Skip to main content Accessibility help
×
Home
Hostname: page-component-747cfc64b6-4xs5l Total loading time: 0.201 Render date: 2021-06-16T13:41:02.050Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true }

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
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
Corresponding
E-mail address:

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.

Type
Research Paper
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below.

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, 10111016.CrossRefGoogle Scholar
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, 70987110.CrossRefGoogle ScholarPubMed
Bordenstein, S.R. & Werren, J.H. (2000) Do Wolbachia influence fecundity in Nasonia vitripennis? Heredity 84, 5462.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, 852853.CrossRefGoogle ScholarPubMed
Dobson, S., Marsland, E. & Rattanadechakul, W. (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160, 10871094.Google ScholarPubMed
Fry, A. & Rand, D. (2002) Wolbachia interactions that determine Drosophila melanogaster survival. Evolution 56, 19761981.CrossRefGoogle 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, 13071317.Google ScholarPubMed
Harcombe, W. & Hoffmann, A.A. (2004) Wolbachia effects in Drosophila melanogaster: in search of fitness benefits. Journal of Invertebrate Pathology 87, 4550.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, 167170.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, 17511755.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, 931942.Google Scholar
Hoffmann, A. & Turelli, M. (1988) Unidirectional incompatibility in Drosophila simulans: geographic variation and fitness effects. Genetics 119, 435444.Google ScholarPubMed
Hoffmann, A.A., Turelli, M. & Harshman, L.G. (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126, 933948.Google ScholarPubMed
Hoffmann, A.A., Hercus, M. & Dagher, H. (1998) Population Dynamics of the Wolbachia Infection Causing Cytoplasmic Incompatibility in Drosophila melanogaster. Genetics 148, 221231.Google 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, 237243.CrossRefGoogle Scholar
Hurst, G.D.D. & Jiggins, F.M. (2000) Male-killing bacteria in insects: mechanisms, incidence and implications. Emerging Infectious Diseases 6, 329336.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, 393405.CrossRefGoogle ScholarPubMed
Johanowicz, D. & Hoy, M. (1999) Wolbachia infection dynamics in experimental laboratory populations of Metaseiulus occidentalis. Entomologia Experimentalis et Applicata 93, 259268.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, 2126 (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, 701706.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, 43324341.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, 235245.CrossRefGoogle ScholarPubMed
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.Google Scholar
Poinsot, D., Charlat, S. & Mercot, H. (2003) On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. BioEssays 25, 259265.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K.A. (2001) Selecting the best-fit model of nucleotide substitution. Systematic Biology 50, 580601.CrossRefGoogle ScholarPubMed
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. 81101in 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, 409416.CrossRefGoogle Scholar
Stouthamer, R. (1997) Wolbachia-induced parthenogenesis. pp. 102124in O'Neill, S.L., Hoffmann, A.A. & Werren, J.H. (Eds) Influential Passengers. Oxford, UK, Oxford University Press.Google 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, 359364.CrossRefGoogle ScholarPubMed
Turelli, M. & Hoffmann, A.A. (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353, 440442.CrossRefGoogle ScholarPubMed
Turelli, M. & Hoffmann, A.A. (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140, 13191338.Google ScholarPubMed
Turelli, M., Hoffmann, A.A. & McKechnie, S.W. (1992) Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics 132, 713723.Google 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, 6772.CrossRefGoogle Scholar
Werren, J.H. (1997) Biology of Wolbachia. Annual Review of Entomology 42, 587607.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, 12771285.CrossRefGoogle ScholarPubMed
Werren, J.H., Windsor, D. & Guo, L. (1995) Distribution of Wolbachia among neotropical arthropods. Proceedings of the Royal Society of London Series B 262, 197204.CrossRefGoogle 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, 509515.CrossRefGoogle ScholarPubMed
20
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

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)
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

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)
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

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)
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *