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Strong cytoplasmic incompatibility and high vertical transmission rate can explain the high frequencies of Wolbachia infection in Japanese populations of Colias erate poliographus (Lepidoptera: Pieridae)

Published online by Cambridge University Press:  09 December 2008

S. Narita ,
Y. Shimajiri  and
M. Nomura
S. Narita*
Affiliation:
Insect-Microbe Research Unit, National Institute of Agrobiological Sciences (NIAS), Owashi 1-2, Tsukuba, Ibaraki 305-8634, Japan
Y. Shimajiri
Affiliation:
Laboratory of Applied Entomology and Zoology, Faculty of Horticulture, Chiba University, Matsudo, Chiba 271-8510, Japan
M. Nomura
Affiliation:
Laboratory of Applied Entomology and Zoology, Faculty of Horticulture, Chiba University, Matsudo, Chiba 271-8510, Japan
*
*Author for correspondence Fax: +81-29-838-6109 E-mail: naritas@affrc.go.jp
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Abstract

Wolbachia, belonging to Alphaproteobacteria, is ubiquitously found in arthropods and filarial nematodes, and is known to manipulate the reproduction of its hosts in various ways, such as feminization, male killing, induction of parthenogenesis or induction of cytoplasmic incompatibility. We found that the Wolbachia infection frequencies of the butterfly Colias erate poliographus were high (85.7–100%) in seven Japanese populations. Crossing experiments and rearing revealed that the Wolbachia strain exhibited strong cytoplasmic incompatibility and perfect vertical transmission in C. erate poliographus. Moreover, a comparison of the survival rates between infected and cured broods suggested that Wolbachia infection had beneficial effects on host fitness. Our findings suggested that the high infection frequencies in Japanese populations have been accomplished by these advantageous traits of the Wolbachia strain. Furthermore, the multilocus sequence typing (MLST) scheme revealed that the Wolbachia in C. erate poliographus is a novel strain (ST141), belonging to supergroup B.

Keywords

Wolbachiacytoplasmic incompatibilityColias erate poliographusperfect vertical transmissionMLST
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 99 , Issue 4 , August 2009 , pp. 385 - 391
Copyright
Copyright © 2008 Cambridge University Press

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References

Arakaki, N., Miyoshi, T. & Noda, H. (2001) Wolbachia-mediated parthenogenesis in the predatory thrips Franklinothrips vespiformis (Thysanoptera: Insecta). Proceedings of the Royal Society of London Series B: Biological Sciences 268, 1011–1016.CrossRefGoogle ScholarPubMed
Baldo, L., Dunning, Hotopp J.C., Jolley, K.A., Bordenstein, S.R., Biber, S.A., Choudhury, R.R., Hayashi, C., Maiden, M.C., Tettelin, H. & Werren, J.H. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Applied and Environmental Microbiology 72, 7098–7110.CrossRefGoogle ScholarPubMed
Bordenstein, S.R. & Werren, J.H. (2000) Do Wolbachia influence fecundity in Nasonia vitripennis? Heredity 84, 54–62.CrossRefGoogle ScholarPubMed
Bourtzis, K. & Miller, T.A. (2003) Insect Symbiosis. 368 pp. Boca Raton, FL, USA, CRC Press.CrossRefGoogle Scholar
Bourtzis, K. & Miller, T.A. (2006) Insect Symbiosis Vol. 2. 304 pp. Boca Raton, FL, USA, CRC Press.CrossRefGoogle Scholar
Bourtzis, K., Dobson, S.L., Braig, H.R. & O'Neill, S.L. (1998) Rescuing Wolbachia have been overlooked. Nature 391, 852–853.CrossRefGoogle ScholarPubMed
Dobson, S., Marsland, E. & Rattanadechakul, W. (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160, 1087–1094.CrossRefGoogle ScholarPubMed
Fry, A. & Rand, D. (2002) Wolbachia interactions that determine Drosophila melanogaster survival. Evolution 56, 1976–1981.Google ScholarPubMed
Giordano, R., O'Neill, S.L. & Robertson, H. (1995) Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophila sechellia and D. mauritiana. Genetics 140, 1307–1317.CrossRefGoogle ScholarPubMed
Harcombe, W. & Hoffmann, A.A. (2004) Wolbachia effects in Drosophila melanogaster: in search of fitness benefits. Journal of Invertebrate Pathology 87, 45–50.CrossRefGoogle ScholarPubMed
Hiroki, M., Kato, Y., Kamito, T. & Miura, K. (2002) Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae). Naturwissenschaften 89, 167–170.CrossRefGoogle Scholar
Hiroki, M., Tagami, Y., Miura, K. & Kato, Y. (2004) Multiple infections with Wolbachia inducing different reproductive manipulations in the butterfly Eurema hecabe. Proceedings of the Royal Society of London Series B: Biological Sciences 271, 1751–1755.CrossRefGoogle ScholarPubMed
Hiroki, M., Ishii, Y. & Kato, Y. (2005) Variation in the prevalence of cytoplasmic incompatibility-inducing Wolbachia in the butterfly Eurema hecabe across the Japanese archipelago. Evolutionary Ecology Research 7, 931–942.Google Scholar
Hoffmann, A. & Turelli, M. (1988) Unidirectional incompatibility in Drosophila simulans: geographic variation and fitness effects. Genetics 119, 435–444.CrossRefGoogle ScholarPubMed
Hoffmann, A.A., Turelli, M. & Harshman, L.G. (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126, 933–948.CrossRefGoogle ScholarPubMed
Hoffmann, A.A., Hercus, M. & Dagher, H. (1998) Population Dynamics of the Wolbachia Infection Causing Cytoplasmic Incompatibility in Drosophila melanogaster. Genetics 148, 221–231.CrossRefGoogle ScholarPubMed
Hoshizaki, S. & Shimada, T. (1995) PCR-based detection of Wolbachia, cytoplasmic incompatibility microorganisms, infected in natural papulations of Laodelphax striatellus (Homoptera: Delphacidae) in central Japan: Has the distribution of Wolbachia spread recently? Insect Molecular Biology 4, 237–243.Google Scholar
Hurst, G.D.D. & Jiggins, F.M. (2000) Male-killing bacteria in insects: mechanisms, incidence and implications. Emerging Infectious Diseases 6, 329–336.CrossRefGoogle ScholarPubMed
Jeyaprakash, A. & Hoy, M.A. (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Molecular Biology 9, 393–405.CrossRefGoogle ScholarPubMed
Johanowicz, D. & Hoy, M. (1999) Wolbachia infection dynamics in experimental laboratory populations of Metaseiulus occidentalis. Entomologia Experimentalis et Applicata 93, 259–268.CrossRefGoogle Scholar
Kato, Y. & Sakakura, F. (1994) Artificial diet rearing of Eurema blanda and some notes on its host-plant. Transactions of the Lepidopterological Society of Japan 45, 21–26 (in Japanese with English summary).Google Scholar
McCullagh, P. & Nelder, J.A. (1989) Generalized Linear Models. 2nd Edn.532 pp. London, UK, Chapman and Hall.CrossRefGoogle Scholar
Masui, S., Sasaki, T. & Ishikawa, H. (1997) groE-Homologous operon of Wolbachia, an intracellular symbiont of arthropods: a new approach for their phylogeny. Zoological Science 14, 701–706.CrossRefGoogle ScholarPubMed
Narita, S., Kageyama, D., Nomura, M. & Fukatsu, T. (2007a) Unexpected mechanism of symbiont-induced reversal of insect sex: feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development for expression of female phenotypes under male genotype. Applied and Environmental Microbiology 73, 4332–4341.CrossRefGoogle Scholar
Narita, S., Nomura, M. & Kageyama, D. (2007b) 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 Microbiology Ecology 61, 235–245.Google Scholar
O'Neill, S.L., Hoffmann, A.A. & Werren, J.H. (1997) Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. 232 pp. New York, USA, Oxford University Press.CrossRefGoogle Scholar
Poinsot, D., Charlat, S. & Mercot, H. (2003) On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. BioEssays 25, 259–265.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K.A. (2001) Selecting the best-fit model of nucleotide substitution. Systematic Biology 50, 580–601.Google Scholar
R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.Google Scholar
Rigaud, T. (1997) Inherited microorganisms and sex determination of arthropod hosts. pp. 81–101in O'Neill, S.L., Hoffmann, A.A. & Werren, J.H. (Eds) Influential Passengers. Oxford, UK, Oxford University Press.Google Scholar
Rigaud, T., Juchault, P. & Mocquard, J.P. (1997) The evolution of sex determination in isopod crustaceans. BioEssays 19, 409–416.CrossRefGoogle Scholar
Stouthamer, R. (1997) Wolbachia-induced parthenogenesis. pp. 102–124in O'Neill, S.L., Hoffmann, A.A. & Werren, J.H. (Eds) Influential Passengers. Oxford, UK, Oxford University Press.CrossRefGoogle Scholar
Swofford, D.L. (2001) PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4.0.Google Scholar
Tagami, Y. & Miura, K. (2004) Distribution and prevalence of Wolbachia in Japanese populations of Lepidoptera. Insect Molecular Biology 13, 359–364.Google Scholar
Turelli, M. & Hoffmann, A.A. (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353, 440–442.CrossRefGoogle ScholarPubMed
Turelli, M. & Hoffmann, A.A. (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140, 1319–1338.CrossRefGoogle ScholarPubMed
Turelli, M., Hoffmann, A.A. & McKechnie, S.W. (1992) Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics 132, 713–723.CrossRefGoogle ScholarPubMed
Vavre, F., Girin, C. & Bouletreau, M. (1999) Phylogenetic status of fecundity-enhancing Wolbachia that does not induce thelytoky in Trichogramma. Insect Molecular Biology 8, 67–72.CrossRefGoogle Scholar
Werren, J.H. (1997) Biology of Wolbachia. Annual Review of Entomology 42, 587–607.CrossRefGoogle ScholarPubMed
Werren, J.H. & Windsor, D. (2000) Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proceedings of the Royal Society of London Series B 267, 1277–1285.Google Scholar
Werren, J.H., Windsor, D. & Guo, L. (1995) Distribution of Wolbachia among neotropical arthropods. Proceedings of the Royal Society of London Series B 262, 197–204.Google Scholar
Zhou, W., Rousset, F. & O'Neill, S. (1998) Phylogeny and PCR based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society of London Series B: Biological Sciences 265, 509–515.CrossRefGoogle ScholarPubMed