Evidence that adaptation in Drosophila is not limited by mutation at single sites

PLoS Genetics

Volumn 6, Issue 6, 2010, Pages 1-10

  Karasov, Talia ^a   Messer, Philipp W ^a   Petrov, Dmitri A ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSECTICIDE;

ALLELE; ARTICLE; DROSOPHILA MELANOGASTER; EVOLUTIONARY ADAPTATION; EXON; GENE LOCUS; GENE MUTATION; GENETIC POLYMORPHISM; GENOTYPE; HAPLOTYPE; INSECTICIDE RESISTANCE; NONHUMAN; POLYMERASE CHAIN REACTION; POPULATION DYNAMICS; POPULATION SIZE; ADAPTATION; ANIMAL; GENETICS; MOLECULAR EVOLUTION; MUTATION;

DROSOPHILA MELANOGASTER; EUKARYOTA;

ADAPTATION, BIOLOGICAL; ALLELES; ANIMALS; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; MUTATION;

EID: 77954167479     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000924     Document Type: Article

References (48)

1. Charlesworth B (2009) Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10: 195-205.
2. Zhu KY, Lee SH, Clark JM (1996) A Point Mutation of Acetylcholinesterase Associated with Azinphosmethyl Resistance and Reduced Fitness in Colorado Potato Beetle. Pestic Biochem Physiol 55: 100-108.
3. Anazawa Y, Tomita T, Aiki Y, Kozaki T, Kono Y (2003) Sequence of a Cdna encoding acetylcholinesterase from susceptible and resistant two-spotted spider mite, Tetranychus urticae. Insect Biochem Mol Biol 33: 509-514.
4. Nabeshima T, Mori A, Kozaki T, Iwata Y, Hidoh O, et al. (2004) An amino acid substitution attributable to insecticide-insensitivity of acetylcholinesterase in a Japanese encephalitis vector mosquito, Culex tritaeniorhynchus. Biochem Biophys Res Commun 313: 794-801.
5. Mutero A, Pralavorio M, Bride JM, Fournier D (1994) Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proc Natl Acad Sci USA 91: 5922-5926.
6. Vontas JG, Hejazi MJ, Hawkes NJ, Cosmidis N, Loukas M, et al. (2002) Resistance-associated point mutations of organophosphate insensitive acetyl-cholinesterase, in the olive fruit fly Bactrocera oleae. Insect Mol Biol 11: 329-336.
7. Walsh SB, Dolden TA, Moores GD, Kristensen M, Lewis T, et al. (2001) Identification and characterization of mutations in housefly (Musca domestica) acetylcholinesterase involved in insecticide resistance. Biochem J 359: 175-181.
8. Aminetzach YT, Macpherson JM, Petrov DA (2005) Pesticide resistance via transposition-mediated adaptive gene truncation in Drosophila. Science 309: 764-767.
9. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Jr., Dickson M, et al. (2005) Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307: 1928-1933.
10. Aldridge WN (1950) Some properties of specific cholinesterase with particular reference to the mechanism of inhibition by diethyl p-nitrophenyl thiophosphate (E 605) and analogues. Biochem J 46: 451-460.
11. Smissaert HR (1964) Cholinesterase Inhibition in Spider Mites Susceptible and Resistant to Organophosphate. Science 143: 129-131.
12. Menozzi P, Shi MA, Lougarre A, Tang ZH, Fournier D (2004) Mutations of acetylcholinesterase which confer insecticide resistance in Drosophila melanogaster populations. BMC Evol Biol 4: 4.
13. Shi MA, Lougarre A, Alies C, Fremaux I, Tang ZH, et al. (2004) Acetylcholinesterase alterations reveal the fitness cost of mutations conferring insecticide resistance. BMC Evol Biol 4: 5.
14. Miyo T, Oguma Y (2002) Negative correlations between resistance to three organophosphate insecticides and productivity within a natural population of Drosophila melanogaster (Diptera: Drosophilidae). J Econ Entomol 95: 1229-1238.
15. David JR, Capy P (1988) Genetic variation of Drosophila melanogaster natural populations. Trends Genet 4: 106-111.
16. Kidwell MG (1983) Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proc Natl Acad Sci USA 80: 1655-1659.
17. Ashburner M (1989) Drosophila: A Laboratory Handbook and Manual. New York: Cold Spring Harbor Laboratory Press.
18. Thornton K, Andolfatto P (2006) Approximate Bayesian inference reveals evidence for a recent, severe bottleneck in a Netherlands population of Drosophila melanogaster. Genetics 172: 1607-1619.
19. Li H, Stephan W (2006) Inferring the demographic history and rate of adaptive substitution in Drosophila. PLoS Genet 2: e166. doi:10.1371/journal.pgen.0020166.
20. Pennings PS, Hermisson J (2006) Soft sweeps III: the signature of positive selection from recurrent mutation. PLoS Genet 2: e186. 10.1371/journal.pgen.0020186.
21. Pennings PS, Hermisson J (2006) Soft sweeps II-molecular population genetics of adaptation from recurrent mutation or migration. Mol Biol Evol 23: 1076-1084.
22. Hermisson J, Pennings PS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169: 2335-2352.
23. Keightley PD, Trivedi U, Thomson M, Oliver F, Kumar S, et al. (2009) Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines. Genome Res 19: 1195-1201.
24. Fiston-Lavier A-S, Singh ND, Lipatov M, Petrov DA (2010) Drosophila melanogaster recombination rate calculator Gene, (in press).
25. Watt WB (1972) Intragenic Recombination as a Source of Population Genetic Variability. American Naturalist 106: 737-753.
26. Hudson RR (2002) Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18: 337-338.
27. 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.
28. Macpherson JM, Sella G, Davis JC, Petrov DA (2007) Genomewide spatial correspondence between nonsynonymous divergence and neutral polymorphism reveals extensive adaptation in Drosophila. Genetics 177: 2083-2099.
29. Lewontin RC (1974) The genetic basis of evolutionary change. New York: Columbia University Press.
30. 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.
31. Gonzalez J, Lenkov K, Lipatov M, Macpherson JM, Petrov DA (2008) High rate of recent transposable element-induced adaptation in Drosophila melanogaster. PLoS Biol 6: e251. doi:10.1371/journal.pbio.0060251.
32. Kouyos RD, Althaus CL, Bonhoeffer S (2006) Stochastic or deterministic: what is the effective population size of HIV-1? Trends Microbiol 14: 507-511.
33. Weissman DB, Desai MM, Fisher DS, Feldman MW (2009) The rate at which asexual populations cross fitness valleys. Theor Popul Biol 75: 286-300
34. Gillespie JH (1991) The Causes of Molecular Evolution. New York: Oxford University Press.
35. Weinreich DM, Delaney NF, Depristo MA, Hartl DL (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111-114.
36. Andolfatto P (2007) Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome. Genome Res 17: 1755-1762.
37. Otto SP, Whitlock MC (1997) The probability of fixation in populations of changing size. Genetics 146: 723-733.
38. Jeong S, Rebeiz M, Andolfatto P, Werner T, True J, et al. (2008) The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132: 783-793.
39. Schlenke TA, Begun DJ (2005) Linkage disequilibrium and recent selection at three immunity receptor loci in Drosophila simulans. Genetics 169: 2013-2022.
40. Labbe P, Berthomieu A, Berticat C, Alout H, Raymond M, et al. (2007) Independent duplications of the acetylcholinesterase gene conferring insecticide resistance in the mosquito Culex pipiens. Mol Biol Evol 24: 1056-1067.
41. Enattah NS, Trudeau A, Pimenoff V, Maiuri L, Auricchio S, et al. (2007) Evidence of still-ongoing convergence evolution of the lactase persistence T-13910 alleles in humans. Am J Hum Genet 81: 615-625.
42. Coop G, Pickrell JK, Novembre J, Kudaravalli S, Li J, et al. (2009) The role of geography in human adaptation. PLoS Genet 5: e1000500. doi:10.1371/journal.pgen.1000500.
43. Sommer SS, Groszbach AR, Bottema CD (1992) PCR amplification of specific alleles (PASA) is a general method for rapidly detecting known single-base changes. Biotechniques 12: 82-87.
44. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9: 1657-1659.
45. Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174-175.
46. Ewens WJ (2004) Mathematical population genetics. New York: Springer-Verlag. v. p.
47. Wright S (1938) The Distribution of Gene Frequencies Under Irreversible Mutation. Proc Natl Acad Sci USA 24: 253-259.
48. Maynard-Smith J (1971) What use is sex? J Theor Biol 30: 319-335.