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Complex invasion history of the Asian long-horned beetle: fifteen years after first detection in Europe

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An Author Correction to this article was published on 15 November 2017

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Abstract

The Asian long-horned beetle (ALB), a Cerambycidae, is an urban tree pest native to East Asia accidentally introduced to other continents via solid wood packing material. It was first detected in Europe in 2001, and since then infestations have been found in ten European countries. Using a 485-bp-long fragment of the mitochondrial barcode gene (COI), we studied the genetic diversity and structure of ALB populations in both native and invaded ranges, with a specific focus on Europe. Three main haplotypes were found across the native and invaded distribution of ALB. The native area in Asia was the most diverse with 23 haplotypes, but a low genetic structure was observed. Our results revealed up to nine distinct haplotypes that was diverged by no more than six mutational steps in European populations collected from 2001 to 2016. Nevertheless, the genetic structure was characterized by one widespread dominant haplotype in Europe. The overall complex genetic structure observed in Europe suggested a convoluted invasion scenario. Indeed, invasion history may include several introduction events as well as secondary dispersal.

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  • 15 November 2017

    In Table 1, longitude of the population 1 (Tallgrass, Canada) and the associated Figs. <InternalRef RefID="Fig1">2</InternalRef>c and <InternalRef RefID="Fig2">5</InternalRef>c were published incorrectly in the original publication of the article.

References

  • Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30

    Article  Google Scholar 

  • An YL, Wang BD, Yang XJ, Lin XJ, Chen JD, Huang XM, Mastro V (2004) Characterizing populations of Anoplophora glabripennis and related taxa with RAPD. Acta Entomol Sin 47:229–235

    CAS  Google Scholar 

  • Auger-Rozenberg M-A, Boivin T, Magnoux E, Courtin C, Roques A, Kerdelhué C (2012) Inferences on population history of a seed chalcid wasp: invasion success despite a severe founder effect from an unexpected source population. Mol Ecol 21:6086–6103

    Article  PubMed  Google Scholar 

  • Aukema JE, McCullough DG, Von Holle B, Liebhold AM, Britton K, Frankel SJ (2010) Historical accumulation of nonindigenous forest pests in the continental United States. Bioscience 60:886–897

    Article  Google Scholar 

  • Bartell SM, Nair SK (2003) Establishment risks for invasive species. Risk Anal 24:833–845

    Article  Google Scholar 

  • Carter M, Casa AM, Zeid M, Mitchell SE, Kresovich S (2008) Isolation and characterization of microsatellite loci for the Asian longhorned beetle, Anoplophora glabripennis. Perm Genet Resour 9:925–928

    Google Scholar 

  • Carter ME, Smith MT, Harrison RG (2009) Patterns of genetic variation among populations of the Asian longhorned beetle (Coleoptera: Cerambycidae) in China and Korea. An Entomol Soc Am 102:895–905

    Article  Google Scholar 

  • Carter ME, Smith MT, Harrison R (2010) Genetic analyses of the Asian longhorned beetle (Coleoptera, Cerambycidae, Anoplophora glabripennis), in North America, Europe and Asia. Biol Invasions 12:1165–1182

    Article  Google Scholar 

  • Ciosi M, Miller NJ, Kim KS, Giordano R, Estoup A, Guillemaud T (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627

    Article  CAS  PubMed  Google Scholar 

  • De-la-Mora M, Piñero D, Núñez-Farfán J (2015) Phylogeography of specialist weevil Trichobaris soror: a seed predator of Datura stramonium. Genetica 143:681–691

    Article  PubMed  Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: Genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  CAS  Google Scholar 

  • Dodds KJ, Orwig DA (2011) An invasive urban forest pest invades natural environments—Asian longhorned beetle in northeastern US hardwood forests. Can J For Res 41:1729–1742

    Article  Google Scholar 

  • Downie DA (2002) Locating the sources of an invasive pest, grape phyloxera, using a mitochondrial DNA genealogy. Mol Ecol 11:2013–2026

    Article  CAS  PubMed  Google Scholar 

  • Drag L, Hauck D, Bérces S, Michalcewicz J, Jelaska LSC, Aurenhammer S, Cizek L (2015) Genetic differentiation of populations of the threatened saproxylic beetle Rosalia longicorn, Rosalia alpina (Coleoptera: Cerambycidae) in Central and South-East Europe. Biol J Linn Soc 116:911–925

    Article  Google Scholar 

  • Eidg. Forschungsanstalt WSL (2014) WSL-Magazin Diagonal, 2/14. 36 S., ISSN 2296-3561

  • Essl F, Bacher S, Blackburn TM, Booy O, Brundu G, Brunel S, Cardoso A-C, Eschen R, Gallardo B, Galil B, García-Berthou E, Genovesi P, Groom Q, Harrower C, Hulme PE, Katsanevakis S, Kenis M, Kühn I, Kumschick S, Martinou AF, Nentwig W, O’Flynn C, Pagad S, Pergl J, Pyšek P, Rabitsch W, Richardson DM, Roques A, Roy HE, Scalera R, Schindler S, Seebens H, Vanderhoeven S, Vilà M, Wilson JRU, Zenetos A, Jeschke JM (2015) Crossing frontiers in tackling pathways of biological invasions. Bioscience 65:769–782

    Article  Google Scholar 

  • Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130

    Article  PubMed  Google Scholar 

  • Estoup A, Ravigné V, Hufbauer R, Vitalis R, Gautier M, Facon B (2016) Is there a genetic paradox of biological invasion? Annu Rev Ecol Evol Syst 47:51–72

    Article  Google Scholar 

  • European and Mediterranean Plant Protection Organization (EPPO) Global Database. https://gd.eppo.int/taxon/ANOLGL/distribution. Accessed 24 Aug 2016

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Laval G, Schneider G (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1:47–50

    Article  CAS  Google Scholar 

  • Favaro R, Battisti A, Faccoli M (2013) Dating Anoplophora glabripennis introduction in North-East Italy by growth-ring analysis. J Entomol Acarol Res 45:35

    Google 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. Mol Mar Biol Biotech 3:294–299

    CAS  Google Scholar 

  • Garnas JR, Auger-Rozenberg M-A, Roques A, Bertelsmeier C, Wingfield MJ, Saccaggi DL, Roy HE, Slippers B (2016) Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences. Biol Invasions 18:935–952

    Article  Google Scholar 

  • Guillemaud T, Beaumont MA, Ciosi M, Cornuet J-M, Estoup A (2010) Inferring introduction routes of invasive species using approximate Bayesian computation on microsatellite data. Heredity 104:88–99

    Article  CAS  PubMed  Google Scholar 

  • Haack RA, Cavey JF, Hoebeke ER, Law KL (1996) Anoplophora glabripennis: a new tree-infesting exotic cerambycid invades New York. Mich Entomol Soc Newsl 41:1–3

    Google Scholar 

  • Haack RA, Hérard F, Sun J, Turgeon JJ (2010) Managing invasive populations of Asian longhorned beetle and citrus longhorned beetle: A worldwide perspective. Annu Rev Entomol 55:521–546

    Article  CAS  PubMed  Google Scholar 

  • Haran J, Koutroumpa F, Magnoux E, Roques A, Roux G (2015) Ghost mtDNA haplotypes generated by fortuitous NUMTs can deeply disturb infra-specific genetic diversity and phylogeographic pattern. J Zool Syst Evol Res 53:109–115

    Article  Google Scholar 

  • Hérard F, Ciampitti M, Maspero M, Krehan H, Benker U, Boegel C, Schrage R, Bouhot-Delduc L, Bialooki P (2006) Anoplophora species in Europe: infestations and management processes. EPPO Bull 36:470–474

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  CAS  Google Scholar 

  • Hu J, Angeli S, Schuetz S, Luo Y, Hajek AE (2009) Ecology and management of exotic and endemic Anoplophora glabripennis (Coleoptera: Cerambycidae). Agric For Entomol 11:359–375

    Article  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Hurley BP, Garnas J, Wingfield MJ, Branco M, Richardson DM, Slippers B (2016) Increasing numbers and intercontinental spread of invasive insects on eucalypts. Biol Invasions 18:921–933

    Article  Google Scholar 

  • Javal M, Roux G, Roques A, Sauvard D (2017) Asian long-horned beetle dispersal potential estimated in computer-linked flight mills. J Appl Entomol. doi:10.1111/jen.12408

    Article  Google Scholar 

  • Kerdelhué C, Boivin T, Burban C (2014) Contrasted invasion processes imprint the genetic structure of an invasive scale insect across southern Europe. Heredity 113:390–400

    Article  PubMed  PubMed Central  Google Scholar 

  • Li WH (2004) Degradation and restoration of forest eco- systems in China. For Ecol Manag 201:33–41

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lingafelter SW, Hoebeke ER (2002) Revision of Anoplophora (Coleoptera: Cerambycidae). Entomological Society of Washington, Washington

    Google Scholar 

  • Lippens C, Estoup A, Hima MK, Loiseau A, Tatard C, Dalecky A, Bâ K, Kane M, Diallo M, Sow A, Niang Y, Berthier K, Leblois R, Duplantier J-M, Brouat C (2017) Genetic structure and invasion history of the house mouse (Mus musculus domesticus) in Senegal, West Africa: a legacy of colonial and contemporary times. Heredity 119:64–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lombaert E, Guillemaud T, Cornuet J-M, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE 5:e9743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez VM, Hoddle MS, Francese JA, Lance DR, Ray AM (2017) Assessing flight potential of the invasive Asian longhorned beetle (Coleoptera: Cerambycidae) with computerized flight mills. J Econ Entomol 110:1070–1077

    Article  PubMed  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the World’s Worst Invasive Alien Species: A Selection from the Global Invasive Species Database. Invasive Species Specialist Group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), Auckland, New Zealand

  • Meng PS, Hoover K, Keena M (2015) Asian longhorned beetle (Coleoptera: Cerambycidae), an introduced pest of maple and other hardwood trees in North America and Europe. J Integr Pest Manag 6:1–13

    Article  Google Scholar 

  • Nicholas KB, Nicholas HB Jr, Deerfield DW II (1997) GeneDoc: analysis and visualization of genetic variation. Embnew News 4:1–4

    Google Scholar 

  • Normile D (2004) Invasive species. Expanding trade with China creates ecological backlash. Science 306:968–969

    Article  CAS  PubMed  Google Scholar 

  • Pan HY (2005) Review of the Asian longhorned beetle: Research, Biology, Distribution and Management in China. Forestry Department. Working Paper FBS/6E, Food and Agriculture Organization of the United Nations, Rome (IT)

  • Pennacchio F, Peverieri GS, Jucker C, Allegro G, Roversi PF (2012) A key for the identification of the larvae of Anoplophora chinensis, Anoplophora glabripennis and Psacothea hilaris (Coleoptera Cerambycidae Lamiinae) in Europe. Redia 95:57–65

    Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Pudlo P, Marin J-M, Estoup A, Cornuet J-M, Gautier M, Robert CP (2015) Reliable ABC model choice via random forests. Bioinformatics 32:859–866

    Article  CAS  PubMed  Google Scholar 

  • Ramsfield TD, Bentz B, Faccoli M, Jactel H, Brockerhoff EG (2016) Forest health in a changing world: effects of globalization and climate change on forest insect and pathogen impacts. For Int J For Res 89:245–252

    Article  CAS  Google Scholar 

  • Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242

    Article  Google Scholar 

  • Roderick GK, Navajas M (2003) Genes in new environments: Genetics and evolution in biological control. Nat Rev Genet 4:889–899

    Article  CAS  PubMed  Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    Article  PubMed  Google Scholar 

  • Roques A (2010) Taxonomy, time and geographic patterns. Chapter 2. In: Roques A et al. (eds) Alien terrestrial arthropods of Europe. BioRisk, Vol 4, pp 11–26

  • Roques A, Auger-Rozenberg M-A, Blackburn TM, Garnas J, Pyšek P, Rabitsch W, Richardson DM, Wingfield MJ, Liebhold AM, Duncan RP (2016) Temporal and interspecific variation in rates of spread for insect species invading Europe during the last 200 years. Biol Invasions 18:907–920

    Article  Google Scholar 

  • Sawyer A (2009) Expected dispersal of Asian longhorned beetles from preferred host trees as a function of infestation level and data of removal during the flight season. Report from the USDA APHIS PPQ Otis Laboratory to the ALB Technical Working Group

  • Smith MT, Bancroft J, Li G, Gao R, Teale S (2001) Dispersal of Anoplophora glabripennis (Cerambycidae). Environ Entomol 30:1036–1040

    Article  Google Scholar 

  • Smith MT, Tobin PC, Bancroft J, Li G, Gao R (2004) Dispersal and spatiotemporal dynamics of Asian longhorned beetle (Coleoptera: Cerambycidae) in China. Environ Entomol 33:435–442

    Article  Google Scholar 

  • Smith M, Turgeon J, De Groot P, Gasman B (2009) Asian longhorned beetle Anoplophora glabripennis (Motschulsky): lessons learned and opportunities to improve the process of eradication and management. Am Entomol 55:21–25

    Article  Google Scholar 

  • Song H, Buhay JE, Whiting MF, Crandall KA (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc Natl Acad Sci USA 105:13486–13491

    Article  PubMed  Google Scholar 

  • Suarez AV, Tsutsui ND, Holway DA, Case TJ (1999) Behavioral and genetic differentiation between native and introduced populations of the Argentine ant. Biol Invasions 1:43–53

    Article  Google Scholar 

  • Trotter RT, Hull-Sanders HM (2015) Quantifying Dispersal of the Asian longhorned beetle (Anoplophora glabripennis, Coleoptera) with incomplete data and behavioral knowledge. Biol Invasions 17:3359–3369

    Article  Google Scholar 

  • Turgeon JJ, Orr M, Grant C, Wu Y, Gasman B (2015) Decade-Old Satellite infestation of Anoplophora glabripennis Motschulsky (Coleoptera: Cerambycidae) found in Ontario, Canada outside regulated area of founder population. Coleopt Bull 69:674–678

    Article  Google Scholar 

  • Walther G, Roques A, Hulme PE, Sykes MT, Pyšek P, Kühn I, Zobel M, Bacher S, Botta-Dukat Z, Bugmann H, Czucz B, Dauber J, Hickler T, Jarošik V, Kenis M, Klotz S, Minchin D, Moora M, Nentwig W, Ott J, Panov VE, Reineking B, Robinet C, Semenchenko V, Solarz W, Thuiller W, Vilà M, Vohland K, Settele J (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24:686–693

    Article  Google Scholar 

  • Williams DW, Lee HP, Kim IK (2004a) Distribution and abundance of Anoplophora glabripennis (Coleoptera: Cerambycidae) in natural Acer stands in South Korea. Environ Entomol 33:540–545

    Article  Google Scholar 

  • Williams DW, Li G, Gao R (2004b) Tracking movements of individual Anoplophora glabripennis (Coleoptera: Cerambycidae) adults: application of harmonic radar. Environ Entomol 33:644–649

    Article  Google Scholar 

  • Yang XM, Sun JT, Xue XF, Li JB, Hong XY (2012) Invasion genetics of the western flower thrips in China: evidence for genetic bottleneck, hybridization and bridgehead effect. PLoS ONE 7:e34567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful to Marie-Claude Bon and Lincoln Smith for comments on the manuscript, and we thank Camille Bagnis, Brigitte Delahaye-Panchout, Christine Daviet, Massimo Faccoli, Jianting Fan, Gernot Hoch, Stephan Koenig, Raphaelle Moutet, Simone Prospero, Rémi Rossignol, Jing Tao, Jean Turgeon, Beat Wermelinger, Jake Wickham and Shixiang Zong for providing information and samples for analysis. We greatfully acknowledge financial support from the French Ministry of Agriculture, Food, and Forestry (Convention DGAL E07/2014 “Estimation de l’impact écologique du Capricorne Asiatique Anoplophora glabripennis sur les populations xylophages natives et leurs organismes associés, et traçage génétique de l’origine de ses populations invasives en France continentale et en Corse”), and from the Région Centre Val de Loire. We also thank three anonymous reviewers for helpful comments on the manuscript.

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Authors and Affiliations

  1. INRA, UR0633, Zoologie Forestière, 45075, Orléans, France

    Marion Javal, Alain Roques, Julien Haran & Géraldine Roux

  2. CBGP, CIRAD, Montpellier SupAgro, INRA, IRD, Univ. Montpellier, Montpellier, France

    Julien Haran

  3. USDA Agricultural Research Service, European Biological Control Laboratory, Campus International de Baillarguet, CS90013 Montferrier-sur-Lez, 34980, Saint-Gély-du-Fesc Cedex, France

    Franck Hérard

  4. Northern Research Station, Northeastern Center for Forest Health Research, USDA Forest Service, Hamden, CT, 06514, USA

    Melody Keena

  5. Université d’Orléans, COST, 45075, Orléans, France

    Géraldine Roux

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None of the authors declare conflict of interest for the present study. Specimens sampled did not involve endangered nor protected species.

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Communicated by J. D. Sweeney.

Special issue on “Invasive insect pests of forests and urban trees: pathways, early detection and management”.

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Javal, M., Roques, A., Haran, J. et al. Complex invasion history of the Asian long-horned beetle: fifteen years after first detection in Europe. J Pest Sci 92, 173–187 (2019). https://doi.org/10.1007/s10340-017-0917-1

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