Pre-invasion history and demography shape the genetic variation in the insecticide resistance-related acetylcholinesterase 2 gene in the invasive Colorado potato beetle

BMC Evolutionary Biology

Alessandro Grapputo³  Victor Izzo²  Yolanda H Chen²  Johanna Mappes¹  Anne Lyytinen¹  Leena Lindström¹  Saija Piiroinen¹ 

[1] Centre of Excellence in Biological Interactions Research, Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, FI-40014, Jyväskylä, Finland;Department of Plant and Soil Sciences, University of Vermont, 63 Carrigan Drive, Burlington, VT, 05405, USA;Department of Biology, University of Padua, Via U. Bassi, 58/B, 35121, Padua, Italy

关键词: Selection;    Resistance evolution;    Pesticide resistance;    Juvenile hormone esterase;    Invasive species;    Invasion biology;    Diapause protein 1;    Acetylcholinesterase;   

Others  :  1130254
DOI  :  10.1186/1471-2148-13-13

 received in 2012-08-02, accepted in 2013-01-17,  发布年份 2013

【 摘 要 】

Background

Invasive pest species offers a unique opportunity to study the effects of genetic architecture, demography and selection on patterns of genetic variability. Invasive Colorado potato beetle (Leptinotarsa decemlineata) populations have experienced a rapid range expansion and intense selection by insecticides. By comparing native and invasive beetle populations, we studied the origins of organophosphate (OP) resistance-associated mutations in the acetylcholinesterase 2 (AChE2) gene, and the role of selection and demography on its genetic variability.

Results

Analysis of three Mexican, two US and five European populations yielded a total of 49 haplotypes. Contrary to the expectations all genetic variability was associated with a point mutation linked to insecticide resistance (S291G), this mutation was found in 100% of Mexican, 95% of US and 71% of European beetle sequences analysed. Only two susceptible haplotypes, genetically very differentiated, were found, one in US and one in Europe. The genetic variability at the AChE2 gene was compared with two other genes not directly affected by insecticide selection, diapause protein 1 and juvenile hormone esterase. All three genes showed reduction in genetic variability indicative of a population bottleneck associated with the invasion.

Conclusions

Stochastic effects during invasion explain most of the observed patterns of genetic variability at the three genes investigated. The high frequency of the S291G mutation in the AChE2 gene among native populations suggests this mutation is the ancestral state and thus, either a pre-adaptation of the beetle for OP resistance or the AChE2 is not the major gene conferring OP resistance. The long historical association with host plant alkaloids together with recombination may have contributed to the high genetic variation at this locus. The genetic diversity in the AChE2 locus of the European beetles, in turn, strongly reflects founder effects followed by rapid invasion. Our results suggest that despite the long history of insecticide use in this species, demographic events together with pre-invasion history have been strongly influential in shaping the genetic diversity of the AChE2 gene in the invasive beetle populations.

【 授权许可】

   
2013 Piiroinen et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Nielsen R: Statistical tests of selective neutrality in the age of genomics. Heredity 2001, 86:641-647.
• [2]McKenzie JA: Pesticide resistance. In Evolutionary Ecology; Concepts and Case Studies. Edited by Fox CA, Rolf DA, Fairbairn DJ. New York: Oxford University Press; 2001:347-360.
• [3]Georghiou GP: The magnitude of the resistance problem. In Pesticide Resistance: Strategies and Tactics for Management. Washington, D.C: National Academy Press; 1986:14-43.
• [4]Daborn PJ, Yen JL, Bogwitz MR, Le Goff G, Feil E, Jeffers S, Tijet N, Perry T, Heckel D, Batterham P, Feyereisen R, Wilson TG, Ffrench-Constant RH: A single P450 allele associated with insecticide resistance in Drosophila. Science 2002, 297:2253-2256.
• [5]Ffrench-Constant RH, Daborn PJ, Goff GL: The genetics and genomics of insecticide resistance. Trends Genet 2004, 20:163-170.
• [6]Labbé P, Berticat C, Berthomieu A, Unal S, Bernard C, Weill M, Lenormand T: Forty years of erratic insecticide resistance evolution in the mosquito Culex pipiens. PLoS Genet 2007, 3:2190-2199.
• [7]Catania F, Kauer MO, Daborn PJ, Yen JL, Ffrench-Constant RH, Schloetterer C: World-wide survey of an Accord insertion and its association with DDT resistance in Drosophila melanogaster. Mol Ecol 2004, 13:2491-2504.
• [8]Nardi F, Carapelli A, Vontas JG, Dallai R, Roderick GK, Frati F: Geographical distribution and evolutionary history of organophosphate-resistant Ace alleles in the olive fly (Bactrocera oleae). Insect Biochem Mol Biol 2006, 36:593-602.
• [9]Maynard-Smith J, Haigh J: Hitch-hiking effect of a favorable gene. Genet Res 1974, 23:23-35.
• [10]Newcomb RD, Gleeson DM, Yong CG, Russell RJ, Oakeshott JG: Multiple mutations and gene duplications conferring organophosphorus insecticide resistance have been selected at the Rop-1 locus of the sheep blowfly, Lucilia cuprina. J Mol Evol 2005, 60:207-220.
• [11]Hermisson J, Pennings PS: Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 2005, 169:2335-2352.
• [12]Przeworski M, Coop G, Wall JD: The signature of positive selection on standing genetic variation. Evolution 2005, 59:2312-2323.
• [13]Hartley CJ, Newcomb RD, Russell RJ, Yong CG, Stevens JR, Yeates DK, La Salle J, Oakeshott JG: Amplification of DNA from preserved specimens shows blowflies were preadapted for the rapid evolution of insecticide resistance. Proc Natl Acad Sci USA 2006, 103:8757-8762.
• [14]Piccinali RV, Mascord LJ, Barker JSF, Oakeshott JG, Hasson E: Molecular population genetics of the α-esterase5 gene locus in original and colonized populations of Drosophila buzzatii and its sibling Drosophila koepferae. J Mol Evol 2007, 64:158-170.
• [15]Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, Neil P, Parker IM, Thompson JN, Weller SG: The population biology of invasive species. Ann Rev Ecol Syst 2001, 32:305-332.
• [16]Excoffier L, Foll M, Petit R: Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 2009, 40:481-501.
• [17]Ffrench-Constant RH, Rocheleau TA, Steichen JC, Chalmers AE: A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 1993, 363:449-451.
• [18]Menozzi P, Shi M, Lougarre A, Tang Z, Fournier D: Mutations of acetylcholinesterase which confer insecticide resistance in Drosophila melanogaster populations. BMC Evol Biol 2004, 4:1-7. BioMed Central Full Text
• [19]Chevillon C, Raymond M, Guillemaud T, Lenormand T, Pasteur N: Population genetics of insecticide resistance in the mosquito Culex pipiens. Biol J Linn Soc 1999, 68:147-157.
• [20]Mutero A, Pralavorio M, Bride JM, Fournier D: Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proc Natl Acad Sci USA 1994, 91:5922-5926.
• [21]Zhu KY, Lee SH, Clark JM: A point mutation of acetylcholinesterase associated with azinphosmethyl resistance and reduced fitness in Colorado potato beetle. Pestic Biochem Physiol 1996, 55:100-108.
• [22]Zhu KY, Clark JM: Validation of a point mutation of acetylcholinesterase in Colorado potato beetle by polymerase chain reaction coupled in enzyme inhibition assay. Pestic Biochem Physiol 1997, 57:28-35.
• [23]Kim HJ, Dunn JB, Yoon KS, Clark JM: Target site insensitivity and mutational analysis of acetylcholinesterase from a carbofuran-resistant population of Colorado potato beetle, Leptinotarsa decemlineata (Say). Pestic Biochem Physiol 2006, 84:165-179.
• [24]Kim HJ, Yoon KS, Clark JM: Functional analysis of mutations in expressed acetylcholinesterase that result in azinphosmethyl and carbofuran resistance in Colorado potato beetle. Pestic Biochem Physiol 2007, 88:181-190.
• [25]Lee SH, Dunn JB, Clark JM, Soderlund DM: Molecular analysis of kdr-like resistance in a permethrin-resistant strain of Colorado potato beetle. Pestic Biochem Physiol 1999, 63:63-75.
• [26]Argentine JA, Lee SH, Sos MA, Barry SR, Clark JM: Permethrin resistance in a near isogenic strain of Colorado potato beetle. Pestic Biochem Physiol 1995, 53:97-115.
• [27]PAN - Pesticide action network UK: Organophosphate insecticides. Pesticides News 1996, 34:20-21.
• [28]Forgash AJ: Insecticide resistance in the Colorado potato beetle. In Proceedings of the Symposium on the Colorado potato beetle. XVII International Congress of Entomology. Edited by Ferro DN, Voss RH. Amherst: University of Massachusetts; 1985:33-53.
• [29]Alyokhin A, Baker M, Mota-Sanchez D, Dively G, Grafius E: Colorado potato beetle resistance to insecticides. Am J Pot Res 2008, 85:395-413.
• [30]Kono Y, Tomita T: Amino acid substitutions conferring insecticide insensitivity in Ace-paralogous acetylcholinesterase. Pestic Biochem Physiol 2006, 85:123-132.
• [31]Casagrande RA: The Colorado potato beetle: 125 years of mismanagement. Bull Entomol Soc Am 1987, 33:142-150.
• [32]EPPO: Distribution Maps of Quarantine Pests for Europe, Leptinotarsa Decemlineata. Nottingham, UK: ADAS; 2006.
• [33]Boman S, Grapputo A, Lindström L, Lyytinen A, Mappes J: Quantitative genetic approach for assessing invasiveness: geographic and genetic variation in life-history traits. Biol Invasions 2008, 10:1135-1145.
• [34]Grapputo A, Boman S, Lindström L, Lyytinen A, Mappes J: The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Mol Ecol 2005, 14:4207-4219.
• [35]Lyytinen A, Lindström L, Mappes J: Genetic variation in growth and development time under two selection regimes in Leptinotarsa decemlineata. Entomol Exp Appl 2008, 127:157-167.
• [36]Hare JD: Ecology and management of the Colorado potato beetle. Annu Rev Entomol 1990, 35:81-100.
• [37]Alyokhin A, Udalov M, Benkovskaya G: The Colorado potato beetle. In Insect Pests of Potato. Global Perspectives on Biology and Management. Edited by Giordanengo P, Vincent P, Alyokhin A. Oxford, UK: Academic Press; 2013:11-29.
• [38]Koopmanschap AB, Lammers JHM, de Kort CAD: The structure of the gene encoding diapause protein 1 of the Colorado potato beetle (Leptinotarsa decemlineata). J Insect Physiol 1995, 41:509-518.
• [39]Vermunt AMW, Koopmanschap AB, Vlak JM, De Kort CAD: Cloning and sequence analysis of cDNA encoding a putative juvenile hormone esterase from the Colorado potato beetle. Insect Biochem Mol Biol 1997, 27:919-928.
• [40]Vermunt AMW, Koopmanschap AB, Vlak JM, De Kort CAD: Evidence for two juvenile hormone esterase-related genes in the Colorado potato beetle. Insect Mol Biol 1998, 7:327-336.
• [41]Salzburger W, Ewing GB, Haeseler A: The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Mol Ecol 2011, 20:1952-1963.
• [42]Felsenstein J: PHYLIP - phylogeny inference package (version 3.2). Cladistics 1989, 5:164-166.
• [43]Argentine JA, Clark JM, Ferro DN: Relative fitness of insecticide-resistant Colorado potato beetle strains (Coleoptera: Chrysomelidae). Environ Entomol 1989, 18:705-710.
• [44]Wierenga JM, Hollingworth RM: Inhibition of insect acetylcholinesterase by the potato glycoalkaloid alpha-chaconine. Nat Toxins 1992, 1:96-99.
• [45]Zhu KY, Clark JM: Comparisons of kinetic properties of acetylcholinesterase purified from azinphosmethyl-susceptible and resistant strains of Colorado potato beetle. Pestic Biochem Physiol 1995, 51:57-67.
• [46]Revuelta L, Ortego F, Díaz-Ruís P, Castañera F, Tenllado P, Hernández-Crespo P: Contribution of Ldace1 gene to acetylcholinesterase activity in Colorado potato beetle. Insect Biochem Mol Biol 2011, 41:795-803.
• [47]Baek JH, Kim JI, Lee DW, Chung BK, Miyata T, Lee SH: Identification and characterization of ace1-type acetylcholinesterase likely associated with organophosphate resistance in Plutella xylostella. Pestic Biochem Physiol 2005, 81:164-175.
• [48]Jiang W, Guo W, Lu W, Shi X, Xiong M, Wang Z, Li G: Target site insensitivity mutations in the AChE and LdVssc1 confer resistance to pyrethroids and carbamates in Leptinotarsa decemlineata in northern Xinjiang Uygur autonomous region. Pestic Biochem Physiol 2011, 100:74-81.
• [49]Zichová T, Kocourek F, Salava J, Nad’ová K, Stará J: Detection of organophosphate and pyrethroid resistance alleles in Czech Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) populations by molecular methods. Pest Manag Sci 2010, 66:853-860.
• [50]Klopfstein S, Currat M, Excoffier L: Tha fate of mutations surfing on the wave of a range expansion. Mol Biol Evol 2006, 23:482-490.
• [51]Tower WL: An Investigation of Evolution in Chrysomelid Beetles of the Genus Leptinotarsa. Washington, D.C.: Carnegie Institution; 1906.
• [52]Lu W, Logan P: Inheritance of host-related feeding and ovipositional bahaviors in Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Environ Entomol 1995, 24:278-287.
• [53]Alyokhin A, Chen YH, Udalov M, Benkovskaya G, Lindström L: Evolutionary considerations in potato pest management. In Insect Pests of Potato. Global Perspectives on Biology and Management. Edited by Giordanengo P, Vincent C, Alyokhin A. Oxford, UK: Academic Press; 2013:543-571.
• [54]Clark JM, Lee SH, Kim HJ, Yoon KS, Zhang AG: DNA-based genotyping techniques for the detection of point mutations associated with insecticide resistance in Colorado potato beetle Leptinotarsa decemlineata. Pest Manag Sci 2001, 57:968-974.
• [55]Zhu KY, Clark JM: Cloning and sequencing of a cDNA encoding acetylcholinesterase in Colorado potato beetle, Leptinotarsa decemlineata (say). Insect Biochem Mol Biol 1995, 25:1129-1138.
• [56]Fournier D, Karch F, Bride JM, Hall LM, Berge JB, Spierer P: Drosophila melanogaster acetylcholinesterase gene: structure, evolution and mutations. J Mol Biol 1989, 210:15-22.
• [57]Stephens M, Smith NI, Donnelly P: A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 2001, 68:978-989.
• [58]Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19:2496-2497.
• [59]Nei M: Molecular Evolutionary Genetics. New York: Columbia University Press; 1987.
• [60]Tajima F: Evolutionary relationship of DNA-sequences in finite populations. Genetics 1983, 105:437-460.
• [61]Watterson GA: Number of segregating sites in genetic models without recombination. Theor Popul Biol 1975, 7:256-276.
• [62]Lewontin RC, Kojima K: The evolutionary dynamics of complex polymorphisms. Evolution 1960, 14:458-472.
• [63]Lewontin RC: Interaction of selection and linkage. I. General considerations; heterotic models. Genetics 1964, 49:49-67.
• [64]Sokal RR, Rohlf FJ: Biometry. 2nd edition. New York: W.H. Freeman and Company; 1981.
• [65]Weir BS: Genetic Data Analysis II. Sinauer Associates, Inc., Sunderland; 1996.
• [66]Hudson RR: Estimating the recombination parameter of a finite population model without selection. Genet Res 1987, 50:245-250.
• [67]Hudson RR, Kaplan NL: Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 1985, 111:147-164.
• [68]Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW: GARD: a genetic algorithm for recombination detection. Bioinformatics 2006, 22:3096-3098.
• [69]Kosakovsky Pond SL, Frost SDW: Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 2005, 21:2531-2533.
• [70]Excoffier L, Laval G, Schneider S: Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinf 2005, 1:47-50.
• [71]Excoffier L, Smouse PE, Quattro JM: Analysis of molecular variance inferred from metric distances among DNA haplotypes - Application to human mitochondrial-DNA restriction data. Genetics 1992, 131:479-491.
• [72]Goudet J: FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). 2001. http://www2.unil.ch/popgen/softwares/fstat.htm webcite
• [73]Tajima F: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
• [74]Fu Y, Li W: Statistical tests of neutrality of mutations. Genetics 1993, 133:693-709.
• [75]Kelly JK: A test of neutrality based on interlocus associations. Genetics 1997, 146:1197-1206.