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Host-plant dependent population genetics of the invading weevil Hypera postica

Published online by Cambridge University Press:  22 October 2014

S.-I. Iwase*
Affiliation:
Institute of Biological Control, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan
K. Nakahira
Affiliation:
Institute of Biological Control, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan
M. Tuda*
Affiliation:
Institute of Biological Control, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan Laboratory of Insect Natural Enemies, Division of Agricultural Bioresource Sciences, Department of Bioresource Sciences, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan
K. Kagoshima
Affiliation:
Institute of Biological Control, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan
M. Takagi
Affiliation:
Institute of Biological Control, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan Laboratory of Insect Natural Enemies, Division of Agricultural Bioresource Sciences, Department of Bioresource Sciences, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan
*
*Authors for correspondence Phone: +81-92-642-3038 Fax: +81-92-642-3040 E-mail: [email protected]; [email protected]
*Authors for correspondence Phone: +81-92-642-3038 Fax: +81-92-642-3040 E-mail: [email protected]; [email protected]

Abstract

Population genetics of invading pests can be informative for understanding their ecology. In this study, we investigated population genetics of the invasive alfalfa weevil Hypera postica in Fukuoka Prefecture, Japan. We analyzed mitochondrial tRNALeu-COII, nuclear EF-1α gene fragments, and Wolbachia infection in relation to three leguminous host plants: Vicia angustifolia, Vicia villosa, and a new host Astragalus sinicus cultivated as a honey source and green manure crop. A parsimony network generated from mitochondrial gene sequences uncovered two major haplotypic groups, Western and Egyptian. In contrast to reported Wolbachia infection of the Western strain in the United States, none of our analyzed individuals were infected. The absence of Wolbachia may contribute to the stable coexistence of mitochondrial strains through inter-strain reproductive compatibility. Hypera postica genetic variants for the mitochondrial and nuclear genes were associated neither with host plant species nor with two geographic regions (Hisayama and Kama) within Fukuoka. Mitochondrial haplogroups were incongruent with nuclear genetic variants. Genetic diversity at the nuclear locus was the highest for the populations feeding on V. angustifolia. The nuclear data for A. sinicus-feeding populations indicated past sudden population growth and extended Bayesian skyline plot analysis based on the mitochondrial and nuclear data showed that the growth of A. sinicus-feeding population took place within the past 1000 years. These results suggest a shorter history of A. sinicus as a host plant compared with V. angustifolia and a recent rapid growth of H. postica population using the new host A. sinicus.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

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References

Blickenstaff, C.C. (1965) Partial intersterility of eastern and western U.S. strains of the alfalfa weevil. Annals of the Entomological Society of America 58, 523526.Google Scholar
Böttger, J.A.A., Bundy, C.S., Oesterle, N. & Hanson, S.F. (2013) Phylogenetic analysis of the alfalfa weevil complex (Coleoptera: Curculionidae) in North America. Journal of Economic Entomology 106, 426436.CrossRefGoogle ScholarPubMed
Clancy, D.J. & Hoffmann, A.A. (1998) Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans . Entomologia Experimentalis et Applicata, 86, 1324.Google Scholar
Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571660.CrossRefGoogle ScholarPubMed
Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.CrossRefGoogle ScholarPubMed
Ehrlich, P.R. & Raven, P.H. (1964) Butterflies and plant: a study in coevolution. Evolution 18, 586608.Google Scholar
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
Felsenstein, J. (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 17, 368376.Google Scholar
Fu, Y.-X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915925.Google Scholar
Gomez-Zurita, J., Juan, C. & Petitpierre, E. (2000) The evolutionary history of the genus Timarcha (Coleoptera, Chrysomelidae) inferred from mitochondrial COII gene and partial 16S rDNA sequences. Molecular Phylogenetics and Evolution 14, 304317.CrossRefGoogle ScholarPubMed
Haran, J., Timmermans, M.J.T.M. & Vogler, A.P. (2013) Mitogenome sequences stabilize the phylogenetics of weevils (Curculionoidea) and establish the monophyly of larval ectophagy. Molecular Phylogenetics and Evolution 67, 156166.Google Scholar
Harpending, H.C. (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66, 591600.Google Scholar
Hasegawa, M., Kishino, H. & Yano, T. (1985) Dating of human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160174.CrossRefGoogle ScholarPubMed
Hayashikawa, S. (1999) Recent damage for Chinese milk vetch by alfalfa weevil in Kagoshima Prefecture. Plant Protection 53, 419422 (in Japanese).Google Scholar
Heled, J. & Drummond, A.J. (2008) Bayesian inference of population size history from multiple loci. BMC Evolutionary Biology 8, 289.Google Scholar
Holden, P.R., Brookfield, J.F.Y. & Jones, P. (1993) Cloning and characterization of an ftsZ homologue from a bacterial symbiont of Drosophila melanogaster . Molecular and General Genetics 240, 213220.CrossRefGoogle ScholarPubMed
Horowitz, A.R., Kontsedalov, S., Khasdan, V. & Ishaaya, I. (2005) Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Archives of Insect Biochemistry and Physiology 58, 216225.Google Scholar
Hsiao, T.H. (1993) Geographic and genetic variation among alfalfa weevil strains. pp. 311327 in Kim, K.C. & McPheron, B.A. (Eds) Evolution of Insect Pests: Patterns of Variation. New York, John Wiley & Sons Inc.Google Scholar
Hsiao, T.H. (1996) Studies of interactions between alfalfa weevil strains, Wolbachia endosymbionts and parasitoids. pp. 5771 in Symondson, W.O.C. & Liddell, J.E. (Eds) The Ecology of Agricultural Pests: Biochemical Approaches. London, Chapman & Hall.Google Scholar
Hsiao, T.H. & Hsiao, C. (1985) Hybridization and cytoplasmic incompatibility among alfalfa weevil strains. Entomologia Experimentalis et Applicata 37, 155159.Google Scholar
Kato, K. (1989) Status of emergence of the alfalfa weevil. Kyushu Plant Control 505, 7 (in Japanese).Google Scholar
Kauwe, J.S.K., Shiozawa, D.K. & Evans, R.P. (2004) Phylogeographic and nested clade analysis of the stonefly Pteronarcys californica (Plecoptera: Pteronarcyidae) in the western USA. Journal of the North American Benthological Society 23, 824838.2.0.CO;2>CrossRefGoogle Scholar
Kimura, H. & Kaku, K. (1991) Rearing and release of imported parasitoids of the alfalfa weevil. Hypera postica. Plant Protection 45, 5054 (in Japanese).Google Scholar
Kimura, H., Okumura, M. & Yoshida, T. (1988) Emergence of and recent damage by the alfalfa weevil. Plant Protection 42, 498501 (in Japanese).Google Scholar
Kondo, N.I., Tuda, M., Toquenaga, Y., Lan, Y.-C., Buranapanichpan, S., Horng, S.-B., Shimada, M. & Fukatsu, T. (2011) Wolbachia infections in world populations of bean beetles (Coleoptera: Chrysomelidae: Bruchinae) infesting cultivated and wild legumes. Zoological Science 28, 501508.Google Scholar
Kuwata, R., Tokuda, M., Yamaguchi, D. & Yukawa, J. (2005) Coexistence of two mitochondrial DNA haplotypes in Japanese populations of Hypera postica (Col., Curculionidae). Journal of Applied Entomology 129, 191197.Google Scholar
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.Google Scholar
Manglitz, G.R., Klostermeyer, L.E. & Keith, D.L. (1981) Comparisons of eastern and western strains of the alfalfa weevil in Nebraska. Journal of Economic Entomology 74, 581588.Google Scholar
Mardulyn, P., Othmezouri, N., Mikhailov, Y.E. & Pasteels, J.M. (2011) Conflicting mitochondrial and nuclear phylogeographic signals and evolution of host-plant shifts in the boreo-montane leaf beetle Chrysomela lapponica . Molecular Phylogenetics and Evolution 61, 686696.CrossRefGoogle ScholarPubMed
Maund, C.M. & Hsiao, T.H. (1991) Differential encapsulation of two Bathyplectes parasitoids among alfalfa weevil strains, Hypera postica (Gyllenhal). The Canadian Entomologist 123, 197203.CrossRefGoogle Scholar
Morimoto, K. (1987) Alfalfa weevil that established in Japan. Kankyo Kanri Gijutsu 5, 13 (in Japanese).Google Scholar
Newton, J.H. (1933) The alfalfa weevil in Colorado. Colorado Agricultural Experimental Station, Bulletin 399, 19.Google Scholar
Nylander, J.A.A. (2004) MrAIC.pl. Program Distributed by the Author. Uppsala, Evolutionary Biology Centre, Uppsala Univ.Google Scholar
Okumura, M. (1991) Alfalfa weevil (Hypera postica) – a serious pest of Chinese milk vetch. Honeybee Science 12, 145150 (in Japanese).Google Scholar
Okumura, M. & Shiraishi, A. (2002) Establishment of the alfalfa weevil parasitoid and its potential for biological control. Plant Protection 56, 329333 (in Japanese).Google Scholar
Papadopoulou, A., Anastasiou, I. & Vogler, A.P. (2010) Revisiting the insect mitochondrial molecular clock: the mid-aegean trench calibration. Molecular Biology and Evolution 27, 16591672.Google Scholar
Pfenninger, M. & Posada, D. (2002) Phylogeographic history of the land snail Candidual unifasciata (Helicellinae: Stylommatophora): fragmentation, corridor migration, and secondary contact. Evolution 56, 17761788.Google Scholar
Pienkowski, R.L., Hsieh, F.K. & LeCato, G.L. III. (1969) Sexual dimorphism and morphometric differences in the eastern, western, and Egyptian alfalfa weevils. Annals of the Entomological Society of America 62, 12681269.CrossRefGoogle Scholar
Radcliffe, E.B. & Flanders, K.L. (1998) Biological control of alfalfa weevil in North America. Integrated Pest Management Reviews 3, 225242.CrossRefGoogle Scholar
Ramos-Onsins, S.E. & Rozas, J. (2002) Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19, 20922100.CrossRefGoogle ScholarPubMed
Rauch, N. & Nauen, R. (2003) Identification of biochemical markers linked to neonicotinoid cross resistance in Bemicia tabaci (Hemiptera: Aleyrodidae). Archives of Insect Biochemistry and Physiology 54, 165176.CrossRefGoogle Scholar
Rogers, A.R. (1995) Genetic evidence for a pleistocene population explosion. Evolution 49, 608615.Google Scholar
Rogers, A.R. & Harpending, H. (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552569.Google Scholar
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721573.Google Scholar
Rubidge, E.M., Patton, J.L., Lim, M., Burton, A.C., Brashares, J.S. & Moritz, C. (2012) Climate-induced range contraction drives genetic erosion in an alpine mammal. Nature Climate Change 2, 285288.CrossRefGoogle Scholar
Sakurai, H., Yamada, Y., Iwatsuki, N. & Inoue, A. (1997) Life cycle and flight activity of the alfalfa weevil, Hypera postica . Research bulletin of the Faculty College of Agriculture Gifu University 62, 2331 (in Japanese).Google Scholar
Shoubu, M., Okumura, M., Shiraishi, A., Kimura, H., Takagi, M. & Ueno, T. (2005) Establishment of Bathyplectes anurus (Hymenoptera: Ichneumonidae), a larval parasitoid of the alfalfa weevil, Hypera postica (Coleoptera: Curculionidae) in Japan. Biological Control 34, 144151.CrossRefGoogle Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651701.Google Scholar
Tajima, F. (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437460.CrossRefGoogle ScholarPubMed
Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.Google ScholarPubMed
Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619633.Google Scholar
Tuda, M., Wasano, N., Kondo, N., Horng, S.-B., Chou, L.-Y. & Tateishi, Y. (2004) Habitat-related mtDNA polymorphism in the stored-bean pest Callosobruchus chinensis (Coleoptera: Bruchidae). Bulletin of Entomological Research 94, 7580.Google Scholar
Tuda, M., Ronn, J., Buranapanichpan, S., Wasano, N. & Arnqvist, G. (2006) Evolutionary diversification of the bean beetle genus Callosobruchus (Coleoptera: Bruchidae): traits associated with stored-product pest status. Molecular Ecology 15, 35413551.Google Scholar
Turelli, M. & Hoffmann, A.A. (1991) Rapid spread of an inherited incompatibility factor in California Drosophila . Nature 353, 440442.Google Scholar
Utsumi, K. (1989) Expansion of areas of emergence of the alfalfa weevil. Kobe Plant Protection Information 854, 44 (in Japanese).Google Scholar
White, C.E., Armbrust, E.J. & Ashley, J. (1972) Cross-mating studies of eastern and western strains of alfalfa weevil. Journal of Economic Entomology 65, 8589.Google Scholar
Wood, K.A., Armbrust, E.J., Bartell, D.P. & Irwin, B.J. (1978) The literature of arthropods associated with alfalfa. V. A bibliography of the alfalfa weevil, Hypera postica (Gyllenhal), and the Egyptian alfalfa weevil, Hypera brunneipennis (Boheman) (Coleoptera: Curculionidae). Illinois Agricultural Experimental Station, Special Publication 54.Google Scholar
Yamaguchi, D., Kamitani, S., Tadauchi, O. & Yukawa, J. (2006) Adult behavior of Hypera postica (Coleoptera: Curculionidae) during the period from the time of emergence in the field of Astragalus sinicus (Fabaceae) to the time of recolonization of the field after aestivation. Science Bulletin of Faculty of Agriculture, Kyushu University 61, 7782.Google Scholar