Abstract
The Asian longhorned beetle, (Coleoptera, Cerambycidae, Anoplophora glabripennis (Motschulsky)), is endemic to China and Korea and an important invasive insect in North America and Europe. We analyzed mitochondrial DNA sequence data of invasive populations of A. glabripennis in North America and Europe, and microsatellite allele frequency data of beetles from North America. We show that populations in New York City and Long Island NY; New Jersey, Chicago, IL, and Toronto, Canada have limited genetic diversity compared to populations in China. In addition, the data suggest that separate introduction events were responsible for many of the populations in North America and for European populations in Austria, France, Germany and Italy. Populations on Long Island, NY are suspected to have been initiated by the transport of cut wood from New York City. A. glabripennis beetles found in Jersey City, NJ appear to be derived from an expansion of the New York City, NY population, whereas beetles found in Linden, NJ are an expansion from the Carteret, NJ population. Limited genetic diversity did not stop this invasive insect from establishing damaging populations in North America. Founders of introduced A. glabripennis populations in North America and Europe are likely derived from populations in China that are themselves invasive, rendering difficult the identification of source populations. Invasiveness in an insect’s natural range could be an important predictor of potential pest status of introduced populations.
Similar content being viewed by others
References
Ahern RG, Hawthorne DJ, Raupp MJ (2009) Founder effects and phenotypic variation in Adelges cooleyi, an insect pest introduced to the eastern United States. Bio Inv 11:959–971
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744
Bartell SM, Nair SK (2003) Establishment risks for invasive species. Risk Anal 24:833–845
Cai Y-W, Cheng X-Y, Xu R-M, Duan D-H, Kirkendall LR (2008) Genetic diversity and biogeography of red turpentine beetle Dendroctonus valens in its native and invasive regions. Insect Sci 15:291–301
Carrol SP (2007) Brave new world: the epistatic foundations of natives adapting to invaders. Genetica 129:193–204
Carter M, Casa AM, Zeid M, Mitchell SE, Kresovich S (2009a) Isolation and characterization of microsatellite loci for the Asian longhorned beetle, Anoplophora glabripennis. Mol Ecol Resour 9:925–928
Carter ME, Smith MS, Harrison RG (2009b) Patterns of genetic variation among populations of the Asian longhorned beetle (Coleoptera: Cerambycidae) in China and Korea. Annals Entomol Soc 102 (in press)
Cavey JF, Hoebeke ER, Passoa S, Lingafelter SW (1998) A new exotic threat to North American hardwood forests: an Asian longhorned beetle, Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae). I. Larval description and diagnosis. Proc Entomol Soc Wash 100:373–381
Cheverud JM, Vaugh TT, Pletscher LS, King-Ellison K, Bailiff J, Adams E, Erickson C, Bonislawski A (1999) Epistasis and the evolution of additive genetic variance in populations that pass through a bottleneck. Evolution 53:1009–1018
Clement MD, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660
Cognato AI, Sun J-H, Anducho-Reyes MA, Owen DR (2005) Genetic variation and origin of red turpentine beetle (Dendroctonus valens LeConte) introduced to the People’s Republic of China. Agr For Entomol 7:87–94
Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329
Crooks JA, Soulé ME (1999) Lag times in population explosions of invasive species: causes and implications. In: Sandlund OT, Schei PF, Viken A (eds) Invasive species and biodiversity management. Kluwer, Dordrecht, pp 103–125
Dlugosch KM, Parker IM (2007) Founding events in species invasions: genetic variation, adaptive evolution and the role of multiple introductions. Mol Ecol 17:431–449
Eales J, Thorpe RS, Malhotra A (2008) Weak founder effect signal in a recent introduction of Caribbean Anolis. Mol Ecol 17:1416–1426
Enserink M (1999) Predicting invasions: biological invaders sweep in. Science 285:1834–1836
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Laval G, Schneider G (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinfom Online 1:47–50
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Ficetola GF, Bonin A, Miaud C (2008) Population genetics reveals origin and number of founders in a biological invasion. Mol Ecol 17:773–782
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Grapputo A, Boman S, Lindström 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
Haack RA (2003) Exotics, exotics, exotics: recently detected bark-and wood-boring insects in the US. Newsl Mich Entomol Soc 48:16–17
Haack RA (2006) Exotic bark- and wood-boring Coleoptera in the United States: recent establishments and interceptions. Can J For Res 36:269–288
Haack RA, Law KR, Mastro VC, Ossenbruggen HS, Raimo BJ (1997) New York’s battle with the Asian long-horned beetle. J For 95:11–15
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. OEPP/EPPO B 36:470–474
Hu J, Angeli S, Schuetz S, Luo Y, Hajek AE (2009) Ecology and management of exotic and endemic Anoplophora glabripennis. Agr For Entomol 11 (in press)
Huelsenbeck JP, Ronquist F, Nielsen R, Bolback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314
Hulme PE, Roy DB, Cunha T, Larsson T-B (2009) A pan-European inventory of alien species: rationale, implementation and implications for managing biological invasions. In: Hulme P, Nentwig W, Pyšek P, Vilà M (eds) DAISIE Handbook of alien species in Europe. Springer, Dordrecht, pp 1–14
Keena MA (2002) Anoplophora glabripennis (Coleoptera: Cerambycidae) fecundity and longevity under laboratory conditions: comparisons of populations from New York and Illinois on Acer saccharum. Environ Entomol 31:490–498
Keena MA (2005) Pourable artificial diet for rearing Anoplophora glabripennis and methods to optimize larval survival and synchronize development. Ann Entomol Soc Am 96:536–547
Krushelnycky PD, Gillespie RG (2008) Compositional and functional stability of arthropod communities in the face of ant invasions. Ecol Appl 18:1547–1562
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary analysis and sequence alignment. Brief Bioinform 5:150–163
Langor DW, DeHaas LJ, Foottit RG (2009) Diversity of non-native terrestrial arthropods on woody plants in Canada. Biol Invasions 11:5–19
Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–392
Liebhold AM, Tobin PC (2008) Population ecology of insect invasions and their management. Annu Rev Entomol 53:387–408
Lingafelter SW, Hoebeke ER (2002) Revision of Anoplophora (Coleoptera: Cerambycidae). Entomological Society of Washington, Washington
Liu K, Muse SV (2005) PowerMarker: integrated analysis environment for genetic marker data. Bioinformatics 21:2128–2129
Maspero M, Jucker C, Colombo M (2007) First record of Anoplophora glabripennis (Motschulsky) (Coleoptera Cerambycidae Lamiinae Lamiini) in Italy. B Zool Agr Bachicoltura 39:161–164
Mattson W, Vanhanen H, Veteli T, Sivonen S, Niemelä P (2007) Few immigrant phytophagous insects on woody plants in Europe: legacy of the European crucible? Biol Invasions 9:957–974
Naciri-Graven Y, Goudet J (2008) The additive genetic variance after bottlenecks is affected by the number of loci involved in epistatic interactions. Evolution 7:706–716
Nei M, Li H (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl A Sci USA 76:5269–5273
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Nowak DJ, Pasek JE, Sequeira RA, Crane DE, Mastro VC (2001) Potential effect of Anoplophora glabripennis (Coleoptera: Cerambycidae) on urban trees in the United States. J Econ Entomol 94:116–122
Nylander JAA (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. http://darwin.uvigo.es/software/modeltest.html. Accessed 30 May 2009
Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:375–378
Pan HY (2005) Review of the Asian longhorned beetle: research, biology, distribution and management in China. Food and Agriculture Organization, Forestry Department. Working Paper FBS/6E. FAO, Roma. http://www.fao.org/forestry/media/66891/1/102/ Accessed 27 May 2008
Sawyer AJ, Panagakos, WS (2009) Spatial dynamics of the Asian longhorned beetle: Carteret, NJ to Staten Island, NY in nine years? In: McManus KA, Gottschalk KW (eds) Proceedings of 19th US Department of Agriculture Interagency Research Forum on Invasive Species 2008. USDA For Serv Gen Tech Rpt NRS-P-36. USDA Forest Service, Newton Square, p 68
Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs associated with non-indigenous species in the United States. Bioscience 50:53–65
Pimentel D, McNair S, Janecka J, Wightman J, Simmonds C, O’Connell C, Wong E, Russell L, Zern J, Aquino T, Tsomondo T (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84:1–20
Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first generation migrant detection. J Hered 95:536–539
Poland TM, McCullough DG (2006) Emerald ash borer: invasion of the urban forest and the threat to North America’s ash resource. J For 104:118–124
Poland TM, Haack RA, Petrice TR (1998) Chicago joins New York in battle with the Asian longhorned beetle. Newsl Mich Entomol Soc 43:15–17
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Puillandre N, Dupas S, Dangles O, Zeddam J-L, Capdevielle-Dulac C, Barbin K, Torres-Leguizamon M, Silvain J-F (2008) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biol Invasions 10:319–333
Qian H, Song J-S, Krestov P, Guo Q, Wu Z, Shen X, Guo X (2003) Large-scale phytogeographical patterns in East Asia in relation to latitudinal and climatic gradients. J. Biogeogr 30:129–141
Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201
Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reich DE, Cargill M, Bolk S, Ireland J, Sabeli PC, Richter DJ, Lavery T, Kouyoumjian R, Farhadian SF, Ward R, Lander ES (2001) Linkage disequilibrium in the human genome. Nature 411:199–204
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Roderick GK, Navajas M (2003) Genes in new environments: genetics and evolution in biological control. Nat Rev Genet 4:889–899
Rogers JS (1972) Measures of genetic similarity and genetic distance. In: Studies in genetics VII. Univ Texas Pub 7213, Austin, pp 145–153
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332
Sawyer AJ (2003) Annotated categorization of ALB host trees. (Revised 8 May 2003) USDA-APHIS-PPQ, Otis Plant Protection Laboratory. http://www.uvm.edu/albeetle/hosts.htm. Accessed 4 Oct 2008
Sawyer AJ (2007) Spatial and temporal dynamics of Asian longhorned beetle infestations in Carteret and Linden, NJ. USDA Emerald ash borer and Asian longhorned beetle research and development review meeting FHTET-2007-04:128–129
Scheffer SJ, Grissell EE (2003) Tracing the geographical origin of Megastigmus transvaalensis (Hymenoptera: Torymidae): an African wasp feeding on a South American plant in North America. Mol Ecol 12:415–421
Schlotterer C (2004) The evolution of molecular markers-just a matter of fashion? Nat Rev Genetics 5:63–69
Sellers C (2004) The Asian long-horned beetle in Ontario. Ont Insects 9:21
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176
Smith MT, Bancroft J, Tropp J (2002) Age-specific fecundity of Anoplophora glabripennis (Coleoptera: Cerambycidae) on three tree species infested in the United States. Environ Entomol 31:76–83
Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360
Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland
Takahashi N, Ito M (2005) Detection and eradication of the Asian longhorned beetle in Yokohama, Japan. Res B Plant Protect Sc 41:83–85 (in Japanese)
Tomiczek C, Krehan H, Menschhorn P (2002) Dangerous Asiatic longicorn beetle found in Austria: new danger for our trees? AFZ/Der Wald. Allg Forst Zeitschrift für Waldwirtschaft und Umweltversorge 57:52–54
Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97:5948–5953
United States Department of Agriculture Animal and Plant Health Inspection Service (2007) Asian Longhorned Beetle. http://www.aphis.usda.gov/plant_health/plant_pest_info/asian_lhb/index.shtml. Accessed 2 Oct 2008
United States Department of Agriculture Animal and Plant Health Inspection Service (2008) Asian Longhorned Beetle. http://www.aphis.usda.gov/plant_health/plant_pest_info/asian_lhb/alb_cargomaps.shtml. Accessed 2 Oct 2008
United States Department of Agriculture Forest Service (2004) Chicago vs. the Asian longhorned beetle: a portrait of success. Misc Publ 1593. US Government Printing Office. Washington, 49 pp
Wade MJ, Shuster SM, Stevens L (1996) Inbreeding: its effect on response to selection for pupal weight and the heritable variance in fitness in the flour beetle, Tribolium castaneum. Evolution 50:723–733
Wares JP, Hughes AR, Grosberg RK (2005) Mechanisms that drive evolutionary change. In: Sax DF, Staachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates, Sunderland, pp 229–257
Wasserman J. (2005) Pest may threaten trees: Asian beetles apparently escaped from a Sacrament warehouse. Sacramento Bee July 14
Westphal MI, Browne M, MacKinnon K, Noble I (2008) The link between international trade and the global distribution of invasive alien species. Biol Invasions 10:391–398
Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615
Acknowledgments
We thank A. Liang for technical assistance. K. Loeffler assisted in the preparation of figures. We are grateful to the following people for providing specimens for analysis: A. Sawyer, M. Keena, E. Richard Hoebeke, J. Liebherr, F. Hérard, C. Tomiczek, S. Lingafelter, B. Emens and D. Lance. USDA-APHIS provided some supplies for this work. This work was supported by a gift from Howard P. Milstein and Leonard Litwin to Cornell University and USDA Specific Cooperative Agreement # 58-1926-6-606 to Richard Harrison and Michael Smith. We thank two anonymous reviewers for constructive and helpful comments on an earlier version of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Carter, M., Smith, M. & Harrison, R. Genetic analyses of the Asian longhorned beetle (Coleoptera, Cerambycidae, Anoplophora glabripennis), in North America, Europe and Asia. Biol Invasions 12, 1165–1182 (2010). https://doi.org/10.1007/s10530-009-9538-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-009-9538-9