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Recent Selective Sweeps in North American Show Signatures of Soft Sweeps


Evolutionary adaptation is a process in which beneficial mutations increase in frequency in response to selective pressures. If these mutations were previously rare or absent from the population, adaptation should generate a characteristic signature in the genetic diversity around the adaptive locus, known as a selective sweep. Such selective sweeps can be distinguished into hard selective sweeps, where only a single adaptive mutation rises in frequency, or soft selective sweeps, where multiple adaptive mutations at the same locus sweep through the population simultaneously. Here we design a new statistical method that can identify both hard and soft sweeps in population genomic data and apply this method to a Drosophila melanogaster population genomic dataset consisting of 145 sequenced strains collected in North Carolina. We find that selective sweeps were abundant in the recent history of this population. Interestingly, we also find that practically all of the strongest and most recent sweeps show patterns that are more consistent with soft rather than hard sweeps. We discuss the implications of these findings for the discovery and quantification of adaptation from population genomic data in Drosophila and other species with large population sizes.


Vyšlo v časopise: Recent Selective Sweeps in North American Show Signatures of Soft Sweeps. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1005004
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005004

Souhrn

Evolutionary adaptation is a process in which beneficial mutations increase in frequency in response to selective pressures. If these mutations were previously rare or absent from the population, adaptation should generate a characteristic signature in the genetic diversity around the adaptive locus, known as a selective sweep. Such selective sweeps can be distinguished into hard selective sweeps, where only a single adaptive mutation rises in frequency, or soft selective sweeps, where multiple adaptive mutations at the same locus sweep through the population simultaneously. Here we design a new statistical method that can identify both hard and soft sweeps in population genomic data and apply this method to a Drosophila melanogaster population genomic dataset consisting of 145 sequenced strains collected in North Carolina. We find that selective sweeps were abundant in the recent history of this population. Interestingly, we also find that practically all of the strongest and most recent sweeps show patterns that are more consistent with soft rather than hard sweeps. We discuss the implications of these findings for the discovery and quantification of adaptation from population genomic data in Drosophila and other species with large population sizes.


Zdroje

1. Fay JC, Wyckoff GJ, Wu CI (2002) Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415: 1024–1026. 11875569

2. Smith NG, Eyre-Walker A (2002) Adaptive protein evolution in Drosophila. Nature 415: 1022–1024. 11875568

3. Bierne N, Eyre-Walker A (2004) The genomic rate of adaptive amino acid substitution in Drosophila. Molecular Biology and Evolution 21: 1350–1360. 15044594

4. Andolfatto P (2005) Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149–1152. 16237443

5. Shapiro JA, Huang W, Zhang C, Hubisz MJ, Lu J, et al. (2007) Adaptive genic evolution in the Drosophila genomes. Proceedings of the National Academy of Sciences of the United States of America 104: 2271–2276. 17284599

6. Eyre-Walker A, Keightley PD (2009) Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change. Molecular Biology and Evolution 26: 2097–2108. doi: 10.1093/molbev/msp119 19535738

7. Sella G, Petrov DA, Przeworski M, Andolfatto P (2009) Pervasive natural selection in the Drosophila genome? PLoS Genetics 5: e1000495. doi: 10.1371/journal.pgen.1000495 19503600

8. Schneider A, Charlesworth B, Eyre-Walker A, Keightley PD (2011) A method for inferring the rate of occurrence and fitness effects of advantageous mutations. Genetics 189: 1427–1437. doi: 10.1534/genetics.111.131730 21954160

9. Kousathanas A, Keightley PD (2013) A comparison of models to infer the distribution of fitness effects of new mutations. Genetics 193: 1197–1208. doi: 10.1534/genetics.112.148023 23341416

10. 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. 18073425

11. Sattath S, Elyashiv E, Kolodny O, Rinott Y, Sella G (2011) Pervasive adaptive protein evolution apparent in diversity patterns around amino acid substitutions in Drosophila simulans. PLoS Genetics 7: e1001302. doi: 10.1371/journal.pgen.1001302 21347283

12. Pritchard JK, Pickrell JK, Coop G (2010) The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Current Biology 20: R208–215. doi: 10.1016/j.cub.2009.11.055 20178769

13. Cutter AD, Payseur BA (2013) Genomic signatures of selection at linked sites: unifying the disparity among species. Nature Reviews Genetics 14: 262–274. doi: 10.1038/nrg3425 23478346

14. Messer PW, Petrov DA (2013) Population genomics of rapid adaptation by soft selective sweeps. Trends in Ecology & Evolution 28: 659–669.

15. Mutero A, Pralavorio M, Bride JM, Fournier D (1994) Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proceedings of the National Academy of Sciences of the United States of America 91: 5922–5926. 8016090

16. Menozzi P, Shi MA, Lougarre A, Tang ZH, Fournier D (2004) Mutations of acetylcholinesterase which confer insecticide resistance in Drosophila melanogaster populations. BMC Evolutionary Biology 4: 4. 15018651

17. Karasov T, Messer PW, Petrov DA (2010) Evidence that adaptation in Drosophila is not limited by mutation at single sites. PLoS Genetics 6: e1000924. doi: 10.1371/journal.pgen.1000924 20585551

18. 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. Molecular Genetics and Genomics 266: 556–563. 11810226

19. Schmidt JM, Good RT, Appleton B, Sherrard J, Raymant GC, et al. (2010) Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLoS Genetics 6: e1000998. doi: 10.1371/journal.pgen.1000998 20585622

20. Aminetzach YT, Macpherson JM, Petrov DA (2005) Pesticide resistance via transposition-mediated adaptive gene truncation in Drosophila. Science 309: 764–767. 16051794

21. Magwire MM, Bayer F, Webster CL, Cao C, Jiggins FM (2011) Successive increases in the resistance of Drosophila to viral infection through a transposon insertion followed by a Duplication. PLoS Genetics 7: e1002337. doi: 10.1371/journal.pgen.1002337 22028673

22. Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genetical Research 23: 23–35. 4407212

23. Kaplan NL, Hudson RR, Langley CH (1989) The “hitchhiking effect” revisited. Genetics 123: 887–899. 2612899

24. Kim Y, Stephan W (2002) Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160: 765–777. 11861577

25. Orr HA, Betancourt AJ (2001) Haldane’s sieve and adaptation from the standing genetic variation. Genetics 157: 875–884. 11157004

26. Innan H, Kim Y (2004) Pattern of polymorphism after strong artificial selection in a domestication event. Proceedings of the National Academy of Sciences of the United States of America 101: 10667–10672. 15249682

27. Hermisson J, Pennings PS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169: 2335–2352. 15716498

28. Przeworski M, Coop G, Wall JD (2005) The signature of positive selection on standing genetic variation. Evolution 59: 2312–2323. 16396172

29. Pennings PS, Hermisson J (2006) Soft sweeps II—molecular population genetics of adaptation from recurrent mutation or migration. Molecular Biology and Evolution 23: 1076–1084. 16520336

30. Ferrer-Admetlla A, Liang M, Korneliussen T, Nielsen R (2014) On detecting incomplete soft or hard selective sweeps using haplotype structure. Molecular Biology and Evolution 31: 1275–1291. doi: 10.1093/molbev/msu077 24554778

31. Begun DJ, Aquadro CF (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356: 519–520. 1560824

32. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595. 2513255

33. Braverman JM, Hudson RR, Kaplan NL, Langley CH, Stephan W (1995) The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140: 783–796. 7498754

34. Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155: 1405–1413. 10880498

35. Nielsen R, Williamson S, Kim Y, Hubisz MJ, Clark AG, et al. (2005) Genomic scans for selective sweeps using SNP data. Genome Research 15: 1566–1575. 16251466

36. Vitti JJ, Grossman SR, Sabeti PC (2013) Detecting natural selection in genomic data. Annual Review of Genetics 47: 97–120. doi: 10.1146/annurev-genet-111212-133526 24274750

37. Hudson RR, Bailey K, Skarecky D, Kwiatowski J, Ayala FJ (1994) Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics 136: 1329–1340. 8013910

38. Depaulis F, Veuille M (1998) Neutrality tests based on the distribution of haplotypes under an infinite-site model. Molecular Biology and Evolution 15: 1788–1790. 9917213

39. Sabeti PC, Reich DE, Higgins JM, Levine HZ, Richter DJ, et al. (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419: 832–837. 12397357

40. Voight BF, Kudaravalli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biology 4: e72. 16494531

41. Pennings PS, Hermisson J (2006) Soft sweeps III: the signature of positive selection from recurrent mutation. PLoS Genetics 2: e186. 17173482

42. Teshima KM, Coop G, Przeworski M (2006) How reliable are empirical genomic scans for selective sweeps? Genome Research 16: 702–712. 16687733

43. Pokalyuk C (2012) The effect of recurrent mutation on the linkage disequilibrium under a selective sweep. Journal of Mathematical Biology 64: 291–317. doi: 10.1007/s00285-011-0411-y 21359840

44. Mackay TF, Richards S, Stone EA, Barbadilla A, Ayroles JF, et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173–178. doi: 10.1038/nature10811 22318601

45. Duchen P, Zivkovic D, Hutter S, Stephan W, Laurent S (2013) Demographic inference reveals African and European admixture in the North American Drosophila melanogaster population. Genetics 193: 291–301. doi: 10.1534/genetics.112.145912 23150605

46. 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. 16299396

47. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD (2009) Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genetics 5: e1000695. doi: 10.1371/journal.pgen.1000695 19851460

48. 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 Research 19: 1195–1201. doi: 10.1101/gr.091231.109 19439516

49. Comeron JM, Ratnappan R, Bailin S (2012) The many landscapes of recombination in Drosophila melanogaster. PLoS Genetics 8: e1002905. doi: 10.1371/journal.pgen.1002905 23071443

50. Przeworski M, Wall JD, Andolfatto P (2001) Recombination and the frequency spectrum in Drosophila melanogaster and Drosophila simulans. Molecular Biology and Evolution 18: 291–298. 11230530

51. Gillespie JH (2004) Population Genetics: A concise guide. Johns Hopkins University Press.

52. Wilson BA, Petrov DA, Messer PW (2014) Soft selective sweeps in complex demographic scenarios. Genetics 198: 669–684. doi: 10.1534/genetics.114.165571 25060100

53. Messer PW, Neher RA (2012) Estimating the strength of selective sweeps from deep population diversity data. Genetics 191: 593–605. doi: 10.1534/genetics.112.138461 22491190

54. Green DM, Swets JA (1966) Signal detection theory and psychophysics. New York: Wiley.

55. Comeron JM (2014) Background selection as baseline for nucleotide variation across the Drosophila genome. PLoS Genetics 10: e1004434. doi: 10.1371/journal.pgen.1004434 24968283

56. Enard D, Messer PW, Petrov DA (2014) Genome-wide signals of positive selection in human evolution. Genome Research 24: 885–895. doi: 10.1101/gr.164822.113 24619126

57. Fagny M, Patin E, Enard D, Barreiro LB, Quintana-Murci L, et al. (2014) Exploring the occurrence of classic selective sweeps in humans using whole-genome sequencing data sets. Molecular Biology and Evolution 31: 1850–1868. doi: 10.1093/molbev/msu118 24694833

58. Ralph P, Coop G (2010) Parallel adaptation: one or many waves of advance of an advantageous allele? Genetics 186: 647–668. doi: 10.1534/genetics.110.119594 20660645

59. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652–654. 1904993

60. Andolfatto P (2007) Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome. Genome Research 17: 1755–1762. 17989248

61. Ewing G, Hermisson J (2010) MSMS: a coalescent simulation program including recombination, demographic structure and selection at a single locus. Bioinformatics 26: 2064–2065. doi: 10.1093/bioinformatics/btq322 20591904

62. Parsch J, Novozhilov S, Saminadin-Peter SS, Wong KM, Andolfatto P (2010) On the utility of short intron sequences as a reference for the detection of positive and negative selection in Drosophila. Molecular Biology and Evolution 27: 1226–1234. doi: 10.1093/molbev/msq046 20150340

63. Lawrie DS, Messer PW, Hershberg R, Petrov DA (2013) Strong purifying selection at synonymous sites in D. melanogaster. PLoS Genetics 9: e1003527. doi: 10.1371/journal.pgen.1003527 23737754

64. Li H, Stephan W (2006) Inferring the demographic history and rate of adaptive substitution in Drosophila. PLoS Genetics 2: e166. 17040129

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