Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-27T07:45:48.912Z Has data issue: false hasContentIssue false

Population genetic differentiation of the black locust gall midge Obolodiplosis robiniae (Haldeman) (Diptera: Cecidomyiidae): a North American pest invading Asia

Published online by Cambridge University Press:  08 September 2015

X. Shang
Affiliation:
Key Laboratory of State Forestry Administration on Forest Protection, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China
Y. Yao
Affiliation:
Key Laboratory of State Forestry Administration on Forest Protection, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China
W. Huai
Affiliation:
Key Laboratory of State Forestry Administration on Forest Protection, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China
W. Zhao*
Affiliation:
Key Laboratory of State Forestry Administration on Forest Protection, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China
*
*Author for correspondence Phone: +86 1062889501 Fax: +86 1062889587 E-mail: [email protected]

Abstract

Obolodiplosis robiniae is native to North America and is an important introduced insect pest that forms leaf margin roll galls on species of genus Robinia (Fabaceae) in China. It was first detected in China in 2004, but subsequently spread and provoked local outbreaks. An analysis of a 676-bp sequence of the mitochondrial DNA cytochrome oxidase subunit I was conducted in 560 individuals from 28 populations, in order to (1) assess population genetic structuring and (2) explore possible explanations for the rapid spread and invasion success of O. robiniae. Yet, only four haplotypes were identified and the nucleotide diversity was low (π = 0.00005) and among the 560 specimens studied, only ten showed haplotypic variation involving no more than three substitutions. The result showed a low degree of genetic diversity among populations of the successful invasive gall midge, which suggested that the pest experienced a severe genetic bottleneck and a loss of genetic diversity after its introduction. The successful establishment and spread of O. robiniae in China is attributed to the wide distribution of its host plant, thus allowing ample opportunities for gene flow in the pest species, and to the advantageous life history characteristics of O. robiniae.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amouroux, P., Normand, F., Nibouche, S. & Delatte, H. (2013) Invasive mango blossom gall midge, Procontarinia mangiferae (Felt) (Diptera: Cecidomyiidae) in Reunion Island: ecological plasticity, permanent and structured populations. Biological Invasions 15, 16771693.Google Scholar
Boubou, A., Migeon, A., Roderick, G. & Navajas, M. (2011) Recent emergence and worldwide spread of the red tomato spider mite, Tetranychus evansi: genetic variation and multiple cryptic invasions. Biological Invasions 13, 8192.Google Scholar
Brown, B., Emberson, R.M. & Paterson, A.M. (1999) Mitochondrial COI and II provide useful markers for Weiseana (Lepidoptera, Hepialidae) species identification. Bulletin of Entomological Research 89, 287294.Google Scholar
Clary, D.O. & Wolstenholme, D.R. (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. Journal of Molecular Evolution 22, 252271.Google Scholar
Csoka, G. (2006) The first occurrence of the gall midge Obolodiplosis robiniae (Haldeman) in Hungary. Az akac–gubacsszunyog Obolodiplosis robiniae (Haldeman) megjelenese magyarorszagon. Novenyvedelem (Bp) 42, 663664.Google Scholar
Davis, M.A. (2009) Invasion Biology. New York, Oxford University Press.Google Scholar
Duso, C., Fontana, P. & Tirello, P. (2005) Spread of the gall midge Obolodiplosis robiniae (Haldeman) injurious to black locust in Italy and Europe. Informatore Fitopatologico 55, 3033.Google Scholar
Duso, C., Boaria, A., Surian, L. & Buhl, P.N. (2011) Seasonal abundance of the nearctic gall midge Obolodiplosis robiniae in Italy and the impact of its antagonist Platygaster robiniae on pest populations. Annals of the Entomological Society of America 104, 180191.Google Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (ver.3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 4750.Google Scholar
Facon, B., Genton, B.J., Shykoff, J., Jarne, P., Estoup, A. & David, P. (2006) A general eco–evolutionary framework for understanding bioinvasions. Trends in Ecology and Evolution 21, 130135.Google Scholar
Folmer, O., Black, M., Hoew, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google Scholar
Funk, D.J., Futuyama, D.J., Orti, G. & Meyer, A. (1995) Mitochondrial DNA sequences and multiple data sets: a phylogenetic study of phytophagous beetles (Chrysomelidae: Ophraella). Molecular Biology and Evolution 12, 627640.Google Scholar
Haldeman, S.S. (1847) Description of several new and interesting animals. American Journal of Agricultural Science 6, 191194.Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. & DeWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B Biological Sciences 270, 313321.Google Scholar
Hoffmann, D., Lichtenberger, T. & Beiderbeck, R. (2007) The American gall wasp Obolodiplosis robiniae (Haldeman, 1847) in Robinia in Germany. DGaaE Nachrichten 21, 8687.Google Scholar
Horst, C.P. & Lau, J.A. (2015) Genetic variation in invasive species response to direct and indirect species interactions. Biological Invasions 17, 651659.Google Scholar
Jorgensen, J. (2009) Obolodiplosis robiniae (Haldeman, 1847) (Cecidomyiidae) and its parasitoid Platygaster robiniae Buhl et Duso, 2007 (Platygastridae) two species new for Denmark. Entomologiske Meddelelser 77, 141144.Google Scholar
Kirk, H., Dorn, S. & Mazzil, D. (2013) Molecular genetics and genomics generate new insights into invertebrate pest invasions. Evolutionary Applications 6, 842856.Google Scholar
Knowlton, N. & Weigt, L.A. (1998) New dates and new rates for divergence across the Isthmus of Panama. Proceedings of the Royal Society of London B Biological Sciences 265, 22572263.Google Scholar
Kodoi, F., Lee, H.S., Uechi, N. & Yukawa, J. (2003) Occurrence of Obolodiplosis robiniae (Diptera: Cecidomyiidae) in Japan and South Korea. Esakia 43, 3541.Google Scholar
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.Google Scholar
Lin, B.M., Qiao, X.R., Xu, D.H. & Han, Y.S. (2007) Investigation and control on Robinia pseudoacacia in Qinhuangdao City. Forestry Science and Technology 32, 3031.Google Scholar
Lin, L.L., Zeng, L., Liang, G.W., Wu, J.J., Gu, Y.J., Liu, H.J. & Hu, X.N. (2010) Genetic differentiation in the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Journal of Environmental Entomology 32, 469475.Google Scholar
Mu, X.F., Sun, J.S., Lu, W.F., Li, M., Qu, H.X. & Gao, Z.Y. (2010) Bionomics and control of Obolodiplosis robiniae in Beijing. Forest Pest and Disease 29, 1518.Google Scholar
Navone, P. & Tavella, L. (2004) Obolodiplosis robiniae, a pest of the false acacia. Informatore Agrario 60, 5758.Google Scholar
Nei, M., Maruyama, T. & Chakraborty, R. (1975) The bottleneck effect and genetic variability in populations. Evolution 29, 110.Google Scholar
Pan, Z.G. & You, Y.T. (1994) Growing Exotic Trees in China. Beijing, China, Science and Technology Press.Google Scholar
Park, J.D., Shin, S.C., Kim, C.S. & Park, I.K. (2009) Biological characteristics of Obolodiplosis robiniae and control effects of some insecticides. Korean Journal of Applied Entomology 48, 327333.Google Scholar
Perdereau, E., Dedeine, F., Christidès, J.P., Dupont, S. & Bagnères, A.G. (2011) Competition between invasive and indigenous species: an insular case study of subterranean termites. Biological Invasions 13, 14571470.Google Scholar
Pernek, M. & Matosevic, D. (2009) Black locust gall midge (Obolodiplosis robiniae), new pest on black locust trees and first record of parasitoid Platygaster robinae in Croatia. Sumarski List 133, 157163.Google Scholar
Prins, H.H.T. & Gordon, L.J. (2014) Invasion Biology and Ecological Theory. New York, Cambrige University Press.Google Scholar
Qiang, W.X., Bing, J.C., Sun, W., Du, W.Q. & Li, J.J. (2002) Occurrence regularity and control of geometrid moths attacking Robinia pseudoacacia in Tianshui. Forest Pest and Disease 21, 2325.Google Scholar
Roman, J. & Darling, J.A. (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends in Ecology and Evolution 22, 454463.Google Scholar
Roskam, H., Aa, H., As, B., Bijkerk, J., Ellis, W. & Moraal, L. (2008) Explosive occurrence of Obolodiplosis robiniae (Diptera: Cecidomyiidae), a gall midge new for the Netherlands. Entomologische Berichten 68, 2728.Google Scholar
Saiki, R.K., Gelfand, D.H., Stoffel, S., Higuchi, R., Horn, G.T., Mullis, K.B. & Erlich, H.A. (1988) Primer–directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 139, 487491.Google Scholar
Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molofsky, J., With, K.A., Baughman, S., Cabin, R.J., Cohen, J.E., Ellstrand, N.M., McCauley, D.E., O'Neil, P., Parker, I.M., Thompson, J.N. & Weller, S.G. (2001) The population biology of invasive species. Annual Review of Ecology and Systematics 32, 305332.Google Scholar
Shao, X.K., Ma, X.G., Shao, K.F., Lv, J. & Han, G.S. (2010) Occurrence, damage and control of Obolodiplosis robiniae . Journal of Liaoning Forestry Science & Technology 4, 3132.Google Scholar
Shirota, Y., Iituka, K., Asano, J., Abe, J. & Yukawa, J. (1999) Intraspecific variations of mitochondrial cytochrome oxidase I sequence in an aphidophagous species, Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Entomological Science 2, 209215.Google Scholar
Skrzypczynska, M. (2008) Gall midge Obolodiplosis robiniae (Haldeman, 1847) – the new pest of Robinia pseudoacacia L. leaves in Poland. Sylwan 152, 1416.Google Scholar
Staden, R., Beal, K.F. & Bonfield, J.K. (1999) The Staden Package, 1998. Methods in Molecular Biology 132, 115130.Google Scholar
Suarez, A.V., Holway, D.A. & Case, T.J. (2001) Patterns of spread in biological invasions dominated by long–distance jump dispersal: insights from Argentine ants. Proceedings of the National Academy of Sciences of the USA 98, 10951100.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.Google Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 48764882.Google Scholar
Tóth, P., Váková, M. & Lukán, J. (2009) The distribution of Obolodiplosis robiniae on black locust in Slovakia. Journal of Pest Science 82, 6166.Google Scholar
Uechi, N., Yukawa, J. & Usuba, S. (2005) Recent distributional records of an alien gall midge, Obolodiplosis robiniae (Diptera: Cecidomyiidae) in Japan, and a brief description of its pupal morphology. Kyushu Plant Protection Research 51, 8993.Google Scholar
Uechi, N., Yukawa, J., Tokuda, M., Ganaha-Kikumura, T. & Taniguchi, M. (2011) New information on host plants and distribution ranges of an invasive gall midge, Contarinia maculipennis (Diptera: Cecidomyiidae), and its congeners in Japan. Applied Entomology and Zoology 46, 383389.Google Scholar
Wang, G.Y. (2009) Primary study on biology, ecology and chemical control of Obolodiplosis robiniae. Master Dissertation, Shandong Agriculture University, Taian, China, p. 32.Google Scholar
Wermelinger, B. & Skuhravá, M. (2007) First records of the gall midge Obolodiplosis robiniae Haldeman) (Diptera: Cecidomyiidae) and its associated parasitoid Platygaster robiniae Buhl & Duso (Hymnenoptera: Platygastridae) in Switzerland. Bulletin de la Société Entomologique Suisse 80, 217221.Google Scholar
Woo, K.S., Choe, H.J. & Kim, H.J. (2003) A report on the occurrence of yellow locust midge Obolodiplosis robiniae (Haldeman, 1847) from Korea. Korean Journal of Applied Entomology 42, 7779.Google Scholar
Xu, X.Q. & Yang, M.S. (2006) Review on utilization of Robinia pseudoacacia . Journal of Hebei Forestry Science and Technology S1, 54.Google Scholar
Yan, J.H., Wang, S.L. & Li, D.J. (2007) A new invasive forest insect pest – Obolodiplosis robiniae (Diptera: Cecidomyiidae) in Shandong. Journal of Shandong Forestry Science and Technology 6, 60.Google Scholar
Yang, Z.Q., Qiao, X.R., Bu, W.J., Yao, Y.X., Xiao, Y. & Han, Y.S. (2006) First discovery of an important invasive insect pest, Obolodiplosis robiniae (Diptera: Cecidomyiidae) in China. Acta Entomologica Sinica 49, 10501053.Google Scholar
Zhang, D.F., Lu, C.K., Wang, X.Q. & Gao, B.J. (2009) Potential risk assessment of Obolodiplosis robiniae (Haldeman) in China. Acta Ecologica Sinica 29, 21552161.Google Scholar
Zhang, D.X. & Hewitt, G.M. (1997) Assessment of the universality and utility of a set of conserved mitochondrial primers in insects. Insect Molecular Biology 6, 143150.Google Scholar
Zhang, W., Fu, J.C., Wei, G.X. & Sun, Y.M. (2008) Occurrence of Obolodiplosis robiniae (Haldeman) in Jilin City. Northern Horticult 6, 207.Google Scholar
Zhou, Z.X., Wan, F.H., Zhang, G.F. & Chen, B. (2007) A rapid method for extraction of genomic DNA of Bemisia tabaci . Plant Protection 33, 131133.Google Scholar