article  PubMed  CAS  Google Scholar 

  2. Jeyaprakash A, Hoy MA (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76 % of sixty-three arthropod species. Insect Mol Biol 9:393–405

    Article  PubMed  CAS  Google Scholar 

  3. Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42:587–609

    Article  PubMed  CAS  Google Scholar 

  4. Hurst G, Hammarton T, Obrycki J, Majerus T, Walker L, Bertrand D, Majerus M (1996) Male-killing bacterium in a fifth ladybird beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). Heredity 77:177–185

    Article  PubMed  Google Scholar 

  5. O'Neill SL, Giordano R, Colbert AME, Karr TL, Robertson HM (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 89:2699–2702

    Article  PubMed  Google Scholar 

  6. Schilthuizen M, Stouthamer R (1998) Distribution of Wolbachia among the guild associated with the parthenogenetic gall wasp Diplolepis rosae. Heredity 81:270–274

    Article  Google Scholar 

  7. Sinkins SP, Braig HR, O'Neill SL (1995) Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proc R Soc Lond B 261:325–330

    Article  CAS  Google Scholar 

  8. Stouthamer R, Breeuwer JAJ, Hurst GDD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Ann Rev Microbiol 53:71–102

    Article  CAS  Google Scholar 

  9. Baldo L, Nadia A, Ayoub NA, Hayashi CY, Russell JA, Stahlhut JK, Werren JH (2008) Insight into the routes of Wolbachia invasion: high levels of horizontal transfer in the spider genus Agelenopsis revealed by Wolbachia strain and mitochondrial DNA diversity. Mol Ecol 17:557–569

    Article  PubMed  CAS  Google Scholar 

  10. Raychoudhury R, Baldo L, Oliveira D, Werren JH (2008) Modes of acquisition of Wolbachia: horizontal transfer, hybrid introgression, and co-divergence in the Nasonia species. Evolution 63:165–183

    Article  PubMed  Google Scholar 

  11. Stahlhut JK, Desjardins CA, Clark ME, Baldo L, Russell JA, Werren JH, Jaenike J (2010) The mushroom habitat as an ecological arena for global exchange of Wolbachia. Mol Ecol 19:1940–1952

    Article  PubMed  Google Scholar 

  12. Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host–parasitoid associations. Mol Biol Evol 16(12):1711–1723

    Article  PubMed  CAS  Google Scholar 

  13. Frost CL, Fernández-Marín H, Smith JE, Hughes WHO (2010) Multiple gains and losses of Wolbachia symbionts across a tribe of fungus-growing ants. Mol Ecol 19(18):4077–4085

    Article  PubMed  CAS  Google Scholar 

  14. Mitsuhashi W, Saiki T, Wei W, Kawakita H, Sato M (2002) Two novel strains of Wolbachia coexisting in both species of mulberry leafhoppers. Insect Mol Biol 11(6):577–584

    Article  PubMed  CAS  Google Scholar 

  15. Russell JA, Goldman-Huertas B, Moreau CS et al (2009) Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies. Evolution 63:624–640

    Article  PubMed  CAS  Google Scholar 

  16. Sintupachee S, Milne JR, Poonchaisri S, Baimai V, Kittayapong P (2006) Closely related Wolbachia strains within the pumpkin arthropod community and the potential for horizontal transmission via the plant. Microb Ecol 51:294–301

    Article  PubMed  CAS  Google Scholar 

  17. Engelstadter J, Telschow A (2009) Cytoplasmic incompatibility and host population structure. Heredity 103:196–207

    Article  PubMed  CAS  Google Scholar 

  18. Shoemaker DD, Machado CA, Molbo D et al (2002) The distribution of Wolbachia in fig wasps: correlation with host phylogeny, ecology and population structure. Proc R Soc Lond B 269:2257–2267

    Article  Google Scholar 

  19. Vavre F, Charlat S (2012) Making (good) use of Wolbachia: what the models say. Curr Opin Microbiol 15:1–6

    Article  Google Scholar 

  20. Bolland HR, Gutierrez J, Flechtmann CHW (1998) World catalogue of the spider mite family (Acari: Tetranychidae), with references to taxonomy, synonymy, host plants and distribution. Brill Academic, Leiden

    Google Scholar 

  21. Breeuwer JAJ (1997) Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani. Heredity 79:41–47

    Article  Google Scholar 

  22. Breeuwer JAJ, Jacobs G (1996) Wolbachia: intracellular manipulators of mite reproduction. Exp Appl Acarol 20:421–434

    Article  PubMed  CAS  Google Scholar 

  23. Gotoh T, Noda H, Hong XY (2003) Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan. Heredity 91:208–216

    Article  PubMed  CAS  Google Scholar 

  24. Gotoh T, Sugasawa J, Nagata T (1999) Reproductive compatibility of the two-spotted spider mite (Tetranychus urticae) infected with Wolbachia. Entomol Sci 2:289–295

    Google Scholar 

  25. Gotoh T, Sugasawa J, Noda H, Kitashima Y (2007) Wolbachia-induced cytoplasmic incompatibility in Japanese populations of Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol 42:1–16

    Article  PubMed  Google Scholar 

  26. Opijnen TV, Breeuwer JAJ (1999) High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Exp Appl Acarol 23:871–881

    Article  PubMed  Google Scholar 

  27. Vala F, Breeuwer JAJ, Sabelis MW (2000) Wolbachia-induced ‘hybrid breakdown’ in the two-spotted spider mite Tetranychus urticae Koch. Proc R Soc Lond B 267:1931–1937

    Article  CAS  Google Scholar 

  28. Xie RR, Chen XL, Hong XY (2010) Variable fitness and reproductive effects of Wolbachia infection in populations of the two-spotted spider mite Tetranychus urticae Koch in China. Appl Entomol Zool 46:95–102

    Article  Google Scholar 

  29. Zhu LY, Zhang KJ, Zhang YK, Cheng G, Gotoh T, Hong XY (2012) Wolbachia strengthens Cardinium-induced cytoplasmic incompatibility in the spider mite Tetranychus piercei McGregor. Curr Microbiol 65:516–523

    Article  PubMed  CAS  Google Scholar 

  30. Werren JH, Bartos JD (2001) Recombination in Wolbachia. Curr Biol 11:431–435

    Article  PubMed  CAS  Google Scholar 

  31. Baldo L, Dunning Hottopp JC, Jolley KA et al (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72:7098–7110

    Article  PubMed  CAS  Google Scholar 

  32. Osakabe M, Kotsubo Y, Tajima R, Hinomoto N (2008) Restriction fragment length polymorphism catalog for molecular identification of Japanese Tetranychus spider mites (Acari: Tetranychidae). J Econ Entomol 101(4):1167–1175

    Article  PubMed  CAS  Google Scholar 

  33. Navajas M, Gutierrez J, Lagnel J, Boursot J (1996) Mitochondrial cytochrome oxidase I in tetranychid mites: a comparison between molecular phylogeny and changes of morphological and life history traits. Bull Entomol Res 86:407–417

    Article  CAS  Google Scholar 

  34. Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics. Chapter 2: Unit 2.3. http://www.ncbi.nlm.nih.gov/pubmed/18792934. Accessed August 2012

  35. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  36. Posada D (2004) Collapse 1.2. Program free available at http://darwin.uvigo.es/. Accessed 2012

  37. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  38. Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262

    Article  PubMed  CAS  Google Scholar 

  39. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  PubMed  CAS  Google Scholar 

  40. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  41. Swofford DL (2000) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4.0 beta version. Sinauer Associates, Sunderland

    Google Scholar 

  42. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  PubMed  CAS  Google Scholar 

  43. Hughes GL, Allsopp PG, Brumbley SM, Woolfit M, McGraw EA, O'Neill SL (2011) Variable infection frequency and high diversity of multiple strains of Wolbachia pipientis in Perkinsiella planthoppers. Appl Environ Microbiol 77(6):2165–2168

    Article  PubMed  CAS  Google Scholar 

  44. Kikuchi Y, Fukatsu T (2003) Diversity of Wolbachia endosymbiont in heteropteran bugs. Appl Environ Microbiol 69(10):6082–6090

    Article  PubMed  CAS  Google Scholar 

  45. Ros VID, Fleming VM, Feil EJ, Breeuwer JAJ (2012) Diversity and recombination in Wolbachia and Cardinium from Bryobia spider mites. BMC Microbiol 12(Suppl 1):S13

    Article  PubMed  Google Scholar 

  46. Werren JH (1998) Wolbachia and speciation. In: Howard D, Berlocher S (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 245–260

    Google Scholar 

  47. Cook JM, Butcher RDJ (1999) The transmission and effects of Wolbachia bacteria in parasitoids. Res Popul Ecol 41:15–28

    Article  Google Scholar 

  48. Noda H, Miyoshi T, Zhang Q, Watanabe K, Deng K, Hoshizaki S (2001) Wolbachia infection shared among planthoppers (Homoptera: Delphacidae) and their endoparasite (Strepsiptera: Elenchidae): a probable case of interspecies transmission. Mol Ecol 10:2101–2106

    Article  PubMed  CAS  Google Scholar 

  49. Hurst GD, Jiggins FM (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc B 272:1525–1534

    Article  PubMed  CAS  Google Scholar 

  50. Ahrens ME, Shoemaker D (2005) Evolutionary history of Wolbachia infections in the fire ant Solenopsis invicta. BMC Evol Biol 5:35

    Article  PubMed  Google Scholar 

  51. Müller MJ, Mühlen CV et al (2012) Wolbachia pipientis is associated with different mitochondrial haplotypes in natural populations of Drosophila willistoni. J Inver Pat 109:152–155

    Article  Google Scholar 

  52. Baudry E, Bartos J, Emerson K, Whitworth T, Werren JH (2003) Wolbachia and genetic variability in the birdnest blowfly Protocalliphora sialia. Mol Ecol 12:1843–1854

    Article  PubMed  CAS  Google Scholar 

  53. Keller GP, Windsor DM, Scucedo JM, Werren JH (2004) Reproductive effects and geographical distributions of two Wolbachia strains infecting the Neotropical beetle, Chelymorpha alternans Boh. (Chrysomelidae, Cassidinae). Mol Ecol 13:2405–2420

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Ming-Hong Lu, Lu-Yu Zhu, Wen-Chao Zhu, Min Xu, Si-Xia Yang, Chao Yang, and Hao-Sen Li of the Department of Entomology, Nanjing Agricultural University (NJAU), for their help with the collection of spider mites. We are also grateful to Ming-Zhi Yu and Dong-Xiao Zhao of the Department of Entomology, NJAU, for their kind help with experiments. This study was supported in part by a grant-in-aid from the Science and Technology Program of the National Public Welfare Professional Fund (no. 201103020) from the Ministry of Agriculture of China, a grant-in-aid from the National Basic Science Program of China (973 Program, no. 2009CB119202), and a grant-in-aid for Scientific Research (nos. 31172131 and 30871635) from the National Natural Science Foundation of China.

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  1. Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, 210095, China

    Yan-Kai Zhang, Kai-Jun Zhang, Jing-Tao Sun, Xian-Ming Yang, Cheng Ge & Xiao-Yue Hong

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  1. Yan-Kai Zhang
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Correspondence to Xiao-Yue Hong.

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Zhang, YK., Zhang, KJ., Sun, JT. et al. Diversity of Wolbachia in Natural Populations of Spider Mites (genus Tetranychus): Evidence for Complex Infection History and Disequilibrium Distribution. Microb Ecol 65, 731–739 (2013). https://doi.org/10.1007/s00248-013-0198-z

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