Recent Selective Sweeps in North American Drosophila melanogaster Show Signatures of Soft Sweeps

Abstract

Adaptation from standing genetic variation or recurrent de novo mutation in large populations should commonly generate soft rather than hard selective sweeps. In contrast to a hard selective sweep, in which a single adaptive haplotype rises to high population frequency, in a soft selective sweep multiple adaptive haplotypes sweep through the population simultaneously, producing distinct patterns of genetic variation in the vicinity of the adaptive site. Current statistical methods were expressly designed to detect hard sweeps and most lack power to detect soft sweeps. This is particularly unfortunate for the study of adaptation in species such as Drosophila melanogaster, where all three confirmed cases of recent adaptation resulted in soft selective sweeps and where there is evidence that the effective population size relevant for recent and strong adaptation is large enough to generate soft sweeps even when adaptation requires mutation at a specific single site at a locus. Here, we develop a statistical test based on a measure of haplotype homozygosity (H12) that is capable of detecting both hard and soft sweeps with similar power. We use H12 to identify multiple genomic regions that have undergone recent and strong adaptation in a large population sample of fully sequenced Drosophila melanogaster strains from the Drosophila Genetic Reference Panel (DGRP). Visual inspection of the top 50 candidates reveals that in all cases multiple haplotypes are present at high frequencies, consistent with signatures of soft sweeps. We further develop a second haplotype homozygosity statistic (H2/H1) that, in combination with H12, is capable of differentiating hard from soft sweeps. Surprisingly, we find that the H12 and H2/H1 values for all top 50 peaks are much more easily generated by soft rather than hard sweeps. We discuss the implications of these results for the study of adaptation in Drosophila and in species with large census population sizes.

Full text

Its licence does not allow us to show the full text. Read it at PubMed Central:

References 64

1. 1.

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

   Not in our library10.1038/4151024a (opens in a new tab)

2. 2.

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

   Not in our library10.1038/4151022a (opens in a new tab)

3. 3.

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

   Not in our library10.1093/molbev/msh134 (opens in a new tab)

4. 4.

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

   Not in our library10.1038/nature04107 (opens in a new tab)

5. 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.

   Not in our library10.1073/pnas.0610385104 (opens in a new tab)

6. 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.

   Not in our library10.1093/molbev/msp119 (opens in a new tab)

7. 7.
   Pervasive Natural Selection in the Drosophila Genome? · 2009

   No notice
8. 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.

   Not in our library10.1534/genetics.111.131730 (opens in a new tab)

9. 9.

   Kousathanas A, Keightley PD (2013 ) A comparison of models to infer the distribution of fitness effects of new mutations. Genetics 193: 1197–1208.

   Not in our library10.1534/genetics.112.148023 (opens in a new tab)

10. 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.

    Not in our library10.1534/genetics.107.080226 (opens in a new tab)

11. 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

    Not in our library10.1371/journal.pgen.1001302 (opens in a new tab)

12. 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.

    Not in our library10.1016/j.cub.2009.11.055 (opens in a new tab)

13. 13.

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

    Not in our library10.1038/nrg3425 (opens in a new tab)

14. 14.

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

    Not in our library10.1016/j.tree.2013.08.003 (opens in a new tab)

15. 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.

    Not in our library10.1073/pnas.91.13.5922 (opens in a new tab)

16. 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

    Not in our library10.1186/1471-2148-4-4 (opens in a new tab)

17. 17.
    Evidence that Adaptation in Drosophila Is Not Limited by Mutation at Single Sites · 2010

    No notice
18. 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.

    Not in our library10.1007/s004380100531 (opens in a new tab)

19. 19.
    Copy Number Variation and Transposable Elements Feature in Recent, Ongoing Adaptation at the Cyp6g1 Locus · 2010

    No notice
20. 20.

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

    Not in our library10.1126/science.1112699 (opens in a new tab)

21. 21.
    Successive Increases in the Resistance of Drosophila to Viral Infection through a Transposon Insertion Followed by a Duplication · 2011

    No notice
22. 22.

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

    Not in our library

23. 23.

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

    Not in our library10.1093/genetics/123.4.887 (opens in a new tab)

24. 24.

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

    Not in our library10.1093/genetics/160.2.765 (opens in a new tab)

25. 25.

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

    Not in our library10.1093/genetics/157.2.875 (opens in a new tab)

26. 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.

    Not in our library10.1073/pnas.0401720101 (opens in a new tab)

27. 27.

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

    Not in our library10.1534/genetics.104.036947 (opens in a new tab)

28. 28.

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

    Not in our library

29. 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.

    Not in our library10.1093/molbev/msj117 (opens in a new tab)

30. 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.

    Not in our library10.1093/molbev/msu077 (opens in a new tab)

31. 31.

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

    Not in our library10.1038/356519a0 (opens in a new tab)

32. 32.

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

    Not in our library10.1093/genetics/123.3.585 (opens in a new tab)

33. 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.

    Not in our library10.1093/genetics/140.2.783 (opens in a new tab)

34. 34.

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

    Not in our library10.1093/genetics/155.3.1405 (opens in a new tab)

35. 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.

    Not in our library10.1101/gr.4252305 (opens in a new tab)

36. 36.

    Vitti JJ, Grossman SR, Sabeti PC (2013 ) Detecting natural selection in genomic data. Annual Review of Genetics 47: 97–120.

    Not in our library10.1146/annurev-genet-111212-133526 (opens in a new tab)

37. 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.

    Not in our library10.1093/genetics/136.4.1329 (opens in a new tab)

38. 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.

    Not in our library10.1093/oxfordjournals.molbev.a025905 (opens in a new tab)

39. 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.

    Not in our library10.1038/nature01140 (opens in a new tab)

40. 40.
    A Map of Recent Positive Selection in the Human Genome · 2006

    Corrected

Cited by papers we hold 19

• Population-scale long-read sequencing uncovers transposable elements associated with gene expression variation and adaptive signatures in Drosophila · 2022
  No notice
• Recommendations for improving statistical inference in population genomics · 2022
  No notice
• Rapid divergence of the male reproductive proteins in the <i>Drosophila dunni</i> group and implications for postmating incompatibilities between species · 2021
  Not checked
• Detection of hard and soft selective sweeps from Drosophila melanogaster population genomic data. · 2021
  Not checked
• Genetic and environmental modulation of transposition shapes the evolutionary potential of Arabidopsis thaliana · 2021
  No notice
• Fitness effects for Ace insecticide resistance mutations are determined by ambient temperature · 2020
  Not checked
• A community-maintained standard library of population genetic models · 2020
  No notice
• Contrasting signatures of genomic divergence during sympatric speciation · 2020
  No notice
• An approximate full-likelihood method for inferring selection and allele frequency trajectories from DNA sequence data · 2019
  No notice
• diploS/HIC: An Updated Approach to Classifying Selective Sweeps · 2018
  No notice
• The Unreasonable Effectiveness of Convolutional Neural Networks in Population Genetic Inference · 2018
  No notice
• Supervised Machine Learning for Population Genetics: A New Paradigm · 2018
  No notice
• Detecting positive selection in the genome · 2017
  No notice
• Soft Sweeps Are the Dominant Mode of Adaptation in the Human Genome · 2017
  No notice
• S/HIC: Robust Identification of Soft and Hard Sweeps Using Machine Learning · 2016
  No notice
• Deep Learning for Population Genetic Inference · 2016
  No notice
• Genomic epidemiology of artemisinin resistant malaria · 2016
  No notice
• A Genomic Map of the Effects of Linked Selection in Drosophila · 2016
  No notice
• Detecting recent selective sweeps while controlling for mutation rate and background selection · 2015
  No notice

Questions about this paper

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.