Role of a gamma-aminobutryic acid (GABA) receptor mutation in the evolution and spread of Diabrotica virgifera virgifera resistance to cyclodiene insecticides

Insect Molecular Biology

Volumn 22, Issue 5, 2013, Pages 473-484

  Wang, H ^a   Coates, B S ^b   Chen, H ^a   Sappington, T W ^b   Guillemaud, T ^c   Siegfried, B D ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c Institut Sophia Agrobiotech   (France)

Author keywords

insecticide resistance; population genetics; range expansion; single nucleotide polymorphism; western corn rootworm

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ALDRIN; CHLORINATED HYDROCARBON; INSECTICIDE;

ANIMAL; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BEETLE; BIOASSAY; DIABROTICA VIRGIFERA; DNA SEQUENCE; DRUG EFFECT; GENETICS; INSECTICIDE RESISTANCE; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; MUTATION; NORTH AMERICA; PHYSIOLOGY; POPULATION GENETICS; RANGE EXPANSION; SINGLE NUCLEOTIDE POLYMORPHISM;

INSECTICIDE RESISTANCE; POPULATION GENETICS; RANGE EXPANSION; SINGLE NUCLEOTIDE POLYMORPHISM; WESTERN CORN ROOTWORM;

ALDRIN; ANIMALS; BEETLES; BIOLOGICAL ASSAY; CHROMOSOMES, ARTIFICIAL, BACTERIAL; EVOLUTION, MOLECULAR; HYDROCARBONS, CHLORINATED; INSECTICIDE RESISTANCE; INSECTICIDES; MUTATION; NORTH AMERICA; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, GABA; SEQUENCE ANALYSIS, DNA;

EID: 84883500137     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/imb.12037     Document Type: Article

References (63)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and, Lipman, D.J., (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Aronstein, A., Ode, P., and, ffrench-Cosntant, R.H., (1995) PCR based monitoring of specific Drosophila (Diptera: Drosophilidae) cyclodiene resistance alleles in the presence and absence of selection. Bull Entomol Res 85: 5-9.
3. Ball, H.J., (1983) Aldrin and dieldrin residues in Nebraska (USA) soils as relatd to decreasing LD50 values for adult western corn rootworm (Diabrotica virgifera), 1962-1981. J Environ Sci Health B18: 735-744. (Pubitemid 14196613)
4. Ball, H.J., and, Hill, R.E., (1953) You can control corn rootworm. Nebraska Experiment Station Quarterly. Winter 1952-53, Nebraska Agricultural Experiment Station, Lincoln, Nebraska.
5. Ball, H.J., and, Roselle, R.E., (1954) You can control corn rootworms. University of Nebraska Extension Circular 1567.
6. Ball, H.J., and, Weekman, G.T., (1962) Insecticide resistance in the adult western corn rootworm in Nebraska. J Econ Entomol 55: 439-441.
7. Ball, H.J., and, Weekman, G.T., (1963) Differential resistance of corn rootworms to insecticides in Nebraska and adjoining states. J Econ Entomol 56: 553-555.
8. Bass, C., Schroeder, I., Turberg, A., Field, L.M., and, Williamson, M.S., (2004) Identification of the Rdl mutation in laboratory and field strains of the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). Pest Manag Sci 60: 1157-1162. (Pubitemid 39577211)
9. Beeman, R.W., and, Stuart, J.J., (1990) A gene for Lindane + cyclodiene resistance in the red flour beetle (Coleoptera: Tenebrionidae). J Econ Entomol 83: 1745-1751.
10. Benjamini, Y., and, Yekutieli, D., (2001) The control of false discovery rate in multiple testing under dependency. Ann Stat 29: 1165-1188. (Pubitemid 33575263)
11. Black, W.C., and, Vontas, J.G., (2007) Affordable assays for genotyping single nucleotide polymorphisms in insects. Insect Mol Biol 16: 377-387. (Pubitemid 47094269)
12. Branson, T.F., (1976) The selection of a non-diapause strain of Diabrotica virgifera (Coleoptera: Chrysomelidae). Entomol Exp Appl 19: 148-154.
13. Buckingham, S.D., Biggin, P.C., Sattelle, B.M., Brown, L.A., and, Sattelle, D.B., (2005) Insect GABA receptors: splicing, editing, and targeting by antiparasitics and insecticides. Mol Pharmacol 68: 942-951. (Pubitemid 41345785)
14. Chen, H., Wang, H., and, Siegfried, B.D., (2012) Genetic differentiation of western corn rootworm populations (Coleoptera: Chrysomelidae) relative to insecticide resistance. Ann Entomol Soc Am 105: 232-240.
15. Ciosi, M., Miller, N.J., Kim, K.S., Giordano, R., Estoup, A., and, 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.
16. Ciosi, M., Toepfer, S., Li, H., Haye, T., Kuhlmann, U., Wang, H., et al. (2009) European populations of Diabrotica virgifera virgifera are resistant to aldrin, but not to methyl-parathion. J Appl Entomol 133: 307-314.
17. Coates, B.S., Sumerford, D.V., Miller, N.J., Kim, K.S., Sappington, T.W., Siegfried, B.D., et al. (2009) Comparative performance of single nucleotide polymorphism and microsatellite markers for population genetic analysis. J Hered 100: 556-564.
18. Coates, B.S., Alves, A.P., Wang, H., Walden, K.K.O., French, B.W., Miller, N.J., et al. (2012) Distribution of genes and repetitive elements in the Diabrotica virgifera virgifera genome estimated using BAC sequencing. J Biomed Biotechnol 212: 1-9.
19. ffrench-Constant, R.H., Rocheleau, T.A., Steichen, J.C., and, Chalmers, A.E., (1993) A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 363: 449-451. (Pubitemid 23179390)
20. ffrench-Constant, R.H., Anthony, N., Aronstein, K., Rocheleau, T., and, Stilwell, G., (2000) Cyclodiene insecticide resistance: from molecular to population genetics. Annu Rev Entomol 48: 449-466. (Pubitemid 30187869)
21. Edmonds, C.A., Lillie, A.S., and, Cavali-Sforze, L.L., (2004) Mutatins arising on the wave from on an expanding population. Proc Natl Acad Sci U S A 101: 975-979. (Pubitemid 38160569)
22. Excoffier, L., and, Lischer, H.E.L., (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows. Mol Ecol Res 10: 564-567.
23. Excoffier, L., and, Ray, N., (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23: 347-351. (Pubitemid 351847653)
24. Gassmann, A.J., Petzold-Maxwell, J.L., Keweshan, R.S., and, Dunbar, M.W., (2011) Field-evolved resistance to Bt maize by western corn rootworm. PLoS ONE 6: e22629.
25. Georghiou, G.P., (1969) Genetics of resistance to insecticides in houseflies and mosquitoes. Exp Parasitol 26: 224-255.
26. Gray, M.E., Sappington, T.W., Miller, N.J., Moeser, J., and, Bohn, M.O., (2009) Adaptation and invasiveness of western corn rootworm: intensifying research on a worsening pest. Annu Rev Entomol 54: 303-321.
27. Hamilton, E.W., (1965) Aldrin resistance in corn rootworm beetles. J Econ Entomol 58: 296-300.
28. Hansen, K.K., Kristensen, M., and, Jensen, K.M., (2005) Correlation of a resistance-associated Rdl mutation in the German cockroach, Blattella germanica (L), with persistent dieldrin resistance in two Danish field populations. Pest Manag Sci 61: 749-753. (Pubitemid 40995648)
29. Hengeveld, R., (1989) Dynamics of Biological Invasions. Chapman & Hall, London.
30. Huang, X., and, Madan, A., (1999) CAP3: a DNA sequence assembly program. Genome Res 9: 868-877. (Pubitemid 29488446)
31. Hughes, P.B., and, McKenzie, J.A., (1987) Isectcide resistance in the Australian sheep blowfly, Lucilia cuprina: speculation, science and strategies. In Combating Resistance to Xenobiotics. Biological and Chemical Approaches (, Ford, M.G., Holloman, D.W., Khambay, B.P.S., and, Sawicki, R.M., eds), pp. 162-167. Ellis Horwood, Chichester.
32. Jackson, J.J., (1985) Diabrotica spp. In Handbook of Insect Rearing Vol. 1 (, Singh, P., and, Moore, R.F., eds), pp. 237-254. Elsevier Science Publishers, Amsterdam.
33. Jensen, J.L., Bohonak, A.J., and, Kelley, S.T., (2005) Isolation by distance, web service. BMC Genet 6: 13.
34. Kim, K.S., and, Sappington, T.W., (2005a) Genetic structuring of western corn rootworm (Coleoptera: Chrysomelidae) populations in the United States based on microsatellite loci analysis. Environ Entomol 34: 494-503. (Pubitemid 40483325)
35. Kim, K.S., and, Sappington, T.W., (2005b) Polymorphic microsatellite loci from the western corn rootworm (Insecta: Coleoptera: Chrysomelidae) and cross-amplification with other Diabrotica spp. Mol Ecol Notes 5: 115-117. (Pubitemid 40350897)
36. Kim, K.S., French, B.W., Sumerford, D.V., and, Sappington, T.W., (2007) Genetic diversity in laboratory colonies of western corn rootworm (Coleoptera: Chrysomelidae), including a nondiapause colony. Environ Entomol 36: 637-645. (Pubitemid 46954971)
37. Kim, K.S., Stolz, U., Miller, N.J., Waits, M.R., Guillemaud, T., Sumerford, D.V., et al. (2008) A core set of microsatellite markers for western corn rootworm (Coleoptera: Chrysomelidae) population genetics studies. Environ Entomol 37: 293-300. (Pubitemid 351685337)
38. Klopfstein, S., Currat, M., and, Excoffier, L., (2005) The fate of mutations surfing on the wave of a range expansion. Mol Biol Evol 23: 482-490. (Pubitemid 43278259)
39. Lehe, R., Hallatschek, O., and, Peliti, L., (2012) The rate of beneficial mutations surfing on the wave of a range expansion. PLoS Comp Biol 8: e1002447.
40. Levine, E., Spencer, J.L., Isard, S.A., Onstad, D.W., and, Gray, M.E., (2002) Adaptation of the western corn rootworm to crop rotation: evolution of a new strain in response to a management practice. Am Entomol 48: 94-107.
41. McKenzie, J.A., (1996) Ecology and Evolutionary Aspects of Insecticide Resistance. Academic Press, Austin.
42. Meinke, L.J., Siegfried, B.D., Wright, R.J., and, Chandler, L.D., (1998) Adult susceptibility of Nebraska western corn rootworm (Coleoptera: Chrysomelidae) populations to selected insecticides. J Econ Entomol 91: 594-600. (Pubitemid 128498835)
43. Meinke, L.J., Sappington, T.W., Onstad, D.W., Guillemaud, T., Miller, N.J., Komaromi, J., et al. (2009) Western corn rootworm (Diabrotica virgifera virgifera LeConte) population dynamics. Agric For. Entomol 11: 29-46.
44. Metcalf, R.L., (1983) Implication and prognosis of resistance to insecticides. In Pest Resistance to Pesticides (, Georghiou, G.P., and, Sato, T., eds), pp. 703-733. Plenum Press, New York, NY.
45. Metcalf, R.L., (1986) Foreword, pp. vii-xv. In Methods for the Study of Pest Diabrotica (, Krysan, J.L., and, Miller, T.A., eds), 260 pp. Springer-Verlag, New York.
46. Miller, N., Estroup, A., Toepfer, S., Bourguet, D., Lapchin, L., Derridj, S., et al,. (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310: 992. (Pubitemid 41611905)
47. Miller, N.J., Guillemaud, T., Giordano, R., Siegfried, B.D., Gray, M.E., Meinke, L.J., et al. (2009) Genes, gene flow and adaptation of Diabrotica virgifera virgifera. Agric For. Entomol 11: 47-60.
48. Muma, M.H., Hill, R.E., and, Hixson, E., (1949) Soil treatments for corn rootworm control. J Econ Entomol 42: 822-824.
49. O'Neal, M.E., DiFonzo, C.D., and, Landis, D.A., (2002) Western corn rootworm (Coleoptera: Chrysomelidae) feeding on corn and soybean leaves affected by corn phenology. Environ Entomol 31: 285-292. (Pubitemid 36178130)
50. Parimi, S., Meinke, L.J., French, B.W., Chandler, L.D., and, Siegfried, B.D., (2006) Stability and persistence of aldrin and methyl-parathion resistance in western corn rootworm populations (Coleoptera: Chrysomelidae). Crop Prot 25: 269-274. (Pubitemid 43098661)
51. Raymond-Delpech, V., Matsuda, K., Sattelle, B.M., Rauh, J.J., and, Sattelle, D.B., (2005) Ion channels: molecular targets of neuroactive insecticides. Invert Neurosci 5: 119-133. (Pubitemid 41504354)
52. Rice, P., Longden, I., and, Bleasby, A., (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16: 276-277.
53. Roselle, R.E., Anderson, L.W., Simpson, R.G., and, Webb, M.C., (1959) Annual Report for 1959, Cooperative Extension Work in Entomology, Lincoln, Nebraska.
54. Roselle, R.E., Anderson, L.W., Simpson, R.C., and, Bergman, P.W., (1960) Annual Report for 1960, Cooperative Extension Work in Entomology, Lincoln, Nebraska.
55. Roselle, R.E., Anderson, L.W., and, Bergman, P.W., (1961) Annual Report for 1961, Cooperative Extension Work in Entomology, Lincoln, Nebraska.
56. Rozen, S., and, Skaletsky, H.J., (2000) Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics: Methods and Protocols: (Methods in Molecular Biology (, Misener, S., and, Krawetz, S.A., eds), pp. 365-386. Humana Press, Totowa, NJ.
57. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M.-A., et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
58. Sappington, T.W., Siegfried, B.D., and, Guillemaud, T., (2006) Coordinated Diabrotica genetics research: accelerating progress on an urgent insect pest problem. Am Entomologist 52: 90-97.
59. Sayed, A., Nekl, E.R., Siqueira, H.A.A., Wang, H.-C., ffrench-Constant, R.H., Bagley, M., et al. (2007) A novel cadherin-like gene from western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae), larval midgut tissue. Insect Mol Biol 16: 591-600. (Pubitemid 47481034)
60. Scharf, M.E., Parimi, S., Meinke, L.J., Chandler, L.D., and, Siegfried, B.D., (2001) Expression and induction of three family 4 cytochrome P450 (CYP4) genes identified from insecticide-resistant and susceptible western corn rootworms, Diabrotica virgifera virgifera. Insect Mol Biol 10: 139-146. (Pubitemid 32324683)
61. Schofield, P.R., Darlison, M.G., Fujita, N., Burt, D.R., Stephenson, F.A., Rodriguez, H., et al. (1987) Sequence and functional expression of the GABA A receptor shows a ligand-gated receptor super-family. Nature 328: 221-227. (Pubitemid 17108271)
62. Siegfried, B.D., Waterfield, N., and, ffrench-Constant, R.H., (2005) Expressed sequence tags from Diabrotica virgifera virgifera midgut identify a coleopteran cadherin and a diversity of cathepsins. Insect Mol Biol 14: 137-143. (Pubitemid 40534279)
63. Zhang, H.-G., ffrench-Constant, R.H., and, Jackson, M.B., (1994) A unique amino acid of the Drosophila GABA receptor with influence on drug sensitivity by two mechanisms. J Physiol 479: 65-75. (Pubitemid 24265677)