Home LiteratureArticle Details
PMID: 21775012 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Weighing the evidence for adaptation at the molecular level.

Trends in genetics : TIG ·Vol. 27 ·No. 9 ·2011-09-00 ·Pages 343-9

Fay JC

Abstract

The abundance of genome polymorphism and divergence data has provided unprecedented insight into how mutation, drift and natural selection shape genome evolution. Application of the McDonald-Kreitman (MK) test to such data indicates a pervasive influence of positive selection, particularly in Drosophila species. However, evidence for positive selection in other species ranging from yeast to humans is often weak or absent. Although evidence for positive selection could be obscured in some species, there is also reason to believe that the frequency of adaptive substitutions could be overestimated as a result of epistatic fitness effects or hitchhiking of deleterious mutations. Based on these considerations it is argued that the common assumption of independence among sites must be relaxed before abandoning the neutral theory of molecular evolution.

MeSH Terms
Adaptation, Biological/genetics Animals Bacteria/genetics Drosophila/genetics Epistasis, Genetic Evolution, Molecular Genetic Fitness Humans Models, Genetic Mutation Selection, Genetic
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Fay Justin C
Department of Genetics and Center for Genome Sciences and Systems Biology, Washington University, St. Louis, MO, USA. [email protected]
References (77)
77 references, click to expand
  1. The evolutionary fate and consequences of duplicate genes.
    Science. 2000 Nov 10;290(5494):1151-5 PMID: 11073452
  2. The neutral theory of molecular evolution in the genomic era.
    Annu Rev Genomics Hum Genet. 2010;11:265-89 PMID: 20565254
  3. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans.
    PLoS Biol. 2007 Nov 6;5(11):e310 PMID: 17988176
  4. Pervasive adaptive protein evolution apparent in diversity patterns around amino acid substitutions in Drosophila simulans.
    PLoS Genet. 2011 Feb 10;7(2):e1001302 PMID: 21347283
  5. Is the population size of a species relevant to its evolution?
    Evolution. 2001 Nov 11;55(11):2161-9 PMID: 11794777
  6. Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change.
    Mol Biol Evol. 2009 Sep;26(9):2097-108 PMID: 19535738
  7. The genomic rate of adaptive amino acid substitution in Drosophila.
    Mol Biol Evol. 2004 Jul;21(7):1350-60 PMID: 15044594
  8. Patterns of molecular variation and evolution in Drosophila americana and its relatives.
    Genetics. 2007 Aug;176(4):2293-305 PMID: 17507679
  9. Changing effective population size and the McDonald-Kreitman test.
    Genetics. 2002 Dec;162(4):2017-24 PMID: 12524367
  10. Genome-wide evidence for efficient positive and purifying selection in Capsella grandiflora, a plant species with a large effective population size.
    Mol Biol Evol. 2010 Aug;27(8):1813-21 PMID: 20194429
  11. Controlling type-I error of the McDonald-Kreitman test in genomewide scans for selection on noncoding DNA.
    Genetics. 2008 Nov;180(3):1767-71 PMID: 18791238
  12. The McDonald-Kreitman test and slightly deleterious mutations.
    Mol Biol Evol. 2008 Jun;25(6):1007-15 PMID: 18195052
  13. Synonymous and nonsynonymous polymorphisms versus divergences in bacterial genomes.
    Mol Biol Evol. 2008 Oct;25(10):2199-209 PMID: 18667439
  14. Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle.
    Proc Natl Acad Sci U S A. 2008 Mar 25;105(12):4957-62 PMID: 18344325
  15. Nonlinear dynamics of nonsynonymous (dN) and synonymous (dS) substitution rates affects inference of selection.
    Genome Biol Evol. 2009 Aug 13;1:308-19 PMID: 20333200
  16. Adaptive protein evolution at the Adh locus in Drosophila.
    Nature. 1991 Jun 20;351(6328):652-4 PMID: 1904993
  17. The rate of adaptive evolution in enteric bacteria.
    Mol Biol Evol. 2006 Jul;23(7):1348-56 PMID: 16621913
  18. Adaptive evolution in humans revealed by the negative correlation between the polymorphism and fixation phases of evolution.
    Proc Natl Acad Sci U S A. 2007 Mar 6;104(10):3907-12 PMID: 17360451
  19. Adaptive evolution of asexual populations under Muller's ratchet.
    Evolution. 2004 Jul;58(7):1403-13 PMID: 15341144
  20. Adaptations to fluctuating selection in Drosophila.
    Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2277-82 PMID: 17287357
  21. Pervasive hitchhiking at coding and regulatory sites in humans.
    PLoS Genet. 2009 Jan;5(1):e1000336 PMID: 19148272
  22. The contribution of epistasis to the architecture of fitness in an RNA virus.
    Proc Natl Acad Sci U S A. 2004 Oct 26;101(43):15376-9 PMID: 15492220
  23. Dobzhansky-Muller incompatibilities in protein evolution.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14878-83 PMID: 12403824
  24. The genomic rate of adaptive evolution.
    Trends Ecol Evol. 2006 Oct;21(10):569-75 PMID: 16820244
  25. Toward a selection theory of molecular evolution.
    Evolution. 2008 Feb;62(2):255-65 PMID: 18302709
  26. Darwinian evolution can follow only very few mutational paths to fitter proteins.
    Science. 2006 Apr 7;312(5770):111-4 PMID: 16601193
  27. QTL-based evidence for the role of epistasis in evolution.
    Genet Res. 2005 Oct;86(2):89-95 PMID: 16356282
  28. Assessing the evolutionary impact of amino acid mutations in the human genome.
    PLoS Genet. 2008 May 30;4(5):e1000083 PMID: 18516229
  29. Estimating the genomewide rate of adaptive protein evolution in Drosophila.
    Genetics. 2006 Jun;173(2):821-37 PMID: 16582427
  30. Positive and negative selection on the human genome.
    Genetics. 2001 Jul;158(3):1227-34 PMID: 11454770
  31. Understanding the overdispersed molecular clock.
    Genetics. 2000 Mar;154(3):1403-17 PMID: 10757779
  32. Preservation of duplicate genes by complementary, degenerative mutations.
    Genetics. 1999 Apr;151(4):1531-45 PMID: 10101175
  33. Evolution and speciation on holey adaptive landscapes.
    Trends Ecol Evol. 1997 Aug;12(8):307-12 PMID: 21238086
  34. Genome wide analyses reveal little evidence for adaptive evolution in many plant species.
    Mol Biol Evol. 2010 Aug;27(8):1822-32 PMID: 20299543
  35. Slightly deleterious mutant substitutions in evolution.
    Nature. 1973 Nov 9;246(5428):96-8 PMID: 4585855
  36. Human SNPs reveal no evidence of frequent positive selection.
    Mol Biol Evol. 2005 Dec;22(12):2504-7 PMID: 16107590
  37. Quantification of adaptive evolution of genes expressed in avian brain and the population size effect on the efficacy of selection.
    Mol Biol Evol. 2009 May;26(5):1073-9 PMID: 19188264
  38. Estimation of the neutrality index.
    Mol Biol Evol. 2011 Jan;28(1):63-70 PMID: 20837603
  39. Patterns of selection on synonymous and nonsynonymous variants in Drosophila miranda.
    Genetics. 2005 Mar;169(3):1495-507 PMID: 15545653
  40. Testing a covariotide model of DNA substitution.
    Mol Biol Evol. 2002 May;19(5):698-707 PMID: 11961103
  41. Comparisons of dN/dS are time dependent for closely related bacterial genomes.
    J Theor Biol. 2006 Mar 21;239(2):226-35 PMID: 16239014
  42. The neutral theory in the genomic era.
    Curr Opin Genet Dev. 2001 Dec;11(6):642-6 PMID: 11682307
  43. Adaptive evolution of non-coding DNA in Drosophila.
    Nature. 2005 Oct 20;437(7062):1149-52 PMID: 16237443
  44. Selection on amino acid substitutions in Arabidopsis.
    Mol Biol Evol. 2008 Jul;25(7):1375-83 PMID: 18390851
  45. Genotype to phenotype: a complex problem.
    Science. 2010 Apr 23;328(5977):469 PMID: 20413493
  46. Natural selection on synonymous and nonsynonymous mutations shapes patterns of polymorphism in Populus tremula.
    Mol Biol Evol. 2010 Mar;27(3):650-60 PMID: 19837657
  47. Evidence for pervasive adaptive protein evolution in wild mice.
    PLoS Genet. 2010 Jan 22;6(1):e1000825 PMID: 20107605
  48. Estimating the parameters of selection on nonsynonymous mutations in Drosophila pseudoobscura and D. miranda.
    Genetics. 2010 Aug;185(4):1381-96 PMID: 20516497
  49. Inferring the distribution of mutational effects on fitness in Drosophila.
    Biol Lett. 2006 Sep 22;2(3):426-30 PMID: 17148422
  50. Similar rates of protein adaptation in Drosophila miranda and D. melanogaster, two species with different current effective population sizes.
    BMC Evol Biol. 2008 Dec 18;8:334 PMID: 19091130
  51. Selection, recombination and demographic history in Drosophila miranda.
    Genetics. 2006 Dec;174(4):2045-59 PMID: 17028331
  52. Quantitative prediction of molecular clock and ka/ks at short timescales.
    Mol Biol Evol. 2009 Nov;26(11):2595-603 PMID: 19661199
  53. Population genomics of domestic and wild yeasts.
    Nature. 2009 Mar 19;458(7236):337-41 PMID: 19212322
  54. Genomewide spatial correspondence between nonsynonymous divergence and neutral polymorphism reveals extensive adaptation in Drosophila.
    Genetics. 2007 Dec;177(4):2083-99 PMID: 18073425
  55. Adaptive protein evolution in Drosophila.
    Nature. 2002 Feb 28;415(6875):1022-4 PMID: 11875568
  56. Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome.
    Genome Res. 2007 Dec;17(12):1755-62 PMID: 17989248
  57. Adaptive genic evolution in the Drosophila genomes.
    Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2271-6 PMID: 17284599
  58. Testing the neutral theory of molecular evolution with genomic data from Drosophila.
    Nature. 2002 Feb 28;415(6875):1024-6 PMID: 11875569
  59. From fitness landscapes to seascapes: non-equilibrium dynamics of selection and adaptation.
    Trends Genet. 2009 Mar;25(3):111-9 PMID: 19232770
  60. Changes in selective effects over time facilitate turnover of enhancer sequences.
    Genetics. 2011 Feb;187(2):567-82 PMID: 21098721
  61. Molecular evolution of sex-biased genes in the Drosophila ananassae subgroup.
    BMC Evol Biol. 2009 Dec 16;9:291 PMID: 20015359
  62. A catalog of neutral and deleterious polymorphism in yeast.
    PLoS Genet. 2008 Aug 29;4(8):e1000183 PMID: 18769710
  63. Variable epistatic effects between mutations at host recognition sites in phiX174 bacteriophage.
    Evolution. 2007 Jul;61(7):1710-24 PMID: 17598750
  64. Statistical models of the overdispersed molecular clock.
    Theor Popul Biol. 1991 Jun;39(3):329-44 PMID: 1896948
  65. The population genomics of plant adaptation.
    New Phytol. 2010 Oct;188(2):313-32 PMID: 20696011
  66. Limits of adaptation: the evolution of selective neutrality.
    Genetics. 1985 Nov;111(3):655-74 PMID: 3932127
  67. Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural woodland site in North America and display different levels of reproductive isolation from European conspecifics.
    FEMS Yeast Res. 2002 Jan;1(4):299-306 PMID: 12702333
  68. Sequence divergence, functional constraint, and selection in protein evolution.
    Annu Rev Genomics Hum Genet. 2003;4:213-35 PMID: 14527302
  69. The origins of genome complexity.
    Science. 2003 Nov 21;302(5649):1401-4 PMID: 14631042
  70. Population genetics of polymorphism and divergence under fluctuating selection.
    Genetics. 2008 Jan;178(1):325-37 PMID: 17947441
  71. A selection model of molecular evolution incorporating the effective population size.
    Evolution. 2009 Feb;63(2):301-5 PMID: 19215289
  72. Correlated evolution of nearby residues in Drosophilid proteins.
    PLoS Genet. 2011 Feb;7(2):e1001315 PMID: 21383965
  73. The other side of the nearly neutral theory, evidence of slightly advantageous back-mutations.
    Proc Natl Acad Sci U S A. 2007 Oct 23;104(43):16992-7 PMID: 17940029
  74. Pervasive natural selection in the Drosophila genome?
    PLoS Genet. 2009 Jun;5(6):e1000495 PMID: 19503600
  75. Pervasive cryptic epistasis in molecular evolution.
    PLoS Genet. 2010 Oct 21;6(10):e1001162 PMID: 20975933
  76. Recombination and hitchhiking of deleterious alleles.
    Evolution. 2011 Sep;65(9):2421-34 PMID: 21884046
  77. Shifts in the intensity of purifying selection: an analysis of genome-wide polymorphism data from two closely related yeast species.
    Genome Res. 2010 Nov;20(11):1558-73 PMID: 20817943
Article Info
Journal
Trends in genetics : TIG
Abbr.
Trends Genet
ISSN
0168-9525
DOI
10.1016/j.tig.2011.06.003
Email
[email protected]
Published
2011-09-00
Epub
2011-00-19
Pages
343-9
Language
English
Region
England
NLM ID
8507085
PMCID
PMC3185218
Subset
IM
Grants
NIGMS NIH HHS · GM080669 · United States
NIGMS NIH HHS · R01 GM080669 · United States
NIGMS NIH HHS · R01 GM080669-04 · United States
NIGMS NIH HHS · GM086412 · United States
NIGMS NIH HHS · R01 GM086412 · United States
NIGMS NIH HHS · R01 GM080669-05 · United States
NIGMS NIH HHS · R21 GM098896 · United States
External Links
PubMed source DOI: 10.1016/j.tig.2011.06.003 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2