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Tracking the origin and dispersal of the Asian chestnut gall wasp Dryocosmus kuriphilus Yasumatsu (Hymenoptera, Cynipidae) in Europe with molecular markers

  • I. Martinez-Sañudo (a1), L. Mazzon (a1), M. Simonato (a1), D. Avtzis (a2), J. Pujade-Villar (a3) and M. Faccoli (a1)...

Abstract

The Asian chestnut gall wasp, Dryocosmus kuriphilus, is an invasive pest causing significant damage to chestnut trees (Castanea spp., Fagaceae). Originating from China, it has recently invaded a wide range of regions in Europe and North America. Understanding the population genetic structure of important invasive pests is very useful for improving the knowledge concerning routes of expansion and colonizing capacity. Despite its economic importance, limited attention has been given to D. kuriphilus origin and spread, or to its genetic structure. In this study, D. kuriphilus populations sampled in eight European countries were screened using both mitochondrial (cytochrome c oxidase subunit 1; COI) and nuclear (internal transcribed spacer 2; ITS2) sequences, and Amplified Fragment Length Polymorphism (AFLP) markers. The molecular markers COI and ITS2 highlighted the presence of a single haplotype in all the studied populations. The recorded mitochondrial haplotype was identical to one of the most widespread haplotypes occurring in the native area (China). AFLP results indicated that D. kuriphilus individuals belong to two genetically distinct clusters without any further geographic clustering. These results suggest that D. kuriphilus populations in Europe could be the result of a single introduction of a Chinese founder population characterized by two genetically distinct lineages that subsequently spread rapidly across Europe. However, the possibility that populations originated from multiple introductions of the same Chinese mitochondrial haplotype cannot be excluded. The reported results provide useful information concerning this invasive species, potentially facilitating integrated pest management.

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*Author for correspondence Tel.: +39 049 8272808 Fax: +39 049 8272810 E-mail: lmazzon@unipd.it

References

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Abe, Y., Melika, G. & Stone, G.N. (2007) The diversity and phylogeography of cynipid gall wasps (Hymenoptera: Cynipidae) of the Oriental and Eastern Palearctic regions, and their associated communities. Oriental Insects 41, 169212.
Ács, Z., Melika, G., Pénzes, Z., Pujade-Villar, J. & Stone, G.N. (2007) The phylogenetic relationships between Dryocosmus chilaspis and allied genera of oak gall wasps (Hymenoptera, Cynipidae: Cynipini). Systematic Entomology 32, 7080.
Aebi, A., Schönrogge, K., Melika, G., Alma, A., Bosio, G., Quacchia, A., Picciau, L., Abe, Y., Moriya, S., Yara, K., Seljak, G. & Stone, G.N. (2006) Parasitoid recruitment to the globally invasive chestnut gall wasp Dryocosmus kuriphilus. pp. 103121 in Ozaki, K., Yukwa, J., Ohgushi, T. & Price, P.W. (Eds) Galling Arthropods and Their Associates. Tokyo, Springer.
Andersen, H.F., Jordal, B. H., Kambestad, M. & Kirkendall, L.R. (2012) Improbable but true: the invasive inbreeding ambrosia beetle Xylosandrus morigerus has generalist genotypes. Ecology and Evolution 2, 247257.
Askew, R.R. (1984) The biology of gall wasps. Biology of gall insects. pp. 223271 in Ananthakrishnan, T.N. (Ed.) The Biology of Gall Insects. New Delhi, Oxford and IBH Publishing Co.
Askew, R.R., Melika, G., Pujade-Villar, J., Schoenrogge, K., Stone, G.N. & Nieves-Aldrey, J.L. (2013) Catalogue of parasitoids and inquilines in cynipid oak galls in the West Palaearctic. Zootaxa 3643, 1133.
Avtzis, D.N. & Matošević, D. (2013) Taking Europe by storm: a first insight in the introduction and expansion of Dryocosmus kuriphilus in central Europe by mtDNA. Šumarski List 137, 387393.
Baker, H. G. (1965) Characteristics and modes of origin of weeds. pp. 147168 in Baker, H.G. & Stebbins, G.L. (Eds.) The Genetics of Colonizing species. New York, Academic Press.
Bahder, B. W., Bahder, L. D., Hamby, K. A., Walsh, D. B. & Zalom, F. G. (2015) Microsatellite variation of two Pacific coast Drosophila suzukii (Diptera: Drosophilidae) populations. Environmental Entomology 44, 14491453.
Barrett, S.C.H. & Kohn, J.R. (1991) Genetic and evolutionary consequences of small population size in plants: implications for conservation. pp. 330 in Falk, D.A. & Holsinger, K.E. (Eds) Genetics and Conservation of Rare Plants. New York, Oxford University Press.
Battisti, A., Benvegnù, I., Colombari, F. & Haack, R. A. (2014) Invasion by the chestnut gall wasp in Italy causes significant yield loss in Castanea sativa nut production. Agricultural and Forest Entomology 16, 7579.
Bernardo, U., Iodice, L., Sasso, R., Tutore, V. A., Cascone, P. & Guerrieri, E. (2013) Biology and monitoring of Dryocosmus kuriphilus on Castanea sativa in Southern Italy. Agricultural and Forest Entomology 15, 6576.
Bray, T. C., Bennett, N. C. & Bloomer, P. (2011) Low levels of polymorphism at novel microsatellite loci developed for bathyergid mole-rats from South Africa. Conservation Genetics Resources 3, 221224.
Brown, J.E., Scholte, E.-J., Dik, M., Den, Hartog, W., Beeuwkes, J. & Powell, J.R. (2011) Aedes aegypti mosquitoes imported into the Netherlands, 2010. Emerging Infectious Diseases 17, 2335.
Brussino, G., Bosio, G., Baudino, M., Giordano, R., Ramello, F. & Melika, G. (2002) Pericoloso insetto esotico per il castagno europeo. L'Informatore Agrario 37, 5961.
CABI (2016) Dryocosmus kuriphilus. In: Invasive species compendium. [www document] URL. Available online at http://www.cabi.org/isc/datasheet/20005.
Çetgdot, G., Orman, E. & Polat, Z. (2014) First record of the oriental chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) in Turkey. Bitki Koruma Bülteni 54, 303309.
Clarke, A.R., Armstrong, K.F., Carmichael, A.E., Milne, J.R., Raghu, S., Roderick, G.K. & Yeates, D.K. (2005) Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annual Review of Entomology 50, 293319.
Clement, M., Posada, D.C.K.A. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571659.
Cognato, A.I., Sun, J.H., Anducho-Reyes, M.A. & Owen, D.R. (2005) Genetic variation and origin of red turpentine beetle (Dendroctonus valens LeConte) introduced to the People's Republic of China. Agricultural and Forest Entomology 7, 8794.
Collins, F.H. & Paskewitz, S.M. (1996) A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Molecular Biology 5, 19.
Colombari, F. & Battisti, A. (2016) Native and introduced parasitoids in the biocontrol of Dryocosmus kuriphilus in Veneto (Italy). EPPO Bulletin 46, 275285.
Csóka, G., Wittmann, F. & Melika, G. (2009) The oriental sweet chestnut gall wasp (Dryocosmus kuriphilus Yatsumatsu 1951) in Hungary. Növényvédelem 45, 359360.
Cunha, L., Montiel, R., Novo, M., Orozco-terWengel, P., Rodrigues, A., Morgan, A.J. & Kille, P. (2014) Living on a volcano's edge: genetic isolation of an extremophile terrestrial metazoan. Heredity 112, 132142.
Delalić, Z. (2016) First record of quarantine pest, oriental chestnut gall wasp (Dryocosmus kuriphilus), in Bosnia and Herzegovina. Biljni Lekar (Plant Doctor) 44, 5865.
Earl, D.A. & Vonholdt, B.M. (2012) Structure Harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conservation Genetics Resources 4, 359361.
EFSA, European Food Safety Agency (2010) Risk assessment of the oriental chestnut gall wasp, Dryocosmus kuriphilus for the EU territory and identification and evaluation of risk management options. EFSA Journal 8, 1619.
Ehrich, D. (2006) AFLPDAT: a collection of R functions for convenient handling of AFLP data, Molecular Ecology Notes 6, 603604.
EPPO, European Plant Protection Organization (2012). First report of Dryocosmus kuriphilus in the Czech Republic. EPPO Reporting Service 7, 5.
EPPO, European Plant Protection Organization (2014) PQR database. Paris, European and Mediterranean Plant Protection Organization. Available online at http://www.eppo.int/DATABASES/pqr/pqr.htm (accessed 11 November 2016).
EPPO, European Plant Protection Organization (2016) First report of Dryocosmus kuriphilus in Belgium. EPPO Reporting Service (Report No. 2).
Evanno, G., Regnaut, S. & Goude, T.J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2262.
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.
Farris, R.E., Ruiz-Arce, R., Ciomperlik, M., Vasquez, J.D. & DeLeón, R. (2010) Development of a ribosomal DNA ITS2 marker for the identification of the thrips, Scirtothrips dorsalis. Journal of Insect Science 10, 26.
Ferracini, C., Bertolino, S., Bernardo, U., Bonsignore, C. P., Faccoli, M., Ferrari, E., Lupi, D., Maini, S., Mazzone, L., Nugnes, F., Rocco, A., Santi, F. & Tavella, L. (2018) Do Torymus sinensis (Hymenoptera: Torymidae) and agroforestry system affect native parasitoids associated with the Asian chestnut gall wasp? Biological Control 121, 3643.
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.
Forster, B., Castellazzi, T., Colombi, L., Fuerst, E., Marazzi, C., Meier, F. & Tettamanti, G. (2009) Die Edelkastaniengallwespe Dryocosmus kuriphilus (Yasumatsu) (Hymenoptera, Cynipidae) tritt erstmals in der Südschweiz auf. Mitteilungen der Schweizen Entomologischen Gesselschaft 82, 271279.
Gninenko, Y.I. & Lyanguzov, M.E. (2017) East chestnut gall wasps Dryocosmus kuriphilus Yasumatsu, 1951 (Hymenoptera, Cynipidae) – New invader in the forests of the North Caucasus. Russian Journal of Biological Invasions 8, 206211.
Grapputo, A., Boman, S., Lindstroem, L., Lyytinen, A. & Mappes, J. (2005) The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Molecular Ecology 14, 42074219.
Graziosi, I. & Rieske, L.K. (2012) Local spread of an exotic invader: using remote sensing and spatial analysis to document proliferation of the invasive Asian chestnut gall wasp. iForest 5, 255261.
Hulme, P.E. (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. Journal of Applied Ecology 46, 1018.
Jensen, L.H., Enghoff, H., Frydenberg, J. & Davis Parker, E. (2002) Genetic diversity and the phylogeography of parthenogenesis: comparing bisexual and thelytokous populations of Nemasoma varicorne (Diplopoda: Nemasomatidae) in Denmark. Hereditas 136, 184194.
Kenis, M., Roques, A., Santini, A. & Liebhold, A.M. (2017) Impact of non-native invertebrates and pathogens on market forest tree resources. pp. 103117 in Vilà, M. & Hulme, P.E. (Eds) Impact of Biological Invasions on Ecosystem Services. Cham, Springer.
Knapič, V., Seljak, G. & Kolšek, M. (2010) Experience with Dryocosmus kuriphilus Yatsumatsu eradication measures in Slovenia. OEPP/EPPO Bulletin 40, 169175.
Kohnen, A., Wissemann, V. & Brandl, R. (2011) No host-associated differentiation in the gall wasp Diplolepis rosae (Hymenoptera: Cynipidae) on three dog rose species. Biological Journal of the Linnean Society 102, 369377.
Lu, P.F., Zhu, D.H., Yang, X.H. & Liu, Z.W. (2012) Phylogenetic analysis of the mtDNA COI gene suggests cryptic Dryocosmus kuriphilus associated with certain populations of Chinese chestnuts (Castanea spp.). Chinese Journal of Applied Entomology 49, 161167.
Lynch, M. & Milligan, B.G. (1994) Analysis of population genetic structure with RAPD markers. Molecular Ecology 3, 9199.
Malacrida, A.R., Marinoni, F., Torti, C., Gomulski, L.M., Sebastiani, F., Bonvicini, C., Gasperi, G. & Guglielmino, C.R. (1998) Genetic aspects of the worldwide colonization process of Ceratitis capitata. Journal of Heredity 89, 501507.
Malumphy, C. (2015) First findings of oriental chestnut gall wasp Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) in the United Kingdom. Cecidology 30, 4547.
Manni, M., Guglielmino, C.R., Scolari, F., Vega-Rua, A., Failloux, A-B., Somboon, P., Lisa, A., Savini, G., Bonizzoni, M., Gomulski, L.M., Malacrida, A.R. & Gasperi, G. (2017) Genetic evidence for a worldwide chaotic dispersion pattern of the arbovirus vector, Aedes albopictus. PLoS Neglected Tropical Diseases 11, e0005332.
Matošević, D., Pernek, M. & Hrašovec, B. (2010) First record of oriental chestnut gall wasp (Dryocosmus kuriphilus) in Croatia. Sumarski list 134, 497502.
Maynard, A.J., Ambrose, L., Cooper, R.D., Chow, W.K., Davis, J.B., Muzari, M.O., Hurk, A.F.V.D., Hall-Mendelin, S., Hasty, J.M., Burkot, T.R., Bangs, M.J., Reimer, L.J., Butafa, C., Loco, N.F., Syafruddin, D., Maung, Y.N.M., Ahmad, R. & Beebe, N.W. (2017) Tiger on the prowl: invasion history and spatio-temporal genetic structure of the Asian tiger mosquito Aedes albopictus (Skuse 1894) in the Indo-Pacific. PLoS Neglected Tropical Diseases 11, e0005546.
Medina, R.F., Barbosa, P., Christman, M. & Battisti, A. (2006) Number of individuals and molecular markers to use in genetic differentiation studies. Molecular Ecology Notes 6, 10101013.
Medina, R.F., Armstrong, S.J. & Harrison, K. (2017) Genetic population structure of sugarcane aphid, Melanaphis sacchari, in sorghum, sugarcane, and Johnsongrass in the continental USA. Entomologia Experimentalis et Applicata 162, 358365.
Michaelakis, A., Papachristos, D., Chytas, D.A., Antonopoulou, P.D., Milonas, P.G. & Avtzis, D.N. (2016) First record of Dryocosmus kuriphilus in Greece. EPPO Bulletin 46, 290294.
Migeon, A., Auger, P., Hufbauer, R. & Navajas, M. (2015) Genetic traits leading to invasion: plasticity in cold hardiness explains current distribution of an invasive agricultural pest, Tetranychus evansi (Acari: Tetranychidae). Biological invasions 17, 22752285.
Nakamura, M. (1964) Population dynamics of the chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). I. Description of the survey stations and the life histories of the gall-wasp and its parasite. Japanese Journal of Applied Entomology and Zoology 8, 149158.
Nicholls, J.A., Challis, R.J., Mutun, S. & Stone, G.N. (2012) Mitochondrial barcodes are diagnostic of shared refugia but not species in hybridizing oak gallwasps. Molecular Ecology 21, 40514062.
Nohara, K. (1956) Considerations on the reproductive capacity of Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). Scientific Bulletin Faculty of Agriculture Kyushu University 15, 441446.
Pannebakker, B.A., Zwaan, B.J., Beukeboom, L.W. & Van Alphen, J.J. (2004) Genetic diversity and Wolbachia infection of the Drosophila parasitoid Leptopilina clavipes in Western Europe. Molecular Ecology 13, 11191128.
Pástor, M., Juhásová, G., Juhás, D. & Bakay, L. (2017) Occurrence of oriental chestnut gall wasp. Plant Protection Science 53, 243246.
Patwary, M.U., Kenchington, E.L., Bird, C.J. & Zouros, E. (1994) The use of random amplified polymorphic DNA markers in genetic studies of the sea scallop Placopecten magellanicus (Gmelin, 1791). Journal of Shellfish Research 13, 547553.
Payne, J.A. (1978) Oriental chestnut gallwasp: a new nut pest in North America. pp. 8688 in Macdonald, W.L., Cech, F.C., Luchok, J. & Smith, C. (Eds) Proceedings of the American Chestnut Symposium. Morgantown, West Virginia University Press.
Peakall, R. & Smouse, P.E. (2005) Genalex 6: genetic analysis in excel. Population genetics software for teaching and research. Molecular Ecology Resources 6, 288295.
Porras-Hurtado, L., Ruiz, Y., Santos, C., Phillips, C., Carracedo, Á. & Lareu, M. (2013) An overview of STRUCTURE: applications, parameter settings, and supporting software. Frontiers in Genetics 4, 98.
Pritchard, JK., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945959.
Pujade-Villar, J., Torrell, A. & Rojo, M. (2013) Primeres troballes a la península Ibèrica de Dryocosmus kuriphilus (Hym., Cynipidae), una espècie de cinípid d'origen asiàtic altament perillosa per al castanyer (Fagaceae). Orsis: Organismes i Sistemes 27, 295301.
Quacchia, A., Moryia, S., Bosio, G., Scapin, I. & Alma, A. (2008) Rearing, release and settlement prospect in Italy of Torymus sinensis, the biological control agent of the chestnut gall wasp Dryocosmus kuriphilus. BioControl 53, 829839.
Quacchia, A., Ferracini, C., Nicholls, J.A., Piazza, E., Saladini, M.A., Tota, F., Melika, G. & Alma, A. (2013) Chalcid parasitoid community associated with the invading pest Dryocosmus kuriphilus in north-western Italy. Insect Conservation and Diversity 6, 114123.
R Core Team (2018). R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing, 2015.
Radócz, L., Szilagyi, A., Nagy, M., Kovács, G. & Melika, G. (2016) Asian sweet chestnut gallwasp, Dryocosmus kuriphilus (Hymenoptera, Cynipidae): first record for Romania. North-Western Journal of Zoology 12, 201204.
Ruiz-Montoya, L., Zúñiga, G., Cisneros, R., Salinas-Moreno, Y., Peña-Martínez, R. & Machkour-M'Rabet, S. (2015) Phenotypic and genetic variations in obligate parthenogenetic populations of Eriosoma lanigerum Hausmann (Hemiptera: Aphididae). Neotropical Entomology 44, 534545.
Samara, R., Monje, J.C., Reineke, A. & Zebitz, C.P.W. (2008) Genetic divergence of Trichogramma aurosum Sugonjaev and Sorokina (Hymenoptera: Trichogrammatidae) individuals based on ITS2 and AFLP analysis. Journal of Applied Entomology 132, 230238.
Schonswetter, P. & Tribsch, A. (2005) Vicariance and dispersal in the alpine perennial Bupleurum stellatum L. (Apiaceae). Taxon 54, 725732.
Simberloff, D., Martin, J.L., Genovesi, P., Maris, V., Wardle, D.A., Aronson, J., Martin Courchamp, F., Galil, B., García-Berthou, E., Pascal, M., Pyšek, P., Sousa, R., Tabacchi, E. & Vilà, M. (2013) Impacts of biological invasions: what's what and the way forward. Trends in Ecology & Evolution 28, 5866.
Tait, G., Vezzulli, S., Sassù, F., Antonini, G., Biondi, A., Baser, N., Sollai, G., Cini, A., Tonina, L., Ometto, L., Anfora, G. (2017) Genetic variability in Italian populations of Drosophila suzukii. BMC Genetics 18, 87.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 27252729.
Traut, W., Vorwerk, S. & Forneck, A. (2007) Analysis of genetic variation within clonal lineages of grape phylloxera (Daktulosphaira vitifoliae Fitch) using AFLP fingerprinting and DNA sequencing. Genome 50, 660667.
Vos, P., Hogers, R., Bleeker, M., Reijans, M., Lee, T.V.D., Hornes, M., Frijters, A., Pot, J., Peleman, J. & Kuiper, M. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23, 44074414.
White, T.J., Bruns, T., Lee, S.J.W.T. & Taylor, J.L. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. pp. 315322 in Innis, M.A., Gelfand, D.H., Shinsky, J.J. & White, T.J. (Eds) PCR Protocols: A Guide to Methods and Applications. San Diego, Academic Press.
Whitlock, R., Hipperson, H., Mannarelli, M., Butlin, R.K. & Burke, T. (2008) An objective, rapid and reproducible method for scoring AFLP peak-height data that minimizes genotyping error. Molecular Ecology Resources 8, 725735.
Xu, J., Fonseca, D.M., Hamilton, G.C., Hoelmer, K.A. & Nielsen, A.L. (2014) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biological Invasions 16, 153166.
Yara, K. (2006) Identification of Torymus sinensis and T. beneficus (hymenoptera: Torymidae), introduced and indigenous parasitoids of the chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae), using the ribosomal ITS2 region. Biological Control 36, 1521.

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