Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus

PLoS Genetics

Volumn 6, Issue 6, 2010, Pages 1-11

  Schmidt, Joshua M ^a,b   Good, Robert T ^a,b   Appleton, Belinda ^a   Sherrard, Jayne ^a   Raymant, Greta C ^a,b   Bogwitz, Michael R ^a   Martin, Jon ^a   Daborn, Phillip J ^a,b   Goddard, Mike E ^a,c   Batterham, Philip ^a,b   Robin, Charles ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c DEPARTMENT OF PRIMARY INDUSTRIES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPHENOTANE; CYTOCHROME P450; CYTOCHROME P450 6G1; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; CONTROLLED STUDY; COPY NUMBER VARIATION; DROSOPHILA MELANOGASTER; GENE FREQUENCY; GENE LOCUS; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHICAL VARIATION (SPECIES); INSECTICIDE RESISTANCE; NATURAL POPULATION; NONHUMAN; PHENOTYPIC VARIATION; STRAIN DIFFERENCE; TRANSPOSON;

DROSOPHILA MELANOGASTER;

EID: 77954154377     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000998     Document Type: Article

References (58)

1. Andolfatto P (2005) Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149-1152.
2. Smith NG, Eyre-Walker A (2002) Adaptive protein evolution in Drosophila. Nature 415: 1022-1024.
3. Sella G, Petrov DA, Przeworski M, Andolfatto P (2009) Pervasive natural selection in the Drosophila genome? PLoS Genet 5: e1000495. doi:10.1371/ journal.pgen.1000495.
4. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, et al. (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461: 1243-1247.
5. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh YP, et al. (2007) Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5: e310. doi:10.1371/journal.pbio.0050310.
6. Orr HA (2005) The genetic theory of adaptation: a brief history. Nature Reviews Genetics 6: 119-127.
7. Gillespie JH (1991) The causes of Molecular Evolution: Oxford University Press Inc.
8. Perfeito L, Fernandes L, Mota C, Gordo I (2007) Adaptive mutations in bacteria: high rate and small effects. Science 317: 813-815.
9. Andreev D, Kreitman M, Phillips TW, Beeman RW, ffrench-Constant RH (1999) Multiple origins of cyclodiene insecticide resistance in Tribolium castaneum (Coleoptera: Tenebrionidae). JME 48: 615-624.
10. ffrench-Constant RH (1994) The molecular and population genetics of cyclodiene insecticide resistance. Insect Biochem Mol Biol 24: 335-345.
11. Soderlund DM, Knipple DC (2003) The molecular biology of knockdown resistance to pyrethroid insecticides. Insect Biochem Mol Biol 33: 563-577.
12. 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 Biochemistry and Molecular Biology 29: 675-686.
13. Daborn PJ, Yen JL, Bogwitz MR, Le Goff G, Feil E, et al. (2002) A single p450 allele associated with insecticide resistance in Drosophila. Science 297: 2253-2256.
14. Joussen N, Heckel DG, Haas M, Schuphan I, Schmidt B (2007) Metabolism of imidacloprid and DDT by P450 CYP6G1 expressed in cell cultures of Nicotiana tabacum suggests detoxification of these insecticides in Cyp6g1-overexpressing strains of Drosophila melanogaster, leading to resistance. Pest Manag Sci.
15. Chung H, Bogwitz MR, McCart C, Andrianopoulos A, Ffrench-Constant RH, et al. (2007) Cis-regulatory elements in the Accord retrotransposon result in tissuespecific expression of the Drosophila melanogaster insecticide resistance gene Cyp6g1. Genetics 175: 1071-1077.
16. Hoekstra HE, Coyne JA (2007) The locus of evolution: Evo devo and the genetics of adaptation. Evolution 61: 995-1016.
17. Catania F, Kauer MO, Daborn PJ, Yen JL, Ffrench-Constant RH, et al. (2004) World-wide survey of an Accord insertion and its association with DDT resistance in Drosophila melanogaster. Mol Ecol 13: 2491-2504.
18. Schlenke TA, Begun DJ (2004) Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proc Natl Acad Sci U S A 101: 1626-1631.
19. Crow JF (1957) Genetics of insect resistance to chemicals. Annual Reviews of Entomology 2: 227-246.
20. Dapkus D, Merrell DJ (1977) Chromosomal analysis of DDT-resistance in a long-term selected population of Drosophila melanogaster. Genetics 87: 685-697.
21. Kikkawa (1961) Genetical studies on the resistance to parathion in Drosophila melanogaster. Annual Report of Scientific Works, Faculty of Science, Osaka University 9: 1-20.
22. Hallstrom I (1985) Genetic regulation of the cytochrome P-450 system in Drosophila melanogaster. II. Localization of some genes regulating cytochrome P- 450 activity. Chem Biol Interact 56: 173-184.
23. Kikkawa H (1964) Genetical studies on the resistance to parathion in Drosophila melanogaster. II. Induction of a resistance gene from its susceptible allele. BotyuKagaku 29: 37-42.
24. Daborn P, Boundy S, Yen J, Pittendrigh B, ffrench-Constant R (2001) DDT resistance in Drosophila correlates with Cyp6g1 over-expression and confers cross-resistance to the neonicotinoid imidacloprid. Mol Genet Genomics 266: 556-563.
25. Pedra JH, McIntyre LM, Scharf ME, Pittendrigh BR (2004) Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila. Proc Natl Acad Sci U S A 101: 7034-7039.
26. Amichot M, Tares S, Brun-Barale A, Arthaud L, Bride JM, et al. (2004) Point mutations associated with insecticide resistance in the Drosophila cytochrome P450 Cyp6a2 enable DDT metabolism. Eur J Biochem 271: 1250-1257.
27. Brandt A, Scharf M, Pedra JH, Holmes G, Dean A, et al. (2002) Differential expression and induction of two Drosophila cytochrome P450 genes near the Rst(2)DDT locus. Insect Mol Biol 11: 337-341.
28. Daborn PJ, Lumb C, Boey A, Wong W, Ffrench-Constant RH, et al. (2007) Evaluating the insecticide resistance potential of eight Drosophila melanogaster cytochrome P450 genes by transgenic over-expression. Insect Biochem Mol Biol 37: 512-519.
29. Emerson JJ, Cardoso-Moreira M, Borevitz JO, Long M (2008) Natural selection shapes genome-wide patterns of copy-number polymorphism in Drosophila melanogaster. Science 320: 1629-1631.
30. Dopman EB, Hartl DL (2007) A portrait of copy-number polymorphism in Drosophila melanogaster. Proc Natl Acad Sci U S A.
31. Pyke FM, Bogwitz MR, Perry T, Monk A, Batterham P, et al. (2004) The genetic basis of resistance to diazinon in natural populations of Drosophila melanogaster. Genetica 121: 13-24.
32. Oshima C (1958) The resistance of strains of D. melanogaster to DDT and Dieldrin. The American Naturalist 92: 171-182.
33. Taylor MF, Heckel DG, Brown TM, Kreitman ME, Black B (1993) Linkage of pyrethroid insecticide resistance to a sodium channel locus in the tobacco budworm. Insect Biochem Mol Biol 23: 763-775.
34. David JR, Capy P (1988) Genetic variation of Drosophila melanogaster natural populations. Trends Genet 4: 106-111.
35. Turner TL, Levine MT, Eckert ML, Begun DJ (2008) Genomic analysis of adaptive differentiation in Drosophila melanogaster. Genetics 179: 455-473.
36. Yang J, McCart C, Woods DJ, Terhzaz S, Greenwood KG, et al. (2007) A Drosophila systems approach to xenobiotic metabolism. Physiological Genomics 30: 223-231.
37. Gibson G, Muse S (2004) A primer of genome science. Sunderland, MA: Sinauer Associations.
38. Lynch M, Walsh B (1998) Genetics and Analysis of Quantitative Traits. Sunderland, MA: Sinauer Associates. 980 p.
39. Smith JM (1970) Natural selection and the concept of a protein space. Nature 225: 563-564.
40. Panhuis TM, Swanson WJ (2006) Molecular evolution and population genetic analysis of candidate female reproductive genes in Drosophila. Genetics 173: 2039-2047.
41. Boussy IA, Itoh M, Rand D, Woodruff RC (1998) Origin and decay of the P element-associated latitudinal cline in Australian Drosophila melanogaster. Genetica 104: 45-57.
42. Kennington W, Gockel J, Partridge L (2003) Testing for asymmetrical gene flow in a Drosophila melanogaster body-size cline. Genetics 165: 667-673.
43. Umina P, Weeks A, Kearney M, McKechnie S, Hoffmann A (2005) A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science 308: 691-693.
44. Anderson PR, Oakeshott JG (1984) Parallel geographical patterns of allozyme variation in two sibling Drosophila species. Nature 308: 729-731.
45. Hoffmann AA, Weeks AR (2007) Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 129: 133-147.
46. Australian Government CPS, Department of the Environment, Water, Heritage, and the Arts (1997) Scheduled Wastes Fact Sheet. In: Department of the Environment W, Heritage, and the Arts, editor.
47. Rooker S, Guillemaud T, Berge J, Pasteur N, Raymond M (1996) Coamplification of esterase A and B genes as a single unit in Culex pipiens mosquitoes. Heredity 77 (Pt 5): 555-561.
48. Guillemaud T, Lenormand T, Bourguet D, Chevillon C, Pasteur N, et al. (1998) Evolution of resistance in Culex pipiens: Allele replacement and changing environment. Evolution 52: 443-453.
49. Lenormand T, Guillemaud T, Bourguet D, Raymond M (1998) Appearance and sweep of a gene duplication: Adaptive response and potential for new functions in the mosquito Culex pipiens. Evolution 52: 1705-1712.
50. Drnevich JM, Reedy MM, Ruedi EA, Rodriguez-Zas S, Hughes KA (2004) Quantitative evolutionary genomics: differential gene expression and male reproductive success in Drosophila melanogaster. Proc Biol Sci 271: 2267-2273.
51. McCart C, Buckling A, Ffrench-Constant RH (2005) DDT resistance in flies carries no cost. Curr Biol 15: R587-589.
52. Li XC, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52: 231-253.
53. Wray GA (2007) The evolutionary significance of cis-regulatory mutations. Nature Reviews Genetics 8: 206-216.
54. Brookfield JF (2005) The ecology of the genome - mobile DNA elements and their hosts. Nature Reviews Genetics 6: 128-136.
55. Dean AM, Thornton JW (2007) Mechanistic approaches to the study of evolution: the functional synthesis. Nature Reviews Genetics 8: 675-688.
56. McGregor AP, Orgogozo V, Delon I, Zanet J, Srinivasan DG, et al. (2007) Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 448: 587-590.
57. Phillips AM, Martin J, Bedo DG (2000) In situ hybridization to polytene chromosomes of Drosophila melanogaster and other dipteran species. Methods Mol Biol 123: 83-102.
58. Sakuma M (1998) Probit analysis of preference data. Applied Entomology and Zoology 33: 339-347.