Abstract
Recent studies have revealed diverse patterns of cytoplasmic incompatibility (CI) induced by Wolbachia in the two spotted spider mite (Tetranychus urticae Koch). The mechanism of CI consists of two steps: modification (mod) of sperm of infected males and the rescue (resc) of these chromosomes by Wolbachia in the egg, which results in female embryonic mortality (FM), male development (MD) or no CI. Our study reports that Wolbachia infections were highly prevalent infecting all T. urticae populations from various crops in 14 commercial greenhouses in Korea, with two Wolbachia strains expressing distinctive phenotypic effects on hosts. Analyses for wsp gene sequences obtained from collected mite populations revealed all sequences were categorized into two groups (group W1 and W2) discriminated by three diagnostic nucleotides while all Wolbachia strains belonged to the subgroup Ori in Wolbachia supergroup B. Host plants of each mite population were also generally correlated this grouping. Various mating experiments with two mite populations from each group showed that CI patterns and host plants of the mite populations were completely matched with the grouping; no CI (mod−resc+) for group W1 and mixed pattern of FM and MD (mod+resc+) for group W2. No distinct changes in fecundity or sex ratio due to Wolbachia infections were observed in four mite populations regardless of Wolbachia grouping. Our study suggests a potential correlation between phenotypic effect of Wolbachia infection and its genetic diversity associated with host plants in Korean mite populations.
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References
Bordenstein SR, Werren JH (2000) Do Wolbachia influence fecundity in Nasonia vitripennis? Heredity 84:54–62
Braig HR, Zhou WG, Dobson SL, O’Neill SL (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol 180:2373–2378
Breeuwer JAJ (1997) Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani. Heredity 79:41–47
Caspi-Fluger A, Inbar M, Mozes-Daube N, Katzir N, Portnoy V, Belausov E, Hunter MS, Zchori-Fein E (2012) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc R Soc B Biol Sci 279:1791–1796
Charlat S, Le Chat L, Mercot H (2003) Characterization of non-cytoplasmic incompatibility inducing Wolbachia in two continental African populations of Drosophila simulans. Heredity 90:49–55
Giordano R, O’Neill SL, Robertson HM (1995) Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophila sechellia and D. mauritiana. Genetics 140:1307–1317
Gomi K, Gotoh T, Noda H (1997) Wolbachia having no effect on reproductive incompatibility in Tetranychus kanzawai Kishida (Acari: Tetranychidae). Appl Entomol Zool 32:485–490
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
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
Helle W (1967) Fertilization in the two-spotted spider mite (Tetranychus urticae: Acari). Entomol Exp Appl 10:103–110
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
Hoffmann AA, Turelli M (1997) Cytoplasmic incompatibility in insects. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential Passengers: inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford, pp 42–80
Hoffmann AA, Clancy D, Duncan J (1996) Naturally-occuring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity 76:1–8
Hoffmann AA, Hercus M, Dagher H (1998) Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster. Genetics 148:221–231
Johanowicz DL, Hoy MA (1996) Wolbachia in a predator-prey system: 16S ribosomal DNA analysis of two phytoseiids (Acari: Phytoseiidae) and their prey (Acari: Tetranychidae). Ann Entomol Soc Am 89:435–441
Kim M, Shin D, Suh E, Cho K (2004) An assessment of the chronic toxicity of fenpyroximate and pyridaben to Tetranychus urticae using a demographic bioassay. Appl Entomol Zool 39:401–409. doi:10.1303/aez.2004.401
Margolies DC, Wrensch DL (1996) Temperature-induced changes in spider mite fitness: offsetting effects of development time, fecundity, and sex ratio. Entomol Exp Appl 78:111–118
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 11:577–584
Navajas M, Lagnel J, Gutierrez J, Boursot P (1998) Species wide homogeneity of nuclear ribosomal ITS2 sequences in the spider mite Tetranychus urticae contrasts with extensive mitochondrial COI polymorphism. Heredity 80:742–752
PerrotMinnot MJ, Guo LR, Werren JH (1996) Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis: effects on compatibility. Genetics 143:961–972
Perrot-Minnot MJ, Cheval B, Migeon A, Navajas M (2002) Contrasting effects of Wolbachia on cytoplasmic incompatibility and fecundity in the haplodiploid mite Tetranychus urticae. J Evol Biol 15:808–817
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
Vala F, Breeuwer JAJ, Sabelis MW (2000) Wolbachia-induced ‘hybrid breakdown’ in the two-spotted spider mite Tetranychus urticae Koch. Proc R Soc B Biol Sci 267:1931–1937
Van Opijnen T, Breeuwer JAJ (1999) High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Exp Appl Acarol 23:871–881
Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42:587–609
Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751
Xie RR, Chen XL, Hong XY (2011) 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
Yoon TJ, Ryoo MI, Cho K (2001) Effect of Wolbachia infection on fitness of resistance to Dicofol in Tetranychus urticae Korean. J Appl Entomol 40:321–326
Zhang YK, Zhang KJ, Sun JT, Yang XM, Ge C, Hong XY (2013) Diversity of Wolbachia in natural populations of spider mites (genus Tetranychus): evidence for complex infection history and disequilibrium distribution. Microb Ecol 65:731–739
Zhao DX, Zhang XF, Chen DS, Zhang YK, Hong XY (2013) Wolbachia-host interactions: host mating patterns affect Wolbachia density dynamics. PLoS One 8(6):e66373
Zhou WG, Rousset F, O’Neill SL (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci 265:509–515
Acknowledgments
We thank the growers for their cooperation regarding mite sample collections. We thank Dr. Mun Il Ryoo and Dr. Ki Hyun Ryu for their helpful suggestions and technical support. This research is supported by Korea Ministry of Environment as “Climate Change Correspondence Program” and Korea University Special Grant to K. Cho.
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Suh, E., Sim, C., Park, JJ. et al. Inter-population variation for Wolbachia induced reproductive incompatibility in the haplodiploid mite Tetranychus urticae . Exp Appl Acarol 65, 55–71 (2015). https://doi.org/10.1007/s10493-014-9846-3
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DOI: https://doi.org/10.1007/s10493-014-9846-3