Abstract
Originating in East Asia, the brown marmorated stink bug, Halyomorpha halys, has established in North America and Europe where it has become an urban and agricultural pest. Although initial populations in Europe were only reported in Switzerland, H. halys has expanded its range to include areas in France, Greece, Hungary, and Italy. Analysis of a portion of the mitochondrial COI gene was used to evaluate the genetic diversity of these populations and to investigate the movement and spread of different COI haplotypes of this pest in Europe. A total of 9 haplotypes are now confirmed in Europe. Four of these haplotypes have not been previously reported elsewhere, and one of these haplotypes has not been previously reported in Europe but is known from Korea. The H. halys population in Greece was the most diverse, with 7 of the 9 haplotypes occurring in the area of collection. Haplotype H1, which is known from North America, Italy, and China, was also present in samples collected in France, Greece, Hungary, and Switzerland. In fact, the H1 haplotype was the dominant haplotype detected in Budapest, Hungary and also occurred frequently in the samples from Athens, Greece. Patterns of haplotype diversity indicate the movement of successful invasive populations to generate secondary invasions within Europe (‘bridgehead effect’), as well as the occurrence of multiple invasions from Asia. Scenarios regarding the movement and spread of particular haplotypes in Europe are discussed.



References
Arnold K (2009) Halyomorpha halys (Stål, 1855), eine für die europäische Fauna neu nachgewiesene Wanzenart (Insecta: Heteroptera: Pentatomidae: Cappaeini). Mitt Thüringer Entomol 16:19
Auger-Rozenberg MA, 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
Bacon SJ, Bacher S, Aebi A (2012) Gaps in border controls are related to quarantine alien insect invasions in Europe. PLoS One 7:e47689
Barr NB (2009) Pathway analysis of Ceratitis capitata (Diptera: Tephritidae) using mitochondrial DNA. J Econ Entomol 102:401–411
Callot H, Brua C (2013) Halyomorpha halys (Stal, 1855), la Punaise diabolique, nouvelle espece pour la faune de France (Heteroptera Pentatomidae). L’Entomologiste 69:69–71
Cesari M, Maistrello L, Ganzerli F, Dioli P, Rebecchi L, Guidetti R (2015) A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J Pest Sci. doi:10.1007/s10340-014-0634-y
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
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Corin SE, Lester PJ, Abbott KL, Ritchie PA (2007) Inferring historical introduction pathways with mitochondrial DNA: the case of introduced Argentine ants (Linepithema humile) into New Zealand. Divers Distrib 13:510–518
deLeón JH, Sétamou M, Gastaminza GA, Buenahora J, Cáceres S, Yamamoto PT, Bouvet JP, Logarzo GA (2011) Two separate introductions of Asian citrus psyllid populations found in the American continents. Ann Entomol Soc Am 104:1392–1398
Duthie C (2012) Risk analysis of Halyomorpha halys (brown marmorated stink bug) on all pathways. Ministry for Primary Industries, Wellington
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47
Floerl O, Inglis GJ, Dey K, Smith A (2009) The importance of transport hubs in stepping-stone invasions. J Appl Ecol 46:37–45
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 Biotechnol 3:294–299
Freers A (2012) Blinde Passagiere: Stinkwanzen, Marmorierte Baumwanze—Halyomorpha halys. https://ssl.bremen.de/lmtvet/sixcms/media.php/13/Blinde_Passagiere_Stinkwanze_3_2012.pdf. Accessed 26 Feb 2015
Gariepy TD, Fraser H, Scott-Dupree CD (2014a) Brown marmorated stink bug (Hemiptera: Pentatomidae) in Canada: recent establishment, occurrence, and pest status in southern Ontario. Can Ent 146:579–582
Gariepy TD, Haye T, Fraser H, Zhang J (2014b) Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland. J Pest Sci 87:17–28
Garrouste R, Haye T, Streito J, Diolo P, Maistrello L (2014) Halyomorpha halys (Hemiptera, Pentatomidae): ten years after in Europe. In: Proceedings of the 5th quadrennial meeting of the International Heteropterists’ Society, pp 29–29
Goodale-Copestake WP, Tarling GA, Murphy EJ (2012) On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity 109:50–56
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. Mol Ecol 14:4207–4219
Haye T, Abdallah S, Gariepy T, Wyniger D (2014a) Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci 87:407–418
Haye T, Wyniger D, Gariepy T (2014b) Recent range expansion of the brown marmorated stink bug in Europe. In: Proceedings of the eighth international conference on urban pests, pp 309–314
Haye T, Gariepy T, Hoelmer K, Rossi J-P, Streito J-C, Tassus X, Desneux N (2015) Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci. doi:10.1007/s10340-015-0670-2
Heckmann R (2012) Erster Nachweis von Halyomorpha halys (STÅL, 1855) (Heteroptera: Pentatomidae) für Deutschland. Heteropteron 36:17–18
Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 105:225–237
Handley LJL, Estoup A, Evans DM, Thomas CE, Lombaert E, Facon B, Aebi A, Roy HE (2011) Ecological genetics of invasive alien species. BioControl 56:409–428
Leskey TC, Hamilton GC, Nielsen AL, Polk DF, Rodriguez-Saona C, Bergh JC, Herbert DA, Kuhar TP, Pfeiffer D, Dively GP et al (2012a) Pest status of the Brown Marmorated Stink Bug, Halyomorpha Halys in the USA. Outlooks Pest Manage 23:218–226
Leskey TC, Short BD, Butler BR, Wright SE (2012b) Impact of the Invasive brown marmorated stink bug, Halyomorpha halys (Stål), in mid-Atlantic tree fruit orchards in the United States: case studies of commercial management. Psyche:1–14.
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
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(3):e9743
MacLellan R (2013) Brown Marmorated Stink Bug: A potential threat to New Zealand. Surveillance (Wellington NZ) 40:3
Maistrello L, Dioli P, Vaccari G, Nannini R, Bortolotto P, Caruso S, Costi E, Montermini A, Casoli L, Bariselli M (2014) First records in Italy of the Asian stinkbug Halyomorpha halys, a new threat to fruit crops. ATTI Giornate Fitopatol 1:283–288
Mayr E (1954) Change of genetic environment and evolution. In: Huxley J, Hardy A, Ford E (eds) Evolution as a process. Allen and Unwin, London, pp 157–180
Miller N, Estoup A, Toepfer S, Bourguet D, Lapchin L, Derridj S, Kim KS, Reynaud P, Furlan L, Guillemaud T (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310:992
Milonas PG, Partsinevelos GK (2014) First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. EPPO Bull 44:183–186
Nei M, Li WH (1979) Mathematical models for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273
Pansa M, Asteggiano L, Costamanga C, Vittone G, Tavella L (2013) First discovery of Halyomorpha halys in peach orchards in Piedmont. Inf Agrar 69:60–61
Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T (2014) Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manag 5:A1–A13
Sauer C (2012) Die Marmorierte Baumwanze tritt neu im Deutschschweizer Gemusebau auf. Extension Gemusebau, Forschungsanstalt Agroscope Changins-Wadenswil, Gemusebau Info 28:4–5
Sax DF, Brown JH (2000) The paradox of invasion. Global Ecol Biogeogr 9:363–371
Slater N, Louzoun Y, Gragert L, Maiers M, Chatterjee A, Albrecht M (2015) Power laws for heavy-tailed distributions: modelling allele and haplotype diversity for National marrow donor program. PLOS Comput Biol 11(4):e1004204
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Vétek G, Papp V, Haltrich A, Redei D (2014) First record of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae), in Hungary, with description of the genitalia of both sexes. Zootaxa 3780:194–200
Walker K. 2009. Brown marmorated stink bug (Halyomorpha halys) Updated on 11/25/2011. Available online: http://www.padil.gov.au
Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506
Ward N (2013) Plants and environment investigation. Surveillance (Wellington NZ) 40:1
Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stal (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitt Schweiz Entomol Ges 81:1–8
Xu J, Fonseca D, Hamilton G, Hoelmer K, Nielsen A (2014) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol Invasions 16:153–166
Acknowledgements
This work was partly supported by the COST Action TD1209, European Information System for Alien Species. The authors would like to thank two anonymous reviewers for their comments and suggestions.
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Research involving Human Participants and/or Animals: This article does not contain any studies with human participants or animals (vertebrates) performed by any of the authors.
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Gariepy, T.D., Bruin, A., Haye, T. et al. Occurrence and genetic diversity of new populations of Halyomorpha halys in Europe. J Pest Sci 88, 451–460 (2015). https://doi.org/10.1007/s10340-015-0672-0
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DOI: https://doi.org/10.1007/s10340-015-0672-0