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PMID: 21218185 Published · ppublish English Journal Article

USING POPULATION GENOMICS TO DETECT SELECTION IN NATURAL POPULATIONS: KEY CONCEPTS AND METHODOLOGICAL CONSIDERATIONS.

International journal of plant sciences ·Vol. 171 ·No. 9 ·2010-11-01 ·Pages 1059-1071

Hohenlohe PA, Phillips PC, Cresko WA

Abstract

Natural selection shapes patterns of genetic variation among individuals, populations, and species, and it does so differentially across genomes. The field of population genomics provides a comprehensive genome-scale view of the action of selection, even beyond traditional model organisms. However, even with nearly complete genomic sequence information, our ability to detect the signature of selection on specific genomic regions depends on choosing experimental and analytical tools appropriate to the biological situation. For example, processes that occur at different timescales, such as sorting of standing genetic variation, mutation-selection balance, or fixed interspecific divergence, have different consequences for genomic patterns of variation. Inappropriate experimental or analytical approaches may fail to detect even strong selection or falsely identify a signature of selection. Here we outline the conceptual framework of population genomics, relate genomic patterns of variation to evolutionary processes, and identify major biological factors to be considered in studies of selection. As data-gathering technology continues to advance, our ability to understand selection in natural populations will be limited more by conceptual and analytical weaknesses than by the amount of molecular data. Our aim is to bring critical biological considerations to the fore in population genomics research and to spur the development and application of analytical tools appropriate to diverse biological systems.

Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hohenlohe Paul A
Center for Ecology and Evolutionary Biology, University of Oregon, Eugene, Oregon 97403, U.S.A.
Phillips Patrick C
Cresko William A
References (84)
84 references, click to expand
  1. Insecticide resistance in the mosquito culex pipiens: what have we learned about adaptation?
    Genetica. 2001;112-113:287-96 PMID: 11838771
  2. Adaptive protein evolution at the Adh locus in Drosophila.
    Nature. 1991 Jun 20;351(6328):652-4 PMID: 1904993
  3. The hitchhiking effect on linkage disequilibrium between linked neutral loci.
    Genetics. 2006 Apr;172(4):2647-63 PMID: 16452153
  4. Soft sweeps: molecular population genetics of adaptation from standing genetic variation.
    Genetics. 2005 Apr;169(4):2335-52 PMID: 15716498
  5. Measures of divergence between populations and the effect of forces that reduce variability.
    Mol Biol Evol. 1998 May;15(5):538-43 PMID: 9580982
  6. The role of geography in human adaptation.
    PLoS Genet. 2009 Jun;5(6):e1000500 PMID: 19503611
  7. The power and promise of population genomics: from genotyping to genome typing.
    Nat Rev Genet. 2003 Dec;4(12):981-94 PMID: 14631358
  8. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene.
    Genetics. 1998 Mar;148(3):929-36 PMID: 9539414
  9. Who believes in whole-genome scans for selection?
    Heredity (Edinb). 2009 Oct;103(4):283-4 PMID: 19654610
  10. Divergent selection and heterogeneous genomic divergence.
    Mol Ecol. 2009 Feb;18(3):375-402 PMID: 19143936
  11. Genetics in geographically structured populations: defining, estimating and interpreting F(ST).
    Nat Rev Genet. 2009 Sep;10(9):639-50 PMID: 19687804
  12. Genomic scans for selective sweeps using SNP data.
    Genome Res. 2005 Nov;15(11):1566-75 PMID: 16251466
  13. Evolution in Mendelian Populations.
    Genetics. 1931 Mar;16(2):97-159 PMID: 17246615
  14. Linkage and association mapping of Arabidopsis thaliana flowering time in nature.
    PLoS Genet. 2010 May 06;6(5):e1000940 PMID: 20463887
  15. Genetic drift in an infinite population. The pseudohitchhiking model.
    Genetics. 2000 Jun;155(2):909-19 PMID: 10835409
  16. The effects of artificial selection on the maize genome.
    Science. 2005 May 27;308(5726):1310-4 PMID: 15919994
  17. Soft selective sweep near a gene that increases plant height in wheat.
    Mol Ecol. 2008 Feb;17(3):741-56 PMID: 18194170
  18. Variation and selection at the CAULIFLOWER floral homeotic gene accompanying the evolution of domesticated Brassica oleracea.
    Genetics. 2000 Jun;155(2):855-62 PMID: 10835404
  19. Detecting positive selection from genome scans of linkage disequilibrium.
    BMC Genomics. 2010 Jan 05;11:8 PMID: 20051139
  20. Pattern of polymorphism after strong artificial selection in a domestication event.
    Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10667-72 PMID: 15249682
  21. The structure of linkage disequilibrium around a selective sweep.
    Genetics. 2007 Mar;175(3):1395-406 PMID: 17194788
  22. Identifying adaptive genetic divergence among populations from genome scans.
    Mol Ecol. 2004 Apr;13(4):969-80 PMID: 15012769
  23. Detecting selective sweeps: a new approach based on hidden markov models.
    Genetics. 2009 Apr;181(4):1567-78 PMID: 19204373
  24. The coalescent in an exponentially growing metapopulation and its application to Arabidopsis thaliana.
    Genetics. 2000 Aug;155(4):2015-9 PMID: 11032470
  25. Properties of statistical tests of neutrality for DNA polymorphism data.
    Genetics. 1995 Sep;141(1):413-29 PMID: 8536987
  26. Inbreeding coefficients and coalescence times.
    Genet Res. 1991 Oct;58(2):167-75 PMID: 1765264
  27. DetSel 1.0: a computer program to detect markers responding to selection.
    J Hered. 2003 Sep-Oct;94(5):429-31 PMID: 14557398
  28. Genome-wide detection and characterization of positive selection in human populations.
    Nature. 2007 Oct 18;449(7164):913-8 PMID: 17943131
  29. Evolutionary rate at the molecular level.
    Nature. 1968 Feb 17;217(5129):624-6 PMID: 5637732
  30. Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. Accurate inference and estimation in population genomics.
    Mol Biol Evol. 2006 May;23(5):911-8 PMID: 16407459
  31. Constructing genomic maps of positive selection in humans: where do we go from here?
    Genome Res. 2009 May;19(5):711-22 PMID: 19411596
  32. Geographical variation in selection, from phenotypes to molecules.
    Am Nat. 2006 Apr;167(4):481-95 PMID: 16670992
  33. The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population.
    Genetics. 2003 Mar;163(3):1201-13 PMID: 12663556
  34. A map of recent positive selection in the human genome.
    PLoS Biol. 2006 Mar;4(3):e72 PMID: 16494531
  35. Next-generation DNA sequencing.
    Nat Biotechnol. 2008 Oct;26(10):1135-45 PMID: 18846087
  36. Strong positive selection drives rapid diversification of R-genes in Arabidopsis relatives.
    J Mol Evol. 2010 Feb;70(2):137-48 PMID: 20044783
  37. Positive natural selection in the human lineage.
    Science. 2006 Jun 16;312(5780):1614-20 PMID: 16778047
  38. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data.
    PLoS Genet. 2009 Oct;5(10):e1000695 PMID: 19851460
  39. Detecting recent positive selection in the human genome from haplotype structure.
    Nature. 2002 Oct 24;419(6909):832-7 PMID: 12397357
  40. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase.
    Am J Hum Genet. 2006 Apr;78(4):629-44 PMID: 16532393
  41. Linkage disequilibrium--understanding the evolutionary past and mapping the medical future.
    Nat Rev Genet. 2008 Jun;9(6):477-85 PMID: 18427557
  42. A composite of multiple signals distinguishes causal variants in regions of positive selection.
    Science. 2010 Feb 12;327(5967):883-6 PMID: 20056855
  43. A test of neutral molecular evolution based on nucleotide data.
    Genetics. 1987 May;116(1):153-9 PMID: 3110004
  44. Coalescent under the evolution of coadaptation.
    Mol Ecol. 2009 Dec;18(24):5018-29 PMID: 19912539
  45. A population genomic approach to map recent positive selection in model species.
    Mol Ecol. 2008 Aug;17(16):3585-98 PMID: 18627454
  46. Estimation of allele frequencies from high-coverage genome-sequencing projects.
    Genetics. 2009 May;182(1):295-301 PMID: 19293142
  47. Sizing up human height variation.
    Nat Genet. 2008 May;40(5):489-90 PMID: 18443579
  48. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags.
    PLoS Genet. 2010 Feb 26;6(2):e1000862 PMID: 20195501
  49. Recurrent gene amplification and soft selective sweeps during evolution of multidrug resistance in malaria parasites.
    Mol Biol Evol. 2007 Feb;24(2):562-73 PMID: 17124182
  50. The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations.
    Genet Res. 1997 Oct;70(2):155-74 PMID: 9449192
  51. Molecular signatures of natural selection.
    Annu Rev Genet. 2005;39:197-218 PMID: 16285858
  52. The effect of linkage on limits to artificial selection.
    Genet Res. 1966 Dec;8(3):269-94 PMID: 5980116
  53. Soft sweeps II--molecular population genetics of adaptation from recurrent mutation or migration.
    Mol Biol Evol. 2006 May;23(5):1076-84 PMID: 16520336
  54. Population genomics of the Arabidopsis thaliana flowering time gene network.
    Mol Biol Evol. 2009 Nov;26(11):2475-86 PMID: 19625391
  55. Genome-wide scans for footprints of natural selection.
    Philos Trans R Soc Lond B Biol Sci. 2010 Jan 12;365(1537):185-205 PMID: 20008396
  56. Hitchhiking mapping--functional genomics from the population genetics perspective.
    Trends Genet. 2003 Jan;19(1):32-8 PMID: 12493246
  57. Linkage disequilibrium under genetic hitchhiking in finite populations.
    Genetics. 2008 May;179(1):527-37 PMID: 18493069
  58. Selective sweeps reveal candidate genes for adaptation to drought and salt tolerance in common sunflower, Helianthus annuus.
    Genetics. 2007 Apr;175(4):1823-34 PMID: 17237516
  59. Testing hypotheses regarding the genetics of adaptation.
    Genetica. 2005 Feb;123(1-2):15-24 PMID: 15881677
  60. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation.
    Curr Biol. 2010 Feb 23;20(4):R208-15 PMID: 20178769
  61. Molecular population genetics and the search for adaptive evolution in plants.
    Mol Biol Evol. 2005 Mar;22(3):506-19 PMID: 15525701
  62. Natural distributions of mitochondrial sequence diversity support new null hypotheses.
    Evolution. 2010 Apr 1;64(4):1136-42 PMID: 19863588
  63. How reliable are empirical genomic scans for selective sweeps?
    Genome Res. 2006 Jun;16(6):702-12 PMID: 16687733
  64. From genotype to phenotype: systems biology meets natural variation.
    Science. 2008 Apr 25;320(5875):495-7 PMID: 18436781
  65. Genomic signatures of positive selection in humans and the limits of outlier approaches.
    Genome Res. 2006 Aug;16(8):980-9 PMID: 16825663
  66. Adaptation and speciation: what can F(st) tell us?
    Trends Ecol Evol. 2005 Aug;20(8):435-40 PMID: 16701414
  67. Recombination and the properties of Tajima's D in the context of approximate-likelihood calculation.
    Genetics. 2005 Dec;171(4):2143-8 PMID: 15998723
  68. Soft sweeps III: the signature of positive selection from recurrent mutation.
    PLoS Genet. 2006 Dec 15;2(12):e186 PMID: 17173482
  69. Personal genomes: The case of the missing heritability.
    Nature. 2008 Nov 6;456(7218):18-21 PMID: 18987709
  70. The effect of deleterious mutations on neutral molecular variation.
    Genetics. 1993 Aug;134(4):1289-303 PMID: 8375663
  71. ESTIMATING F-STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE.
    Evolution. 1984 Nov;38(6):1358-1370 PMID: 28563791
  72. LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method.
    BMC Bioinformatics. 2008 Jul 28;9:323 PMID: 18662398
  73. Effects of spatially varying selection on nucleotide diversity and linkage disequilibrium: insights from deer mouse globin genes.
    Genetics. 2008 Sep;180(1):367-79 PMID: 18716337
  74. The signature of positive selection on standing genetic variation.
    Evolution. 2005 Nov;59(11):2312-23 PMID: 16396172
  75. Evolution of the ancestral recombination graph along the genome in case of selective sweep.
    J Math Biol. 2010 Dec;61(6):819-41 PMID: 20077118
  76. Molecular networks as sensors and drivers of common human diseases.
    Nature. 2009 Sep 10;461(7261):218-23 PMID: 19741703
  77. Human genetic variation and its contribution to complex traits.
    Nat Rev Genet. 2009 Apr;10(4):241-51 PMID: 19293820
  78. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
    Genetics. 1989 Nov;123(3):585-95 PMID: 2513255
  79. Balancing selection and its effects on sequences in nearby genome regions.
    PLoS Genet. 2006 Apr;2(4):e64 PMID: 16683038
  80. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective.
    Genetics. 2008 Oct;180(2):977-93 PMID: 18780740
  81. The molecular genetics of crop domestication.
    Cell. 2006 Dec 29;127(7):1309-21 PMID: 17190597
  82. Detecting loci under selection in a hierarchically structured population.
    Heredity (Edinb). 2009 Oct;103(4):285-98 PMID: 19623208
  83. Using genome scans of DNA polymorphism to infer adaptive population divergence.
    Mol Ecol. 2005 Mar;14(3):671-88 PMID: 15723660
  84. Statistical tests of neutrality of mutations.
    Genetics. 1993 Mar;133(3):693-709 PMID: 8454210
Article Info
Journal
International journal of plant sciences
Abbr.
Int J Plant Sci
ISSN
1058-5893
Published
2010-11-01
Pages
1059-1071
Language
English
Region
United States
NLM ID
9886579
PMCID
PMC3016716
Grants
NIA NIH HHS · P01 AG022500 · United States
NIGMS NIH HHS · R24 GM079486 · United States
NIGMS NIH HHS · R24 GM079486-01A1 · United States
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