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Microbial Ecology

, Volume 77, Issue 1, pp 257–266 | Cite as

Multiple Infection and Reproductive Manipulations of Wolbachia in Homona magnanima (Lepidoptera: Tortricidae)

  • Hiroshi Arai
  • Tatsuya Hirano
  • Naoya Akizuki
  • Akane Abe
  • Madoka Nakai
  • Yasuhisa Kunimi
  • Maki N. InoueEmail author
Host Microbe Interactions

Abstract

Endosymbiotic bacterium Wolbachia interacts with host in either a mutualistic or parasitic manner. Wolbachia is frequently identified in various arthropod species, and to date, Wolbachia infections have been detected in different insects. Here, we found a triple Wolbachia infection in Homona magnanima, a serious tea pest, and investigated the effects of three infecting Wolbachia strains (wHm-a, -b, and -c) on the host. Starting with the triple-infected host line (Wabc), which was collected in western Tokyo in 1999 and maintained in laboratory, we established an uninfected line (W) and three singly infected lines (Wa, Wb, and Wc) using antibiotics. Mating experiments with the host lines revealed that only wHm-b induced cytoplasmic incompatibility (CI) in H. magnanima, with the intensities of CI different between the Wb and Wabc lines. Regarding mutualistic effects, wHm-c shortened larval development time and increased pupal weight in both the Wc and Wabc lines to the same extent, whereas no distinct phenotype was observed in lines singly infected with wHm-a. Based on quantitative PCR analysis, Wolbachia density in the Wa line was higher than in the other host lines (p < 0.01, n = 10). Wolbachia density in the Wb line was also higher than in the Wc and Wabc lines, while no difference was observed between the Wc and Wabc lines. These results indicate that the difference in the CI intensity between a single or multiple infection may be attributed to the difference in wHm-b density. However, no correlation was observed between mutualistic effects and Wolbachia density.

Keywords

Wolbachia density Reproductive fitness Cytoplasmic incompatibility Homona magnanima 

References

  1. 1.
    Buchner P (1965) Endosymbiosis of animals with plant microorganisms. John Wiley & Sons Inc., New YorkGoogle Scholar
  2. 2.
    Bourtzis K, Miller TA (2003) Insect symbiosis. CRC Press, FloridaCrossRefGoogle Scholar
  3. 3.
    Kikuchi Y, Hosokawa T, Nikoh N, Meng XY, Kamagata Y, Fukatsu T (2009) Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol. 7:2CrossRefGoogle Scholar
  4. 4.
    Roberts LW, Rapmund G, Cadigan Jr FC (1977) Sex ratios in Rickettsia tsutsugamushi-infected and noninfected colonies of Leptotrombidium (Acari: Trombiculidae). J. Med. Entomol. 14:89–92CrossRefGoogle Scholar
  5. 5.
    Gherna RL, Werren JH, Weisburg W, Cote R, Woese CR, Mandelco L, Brenner DJ (1991) Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. Int. J. Syst. Bacteriol. 41:563–565CrossRefGoogle Scholar
  6. 6.
    Werren JH (1997) Biology of Wolbachia. Annu. Rev. Entomol. 42:587–609CrossRefGoogle Scholar
  7. 7.
    Williamson DL, Sakaguchi B, Hackett KJ, Whitcomb RF, Tully JG, Carle P, Bové JM, Adams JR, Konai M, Henegar RB (1999) Spiroplasma poulsonii sp. nov., a new species associated with male-lethality in Drosophila willistoni, a neotropical species of fruit fly. Int. J. Syst. Bacteriol. 49:611–618CrossRefGoogle Scholar
  8. 8.
    Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol. Ecol. 13:2009–2016CrossRefGoogle Scholar
  9. 9.
    Andreadis TG, Hall DW (1979) Development, ultrastructure, and mode of transmission of Amblyospora sp. (Microspora) in the mosquito. J. Protozool. 26:444–452CrossRefGoogle Scholar
  10. 10.
    Nakanishi K, Hoshino M, Nakai M, Kunimi Y (2008) Novel RNA sequences associated with late male killing in Homona magnanima. Proc. R. Soc. B 275:1249–1254CrossRefGoogle Scholar
  11. 11.
    Stouthamer R, Breeuwer JA, Hurst GD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53:71–102CrossRefGoogle Scholar
  12. 12.
    Zug R, Hammerstein P (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 7:e38544CrossRefGoogle Scholar
  13. 13.
    Vavre F, Girin C, Boulétreau M (1999) Phylogenetic status of a fecundity-enhancing Wolbachia that does not induce thelytoky in Trichogramma. Insect Mol. Biol. 8:67–72CrossRefGoogle Scholar
  14. 14.
    Fry AJ, Rand DM (2002) Wolbachia interactions that determine Drosophila melanogaster survival. Evolution 56:1976–1981CrossRefGoogle Scholar
  15. 15.
    Brownlie JC, Cass BN, Riegler M, Witsenburg JJ, Iturbe-Ormaetxe I, McGraw EA, O’Neill SL (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog. 5:e1000368CrossRefGoogle Scholar
  16. 16.
    Teixeira L, Ferreira A, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 6:e1000002CrossRefGoogle Scholar
  17. 17.
    Bordenstein SR, Werren JH (2000) Do Wolbachia influence fecundity in Nasonia vitripennis? Heredity 84:54–62CrossRefGoogle Scholar
  18. 18.
    Harcombe W, Hoffmann AA (2004) Wolbachia effects in Drosophila melanogaster: in search of fitness benefits. J. Invertebr. Pathol. 87:45–50CrossRefGoogle Scholar
  19. 19.
    Jaenike J, Unckless R, Cockburn SN, Boelio LM, Periman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–215CrossRefGoogle Scholar
  20. 20.
    Zhao DX, Zhang XF, Hong XY (2013) Host-symbiont interactions in spider mite Tetranychus truncates doubly infected with Wolbachia and Cardinium. Environ. Entomol. 42:445–452CrossRefGoogle Scholar
  21. 21.
    Kondo N, Ijichi N, Shimada M, Fukatsu T (2002) Prevailing triple infection with Wolbachia in Callosobruchus chinensis (Coleoptera: Bruchidae). Mol. Ecol. 11:167–180CrossRefGoogle Scholar
  22. 22.
    Malloch G, Fenton B, Butcher RD (2000) Molecular evidence for multiple infections of a new subgroup of Wolbachia in the European raspberry beetle Byturus tomentosus. Mol. Ecol. 9:77–90CrossRefGoogle Scholar
  23. 23.
    Reuter M, Keller L (2003) High levels of multiple Wolbachia infection and recombination in the ant Formica exsecta. Mol. Biol. Evol. 20:748–753CrossRefGoogle Scholar
  24. 24.
    Narita S, Nomura M, Kageyama D (2007) Naturally occurring single and double infection with Wolbachia strains in the butterfly Eurema hecabe: transmission efficiencies and population density dynamics of each Wolbachia strain. FEMS Microbiol. Ecol. 61:235–245CrossRefGoogle Scholar
  25. 25.
    Atyame CM, Pasteur N, Dumas E, Tortosa P, Tantely ML, Pocquet N, Licciardi S, Bheecarry A, Zumbo B, Weill M, Duron O (2011) Cytoplasmic incompatibility as a means of controlling Culex pipiens quinquefasciatus mosquito in the islands of the south-western Indian Ocean. PLoS Negl. Trop. Dis. 5:e1440CrossRefGoogle Scholar
  26. 26.
    White JA, Kelly SE, Cockburn SN, Perlman SJ, Hunter MS (2011) Endosymbiont costs and benefits in a parasitoid infected with both Wolbachia and Cardinium. Heredity 106:585–591CrossRefGoogle Scholar
  27. 27.
    Watanabe M, Miura K, Hunter MS, Wajnberg E (2011) Superinfection of cytoplasmic incompatibility-inducing Wolbachia is not additive in Orius strigicollis (Hemiptera: Anthocoridae). Heredity 106:642–648CrossRefGoogle Scholar
  28. 28.
    Kondo N, Shimada M, Fukatsu T (2005) Infection density of Wolbachia endosymbiont affected by co-infection and host genotype. Biol. Lett. 1:488–491CrossRefGoogle Scholar
  29. 29.
    Goto S, Anbutsu H, Fukatsu T (2006) Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Appl. Environ. Microbiol. 72:4805–4810CrossRefGoogle Scholar
  30. 30.
    Morimoto S, Nakai M, Ono A, Kunimi Y (2001) Late male-killing phenomenon found in a Japanese population of the oriental tea tortrix, Homona magnanima (Lepidoptera: Tortricidae). Heredity 87:435–440CrossRefGoogle Scholar
  31. 31.
    Tsugeno Y, Koyama H, Takamatsu T, Nakai M, Kunimi Y, Inoue MN (2017) Identification of an early male-killing agent in the oriental tea tortrix, Homona magnanima. J. Hered. 108:553–560CrossRefGoogle Scholar
  32. 32.
    Dobson SL, Bourtzis K, Braig HR, Jones BF, Zhou W, Rousset F, O'Neill SL (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem. Mol. Biol. 29:153–160CrossRefGoogle Scholar
  33. 33.
    Lalzar I, Friedmann Y, Gottlieb Y (2014) Tissue tropism and vertical transmission of Coxiella in Rhipicephalus sanguineus and Rhipicephalus turanicus ticks. Environ. Microbiol. 16:3657–3668CrossRefGoogle Scholar
  34. 34.
    Zhou W, Rousset F, O’Neill S (1998) Phylogeny and PCR–based classification of Wolbachia strains using wsp gene sequences. Proc. Biol. Sci. 265:509–515CrossRefGoogle Scholar
  35. 35.
    Hurst GDD, Jiggins FM, von der Schulenburg JHG, Bertrand D, West SA, Goriacheva II, Zakharov IA, Werren JH, Stouthamer R, Majerus MEN (1999) Male-killing Wolbachia in two species of insect. Proc. Biol. Sci. 266:735–740CrossRefGoogle Scholar
  36. 36.
    Regnery RL, Spruill CL, Plikaytis BD (1991) Genotypic identification of Rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J. Bacteriol. 173:1576–1589CrossRefGoogle Scholar
  37. 37.
    Noda H, Koizumi Y, Zhang Q, Deng K (2001) Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochem. Mol. Biol. 31:727–737CrossRefGoogle Scholar
  38. 38.
    Sanada-Morimura S, Matsumura M, Noda H (2013) Male killing caused by a Spiroplasma symbiont in the small brown planthopper, Laodelphax striatellus. J. Hered. 104:821–829CrossRefGoogle Scholar
  39. 39.
    Noda H, Watanabe K, Kawai S, Yukuhiro F, Miyoshi T, Tomizawa M, Koizumi Y, Nikoh N, Fukatsu T (2012) Bacteriome-associated endosymbionts of the green rice leafhopper Nephotettix cincticeps (Hemiptera: Cicadellidae). Appl. Entomol. Zool. 47:217–225CrossRefGoogle Scholar
  40. 40.
    Baldo L, Hotopp JCD, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, Hayashi C, Maiden MCJ, Tettelin H, Werren JH (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl. Environ. Microbiol. 72:7098–7110CrossRefGoogle Scholar
  41. 41.
    Iwata K, Haas-Stapleton E, Kunimi Y, Inoue MN, Nakai M (2017) Midgut-based resistance to oral infection by a nucleopolyhedrovirus in the laboratory-selected strain of the smaller tea tortrix, Adoxophyes honmai (Lepidoptera: Tortricidae). J. Gen. Virol. 98:296–304CrossRefGoogle Scholar
  42. 42.
    Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673–4680CrossRefGoogle Scholar
  43. 43.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725–2729CrossRefGoogle Scholar
  44. 44.
    Turelli M, Hoffmann AA (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353:440–442CrossRefGoogle Scholar
  45. 45.
    Cheng HH (1972) Oviposition and longevity of the dark-sided cutworm, Euxoa messoria (Lepidoptera: Noctuidae), in the laboratory. Can. Entomol. 104:919–925CrossRefGoogle Scholar
  46. 46.
    Hough JA, Pimentel D (1978) Influence of host foliage on development, survival, and fecundity of the gypsy moth. Environ. Entomol. 7:97–102CrossRefGoogle Scholar
  47. 47.
    Honěk A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–492CrossRefGoogle Scholar
  48. 48.
    Sato T, Oho N, Kodomari S (1980) A granulosis virus of the tea tortrix, Homona magnanima Diaknoff (Lepidoptera: Tortricidae): its pathogenicity and mass-production method. Appl. Entomol. Zool. 15:409–415CrossRefGoogle Scholar
  49. 49.
    Mao HX, Kunimi Y (1991) Pupal mortality of the oriental tea tortrix, Homona magnanima Diakonoff (Lepidoptera: Tortricidae), caused by parasitoids and pathogens. Jpn. J. Appl. Entomol. Zool. 35:241–245CrossRefGoogle Scholar
  50. 50.
    Takatsuka J, Okuno S, Ishii T, Nakai M, Kunimi Y (2010) Fitness-related traits of entomopoxviruses isolated from Adoxophyes honmai (Lepidoptera: Tortricidae) at three localities in Japan. J. Invertebr. Pathol. 105:121–131CrossRefGoogle Scholar
  51. 51.
    Veneti Z, Clark ME, Karr TL, Savakis C, Bourtzis K (2004) Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl. Environ. Microbiol. 70:5366–5372CrossRefGoogle Scholar
  52. 52.
    Hoffmann AA, Clancy D, Duncan J (1996) Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity 76:1–8CrossRefGoogle Scholar
  53. 53.
    McGraw EA, Merritt DJ, Droller JN, O’Neill SL (2002) Wolbachia density and virulence attenuation after transfer into a novel host. Proc. Natl. Acad. Sci. U. S. A. 99:2918–2923CrossRefGoogle Scholar
  54. 54.
    Reynolds KT, Thomson LJ, Hoffmann AA (2003) The effects of host age, host nuclear background and temperature on phenotypic effects of the virulent Wolbachia strain popcorn in Drosophila melanogaster. Genetics 164:1027–1034PubMedPubMedCentralGoogle Scholar
  55. 55.
    Unckless RL, Boelio LM, Herren JK, Jaenike J (2009) Wolbachia as populations within individual insects: causes and consequences of density variation in natural populations. Proc. R. Soc. B 276:2805–2811CrossRefGoogle Scholar
  56. 56.
    Hurst GD, Jiggins FM (2000) Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg. Infect. Dis. 6:329–336CrossRefGoogle Scholar
  57. 57.
    Sasaki T, Ishikawa H (2000) Transinfection of Wolbachia in the Mediterranean flour moth, Ephestia kuehniella, by embryonic microinjection. Heredity 85:130–135CrossRefGoogle Scholar
  58. 58.
    Sasaki T, Massaki N, Kubo T (2005) Wolbachia variant that induces two distinct reproductive phenotypes in different hosts. Heredity 95:389–393CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Applied Biological ScienceTokyo University of Agriculture and TechnologyTokyoJapan

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