Hostname: page-component-848d4c4894-p2v8j Total loading time: 0 Render date: 2024-04-30T10:54:24.351Z Has data issue: false hasContentIssue false
  • English
  • Français

High regional genetic diversity and lack of host-specificity in Ostrinia nubilalis (Lepidoptera: Crambidae) as revealed by mtDNA variation

Published online by Cambridge University Press:  28 March 2016

M. Piwczyński ,
M. Pabijan ,
A. Grzywacz ,
W. Glinkowski ,
P.K. Bereś  and
J. Buszko
M. Piwczyński*
Affiliation:
Chair of Ecology and Biogeography, Nicolaus Copernicus University in Toruń, Lwowska 1, PL-87-100 Toruń, Poland
M. Pabijan
Affiliation:
Department of Comparative Anatomy, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland
A. Grzywacz
Affiliation:
Chair of Ecology and Biogeography, Nicolaus Copernicus University in Toruń, Lwowska 1, PL-87-100 Toruń, Poland
W. Glinkowski
Affiliation:
Chair of Ecology and Biogeography, Nicolaus Copernicus University in Toruń, Lwowska 1, PL-87-100 Toruń, Poland
P.K. Bereś
Affiliation:
Institute of Plant Protection – National Research Institute, Regional Experimental Station, Langiewicza 28, 35-101 Rzeszów, Poland
J. Buszko
Affiliation:
Chair of Ecology and Biogeography, Nicolaus Copernicus University in Toruń, Lwowska 1, PL-87-100 Toruń, Poland
*
*Author for correspondence Phone: +48 56 611 26 49 Fax: +48 56 611 44 43 E-mail: piwczyn@umk.pl
Get access Rights & Permissions [Opens in a new window]

Abstract

The European corn borer (Ostrinia nubilalis) infests a wide array of host plants and is considered one of the most serious pests of maize in Europe. Recent studies suggest that individuals feeding on maize in Europe should be referred to O. nubilalis (sensu nov.), while those infesting dicots as Ostrinia scapulalis (sensu nov.). We test if the clear genetic distinctiveness among individuals of O. nubilalis living on maize vs. dicots is tracked by mitochondrial DNA (mtDNA). We used fragments of COI and COII genes of 32 individuals traditionally recognized as O. nubilalis collected on three host plants, maize, mugwort and hop, growing in different parts of Poland. In addition, we reconstructed the mtDNA phylogeny of Ostrinia species based on our data and sequences retrieved from GenBank to assess host and/or biogeographic patterns. We also compared haplotype variation found in Poland (east-central Europe) with other regions (Anatolia, Eastern Europe, Balkans, Far East, North America). Our study showed high mtDNA diversity of O. nubilalis in Poland in comparison with other regions and revealed rare haplotypes likely of Asian origin. We did not find distinct mtDNA haplotypes in larvae feeding on maize vs. dicotyledonous plants. Phylogenetic analyses showed an apparent lack of mtDNA divergence among putatively distinct lineages belonging to the O. nubilalis group as identical haplotypes are shared by Asian and European individuals. We argue that human-mediated dispersal, hybridization and sporadic host jumps are likely responsible for the lack of a geographic pattern in mtDNA variation.

Keywords

COICOIIEuropean corn borergenealogical sorting index (gsi)nucleotide diversity (π)Ostrinia scapulalis
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 4 , August 2016 , pp. 512 - 521
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bandelt, H.J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Bereś, P.K. & Konefał, T. (2010) Distribution range of the European corn borer (Ostrinia nubilalis Hbn.) on maize in 2004–2008 in Poland. Journal of Plant Protection Research 50, 326–334.CrossRefGoogle Scholar
Bethenod, M., Thomas, Y., Rousset, F., Frérot, B., Pélozuelo, L., Genestier, G. & Bourguet, D. (2005) Genetic isolation between two sympatric host plant races of the European corn borer, Ostrinia nubilalis Hubner. II: assortative mating and host-plant preferences for oviposition. Heredity 94, 264–270.CrossRefGoogle ScholarPubMed
Bourguet, D., Ponsard, S., Streiff, R., Meusnier, S., Audiot, P., Li, J. & Wang, Z.Y. (2014) ‘Becoming a species by becoming a pest’ or how two maize pests of the genus Ostrinia possibly evolved through parallel ecological speciation events. Molecular Ecology 23, 325–342.CrossRefGoogle ScholarPubMed
Büttner, F.O. (1880) Die Pommerschen, insbesondere die Stettiner Microlepidopteren. Stettiner Entomologische Zeitung 41, 383–473.Google Scholar
Calcagno, V., Thomas, Y. & Bourguet, D. (2007) Sympatric host races of the European corn borer: adaptation to host plants and hybrid performance. Journal of Evolutionary Biology 20, 1720–1729.CrossRefGoogle ScholarPubMed
Clark, A.G. (1997) Neutral behavior of shared polymorphism. Proceedings of the National Academy of Sciences 94, 7730–7734.CrossRefGoogle ScholarPubMed
Coates, B., Sumerford, D.V. & Hellmich, R.L. (2004) Geographic and voltinism differentiation among North American Ostrinia nubilalis (European corn borer) mitochondrial cytochrome c oxidase haplotypes. Journal of Insect Science 4, 35.CrossRefGoogle ScholarPubMed
Cummings, M.P., Neel, M.C. & Shaw, K.L. (2008) A genealogical approach to quantifying lineage divergence. Evolution 62, 2411–2422.CrossRefGoogle ScholarPubMed
Darriba, D., Taboada, G., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Dopman, E.B., Pérez, L., Bogdanowicz, S.M. & Harrison, R.G. (2005) Consequences of reproductive barriers for genealogical discordance in the European corn borer. Proceedings of the National Academy of Sciences 102, 14706–14711.CrossRefGoogle ScholarPubMed
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Frolov, A.N. (1981) Geneticheskij analiz ‘krupnoj’ goleni – taksonomicheskogo priznaka shhetkonogogo motylka Ostrinia scapulalis Wlk. (Lepidoptera, Pyraustidae). Genetika 17, 2160–2166.Google Scholar
Frolov, A.N. (1984) Biotaksonomicheskij analiz wrednych vidov roda Ostrinia Hbn. Etologia Nasekomyh, Trudy Vsesoyuznogo Entomologitsheskogo Obshchestva 66, 4–100.Google Scholar
Frolov, A.N., Bourguet, D. & Ponsard, S. (2007) Reconsidering the taxonomy of several Ostrinia species in the light of reproductive isolation: a tale for E. Mayr. Biological Journal of the Linnean Society 91, 49–72.CrossRefGoogle Scholar
Frolov, A.N., Audiot, P., Bourguet, D., Kononchuk, A.G., Malysh, J.M., Ponsard, S., Streiff, R. & Tokarev, Y.S. (2012) From Russia with lobe: genetic differentiation in trilobed uncus Ostrinia spp. follows food plant, not hairy legs. Heredity 108, 147–156.CrossRefGoogle Scholar
Funk, D.J. & Omland, K.E. (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics 34, 397–423.CrossRefGoogle Scholar
Gouy, M., Guindon, S. & Gascuel, O. (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221–224.CrossRefGoogle ScholarPubMed
Guindon, S. & Gascuel, O. (2003) PhyML: a simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Hoshizaki, S., Washimori, R., Kubota, S., Frolov, A.N., Kageyama, D., Gomboc, S., Ohno, S., Tatsuki, S. & Ishikawa, Y. (2008) Limited variation in mitochondrial DNA of maize-associated Ostrinia nubilalis (Lepidoptera: Crambidae) in Russia, Turkey and Slovenia. European Journal of Entomology 105, 545–552.CrossRefGoogle Scholar
Huelsenbeck, J.P. & Rannala, B. (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology 53, 904–913.CrossRefGoogle ScholarPubMed
Judenko, E. (1938) Badania nad omacnica prosowianka (Pyrausta nubilalis Hbn.) w zwiazku z jej zerowaniem na chmielu (Humulus lupulus L.) i prosie (Panicum miliaceum L.). Prace Wydzialu Chorob i Szkodnikow Roslin 17, 19–122.Google Scholar
Kageyama, D., Nishimura, G., Ohno, S., Takanashi, T., Hoshizaki, S. & Ishikawa, Y. (2004) Wolbachia infection and an allfemale trait in Ostrinia orientalis and Ostrinia zaguliaevi (Lepidoptera: Crambidae). Entomologia Experimentalis et Applicata 111, 79–83.CrossRefGoogle Scholar
Kalinowski, S.T. (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conservation Genetics 5, 539–543.Google Scholar
Kania, C. (1966) Badania nad omacnicą prosowianką – Ostrinia nubilalis (Hbn.) (Lep., Pyralidae) na kukurydzy w warunkach południowo-zachodniej Polski. [Investigations on the European corn borer – Ostrinia nubilalis (Hbn.) (Lep., Pyralidae) in maize in conditions of south-west Poland]. Polskie Pismo Entomologiczne 3–4, 191–243.Google Scholar
Karpova, A.I. (1959) Razvitie i kormovye sviazi steblevogo motylka Pyrausta nubilalis (Lepidoptera, Pyralidae) v novyh rajonach vozdelyvanija kukuruzy. Entomologicheskoye Obozrenie 38, 724–733.Google Scholar
Kim, C.G., Hoshizaki, S., Huang, Y., Tatsuki, S. & Ishikawa, Y. (1999) Usefulness of mitochondrial COII gene sequences in examining phylogenetic relationships in the Asian corn borer, Ostrinia furnacalis, and allied species (Lepidoptera: Pyralidae). Applied Entomology and Zoology 34, 405–412.CrossRefGoogle Scholar
Librado, P. & Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
Lisowicz, F. & Tekiela, A. (2004) Szkodniki i choroby kukurydzy oraz ich zwalczanie [Pests and diseases of maize and their control]. pp. 52–64 in Dubas, A. (Ed.) Technologia Produkcji Kukurydzy [Maize Production Technology]. Wieś Jutra, Warsaw [in Polish].Google Scholar
Liu, H. & Beckenbach, A.T. (1992) Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects. Molecular Phylogenetics and Evolution 1, 41–52.CrossRefGoogle ScholarPubMed
Martel, C., Réjasse, A., Rousset, F., Bethenod, M.-T. & Bourguet, D. (2003) Host-plant-associated genetic differentiation in northern French populations of the European corn borer. Heredity 90, 141–149.CrossRefGoogle ScholarPubMed
Meissle, M., Mouron, P., Musa, T., Bigler, F., Pons, X., Vasileiadis, V.P., Otto, S., Antichi, D., Kiss, J., Pálinkás, Z., Dorner, Z., Van Der Weide, R., Groten, J., Czembor, E., Adamczyk, J., Thibord, B., Melander, G., Nielsen, C., Poulsen, R.T., Zimmermann, O., Verschwele, A. & Oldenburg, E. (2010) Pests, pesticide use and alternative options in European maize production: current status and future prospects. Journal of Applied Entomology 134, 357–375.CrossRefGoogle Scholar
Mutuura, A. & Munroe, E. (1970) Taxonomy and distribution of the European corn borer and allied species: genus Ostrinia (Lepidoptera: Pyralidae). Memoirs of the Entomological Society of Canada 102, 1–112.CrossRefGoogle Scholar
Pabijan, M. & Babik, W. (2006). Genetic structure in northeastern populations of the Alpine newt (Triturus alpestris): evidence for post-Pleistocene differentiation. Molecular Ecology 15, 2397–2407.CrossRefGoogle ScholarPubMed
Pélozuelo, L., Meusnier, S., Audiot, P., Bourguet, D. & Ponsard, S. (2007) Sex pheromones are for meeting not for mating. PLoS ONE 2, e555.Google Scholar
Piwczyński, M., Szpila, K., Grzywacz, A. & Pape, T. (2014) A large-scale molecular phylogeny of flesh flies (Diptera: Sarcophagidae). Systematic Entomology 39, 783–799.CrossRefGoogle Scholar
Ratnasingham, S. & Hebert, P.D.N. (2007) BOLD: the barcode of life data system (www.barcodinglife.org). Molecular Ecology Notes 7, 355–364.CrossRefGoogle ScholarPubMed
Romaniszyn, J. & Schille, F. (1930) Fauna motyli Polski (Fauna Lepidopterorum Poloniae), Vol. VII. Polska Akademija Umiejętności, Kraków, Poland.Google Scholar
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian MCMC inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Thompson, W.R. & Parker, H.L. (1928) The European corn borer and its controlling factors in Europe. United States Department of Agriculture Technical Bulletin 59, 62.Google Scholar
Toews, D.P.L. & Brelsford, A. (2012) The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 16, 3907–4030.CrossRefGoogle Scholar
Vigouroux, Y., Barnaud, A., Scarcelli, N. & Thuillet, A.C. (2011) Biodiversity, evolution and adaptation of cultivated crops. Comptes Rendus Biologies 334, 450–457.CrossRefGoogle ScholarPubMed
Wiemers, M., Stradomsky, B.V. & Vodolazhsky, D.I. (2010) A molecular phylogeny of Polyommatus s. str. and Plebicula based on mitochondrial COI and nuclear ITS2 sequences (Lepidoptera: Lycaenidae). European Journal of Entomology 107, 325–336.CrossRefGoogle Scholar
Wocke, M.F. (1874) Verzeichniss der Falter Schlesiens. Zeitschrift für Entomologie 4, 4.Google Scholar
Zhou, C., Chen, X. & He, R. (2012) COII phylogeography reveals surprising divergencies within the cryptic butterfly Kallima inachus (Doyére, 1840) (Lepidoptera: Nymphalidae: Kallimini) in southeastern Asia. Pan-Pacific Entomologist 88, 381–398.Google Scholar
Supplementary material: File

Piwczyński supplementary material

Table S1

Download Piwczyński supplementary material(File)
File 73.7 KB
Supplementary material: File

Piwczyński supplementary material

Table S2

Download Piwczyński supplementary material(File)
File 40.1 KB