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PMID: 20299543 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Genome wide analyses reveal little evidence for adaptive evolution in many plant species.

Molecular biology and evolution ·Vol. 27 ·No. 8 ·2010-08-00 ·Pages 1822-32

Gossmann TI, Song BH, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A

Abstract

The relative contribution of advantageous and neutral mutations to the evolutionary process is a central problem in evolutionary biology. Current estimates suggest that whereas Drosophila, mice, and bacteria have undergone extensive adaptive evolution, hominids show little or no evidence of adaptive evolution in protein-coding sequences. This may be a consequence of differences in effective population size. To study the matter further, we have investigated whether plants show evidence of adaptive evolution using an extension of the McDonald-Kreitman test that explicitly models slightly deleterious mutations by estimating the distribution of fitness effects of new mutations. We apply this method to data from nine pairs of species. Altogether more than 2,400 loci with an average length of approximately 280 nucleotides were analyzed. We observe very similar results in all species; we find little evidence of adaptive amino acid substitution in any comparison except sunflowers. This may be because many plant species have modest effective population sizes.

MeSH Terms
Amino Acid Substitution Animals Base Sequence Biological Evolution Genetic Fitness Genome, Plant Mice Molecular Sequence Data Mutation Plants/genetics Population Density Sequence Analysis, DNA
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Gossmann Toni I
Centre for the Study of Evolution, School of Life Sciences, University of Sussex, Brighton, United Kingdom.
Song Bao-Hua
Windsor Aaron J
Mitchell-Olds Thomas
Dixon Christopher J
Kapralov Maxim V
Filatov Dmitry A
Eyre-Walker Adam
References (74)
74 references, click to expand
  1. On the number of segregating sites in genetical models without recombination.
    Theor Popul Biol. 1975 Apr;7(2):256-76 PMID: 1145509
  2. Evidence for variation in the effective population size of animal mitochondrial DNA.
    PLoS One. 2009;4(2):e4396 PMID: 19198657
  3. Adaptive evolution of young gene duplicates in mammals.
    Genome Res. 2009 May;19(5):859-67 PMID: 19411603
  4. Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination.
    Genetics. 1999 Jan;151(1):221-38 PMID: 9872962
  5. The genomic rate of adaptive amino acid substitution in Drosophila.
    Mol Biol Evol. 2004 Jul;21(7):1350-60 PMID: 15044594
  6. Accumulation of slightly deleterious mutations in mitochondrial protein-coding genes of large versus small mammals.
    Proc Natl Acad Sci U S A. 2007 Aug 14;104(33):13390-5 PMID: 17679693
  7. Testing the neutral theory of molecular evolution with genomic data from Drosophila.
    Nature. 2002 Feb 28;415(6875):1024-6 PMID: 11875569
  8. Adaptive protein evolution in Drosophila.
    Nature. 2002 Feb 28;415(6875):1022-4 PMID: 11875568
  9. Population size and molecular evolution on islands.
    Proc Biol Sci. 2005 Nov 7;272(1578):2277-82 PMID: 16191640
  10. Assessing the evolutionary impact of amino acid mutations in the human genome.
    PLoS Genet. 2008 May;4(5):e1000083 PMID: 18516229
  11. Quantifying the slightly deleterious mutation model of molecular evolution.
    Mol Biol Evol. 2002 Dec;19(12):2142-9 PMID: 12446806
  12. The effects of artificial selection on the maize genome.
    Science. 2005 May 27;308(5726):1310-4 PMID: 15919994
  13. Adaptive protein evolution at the Adh locus in Drosophila.
    Nature. 1991 Jun 20;351(6328):652-4 PMID: 1904993
  14. Selection on rapidly evolving proteins in the Arabidopsis genome.
    Genetics. 2003 Feb;163(2):723-33 PMID: 12618409
  15. Nonrandom mating in an open-pollinated maize population.
    Genetics. 1986 Mar;112(3):669-80 PMID: 17246321
  16. High outcrossing rates in fields with mixed sorghum landraces: how are landraces maintained?
    Heredity (Edinb). 2008 Nov;101(5):445-52 PMID: 18685567
  17. The cost of inbreeding in Arabidopsis.
    Nature. 2002 Apr 4;416(6880):531-4 PMID: 11932744
  18. Changing effective population size and the McDonald-Kreitman test.
    Genetics. 2002 Dec;162(4):2017-24 PMID: 12524367
  19. Molecular demographic history of the annual sunflowers Helianthus annuus and H. petiolaris--large effective population sizes and rates of long-term gene flow.
    Evolution. 2008 Aug;62(8):1936-50 PMID: 18462213
  20. Phylogeographic patterns and demographic history of Schiedea globosa (Caryophyllaceae) on the Hawaiian Islands.
    Am J Bot. 2009 May;96(5):958-67 PMID: 21628248
  21. Extensive chloroplast haplotype variation indicates Pleistocene hybridization and radiation of North American Arabis drummondii, A. x divaricarpa, and A. holboellii (Brassicaceae).
    Mol Ecol. 2004 Feb;13(2):349-70 PMID: 14717892
  22. 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
  23. A flexible forward simulator for populations subject to selection and demography.
    Bioinformatics. 2008 Dec 1;24(23):2786-7 PMID: 18842601
  24. DNA diversity in Hawaiian endemic plant Schiedea globosa.
    Heredity (Edinb). 2004 May;92(5):452-8 PMID: 15014424
  25. A multilocus sequence survey in Arabidopsis thaliana reveals a genome-wide departure from a neutral model of DNA sequence polymorphism.
    Genetics. 2005 Mar;169(3):1601-15 PMID: 15654111
  26. Recent speciation associated with the evolution of selfing in Capsella.
    Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5241-5 PMID: 19228944
  27. Evidence for pervasive adaptive protein evolution in wild mice.
    PLoS Genet. 2010 Jan;6(1):e1000825 PMID: 20107605
  28. Genomics and evolution of heritable bacterial symbionts.
    Annu Rev Genet. 2008;42:165-90 PMID: 18983256
  29. Genome-wide patterns of nucleotide polymorphism in domesticated rice.
    PLoS Genet. 2007 Sep;3(9):1745-56 PMID: 17907810
  30. Fixation probability and time in subdivided populations.
    Genetics. 2003 Jun;164(2):767-79 PMID: 12807795
  31. Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula.
    Genetics. 2008 Sep;180(1):329-40 PMID: 18716330
  32. Evolutionary relationship of DNA sequences in finite populations.
    Genetics. 1983 Oct;105(2):437-60 PMID: 6628982
  33. Genomic diversity, population structure, and migration following rapid range expansion in the Balsam poplar, Populus balsamifera.
    Mol Ecol. 2010 Mar;19(6):1212-26 PMID: 20163548
  34. Population genomics of domestic and wild yeasts.
    Nature. 2009 Mar 19;458(7236):337-41 PMID: 19212322
  35. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae).
    Mol Biol Evol. 2000 Oct;17(10):1483-98 PMID: 11018155
  36. The Sorghum bicolor genome and the diversification of grasses.
    Nature. 2009 Jan 29;457(7229):551-6 PMID: 19189423
  37. Selection on amino acid substitutions in Arabidopsis.
    Mol Biol Evol. 2008 Jul;25(7):1375-83 PMID: 18390851
  38. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes.
    Plant Cell. 2004 Jul;16(7):1667-78 PMID: 15208399
  39. Molecular evolution of synonymous codon usage in Populus.
    BMC Evol Biol. 2008;8:307 PMID: 18983655
  40. 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
  41. Evidence for abundant slightly deleterious polymorphisms in bacterial populations.
    Genetics. 2005 Feb;169(2):533-8 PMID: 15545641
  42. Multilocus patterns of nucleotide diversity, population structure and linkage disequilibrium in Boechera stricta, a wild relative of Arabidopsis.
    Genetics. 2009 Mar;181(3):1021-33 PMID: 19104077
  43. Naturally occurring genetic variation in Arabidopsis thaliana.
    Annu Rev Plant Biol. 2004;55:141-72 PMID: 15377217
  44. The map-based sequence of the rice genome.
    Nature. 2005 Aug 11;436(7052):793-800 PMID: 16100779
  45. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans.
    Mol Biol Evol. 2001 Mar;18(3):279-90 PMID: 11230529
  46. Challenges of detecting directional selection after a bottleneck: lessons from Sorghum bicolor.
    Genetics. 2006 Jun;173(2):953-64 PMID: 16547110
  47. Initial sequence of the chimpanzee genome and comparison with the human genome.
    Nature. 2005 Sep 1;437(7055):69-87 PMID: 16136131
  48. Historical divergence and gene flow in the genus Zea.
    Genetics. 2009 Apr;181(4):1399-413 PMID: 19153259
  49. The McDonald-Kreitman test and slightly deleterious mutations.
    Mol Biol Evol. 2008 Jun;25(6):1007-15 PMID: 18195052
  50. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  51. Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes.
    Mol Biol Evol. 2003 Sep;20(9):1545-55 PMID: 12832648
  52. Nucleotide diversity and linkage disequilibrium in balsam poplar (Populus balsamifera).
    New Phytol. 2010 Apr;186(2):526-36 PMID: 20122131
  53. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray).
    Science. 2006 Sep 15;313(5793):1596-604 PMID: 16973872
  54. Estimating the genomewide rate of adaptive protein evolution in Drosophila.
    Genetics. 2006 Jun;173(2):821-37 PMID: 16582427
  55. The role of hybridization in plant speciation.
    Annu Rev Plant Biol. 2009;60:561-88 PMID: 19575590
  56. The pattern of polymorphism in Arabidopsis thaliana.
    PLoS Biol. 2005 Jul;3(7):e196 PMID: 15907155
  57. Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata.
    PLoS One. 2008;3(6):e2411 PMID: 18545707
  58. Close split of sorghum and maize genome progenitors.
    Genome Res. 2004 Oct;14(10A):1916-23 PMID: 15466289
  59. PAML: a program package for phylogenetic analysis by maximum likelihood.
    Comput Appl Biosci. 1997 Oct;13(5):555-6 PMID: 9367129
  60. Characterization of single-nucleotide polymorphisms in coding regions of human genes.
    Nat Genet. 1999 Jul;22(3):231-8 PMID: 10391209
  61. Human SNPs reveal no evidence of frequent positive selection.
    Mol Biol Evol. 2005 Dec;22(12):2504-7 PMID: 16107590
  62. Quantifying adaptive evolution in the Drosophila immune system.
    PLoS Genet. 2009 Oct;5(10):e1000698 PMID: 19851448
  63. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  64. 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
  65. Similar rates of protein adaptation in Drosophila miranda and D. melanogaster, two species with different current effective population sizes.
    BMC Evol Biol. 2008;8:334 PMID: 19091130
  66. Positive and negative selection on the human genome.
    Genetics. 2001 Jul;158(3):1227-34 PMID: 11454770
  67. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  68. Quality assessment of maize assembled genomic islands (MAGIs) and large-scale experimental verification of predicted genes.
    Proc Natl Acad Sci U S A. 2005 Aug 23;102(34):12282-7 PMID: 16103354
  69. Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice.
    PLoS Comput Biol. 2006 Sep 1;2(9):e115 PMID: 16948529
  70. Recombination and the nature of bacterial speciation.
    Science. 2007 Jan 26;315(5811):476-80 PMID: 17255503
  71. The rate of adaptive evolution in enteric bacteria.
    Mol Biol Evol. 2006 Jul;23(7):1348-56 PMID: 16621913
  72. The effect of background selection against deleterious mutations on weakly selected, linked variants.
    Genet Res. 1994 Jun;63(3):213-27 PMID: 8082838
  73. Genomic patterns of adaptive divergence between chromosomally differentiated sunflower species.
    Mol Biol Evol. 2009 Jun;26(6):1341-55 PMID: 19276154
  74. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla.
    Nature. 2007 Sep 27;449(7161):463-7 PMID: 17721507
Article Info
Journal
Molecular biology and evolution
Abbr.
Mol Biol Evol
ISSN
1537-1719
DOI
10.1093/molbev/msq079
Published
2010-08-00
Epub
2010-00-18
Pages
1822-32
Language
English
Region
United States
NLM ID
8501455
PMCID
PMC2915642
Subset
IM
Grants
NIGMS NIH HHS · R01 GM086496-03 · United States
NIGMS NIH HHS · R01 GM086496-02S1 · United States
NIGMS NIH HHS · R01 GM086496 · United States
Biotechnology and Biological Sciences Research Council · BB/C512310/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/C512310/2 · United Kingdom
External Links
PubMed source DOI: 10.1093/molbev/msq079 PMC Full Text View journal details
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