Selective sweeps at the organophosphorus insecticide resistance locus, Rop-1, have affected variation across and beyond the α-esterase gene cluster in the Australian sheep blowfly, Lucilia cuprina

Molecular Biology and Evolution

Volumn 28, Issue 6, 2011, Pages 1835-1846

  Rose, Caroline J ^a,b   Chapman, Joanne R ^a   Marshall, Sean D G ^a   Lee, Siu F ^c   Batterham, Philip ^c   Ross, Howard A ^b   Newcomb, Richard D ^a,b,d  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d Allan Wilson Centre for Molecular Ecology & Evolution   (New Zealand)

Author keywords

genetic hitchhiking; linkage disequilibrium; microsatellite evolution; organophosphorus insecticide resistance; Rop 1; selective sweep

Indexed keywords

ALPHA ESTERASE; ESTERASE; ORGANOPHOSPHATE INSECTICIDE; ORGANOPHOSPHORUS INSECTICIDE RESISTANCE LOCUS ROP 1; UNCLASSIFIED DRUG;

ARTICLE; CALLIPHORIDAE; CHROMOSOME 4; GENE CLUSTER; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETIC VARIABILITY; HAPLOTYPE; INSECTICIDE RESISTANCE; INTRON; LUCILIA CUPRINA; MICROSATELLITE MARKER; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PROMOTER REGION;

ANIMALS; BASE SEQUENCE; CLUSTER ANALYSIS; DIPTERA; ESTERASES; EVOLUTION, MOLECULAR; GENES, INSECT; GENETIC VARIATION; HAPLOTYPES; INSECTICIDE RESISTANCE; INSECTICIDES; LINKAGE DISEQUILIBRIUM; MALE; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; POLYMORPHISM, GENETIC; SEQUENCE ALIGNMENT;

LUCILIA CUPRINA; LUCILIA SERICATA;

EID: 79957477731     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr006     Document Type: Article

References (60)

1. Barton NH. 1995. Linkage and the limits to natural selection.Genetics 140:821-841.
2. Batterham P, Hill-Williams A, Levot G, Sales N, McKenzie JA. 2006.The genetic bases of high-level resistance to diflubenzuron and low-level resistance to cyromazine in a field strain of the Australian sheep blowfly, Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae). Aust J Entomol. 45:87-90. (Pubitemid 44185169)
3. Birky CW, Walsh JB. 1988. Effects of linkage on rates of molecular evolution. Proc Natl Acad Sci USA. 85:6414-6418.
4. Bosco G, Campbell P, Leiva-Neto JT, Markow TA. 2007. Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics 177:1277-1290. (Pubitemid 350277032)
5. Campbell PM, Newcomb RD, Russell RJ, Oakeshott JG. 1998. Two different amino acid substitutions in the ali-esterase, E3, confer alternative types of organophosphorus insecticide resistance in the sheep blowfly, Lucilia cuprina. Insect Biochem Mol Biol. 28:139-150. (Pubitemid 28287745)
6. Chen Z, Newcomb RD, Forbes E, McKenzie J, Batterham P. 2001. The acetylcholinesterase gene and organophosphorus resistance in the Australian sheep blowfly, Lucilia cuprina. Insect Biochem Mol Biol. 31:805-816. (Pubitemid 32587303)
7. Claudianos C, Russell RJ, Oakeshott JG. 1999. The same amino acid substitution in orthologous esterases confers organophosphate resistance on the house fly and a blowfly. Insect Mol Biol. 29:675-686. (Pubitemid 29347310)
8. Depaulis F, Veuille M. 1998. Neutrality tests based on the distribution of haplotypes under an infinite-site model. Mol Biol Evol. 15:1788-1790. (Pubitemid 28551002)
9. Fay JC, Wu C-I. 2000. Hitchhiking under positive darwinian selection.Genetics 155:1405-1413. (Pubitemid 30463447)
10. Foster GG, Smith PH. 1991. Genetic control of Lucilia cuprina: Analysis of field trial data using simulation techniques. Theor Appl Genet. 82:33-43.
11. GeneCodes. 2000. Sequencher Version 4.5. Ann Arbor (MI): Gene-Codes Corporation.
12. Gleeson DM, Heath ACG. 1997. The population biology of the Australian sheep blowfly, Lucilia cuprina, in New Zealand. New Zeal J Agr Res. 40:529-535. (Pubitemid 28202490)
13. Hartley CJ, Newcomb RD, Russell RJ, Yong CG, Stevens JR, Yeates DK, La Salle J, Oakeshott JG. 2006. Amplification of DNA from preserved specimens shows blowflies were preadapted for the rapid evolution of insecticide resistance. Proc Natl Acad Sci USA. 103:8757-8762. (Pubitemid 43878092)
14. Heidari R, Devonshire AL, Campbell BE, Bell KL, Dorrian SJ, Oakeshott JG, Russel RJ. 2004. Hydrolysis of organophosphorus insecticides by in vitro modified carboxylesterase E3 from Lucilia cuprina. Insect Biochem Mol Biol. 34:353-363. (Pubitemid 38431046)
15. Hermisson J, Pennings PS. 2005. Soft sweeps: Molecular population genetics of adaptation from standing genetic variation. Genetics 169:2335-2352. (Pubitemid 40695640)
16. Kaplan NL, Hudson RR, Langley CH. 1989. The "hitchhiking effect" revisited. Genetics 123:887-899.
17. Kim Y, Nielsen R. 2004. Linkage disequilibrium as a signature of selective sweeps. Genetics 167:1513-1524. (Pubitemid 39045653)
18. Levot GW. 1995. Resistance and the control of sheep ectoparasites.Int J Parasitol. 25:1355-1362.
19. Levot GW, Sales N. 2002. New high level resistance to diflubenzuron detected in the Australian sheep blowfly, Lucilia cuprina (Weidemann) (Diptera: Calliphoridae). Gen Appl Entomol. 31:43-45.
20. Maynard Smith J, Haigh J. 1974. The hitch-hiking effect of a favourable gene. Genet Res 23:23-35.
21. McDonald JH, Kreitman M. 1991. Adaptive protein evolution at Adh locus in Drosophila. Nature 351:652-654. (Pubitemid 21896661)
22. McKenzie JA, Whitten MJ, Adena MA. 1982. The effect of genetic background on the fitness of diazinon resistance genotypes of the Australian sheep blowfly, Lucilia cuprina. Heredity 49:1-9.
23. McVean G. 2002. A genealogical interpretation of linkage disequilibrium.Genetics 162:987-991. (Pubitemid 35365058)
24. McVean G. 2007. The structure of linkage disequilibrium around a selective sweep. Genetics 175:1395-1406. (Pubitemid 46798239)
25. Mousset S, Brazier L, Cariou M-L, Chartios F, Depaulis F, Veuille M. 2003. Evidence of a high rate of selective sweeps in African Drosophila melanogaster. Genetics 163:599-699.
26. Mutero A, Pralavorio M, Bride JM, Fournier D. 1994. Resistanceassociated point mutations in insecticide-insensitive acetylcholinesterase.Proc Nat Acad Sci USA. 91:5922-5926. (Pubitemid 24188254)
27. Nair S, Williams JT, Brockman A, et al. (12 co-authors). 2003. A selective sweep driven by pyrimethamine treatment in southeast Asian malaria parasites. Mol Biol Evol. 20:1526-1536. (Pubitemid 37082588)
28. Nei M. 1987. Molecular evolutionary genetics. New York: Columbia University Press.
29. Nei M, Li W-H. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA. 76:5269-5273. (Pubitemid 10236121)
30. Newcomb RD, Campbell PM, Ollis DL, Cheah E, Russell RJ, Oakeshott JG. 1997a. A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. Proc Natl Acad Sci USA. 94:7464-7468.
31. Newcomb RD, Campbell PM, Russell RJ, Oakeshott JG. 1997b. cDNA cloning, baculovirus-expression and kinetic properties of the esterase, E3, involved in organophosphorus resistance in Lucilia cuprina. Insect Biochem Mol Biol. 27:15-25. (Pubitemid 27089847)
32. Newcomb RD, East PD, Russell RJ, Oakeshott JG. 1996. Isolation of a cluster esterase genes associated with organophosphate resistance in Lucilia cuprina. Insect Mol Biol. 5:211-216. (Pubitemid 126439996)
33. Newcomb RD, Gleeson DM, Yong CG, Russell RJ, Oakeshott JG. 2005. 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. 60 207-220. (Pubitemid 40568860)
34. Nielsen R. 2005. Molecular signatures of natural selection. Annu Rev Genet. 39:197-218. (Pubitemid 43011113)
35. Nurminsky D, De Aguiar D, Bustamante C, Hartl D. 2001.Chromosomal effects of rapid gene evolution in Drosophila melanogaster. Science 291:128-130. (Pubitemid 32056680)
36. Nurminsky DI. 2001. Genes in sweeping competition. Cell Mol Life Sci. 58:125-134. (Pubitemid 32143967)
37. Oakeshott JG, Home I, Sutherland TD, Russell RJ. 2003. The genomics of insecticide resistance. Genome Biol. 4:202.
38. Page RDM. 1996. Treeview: An application to display phylogenetic trees on personal computers. Comput Appl Biosci. 12:357-358.
39. Pennings PS, Hermisson J. 2006a. Soft Sweeps II: Molecular population genetics of adaptation from recurrent mutation or migration. Mol Biol Evol. 23:1076-1084. (Pubitemid 43726073)
40. Pennings PS, Hermisson J. 2006b. Soft Sweeps III: The signature of positive selection from recurrent mutation. PLoS Genet 2:e186.
41. Perlitz M, Stephan W. 1997. The mean and variance of the number of segregating sites since the last hitchhiking event. J Math Biol. 36:1-23. (Pubitemid 127759388)
42. Przeworski M. 2002. The signature of positive selection at randomly chosen loci. Genetics 160:1179-1189. (Pubitemid 34263478)
43. Robin C, Russell RJ, Medveczky KM, Oakeshott JG. 1996. Duplication and diversgence of the genes of the a-esterase cluster of Drosophila melanogaster. J Mol Evol. 43:241-252. (Pubitemid 26315126)
44. Rozas J, Sanchez-Del Barrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497. (Pubitemid 38016658)
45. Russell RJ, Robin GC, Kostakos P, Newcomb RD, Boyce TM, Medveczky KM, Oakeshott JG. 1996. Molecular cloning of an a-esterase gene cluster on chromosome 3R of Drosophila melanogaster. Insect Biochem Mol Biol. 26:235-247.
46. Sabeti PC, Schaffner SF, Fry B, Lohmueller J, Varilly P, Shamovsky O, Palma A, Mikkelsen TS, Altshuler D, Lander ES. 2006. Positive natural selection in the human lineage. Science 312:1614-1620. (Pubitemid 43902654)
47. Saez AG, Tatarenkov A, Barrio E, Becerra NH, Ayala FJ. 2003. Patterns of DNA sequence polymorphism at Sod vicinities in Drosophila melanogaster: Unraveling the footprint of a recent selective sweep. Proc Natl Acad Sci USA. 100:1793-1798. (Pubitemid 36254527)
48. Schlenke TA, Begun DJ. 2004. Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proc Natl Acad Sci USA. 101:1626-1631. (Pubitemid 38234205)
49. Shanahan GJ, Hart RJ. 1966. Change in response of Lucilia cuprina Weid. to organophosphorous insecticides in Australia. Nature 212:1466-1467.
50. Smyth K, Boyce TM, Russell RJ, Oakeshott JG. 2000. MCE activities and malathion resistances in field populations of the Australian sheep blowfly (Lucilia cuprina). Heredity. 84:63-72. (Pubitemid 30165744)
51. Smyth KA, Russell RJ, Oakeshott JG. 1994. A cluster of at least three esterase genes in Lucilia cuprina includes malathion carboxylesterase and two other esterase genes implicated in resistance to organophosphates. Biochem Genet. 32:437-453.
52. Stephan W, Song YS, Langley CH. 2006. The hitchhiking effect on linkage disequilibrium between linked neutral loci. Genetics 172:2647-2663.
53. Swofford DL. 2002. PAUP* phylogenetic analysis using parsimony (* and other methods) Version 4. Sunderland (MA): Sinauer Associates.
54. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 123:585-595. (Pubitemid 19274682)
55. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.Mol Biol Evol. 24:1596-1599. (Pubitemid 47236692)
56. Ullreich F-H, Schöttke M. 2006. Karyotypes, constitutive heterochromatin, and genomic DNA values in the blowfly genera Chrysomya, Lucilia, and Protophormia (Diptera: Calliphoridae).Genome 49:584-597. (Pubitemid 44379476)
57. Weller GL, Foster GG. 1993. Genetic maps of the sheep blowfly Lucilia cuprina: Linkage-group correlations with other dipteran genera. Genome 36:495-506. (Pubitemid 23247278)
58. Yen YL, BatterhamP, Gelder B,McKenzie JA. 1996. Predicting resistance and managing susceptibility to cyromazine in the Australian sheep blowfly Lucilia cuprina. Aust J Exp Agr. 36:413-420.
59. Zaykin DV, Pudovkin A, Weir BS. 2008. Correlation-based inference for linkage disequilibrium with multiple alleles. Genetics 180:533-545.
60. Zeng K, Fu YX, Shi S, Wu CI. 2006. Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174:1431-1439. (Pubitemid 44808312)