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Deep divergence and evidence for translocations between Iranian and European populations of the alfalfa weevil (Coleoptera: Curculionidae) based on mitochondrial DNA

Published online by Cambridge University Press:  13 June 2016

E. Sanaei
Department of Applied Biology, College of Agriculture & Life Sciences, Chonnam National University, Gwangju, Republic of Korea School of Biology and Center of Excellence in Phylogeny of Living Organisms, College of Science, University of Tehran, Tehran, Iran
M. Seiedy*
School of Biology and Center of Excellence in Phylogeny of Living Organisms, College of Science, University of Tehran, Tehran, Iran
J. Skuhrovec
Group Function of Invertebrate and Plant Biodiversity in Agrosystems, Crop Research Institute, Prague, Czech Republic
M.A. Mazur
Department of Biosystematics, Center for Biodiversity Studies, Opole University, Opole, Poland
Ł. Kajtoch
Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Krakow, Poland
M. Husemann
General Zoology, Martin-Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany
1Corresponding author (e-mail:


The alfalfa weevil (Hypera postica (Gyllenhal): Coleoptera: Curculionidae) is an invasive pest of alfalfa (Medicago sativa Linnaeus; Fabaceae) in the Holarctic region. Across the wide geographic distribution of the species different local adaptions have been observed. Further, several distinct mitochondrial lineages have been discovered, which have been treated as western and Egyptian/eastern strains. However, our knowledge of the biogeography of H. postica is largely limited to North American and Japanese populations. We sampled the species from four locations in Iran and two countries in Europe (Poland and Czech Republic) and sequenced the mitochondrial COI gene to detect patterns of mitochondrial DNA divergence among Iranian and European strains. We detected two groups separated by a deep molecular split, even justifying the distinction of two molecular operational taxonomic units. Joint analyses with previously published sequences suggest that the European samples may represent the western strain, whereas both the western and Egyptian/eastern strains can be found in Iran. This distribution of genetic lineages may be the result of human-mediated translocations. The directionality, however, cannot be inferred. Our data suggest that translocations may have led to the coexistence of multiple H. postica lineages in some parts of the world, e.g., Iran. We discuss these findings against the background of the current taxonomy of H. postica.

Biodiversity & Evolution
© Entomological Society of Canada 2016 

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Bandelt, H.J., Forster, P., and Röhl, A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16: 3748.CrossRefGoogle ScholarPubMed
Bilgin, R. 2011. Back to the suture: the distribution of intraspecific genetic diversity in and around Anatolia. International Journal of Molecular Sciences, 12: 40804103.CrossRefGoogle ScholarPubMed
Bland, R. 1984. Mouthpart sensilla and mandibles of the adult alfalfa weevil Hypera postica and the Egyptian alfalfa weevil H. brunneipennis (Coleoptera: Curculionidae). Annals of the Entomological Society of America, 77: 720724.CrossRefGoogle Scholar
Böttger, J.A.A., Bundy, C.S., Oesterle, N., and Hanson, S.F. 2013. Phylogenetic analysis of the alfalfa weevil complex (Coleoptera: Curculionidae) in North America. Journal of Economic Entomology, 106: 426436.CrossRefGoogle Scholar
Bundy, C.S., Smith, P.F., English, L.M., Sutton, D., and Hanson, S. 2005. Strain distribution of alfalfa weevil (Coleoptera: Curculionidae) in an intergrade zone. Journal of Economic Entomology, 98: 20282032.CrossRefGoogle Scholar
Chandra, A. 2009. Screening global Medicago germplasm for weevil (Hypera postica Gyll.) tolerance and estimation of genetic variability using molecular markers. Euphytica, 169: 363374.CrossRefGoogle Scholar
Chandra, A. and Pandey, K.C. 2011. Assessment of genetic variation in lucerne (Medicago sativa L.) using protease inhibitor activities and RAPD markers. Journal of Enviromental Biology, 32: 559565.Google ScholarPubMed
Coles, L. and Day, W. 1977. The fecundity of Hypera postica from three locations in the eastern United States. Environmental Entomology, 6: 211212.CrossRefGoogle Scholar
Coskuncu, K.S. and Gencer, N.S. 2010. Determination of the species of Curculionoidea superfamily on alfalfa fields (Medicago sativa L.) and their distribution in Bursa province of Turkey. Journal of Biology and Enviromental Science, 4: 123131.Google Scholar
Croll, D., Wille, L., Gamper, H.A., Mathimaran, N., Lammers, P.J., Corradi, N., and Sanders, I.R. 2008. Genetic diversity and host plant preferences revealed by simple sequence repeat and mitochondrial markers in a population of the arbuscular mycorrhizal fungus Glomus intraradices . New Phytologist, 178: 672687.CrossRefGoogle Scholar
Dalmon, A., Halkett, F., Granier, M., Delatte, H., and Peterschmitt, M. 2008. Genetic structure of the invasive pest Bemisia tabaci: evidence of limited but persistent genetic differentiation in glasshouse populations. Heredity, 100: 316325.CrossRefGoogle ScholarPubMed
Dewitt, J.R. and Armbrust, E.J. 1972. Photoperiodic sensitivity of the alfalfa weevil during larval development. Journal of Economic Entomology, 65: 12891292.CrossRefGoogle Scholar
Drummond, A. J., Suchard, M.A., Xie, D., and Rambaut, A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29: 19691973.CrossRefGoogle ScholarPubMed
Erney, S., Pruess, K., Danielson, S., and Powers, T. 1996. Molecular differentiation of alfalfa weevil strains (Coleoptera: Curculionidae). Annals of the Entomological Society of America, 89: 804811.CrossRefGoogle Scholar
Excoffier, L. and Lischer, H. 2010. ARLEQUIN version 3.5. 1.2 user manual. Computational and Molecular Population Genetics Laboratory, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland.Google Scholar
Ferrari, J., Müller, C.B., Kraaijeveld, A.R., and Godfray, H.C.J. 2001. Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution, 55: 18051814.CrossRefGoogle Scholar
Galtier, N., Nabholz, B., Glémin, S., and Hurst, G. 2009. Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology, 18: 45414550.CrossRefGoogle ScholarPubMed
Gotoh, T., Bruin, J., Sabelis, M., and Menken, S. 1993. Host race formation in Tetranychus urticae: genetic differentiation, host plant preference, and mate choice in a tomato and a cucumber strain. Entomologia Experimentalis et Applicata, 68: 171178.CrossRefGoogle Scholar
Gould, F. 1991. The evolutionary potential of crop pests. American Scientist, 79: 496507.Google Scholar
Gould, F., Kennedy, G., and Johnson, M. 1991. Effects of natural enemies on the rate of herbivore adaptation to resistant host plants. Entomologia Experimentalis et Applicata, 58: 114.CrossRefGoogle Scholar
Gould, F. and Schliekelman, P. 2004. Population genetics of autocidal control and strain replacement. Annual Reviews in Entomology, 49: 193217.CrossRefGoogle ScholarPubMed
Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 9598.Google Scholar
Hebert, P.D., Ratnasingham, S., and de Waard, J.R. 2003. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London B: Biological Sciences, 270: S96S99.CrossRefGoogle ScholarPubMed
Herczeg, G., Gonda, A., and Merilä, J. 2009. Predation mediated population divergence in complex behaviour of nine‐spined stickleback (Pungitius pungitius). Journal of Evolutionary Biology, 22: 544552.CrossRefGoogle Scholar
Hewitt, G.M. 1999. Post‐glacial re‐colonization of European biota. Biological Journal of the Linnean Society, 68: 87112.CrossRefGoogle Scholar
Hsiao, T.H. 1993. Geographic and genetic variation among alfalfa weevil strains. In Evolution of insect pests: patterns of variation. Edited by K.C. Kim and B.A. McPheron. John Wiley & Sons, New York, New York, United States of America. Pp. 310328.Google Scholar
Hsiao, T.H. 1996. Studies of interactions between alfalfa weevil strains, Wolbachia endosymbionts and parasitoids. In The ecology of agriculture pests. Edited by W.O.C. Symondson and J.E. Liddel. Chapman & Hall, London, United Kingdom. Pp. 5172.Google Scholar
Hsiao, T.H. and Hsiao, C. 1985. Hybridization and cytoplasmic incompatibility among alfalfa weevil strains. Entomologia Experimentalis et Applicata, 37: 155159.CrossRefGoogle Scholar
Husemann, M., Ray, J.W., King, R.S., Hooser, E.A., and Danley, P.D. 2012. Comparative biogeography reveals differences in population genetic structure of five species of stream fishes. Biological Journal of Linnean Society, 107: 867885.CrossRefGoogle Scholar
Huson, D.H. and Bryant, D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23: 254267.CrossRefGoogle ScholarPubMed
International Commission on Zoological Nomenclature. 1999. International Code of Zoological nomenclature. International Trust for Zoological Nomenclature, London, United Kingdom.Google Scholar
Iwase, S.I., Nakahira, K., Tuda, M., Kagoshima, K., and Takagi, M. 2015a. Host-plant dependent population genetics of the invading weevil Hypera postica . Bulletin of Entomological Research, 105: 92100.CrossRefGoogle ScholarPubMed
Iwase, S.I., Tani, S., Saeki, Y., Tuda, M., Haran, J., Skuhrovec, J., and Takagi, M. 2015b. Dynamics of infection with Wolbachia in Hypera postica (Coleoptera: Curculionidae) during invasion and establishment. Biological Invasions, 17: 36393648.CrossRefGoogle Scholar
Kajtoch, Ł., Korotyaev, B., and Lachowska‐Cierlik, D. 2012. Genetic distinctness of parthenogenetic forms of European Polydrusus weevils of the subgenus Scythodrusus . Insect Science, 19: 183194.CrossRefGoogle Scholar
Kajtoch, Ł., Kubisz, D., Gutowski, J.M., and Babik, W. 2014. Evolutionary units of Coraebus elatus (Coleoptera: Buprestidae) in central and eastern Europe–implications for origin and conservation. Insect Conservation and Diversity, 71: 4154.CrossRefGoogle Scholar
Khanjani, M. 2012. Field crop pests in Iran (insects and mites), 6th edition. Bu-Ali Sina University Publication, Hamedan, Iran.Google Scholar
Khanjani, M. and Pourmirza, A.A. 2004. A comparison of various control methods of alfalfa weevil, Hypera postica (Col: Curculionidae) in Hamadan. Journal of Entomological Society of Iran, 24: 6781.Google Scholar
Kuwata, R., Tokuda, M., Yamaguchi, D., and Yukawa, J. 2005. Coexistence of two mitochondrial DNA haplotypes in Japanese populations of Hypera postica (Col., Curculionidae). Journal of Applied Entomology, 129: 191197.CrossRefGoogle Scholar
Librado, P. and Rozas, J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25: 14511452.CrossRefGoogle ScholarPubMed
Litsinger, J.A. and Apple, J.W. 1973. Oviposition of the alfalfa weevil in Wisconsin. Annals of the Entomological Society of America, 66: 1720.CrossRefGoogle Scholar
Martinsen, L., Venanzetti, F., and Bachmann, L. 2009. Phylogeography and mitochondrial DNA divergence in Dolichopoda cave crickets (Orthoptera, Rhahidophoridae). Hereditas, 146: 3345.CrossRefGoogle Scholar
Mayr, E. and Ashlock, P.D. 1991. Principles of systematic zoology. McGraw-Hill, New York, New York, United States of America.Google Scholar
Miller, M., Pfeiffer, W., and Schwartz, T. 2010. Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings Gateway computing environments workshop, 14 Nov. 2010, IEEE, New Orleans, LA. pp. 1–8.Google Scholar
Montazar, A. and Sadeghi, M. 2008. Effects of applied water and sprinkler irrigation uniformity on alfalfa growth and hay yield. Agricultural Water Management, 95: 12791287.CrossRefGoogle Scholar
Moradi-Vajargah, M., Golizadeh, A., Rafiee-Dastjerdi, H., Zalucki, M.P., Hassanpour, M., and Naseri, B. 2011. Population density and spatial distribution pattern of Hypera postica (Coleoptera: Curculionidae) in Ardabil, Iran. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 39: 4248.CrossRefGoogle Scholar
Mutun, S. 2010. Intraspecific genetic variation and phylogeography of the oak gallwasp Andricus caputmedusae (Hymenoptera: Cynipidae): effects of the Anatolian diagonal. Acta Zoologica Academiae Scientiarum Hungaricae, 56: 153172.Google Scholar
Myers, N., Mittermeier, R.A., Mittermeier, C.G., Da Fonseca, G.A., and Kent, J. 2000. Biodiversity hotspots for conservation priorities. Nature, 403: 853858.CrossRefGoogle ScholarPubMed
Nylander, J. 2004. MrModeltest v2. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.Google Scholar
Olden, J.D., Poff, N.L., Douglas, M.R., Douglas, M. E., and Fausch, K.D. 2004. Ecological and evolutionary consequences of biotic homogenization. Trends in Ecology and Evolution, 19: 1824.CrossRefGoogle ScholarPubMed
Oliver, C.J. 2006. Population genetic effects of human‐mediated plant range expansions on native phytophagous insects. Oikos, 112: 456463.CrossRefGoogle Scholar
Pienkowski, R.L., Hsieh, F.-K., and Lecato, G.L. 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
Pons, J., Fujisawa, T., Claridge, E.M., Savill, R.A., Barraclough, T.G., and Vogler, A.P. 2011. Deep mtDNA subdivision within Linnean species in an endemic radiation of tiger beetles from New Zealand (genus Neocicindela). Molecular Phylogenetics and Evolution, 59: 251262.CrossRefGoogle Scholar
Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G. 2012. ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology, 21: 18641877.CrossRefGoogle ScholarPubMed
Radcliffe, E.B. and Flanders, K.L. 1998. Biological control of alfalfa weevil in North America. Integrated Pest Management Reviews, 3: 225242.CrossRefGoogle Scholar
Rambaut, A. and Drummond, A. 2010. FigTree v1. 3.1. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom.Google Scholar
Rauch, N. and Nauen, R. 2003. Identification of biochemical markers linked to neonicotinoid cross resistance in Bemisia tabaci (Hemiptera: Aleyrodidae). Archives of Insect Biochemistry and Physiology, 54: 165176.CrossRefGoogle Scholar
Ronquist, F. and Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 15721574.CrossRefGoogle ScholarPubMed
Salvaudon, L., Giraud, T., and Shykoff, J.A. 2008. Genetic diversity in natural populations: a fundamental component of plant–microbe interactions. Current Opinion in Plant Biology, 11: 135143.CrossRefGoogle ScholarPubMed
Sanaei, E. and Seiedy, M. In press. Developmental differences of local populations of the alfalfa weevils’s (Hypera postica) (Coleoptera: Curculionidae). Turkish Journal of Zoology. doi:10.3906/zoo-1506-7.Google Scholar
Sanaei, E., Seiedy, M., and Momtazi, F. 2015a. A uni- and multivariate analysis approch revealed sexual size dimorphism in Iranian populations of Hypera postica (Coleoptera: Curculionidae). Biologia, 70: 12281233.Google Scholar
Sanaei, E., Seiedy, M., and Momtazi, F. 2015b. Evolutionary view on sexual dimorphism and shape variation in Iranian populations of Hypera postica (Coleoptera: Curculionidae). Zoomorphology, 134: 451552.CrossRefGoogle Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., and 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.CrossRefGoogle Scholar
Skuhrovec, J. 2005. Živné rostliny nosatců rodu Hypera (Coleoptera: Curculionidae) vyskytujících se na území České republiky. [Host plants of weevils of the genus Hypera (Coleoptera: Curculionidae) occuring in the Czech Republic]. Klapalekiana, 41: 215255.Google Scholar
Skuhrovec, J. 2009. Digital-weevil-determination for Curculionoidea of west Palaearctic. Transalpina: Hypera/Limobius/Metadonus (Hyperinae: Hyperini). In Snudebiller 10, studies on taxonomy, biology and ecology of Curculionoidea. CURCULIO-Institute, Mönchengladbach, Germany. Pp. 3947.Google Scholar
Skuhrovec, J. 2013. Hyperinae. In Catalogue of Palaearctic Coleoptera. Edited by I. Löbl and A. Smetana. Apollo Books, Stenstrup, Denmark. Pp. 9396.Google Scholar
Song, H., Buhay, J.E., Whiting, M.F., and Crandall, K.A. 2008. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences, 105: 1348613491.CrossRefGoogle ScholarPubMed
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30: 13121313.CrossRefGoogle ScholarPubMed
Stockle, M.Y. and Hebert, P.D. 2008. Barcode of Life. Scientific American, 299: 8288.CrossRefGoogle Scholar
Summers, C.G. 1998. Integrated pest management in forage alfalfa. Integrated Pest Management Reviews, 3: 127154.CrossRefGoogle Scholar
Tabashnik, B.E., Carrière, Y., Dennehy, T.J., Morin, S., Sisterson, M.S., Roush, R.T., et al. 2003. Insect resistance to transgenic Bt crops: lessons from the laboratory and field. Journal of Economic Entomology, 96: 10311038.CrossRefGoogle Scholar
Telschow, A., Hammerstein, P., and Werren, J.H. 2002. The effect of Wolbachia on genetic divergence between populations: models with two‐way migration. The American Naturalist, 160: S54S66.Google ScholarPubMed
Thompson, J., Higgins, D., and Gibson, T. 1997. CLUSTAL X multiple sequence alignment program. European Molecular Biology Organization, Hamburg, Germany.Google Scholar
Titus, E. 1909. The alfalfa leaf-weevil. Journal of Economic Entomology, 2: 148154.CrossRefGoogle Scholar
Vervust, B., Grbac, I., and Van Damme, R. 2007. Differences in morphology, performance and behaviour between recently diverged populations of Podarcis sicula mirror differences in predation pressure. Oikos, 116: 13431352.CrossRefGoogle Scholar
Warner, R.E. 1962. The scientific name of the alfalfa weevil (Coleoptera: Curculionidae). The Coleopterists Bulletin, 16: 107108.Google Scholar
Werren, J.H. 1998. Wolbachia and speciation. In Endless forms: species and speciation. Edited by D.J. Howard and S.H. Berlocher. Oxford University Press, New York, New York, United States of America.Google Scholar
White, B.J., Lawniczak, M.K., Cheng, C., Coulibaly, M.B., Wilson, M.D., Sagnon, N.F., et al. 2011. Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium . Proceedings of the National Academy of Sciences, 108: 244249.CrossRefGoogle ScholarPubMed
Yardim, E.N., Yilmaz, I.H., Arvas, O., and Candan, C. 2006. Populations of alfalfa weevils (Coleoptera: Curculionidae) and aphids (Homoptera: Aphididae) on different alfalfa cultivars. Journal of Entomology, 3: 194197.Google Scholar
Živković, B., Radović, J., Sokolović, D., Šiler, B., Banjanac, T., and Štrbanović, R. 2012. Assessment of genetic diversity among alfalfa (Medicago sativa) genotypes by morphometry, seed storage proteins and RAPD analysis. Industrial Crops and Products, 40: 285291.CrossRefGoogle Scholar
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Deep divergence and evidence for translocations between Iranian and European populations of the alfalfa weevil (Coleoptera: Curculionidae) based on mitochondrial DNA
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Deep divergence and evidence for translocations between Iranian and European populations of the alfalfa weevil (Coleoptera: Curculionidae) based on mitochondrial DNA
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