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Population genetic structure and Wolbachia infection in an endangered butterfly, Zizina emelina (Lepidoptera, Lycaenidae), in Japan

Published online by Cambridge University Press:  12 December 2014

Y. Sakamoto*
Affiliation:
Entomological Laboratory, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai, Osaka 599-8531, Japan
N. Hirai
Affiliation:
Entomological Laboratory, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai, Osaka 599-8531, Japan
T. Tanikawa
Affiliation:
Entomological Laboratory, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai, Osaka 599-8531, Japan
M. Yago
Affiliation:
The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
M. Ishii
Affiliation:
Entomological Laboratory, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai, Osaka 599-8531, Japan
*
*Author for correspondence Phone: +81-29-850-2480 Fax: +81-29-850-2480 E-mail: [email protected]

Abstract

Zizina emelina (de l'Orza) is listed on Japan's Red Data List as an endangered species because of loss of its principal food plant and habitat. We compared parts of the mitochondrial and nuclear genes of this species to investigate the level of genetic differentiation among the 14 extant populations. We also examined infection of the butterfly with the bacterium Wolbachia to clarify the bacterium's effects on the host population's genetic structure. Mitochondrial and nuclear DNA analyses revealed that haplotype composition differed significantly among most of the populations, and the fixation index FST was positively correlated with geographic distance. In addition, we found three strains of Wolbachia, one of which was a male killer; these strains were prevalent in several populations. There was linkage between some host mitochondrial haplotypes and the three Wolbachia strains, although no significant differences were found in a comparison of host mitochondrial genetic diversity with nuclear genetic diversity in Wolbachia-infected or -uninfected populations. These genetic analyses and Wolbachia infection findings show that Z. emelina has little migratory activity and that little gene flow occurs among the current populations.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

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References

Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716723.CrossRefGoogle Scholar
Avise, J.C. (1994) Molecular Markers, Natural History, and Evolution. 511 pp. New York, Chapman & Hall.CrossRefGoogle Scholar
Avise, J.C. (2000) Phylogeography: The History and Formation of Species. 447 pp. Cambridge, Massachusetts, Harvard University Press.CrossRefGoogle Scholar
Bonnell, M.L. & Selander, R. K. (1974) Elephant seals: genetic variation and near extinction. Science 184, 908909.CrossRefGoogle Scholar
Bonte, D., Hovestadt, T. & Poethke, H.J. (2009) Sex-specific dispersal and evolutionary rescue in metapopulations infected by male killing endosymbionts. BMC Evolutionary Biology 9, 16.CrossRefGoogle ScholarPubMed
Braig, H.R., Zhou, W.G., Dobson, S.L. & O'Neill, S.L. (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis . Journal of Bacteriology 180, 23732378.CrossRefGoogle ScholarPubMed
Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571659.CrossRefGoogle ScholarPubMed
Dvořáková, H., Fér, T. & Marhold, K. (2010) Phylogeographic pattern of the European forest grass species Hordelymus europaeus: cpDNA evidence. Flora 205, 418423.CrossRefGoogle Scholar
Ellegren, H., Mikko, S., Wallin, K. & Andersson, L. (1996) Limited polymorphism at major histocompatibility complex (MHC) loci in the Swedish moose A. alces . Molecular Ecology 5, 39.CrossRefGoogle ScholarPubMed
Excoffier, L. & Lischer, H.E.L. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564567.CrossRefGoogle ScholarPubMed
Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial-DNA restriction data. Genetics 131, 479491.CrossRefGoogle ScholarPubMed
Fay, J.C. & Wu, C.I. (1999) A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Molecular Biological Evolution 16, 10031005.CrossRefGoogle ScholarPubMed
Fialho, R.F. & Stevens, L. (2000) Male-killing Wolbachia in a flour beetle. Proceedings of the Royal Society of London Series B-Biological Sciences 267, 14691473.CrossRefGoogle Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial Cytochrome C oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google ScholarPubMed
Forbes, S.H. & Hogg, J.T. (1999) Assessing population structure at high levels of differentiation: microsatellite comparisons of bighorn sheep and large carnivores. Animal Conservation 2, 223233.CrossRefGoogle Scholar
Frankham, R. (1995) Conservation genetics. Annual Review of Genetics 29, 305327.CrossRefGoogle ScholarPubMed
Frankham, R., Briscoe, D.A. & Ballou, J.D. (2002) Introduction to Conservation Genetics. 617 pp. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Fukuda, H., Hama, E., Kuzuya, T., Takahashi, A., Takahashi, M., Tanaka, B., Tanaka, H., Wakabayashi, M. & Watanabe, Y. (1984) The Life Histories of Butterflies in Japan, Vol. 3. Osaka, Japan, Hoikusha. (in Japanese with English abstract).Google Scholar
Groombridge, J.J., Jones, C.J., Bruford, M.W. & Nichols, R.A. (2000) ‘Ghost’ alleles of the Mauritius kestrel. Nature 403, 616.CrossRefGoogle ScholarPubMed
Haig, S.M., Wagner, R.S., Forsman, E.D. & Mullins, T.D. (2001) Geographic variation and genetic structure in spotted owls. Conservation Genetics 2, 2540.CrossRefGoogle Scholar
Hamrick, J.L. & Godt, M.J.W. (1996) Conservation genetics of endemic plant species. pp. 281304 in Avice, J.C. & Hamrick, J.L. (Ed.) Conservation Genetics: Case Histories from Nature. New York, Chapman and Hall.CrossRefGoogle Scholar
Hastings, A. & Harrison, S. (1994) Metapopulation dynamics and genetics. Annual Review of Ecology, Evolution, and Systematics 25, 167188.CrossRefGoogle Scholar
Hewitt, G.M. (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society 58, 247276.CrossRefGoogle Scholar
Hewitt, G.M. (2000) The genetic legacy of the Quaternary ice ages. Nature 405, 907913.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
Hoffmann, A.A., Turelli, M. & Harshman, L.G. (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans . Genetics 126, 933948.CrossRefGoogle ScholarPubMed
Hucka, S., Büdelb, B. & Schmitta, T. (2012) Ice-age isolation, postglacial hybridization and recent population bottlenecks shape the genetic structure of Meum athamanticum in Central Europe. Flora 207, 399407.CrossRefGoogle Scholar
Hudson, R.R., Kreitman, M. & Aguade, M. (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153159.CrossRefGoogle ScholarPubMed
Hurst, G.D.D. & Jiggins, F.M. (2000) Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerging Infectious Diseases 6, 329336.CrossRefGoogle ScholarPubMed
Hurst, G.D.D., Jiggins, F.M., von der Schulenburg, J.H.G., Bertrand, D., West, S.A., Goriacheva, I.I. Zakharov, I.A., Werren, J.H., Stouthamer, R. & Majerus, M.E.N. (1999) Male-killing Wolbachia in two species of insect. Proceedings of the Royal Society of London Series B-Biological Sciences 266, 735740.CrossRefGoogle Scholar
Ibrahim, K.M., Nichols, R.A. & Hewitt, G.M. (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77, 282291.CrossRefGoogle Scholar
Ikeda, H., Kubota, K., Cho, Y., Liang, H. & Sota, T. (2009) Different phylogeographic patterns in two Japanese Silpha species (Coleoptera: Silphidae) affected by climatic gradients and topography. Biological Journal of the Linnean Society 98, 452467.CrossRefGoogle Scholar
Ishii, M. (2009) Importance of the Satoyama Landscapes for Conservation of Biodiversity . pp. 311 in Mano, T. and Fujii, H. (Ed.) Decline and Conservation of Butterflies and Moths in Japan VI. Tokyo, The Lepidopterological Society of Japan (In Japanese).Google Scholar
Ishii, M., Hirai, N. & Hirowatari, T. (2008) The occurrence of an endangered lycaenid, Zizina emelina (de l'Orza) (Lepidoptera, Lycaenidae), in Osaka International Airport, central Japan. Transaction of the Lepidopterological Society of Japan 59, 7882.Google Scholar
Jeratthitikul, E., Hara, T., Yago, M., Itoh, T., Wang, M., Usami, S. & Hikida, T. (2013) Phylogeography of Fischer's blue, Tongeia fischeri, in Japan: evidence for introgressive hybridization. Molecular Phylogenetics and Evolution 66, 316326.CrossRefGoogle ScholarPubMed
Jiggins, C.D., Linares, M., Naisbit, R.E., Salazar, C., Yang, Z.H. & Mallet, J. (2001) Sex-linked hybrid sterility in a butterfly. Evolution 55, 16311638.Google Scholar
Jiggins, F.M. (2003) Male-killing Wolbachia and mitochondrial DNA: selective sweeps, hybrid introgression and parasite population dynamics. Genetics 164, 512.CrossRefGoogle ScholarPubMed
Jiggins, F.M., Hurst, G.D.D. & Majerus, M.E.N. (2000) Sex-ratio-distorting Wolbachia cause sexrole reversal in its butterfly hosts. Proceedings of the Royal Society of London Series B-Biological Sciences 267, 6973.CrossRefGoogle Scholar
Johnstone, R.A. & Hurst, G.D.D. (1996) Maternally inherited male-killing microorganisms may confound interpretation of mtDNA variation in insects. Biological Journal of the Linnean Society 53, 453470.CrossRefGoogle Scholar
Leturque, H. & Rousset, F. (2003) Joint evolution of sex ratio and dispersal: conditions for higher dispersal rates from good habitats. Evolutionary Ecology 17, 6784.CrossRefGoogle Scholar
Logsden, J.M., Tyshenko, M.G., Dixon, C., Jafari, J.D., Walker, V.K. & Palmer, J.D. (1995) Seven newly discovered intron positions in the triose-phosphate isomerase gene: evidence for the introns-late theory. Proceedings of the National Academy of Sciences 92, 85078511.CrossRefGoogle Scholar
Mano, T. & Fujii, H. (Ed.) (2009) The red data lists of butterflies in 43 Prefectures, Japan. pp. 107265 in Mano, T. & Fujii, H. (Ed.) Decline and conservation of butterflies and moths in Japan VI. Tokyo, The Lepidopterological Society of Japan. (In Japanese)Google Scholar
Meffe, G.K. & Carroll, C.R. (1997) Principles of Conservation Biology. 2nd edn. 729 pp. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Ministry of Environment, Japan (2006) Listed species of Red Data book. pp. 2429 in Threatened Wildlife of Japan (Red Data book, 2nd edn) 5. Insecta. Tokyo, Japan, Japan Wildlife Research Center.Google Scholar
Ministry of Environment, Japan (2012) The 4th Red Data List of Threatened Insect of Japan. Japan Integrated Biodiversity Information System HP. Available online at http://www.biodic.go.jp/english/rdb/rdb_f.html Google Scholar
Minohara, S., Morichi, S., Hirai, N. & Ishii, M. (2007) Distribution and seasonal occurrence of the lycaenid, Zizina emelina (de l'Orza) (Lepidoptera, Lycaenidae), around the Osaka International Airport, central Japan. Transaction of the Lepidopterological Society of Japan 58, 421432.Google Scholar
Moritz, C. (1994) Defining evolutionary significant units for conservation. Trends in Ecology and Evolution 9, 373376.CrossRefGoogle Scholar
Nakamura, Y. (2003) Current status and the future of butterfly conservation in Japan. pp. 171176 in Sunose, T. & Eda, K. (Ed.) Decline and Conservation of Butterflies in Japan, V: Tokyo, Lepidopterological Society of Japan. (In Japanese).Google Scholar
Nakamura, Y. (2010) Conservation of butterflies in Japan: status, action and strategy. Journal of Insect Conservation 15, 522.CrossRefGoogle Scholar
Nakatani, T., Tashita, M., Maruyama, K., Usami, S. & Itou, T. (2006) Genetic structure of populations in the alpine butterfly, Erebia niphonica . Insect DNA Research Society, Newsletter 5, 2840. (in Japanese).Google Scholar
Narita, S., Nomura, M., Kato, Y. & Fukatsu, T. (2006) Genetic structure of sibling butterfly species affected by Wolbachia infection sweep: evolutionary and biogeographical implications. Molecular Ecology 15, 10951108.CrossRefGoogle ScholarPubMed
Negri, I., Pellecchia, M., Mazzoglio, P.J., Patetta, A. & Alma, A. (2006) Feminizing Wolbachia in Zyginidia pullula (Insecta, Hemiptera), a leafhopper with an XX/XO sex determination system. Proceedings of the Royal Society of London Series B-Biological Sciences 273, 24092416.Google Scholar
Nice, C.C., Gompert, Z., Forister, M.L. & Fordyce, J.A. (2009) An unseen foe in arthropod conservation efforts: the case of Wolbachia infections in the Karner blue butterfly. Biological Conservation 142, 31373146.CrossRefGoogle Scholar
Nichols, R.A. & Hewitt, G.M. (1994) The genetic consequences of long distance dispersal during colonization. Heredity 72, 312317.CrossRefGoogle Scholar
O'Brien, S.J., Wildt, D.E., Goldman, D., Merril, C.R. & Bush, M. (1983) The cheetah is depauperate in genetic variation. Science 221, 459462.CrossRefGoogle ScholarPubMed
Ohshima, I., Tanikawa-Dodo, Y., Saigusa, T., Nishiyama, T., Kitani, M., Hasebe, M. & Mohri, H. (2010) Phylogeny, biogeography, and host-plant association in the subfamily Apaturinae (Insecta: Lepidoptera: Nymphalidae) inferred from eight nuclear and seven mitochondrial genes. Molecular Phylogenetics and Evolution 57, 10261036.CrossRefGoogle ScholarPubMed
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. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle ScholarPubMed
Primack, R.B. (2004) A Primer of Conservation Biology, 3rd edn. 320 pp. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Rigaud, T., Soutygrosset, C., Raimond, R., Mocquard, J.P. & Juchault, P. (1991) Feminizing endocytobiosis in the terrestrial crustacean armadillidium-vulgare Latr. (Isopoda) – recent acquisitions. Endocytobiosis and Cell Research 7, 259273.Google Scholar
Ritter, S., Michalski, S.G., Settele, J., Wiemers, M., Fric, Z.F., Sielezniew, M., Sasic, M., Rozier, Y. & Durka, W. (2013) Wolbachia infections mimic cryptic speciation in two parasitic butterfly species, Phengaris teleius and P. nausithous (Lepidoptera: Lycaenidae). PLOS ONE 8, e78107.CrossRefGoogle ScholarPubMed
Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 24962497.CrossRefGoogle ScholarPubMed
Saigusa, T., Nakanishi, A., Yata, O., Odagiri, K., Yago, M., Masunaga, K., Tanikawa, Y., Nishiyama, T., Hasebe, M. & Mohri, H. (2001) Phylogenetic relationships of the family Nymphalidae of Japan, inferred from the ND5 region of mitochondrial DNA (Lepidoptera, Papilionoidea) (additional report). Butterfly DNA Research Society, News Letter 6, 1526.Google Scholar
Saitoh, S., Miyai, S. & Katakura, H. (2008) Geographical variation and diversification in the flightless leaf beetles of the Chrysolina angusticollis species complex (Chrysomelidae, Coleoptera) in northern Japan. Biological Journal of the Linnean Society 93, 557578.CrossRefGoogle Scholar
Sakamoto, Y., Hirai, N., Hirowatari, T., Yago, M. & Ishii, M. (2010) Genital segments of sexual mosaic offspring from Wolbachia-infected female Zizina emelina (Lepidoptera: Lycaenidae). Entomological News 121, 443450.CrossRefGoogle Scholar
Sakamoto, Y., Hirai, N., Tanikawa, T., Yago, M. & Ishii, M. (2011) Infection of two strains of Wolbachia and sex ratio distortion in a population of an endangered lycaenid butterfly, Zizina emelina, in northern Osaka Prefecture, central Japan. Annals of the Entomological Society of America 104, 483487.CrossRefGoogle Scholar
Schmitt, T. & Müller, P. (2007) Limited hybridization along a large contact zone between two genetic lineages of the butterfly Erebia medusa (Satyrinae: Lepidoptera) in Central Europe. Journal of Zoological Systematics and Evolutionary Research 45, 3946.CrossRefGoogle Scholar
Šmídová, A., Münzbergová, Z. & Plačková, I. (2011) Genetic diversity of a relict plant species, Ligularia sibirica (L.) Cass. (Asteraceae). Flora 206, 151157.CrossRefGoogle Scholar
Stouthamer, R., Luck, R.F. & Hamilton, W.D. (1990) Antibiotics cause parthenogenetic Trichogramma (Hymenoptera, Trichogrammatidae) to revert to sex. Proceedings of the National Academy of Sciences of the United States of America 87, 24242427.CrossRefGoogle ScholarPubMed
Sunose, T. & Eda, K. (Ed.) (2003) The red data lists of butterflies in 43 Prefectures pp. 1169 in Sunose, T. & Eda, K. (Ed.) Decline and Conservation of Butterflies in Japan, V. Tokyo, Lepidopterological Society of Japan. (In Japanese)Google Scholar
Suzuki, Y. (2007) A habitation condition and the conservation of the Z. otis . The Nature and Insects. (559), 1012. (in Japanese)Google Scholar
Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis using Parsimony (*and other Methods), Version 4. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Taberlet, P., Fumagalli, L., Wust-Saucy, A.G. & Cosson, J.F. (1998) Comparative phylogeography and postglacial colonisation routes in Europe. Molecular Ecology 7, 453464.CrossRefGoogle ScholarPubMed
Takei, H. (2005) Let's look for Z. otis . Nature and Insects 20, 2426. (in Japanese)Google Scholar
Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. III. Cladogram estimation. Genetics 132, 619633.CrossRefGoogle ScholarPubMed
Tscharntke, T., Steffan-Dewenter, I., Kruess, A. & Thies, C. (2002) The contribution of small habitat fragments to the conservation of insect communities of grassland-cropland landscape mosaics. Ecological Applications 12, 354363.Google Scholar
Turelli, M. & Hoffmann, A.A. (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140, 13191338.CrossRefGoogle ScholarPubMed
Yagi, T., Sasaki, G. & Takebe, H. (1999) Phylogeny of Japanese papilionid butterflies inferred from nucleotide sequences of the mitochondrial ND5 gene. Journal of Molecular Evolution 48, 4248.CrossRefGoogle ScholarPubMed
Yago, M., Hirai, N., Kondo, M., Tanikawa, T., Ishii, M., Wang, M., Williams, M. & Ueshima, R. (2008) Molecular systematics and biogeography of the genus Zizina (Lepidoptera: Lycaenidae). Zootaxa 1746, 1538.CrossRefGoogle Scholar
Yoshio, M. (2005) Analysis of mitochondrial genome and population structure of Papilio memnon L. in Japan. Insect DNA Research Society, Newsletter 2, 3843. (in Japanese)Google Scholar
Weeks, A.R. & Breeuwer, J.A. (2001) Wolbachia-induced parthenogenesis in a genus of phytophagous mites. Proceedings of the Royal Society of London Series B-Biological Sciences 268, 22452251.CrossRefGoogle Scholar
Wenseleers, T., Ito, F., Van Borm, S., Huybrechts, R., Volckaert, F., Billen, J. (1998) Widespread occurrence of the micro-organism Wolbachia in ants. Proceedings of the Royal Society of London, Series B-Biological Sciences 265, 14471452.CrossRefGoogle ScholarPubMed
Werren, J.H. (1997) Biology of Wolbachia . Annual Review of Entomology 42, 587609.CrossRefGoogle ScholarPubMed
Werren, J.H., Zhang, W. & Guo, L.R. (1995) Evolution and phylogeny of Wolbachia reproductive parasites of arthropods. Proceedings of the Royal Society of London Series B-Biological Sciences 261, 5563.Google ScholarPubMed