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Journal of Pest Science

, Volume 92, Issue 1, pp 173–187 | Cite as

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

  • Marion JavalEmail author
  • Alain Roques
  • Julien Haran
  • Franck Hérard
  • Melody Keena
  • Géraldine Roux
Original Paper

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.

Keywords

Biological invasion Anoplophora glabripennis ALB, genetic structure Mitochondrial marker Cytochrome oxidase I (COI) 

Notes

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.

Compliance with ethical standards

Conflict of interests

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

Supplementary material

10340_2017_917_MOESM1_ESM.docx (181 kb)
Fig S1: Variable sites of mtDNA COI haplotypes in A. glabripennis, on the 485-bp-long fragment analyzed (DOCX 181 kb)
10340_2017_917_MOESM2_ESM.docx (19 kb)
Table S1: Accession numbers of the sequences used in the study (DOCX 19 kb)

References

  1. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30CrossRefGoogle Scholar
  2. 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 47:229–235Google Scholar
  3. 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 21:6086–6103CrossRefGoogle Scholar
  4. 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 60:886–897CrossRefGoogle Scholar
  5. Bartell SM, Nair SK (2003) Establishment risks for invasive species. Risk Anal 24:833–845CrossRefGoogle Scholar
  6. 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 9:925–928Google Scholar
  7. 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 102:895–905CrossRefGoogle Scholar
  8. 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 12:1165–1182CrossRefGoogle Scholar
  9. 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 17:3614–3627CrossRefGoogle Scholar
  10. De-la-Mora M, Piñero D, Núñez-Farfán J (2015) Phylogeography of specialist weevil Trichobaris soror: a seed predator of Datura stramonium. Genetica 143:681–691CrossRefGoogle Scholar
  11. Dlugosch KM, Parker IM (2008) Founding events in species invasions: Genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449CrossRefGoogle Scholar
  12. 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 41:1729–1742CrossRefGoogle Scholar
  13. Downie DA (2002) Locating the sources of an invasive pest, grape phyloxera, using a mitochondrial DNA genealogy. Mol Ecol 11:2013–2026CrossRefGoogle Scholar
  14. 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 116:911–925CrossRefGoogle Scholar
  15. Eidg. Forschungsanstalt WSL (2014) WSL-Magazin Diagonal, 2/14. 36 S., ISSN 2296-3561Google Scholar
  16. 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 65:769–782CrossRefGoogle Scholar
  17. Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130CrossRefGoogle Scholar
  18. 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 47:51–72CrossRefGoogle Scholar
  19. European and Mediterranean Plant Protection Organization (EPPO) Global Database. https://gd.eppo.int/taxon/ANOLGL/distribution. Accessed 24 Aug 2016
  20. 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 131:479–491Google Scholar
  21. Excoffier L, Laval G, Schneider G (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1:47–50CrossRefGoogle Scholar
  22. Favaro R, Battisti A, Faccoli M (2013) Dating Anoplophora glabripennis introduction in North-East Italy by growth-ring analysis. J Entomol Acarol Res 45:35Google Scholar
  23. 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 3:294–299Google Scholar
  24. 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 18:935–952CrossRefGoogle Scholar
  25. 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 104:88–99CrossRefGoogle Scholar
  26. Haack RA, Cavey JF, Hoebeke ER, Law KL (1996) Anoplophora glabripennis: a new tree-infesting exotic cerambycid invades New York. Mich Entomol Soc Newsl 41:1–3Google Scholar
  27. 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 55:521–546CrossRefGoogle Scholar
  28. 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 53:109–115CrossRefGoogle Scholar
  29. 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 36:470–474CrossRefGoogle Scholar
  30. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913CrossRefGoogle Scholar
  31. 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 11:359–375CrossRefGoogle Scholar
  32. Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18CrossRefGoogle Scholar
  33. 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 18:921–933CrossRefGoogle Scholar
  34. 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 Google Scholar
  35. Kerdelhué C, Boivin T, Burban C (2014) Contrasted invasion processes imprint the genetic structure of an invasive scale insect across southern Europe. Heredity 113:390–400CrossRefGoogle Scholar
  36. Li WH (2004) Degradation and restoration of forest eco- systems in China. For Ecol Manag 201:33–41CrossRefGoogle Scholar
  37. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  38. Lingafelter SW, Hoebeke ER (2002) Revision of Anoplophora (Coleoptera: Cerambycidae). Entomological Society of Washington, WashingtonGoogle Scholar
  39. 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 119:64–75CrossRefGoogle Scholar
  40. 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:e9743CrossRefGoogle Scholar
  41. 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 110:1070–1077CrossRefGoogle Scholar
  42. 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 ZealandGoogle Scholar
  43. 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 6:1–13CrossRefGoogle Scholar
  44. Nicholas KB, Nicholas HB Jr, Deerfield DW II (1997) GeneDoc: analysis and visualization of genetic variation. Embnew News 4:1–4Google Scholar
  45. Normile D (2004) Invasive species. Expanding trade with China creates ecological backlash. Science 306:968–969CrossRefGoogle Scholar
  46. 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)Google Scholar
  47. 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 95:57–65Google Scholar
  48. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  49. Pudlo P, Marin J-M, Estoup A, Cornuet J-M, Gautier M, Robert CP (2015) Reliable ABC model choice via random forests. Bioinformatics 32:859–866CrossRefGoogle Scholar
  50. 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 89:245–252CrossRefGoogle Scholar
  51. Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242CrossRefGoogle Scholar
  52. Roderick GK, Navajas M (2003) Genes in new environments: Genetics and evolution in biological control. Nat Rev Genet 4:889–899CrossRefGoogle Scholar
  53. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464CrossRefGoogle Scholar
  54. 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 11–26Google Scholar
  55. 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 18:907–920CrossRefGoogle Scholar
  56. 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 GroupGoogle Scholar
  57. Smith MT, Bancroft J, Li G, Gao R, Teale S (2001) Dispersal of Anoplophora glabripennis (Cerambycidae). Environ Entomol 30:1036–1040CrossRefGoogle Scholar
  58. 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 33:435–442CrossRefGoogle Scholar
  59. 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 55:21–25CrossRefGoogle Scholar
  60. 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 105:13486–13491CrossRefGoogle Scholar
  61. Suarez AV, Tsutsui ND, Holway DA, Case TJ (1999) Behavioral and genetic differentiation between native and introduced populations of the Argentine ant. Biol Invasions 1:43–53CrossRefGoogle Scholar
  62. Trotter RT, Hull-Sanders HM (2015) Quantifying Dispersal of the Asian longhorned beetle (Anoplophora glabripennis, Coleoptera) with incomplete data and behavioral knowledge. Biol Invasions 17:3359–3369CrossRefGoogle Scholar
  63. 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 69:674–678CrossRefGoogle Scholar
  64. 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 24:686–693CrossRefGoogle Scholar
  65. Williams DW, Lee HP, Kim IK (2004a) Distribution and abundance of Anoplophora glabripennis (Coleoptera: Cerambycidae) in natural Acer stands in South Korea. Environ Entomol 33:540–545CrossRefGoogle Scholar
  66. Williams DW, Li G, Gao R (2004b) Tracking movements of individual Anoplophora glabripennis (Coleoptera: Cerambycidae) adults: application of harmonic radar. Environ Entomol 33:644–649CrossRefGoogle Scholar
  67. 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:e34567CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.INRA, UR0633OrléansFrance
  2. 2.CBGP, CIRAD, Montpellier SupAgro, INRA, IRDUniv. MontpellierMontpellierFrance
  3. 3.USDA Agricultural Research ServiceEuropean Biological Control LaboratorySaint-Gély-du-Fesc CedexFrance
  4. 4.Northern Research Station, Northeastern Center for Forest Health ResearchUSDA Forest ServiceHamdenUSA
  5. 5.Université d’Orléans, COSTOrléansFrance

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