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Analysis of genetic diversity in an invasive population of Asian long-horned beetles in Ontario, Canada

Published online by Cambridge University Press:  02 April 2012

Maureen E. Carter*
Affiliation:
Department of Entomology, Comstock Hall, Cornell University, Ithaca, New York 14853-2601, United States of America
Michael T. Smith
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Beneficial Insect Introduction Research Unit, Newark, Delaware 19713, United States of America
Jean J. Turgeon
Affiliation:
Great Lakes Forestry Centre, Canadian Forest Service, Natural Resources Canada, Sault Ste. Marie, Ontario, Canada P6A 2E5
Richard G. Harrison
Affiliation:
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853, United States of America
*
1Corresponding author (e-mail: [email protected]).

Abstract

Adult Asian long-horned beetles, Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae: Lamiinae), were discovered in Ontario, Canada, in 2003 in the vicinity of a commercial warehouse. Trees were heavily scarred with signs of attack and larvae and adult beetles were common, suggesting that there had been multiple generations at the site. We amplified 16 microsatellite loci from 326 beetles to examine genetic diversity in this population. Based on Hardy – Weinberg equilibrium, 6 of 16 loci were monomorphic and 8 were not, indicating nonrandom mating. Measures of microsatellite genetic diversity and mitochondrial DNA haplotype diversity were significantly lower than those in A. glabripennis from China and Korea but were not significantly different from those in the New York City population. The proportion of different multilocus genotypes in the Ontario population was lower than in the populations in New York City and Linden, New Jersey. These results suggest that limited genetic diversity in the Ontario population has not hampered reproduction of this invasive insect. This genetic signature is common in other invasive species, likely because a population is founded by a few closely related individuals, or a large founding population suffers subsequent genetic bottlenecks.

Résumé

Des adultes du longicorne asiatique, Anoplophora glabripennis (Motschulsky) (Coleoptera : Cerambycidae : Lamiinae), ont été découverts en Ontario, Canada, en 2003 près d’un entrepôt commercial. Les arbres portaient de fortes lacérations dues à l’attaque des coléoptères et les larves et les adultes y étaient nombreux, ce qui laisse croire qu’il y avait eu plusieurs générations à ce site. Nous avons examiné la diversité génétique de la population en amplifiant 16 locus microsatellites chez 326 coléoptères. Six des 16 locus sont monomorphes et 8 locus ne suivent pas l’équilibre Hardy – Weinberg, ce qui indique que les accouplements ne sont pas aléatoires. Les mesures de diversité génétique des microsatellites et de diversité des haplotypes d’ADN mitochondrial sont significativement plus faibles que celles d’A. glabripennis en Chine et en Corée, mais elles ne diffèrent pas significativement des mesures de la population de la ville de New York. La proportion de génotypes différents à locus multiples est plus faible dans la population d’Ontario que dans les populations de la ville de New York et de Linden (New Jersey). Ces résultats indiquent que la diversité génétique restreinte de la population d’Ontario n’a pas nui à la reproduction de cet insecte envahissant. Une telle signature génétique est commune chez d’autres espèces envahissantes, vraisemblablement parce que la population est fondée sur un petit nombre d’individus fortement apparentés ou alors parce qu’une population fondatrice de grande taille subit plus tard des goulots d’étranglement génétiques.

[Traduit par la Rédaction]

Type
Articles
Copyright
Copyright © Entomological Society of Canada 2009

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References

Cai, Y.-W., Cheng, X.-Y., Xu, R.-M., Duan, D.-H., and Kirkendall, L.R. 2008. Genetic diversity and biogeography of red turpentine beetle Dendroctonus valens in its native and invasive regions. Insect Science 15(4): 291301 doi:10.1111/j.1744-7917.2008.00213.x.CrossRefGoogle Scholar
Canadian Food Inspection Agency. 2003. Toronto—Vaughan, Ontario _ regulated area [online]. Canadian Food Inspection Agency. Available from http://www.inspection.gc.ca/english/plaveg/pestrava/anogla/mc/mapcarrege.shtml [accessed 4 February 2009].Google Scholar
Canadian Food Inspection Agency. 2008. Asian longhorned beetle _ latest information [online]. Canadian Food Inspection Agency. Available from http://www.inspection.gc.ca/english/plaveg/pestrava/anogla/situatione.shtml [accessed 20 October 2008].Google Scholar
Carroll, S.P. 2007. Brave New World: the epistatic foundations of natives adapting to invaders. Genetica, 129(2): 193204 PMID:16924403doi:10.1007/s10709-006-9014-8.CrossRefGoogle ScholarPubMed
Carter, M., Casa, A.M., Zeid, M., Mitchell, S.E., and Kresovich, S. 2009 a. Isolation and characterization of microsatellite loci for the Asian longhorned beetle, Anoplophora glabripennis. Molecular Ecology Resources, 9(3): 925928 doi:10.1111/j.1755-0998.2008.02485.x.Google ScholarPubMed
Carter, M., Smith, M., and Harrison, R. 2009 b. Genetic analyses of the Asian longhorned beetle (Coleoptera, Cerambycidae, Anoplophora glabripennis), in North America, Europe and Asia. Biological Invasions. In press. doi:10.1007/s10530-009-9538-9.CrossRefGoogle Scholar
Carter, M.E., Smith, M.T., and Harrison, R.G. 2009 c. Patterns of genetic variation among populations of the Asian longhorned beetle (Coleoptera: Cerambycidae) in China and Korea. Annals of the Entomological Society of America, 102(5): 985–905.CrossRefGoogle Scholar
Cavey, J.F., Hoebeke, E.R., Passoa, S., and Lingafelter, S.W. 1998. A new exotic threat to North American hardwood forests: an Asian longhorned beetle, Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae). I. Larval description and diagnosis. Proceedings of the Entomological Society of Washington, 100: 373381.Google Scholar
Cheverud, J.M., Vaughn, T.T., Pletscher, L.S., King-Ellison, K., Bailiff, J., Adams, E., et al. 1999. Epistasis and the evolution of additive genetic variance in populations that pass through a bottleneck. Evolution, 53(4): 10091018 doi:10.2307/2640806.CrossRefGoogle Scholar
Colautti, R.I., Bailey, S.A., van Overdijk, C.D.A., Amundsen, K., and MacIssac, H.J. 2006. Characterised and projected costs of nonindigenous species in Canada. Biological Invasions, 8(1): 4559 doi:10.1007/s10530-005-0236-y.CrossRefGoogle Scholar
Dlugosch, K.M., and Parker, I.M. 2008. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology, 17(1): 431449 PMID:17908213 doi:10.1111/j.1365-294X.2007.03538.x.CrossRefGoogle ScholarPubMed
Eales, J., Thorpe, R.S., and Malhotra, A. 2008. Weak founder effect signal in a recent introduction of Caribbean Anolis. Molecular Ecology, 17(6): 14161426 PMID:18266633 doi:10.1111/j.1365-294X.2007.03684.x.CrossRefGoogle Scholar
Falush, D., Stephens, M., and Pritchard, J.K. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164(4): 15671587 PMID:12930761.CrossRefGoogle ScholarPubMed
Ficetola, G.F., Bonin, A., and Miaud, C. 2008. Population genetics reveals origin and number of founders in a biological invasion. Molecular Ecology, 17(3): 773782 PMID:18194168.CrossRefGoogle Scholar
Goudet, J. 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity, 86: 485486.CrossRefGoogle Scholar
Grapputo, A., Boman, S., Lindström, L., Lyytinen, A., and 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(14): 42074219 PMID:16313587.CrossRefGoogle ScholarPubMed
Haack, R.A., Law, K.R., Mastro, V.C., Ossenbruggen, H.S., and Raimo, B.J. 1997. New York's battle with the Asian longhorned beetle. Journal of Forestry, 95(1): 1115.Google Scholar
Hajek, A.E., and Kalb, D.M. 2007. Suitability of Acer saccharum and Acer pensylvanicum (Aceraceae) for rearing Anoplophora glabripennis (Coleoptera: Cerambycidae). The Canadian Entomologist, 139(5): 751755 doi:10.4039/N06-107.CrossRefGoogle Scholar
Hérard, F., Ciampitti, M., Maspero, M., Krehan, H., Benker, U., Boegel, C., et al. 2006. Anoplophora species in Europe: infestations and management processes. EPPO (European and Mediterranean Plant Protection Organization) Bulletin, 36: 470474.Google Scholar
Hunter, W.B., Smith, M.T., and Hunnicutt, L.E. 2009. Analysis and functional annotation of expressed sequence tags from the Asian longhorned beetle, Anoplophora glabripennis. Journal of Insect Science, 9(21): 113 doi:10.1673/031.009.2101.CrossRefGoogle ScholarPubMed
Jarne, P., and Lagoda, P.J.L. 1996. Microsatellites, from molecules to populations and back. Trends in Ecology and Evolution, 11(10): 424429 doi:10.1016/0169-5347(96)10049-5.CrossRefGoogle ScholarPubMed
Keena, M.A. 2002. Anoplophora glabripennis (Coleoptera: Cerambycidae) fecundity and longevity under laboratory conditions: comparisons of populations from New York and Illinois on Acer saccharum. Environmental Entomology, 31: 490498.CrossRefGoogle Scholar
Keena, M.A. 2005. Pourable artificial diet for rearing Anoplophora glabripennis (Coleoptera: Cerambycidae) and methods to optimize larval survival and synchronize development. Annals of the Entomological Society of America, 98(4): 536547 doi:10.1603/0013-8746(2005)098[0536:PADFRA]2.0.CO;2.CrossRefGoogle Scholar
Laffin, R.D., Dosdall, L.M., and Sperling, F.A.H. 2005. Population structure of the cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) (Coleoptera Curculionidae): origins of North American introductions. Environmental Entomology, 34(2): 504510.CrossRefGoogle Scholar
Lingafelter, S.W., and Hoebeke, E.R. 2002. Revision of Anoplophora (Coleoptera: Cerambycidae) Entomological Society of Washington, Washington, D.C.Google Scholar
Liu, K., and Muse, S.V. 2005. Power Marker: an integrated analysis environment for genetic marker analysis. Bioinformatics, 21(9): 21282129 PMID:15705655 doi:10.1093/bioinformatics/bti282.CrossRefGoogle Scholar
Maspero, M., Jucker, C., and Colombo, M. 2007. First record of Anoplophora glabripennis (Motschulsky) (Coleoptera Cerambycidae Lamiinae Lamiini) in Italy. Bollettino di Zoologia Agraria e di Bachicoltura, 39(2): 161164.Google Scholar
Moore, R., and Russell, R. 1990. The “Three North” forest protection system — China. Agroforestry Systems, 10(1): 7188 doi:10.1007/BF00118728.Google Scholar
Morewood, W.D., Neiner, P.R., McNeil, J.R., Sellmer, J.C., and Hoover, K. 2003. Oviposition preference and larval performance of Anoplophora glabripennis (Coleopterea: Cerambycidae) in four eastern North American hardwood tree species. Environmental Entomology, 32(5): 10281034.CrossRefGoogle Scholar
Morewood, W.D., Neiner, P.R., Sellmer, J.C., and Hoover, K. 2004. Behavior of adult Anoplophora glabripennis on different tree species under greenhouse conditions. Journal of Insect Behavior, 17(2): 215226 doi:10.1023/B:JOIR.0000028571.52739.50.CrossRefGoogle Scholar
Naciri-Graven, Y., and Goudet, J. 2008. The additive genetic variance after bottlenecks is affected by the number of loci involved in epistatic interactions. Evolution, 7: 706716.Google Scholar
Nei, M., Maruyama, T., and Chakraborty, R. 1975. The bottleneck effect and genetic variability in populations. Evolution, 29(1): 110 doi:10.2307/2407137.CrossRefGoogle ScholarPubMed
North American Plant Protection Organization. 2007. Update on the Asian longhorned beetle (Anoplophora glabripennis) — Canada. Phytosanitary Alert Official Pest Report 10/12/2007 [online]. Available from http://www.pestalert.org/oprDetail.cfm?oprID=288 [accessed 19 October 2008].Google Scholar
Nowak, D.J., Pasek, J.E., Sequeira, R.A., Crane, D.E., and Mastro, V.C. 2001. Potential effect of Anoplophora glabripennis (Coleoptera: Cerambycidae) on urban trees in the United States. Journal of Economic Entomology, 94(1): 116122 PMID:11233100.CrossRefGoogle ScholarPubMed
Oliveira, E.J., Padua, J.G., Zucchi, M.I., Vencovsky, R., and Vieira, M.L.C. 2006. Origin, evolution and genome distribution of microsatellites. Genetics and Molecular Biology, 29(2): 294307 doi:10.1590/S1415-47572006000200018.CrossRefGoogle Scholar
Pan, H.Y. 2005. Review of the Asian longhorned beetle: research, biology, distribution and management in China [online]. Working Paper FBS/6E, Forestry Department, Food and Agriculture Organization, Rome, Italy. Available from http://www.fao.org/forestry/media/66891/1/102/ [accessed 27 May 2008].Google Scholar
Park, S.D.E. 2001. Trypanotolerance in West African cattle and the population genetic effects of selection [online]. Ph.D. thesis, University of Dublin, Dublin, Eire. Available from http://animalgenomics.ucd.ie/sdepark/ms-toolkit/ [accessed 12 June 2009].Google Scholar
Piry, S., Alapetite, A., Cornuet, J.-M., Paetkau, D., Baudouin, L., and Estoup, A. 2004. GENECLASS2: a software for genetic assignment and first-generation migrant detection. Journal of Heredity, 95(6): 536539 PMID:15475402 doi:10.1093/jhered/esh074.CrossRefGoogle ScholarPubMed
Poland, T.M., Haack, R.A., and Petrice, T.R. 1998. Chicago joins New York in battle with the Asian longhorned beetle. Newsletter of the Michigan Entomological Society, 43: 1517.Google Scholar
Rannala, B., and Mountain, J.L. 1997. Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences of the United States of America, 94(17): 91979201 PMID:9256459 doi:10.1073/pnas.94.17.9197.CrossRefGoogle ScholarPubMed
Raymond, M., and Rousset, F. 1995. Genepop (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86(3): 248249.CrossRefGoogle Scholar
Ric, J., de Groot, P., Gasman, B., Orr, M., Doyle, J., Smith, M.T., et al. 2007. Detecting signs and symptoms of Asian longhorned beetle injury: a training guide [online]. Canadian Forest Service, Sault Ste. Marie, Ontario. Available from http://warehouse.pfc.forestry.ca/glfc/26860.pdf [accessed 19 November 2008].Google Scholar
Roderick, G.K., and Navajas, M. 2003. Genes in new environments: genetics and evolution in biological control. Nature Reviews Genetics, 4(11): 889899 PMID:14634636 doi:10.1038/nrg1201.CrossRefGoogle ScholarPubMed
Sabol, O. 2006. Faunistic records from the Czech Republic — 196. Klapalekiana, 42: 78.Google Scholar
Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molofsky, J., With, K.A., et al. 2001. The population biology of invasive species. Annual Revue of Ecology and Systematics, 32(1): 305332 doi:10.1146/annurev.ecolsys.32.081501.114037.CrossRefGoogle Scholar
Sawyer, A.J. 2003. Annotated categorization of ALB host trees [online]. United States Department of Agriculture, Animal and Plant Health Protection Service, Plant Protection and Quarantine, Otis Plant Protection Laboratory, Otis Air National Guard Base, Otis, Massachusetts. Available from http://www.uvm.edu/albeetle/hosts.htm [accessed 4 October 2008].Google Scholar
Sawyer, A.J. 2006. A controlled study of the healing response of host trees to simulated Asian longhorned beetle damage. In Emerald Ash Borer and Asian Longhorned Beetle Research and Development Review Meeting, Cincinnati, Ohio, 29 October — 2 November 2006. Compiled by Mastro, V., Lance, D., Reardon, R., and Parra, G.. FHTET-2007–04, United States Department of Agriculture, Animal and Plant Health Protection Service, Plant Protection and Quarantine, Otis Air National Guard Base, Otis, Massachusetts pp. 126128.Google Scholar
Schlötterer, C. 2004. The evolution of molecular markers — just a matter of fashion? Nat. Rev. Genet. 5(1): 6369 PMID:14666112 doi:10.1038/nrg1249.CrossRefGoogle ScholarPubMed
Sellers, C. 2004. The Asian longhorned beetle in Ontario. Ontario Insects, 9: 21.Google Scholar
Smith, M.T., Bancroft, J., and Tropp, J. 2002. Agespecific fecundity of Anoplophora glabripennis (Coleoptera: Cerambycidae) on three tree species infested in the United States. Environmental Entomology, 31(1): 7683.CrossRefGoogle Scholar
Smith, M.T., Tobin, P., Bancroft, J.S., Li, G., and Gao, R. 2004. Dispersal and spatiotemporal dynamics of Asian longhorned beetle (Coleoptera: Cerambycidae) in China. Environmental Entomology, 33(2): 435442.CrossRefGoogle Scholar
Tomiczek, C., Krehan, H., and Menschhorn, P. 2002. Dangerous Asiatic longicorn beetle found in Austria: new danger for our trees?. AFZ/der Wald: allgemeine Forst Zeitschrift für Wald-wirtschaft und Umweltversorge, 57(2): 5254.Google Scholar
Turgeon, J.J., Ric, J., DeGroot, P., Gasman, B., Orr, M., Doyle, J., et al. 2007.c Détection des signes et des symptômes d'attaque par le longicone étoilé: guide de formation [online]. Agence canadienne d'inspection des aliments, Sault Ste. Marie, Ontario. Available from http://warehouse.pfc.forestry.ca/glfc/26861.pdf [accessed 16 June 2009].Google Scholar
Uchida, E., Xu, J., and Rozelle, S. 2005. Grain for green: cost-effectiveness and sustainability of China's conservation set-aside program. Land Economics 81(2): 247264.CrossRefGoogle Scholar
Wade, M.J., Shuster, S.M., and 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(2): 723733 doi:10.2307/2410845.CrossRefGoogle ScholarPubMed
Wang, Z. 2004. Occurrence of Anoplophora glabripennis (Motsch.) and control in China. Ph.D. thesis, Northeast Forestry University of China, Harbin, Heilongjiang Province, People's Republic of China.Google Scholar
Wares, J.P., Hughes, A.R., and Grosberg, R.K. 2005. Mechanisms that drive evolutionary change. In Species invasions: insights into ecology, evolution, and biogeography. Edited by Sax, D.F., Staachowicz, J.J., and Gaines, S.D.. Sinauer Associates Inc., Sunderland, Massachusetts. pp. 229257.Google Scholar
Weir, B.S., and Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38(6): 13581370 doi:10.2307/2408641.Google ScholarPubMed
Williams, D.W., Lee, H.P., and Kim, I.K. 2004. Distribution and abundance of Anoplophora glabripennis (Coleoptera: Cerambycidae) in natural Acer stands in South Korea. Environmental Entomology, 33(3): 540545.CrossRefGoogle Scholar
Xiao, G. 1992. Forest insects of China. China Forestry Publishing House, Bejing, People's Republic of China.Google Scholar
Yin, W., and Lu, W. 2005. Review of tree selection and afforestation for control of Asian long-horned beetle in north China [online]. Forestry Department Working Paper FBS/7E, Food and Agriculture Organization, Rome, Italy. Available from http://www.fao.org/forestry/media/7175/102/ [accessed 27 May 2008].Google Scholar
Zayed, A., Constantin, S.A., and Packer, L. 2007. Successful biological invasion despite a severe genetic load. PLoS One, 9: 16.Google Scholar
Zhang, P., Shao, G., Zhao, G., Le Master, D.C., Parker, G.R., Dunning, J.B. Jr., Li, Q. 2000. China's forest policy for the 21st century. Science (Washington, D.C.), 288(5474): 21352136 PMID:10896587 doi:10.1126/science.288.5474.2135.Google Scholar