Home LiteratureArticle Details
PMID: 17449636 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

More genes underwent positive selection in chimpanzee evolution than in human evolution.

Bakewell MA, Shi P, Zhang J

Abstract

Observations of numerous dramatic and presumably adaptive phenotypic modifications during human evolution prompt the common belief that more genes have undergone positive Darwinian selection in the human lineage than in the chimpanzee lineage since their evolutionary divergence 6-7 million years ago. Here, we test this hypothesis by analyzing nearly 14,000 genes of humans and chimps. To ensure an accurate and unbiased comparison, we select a proper outgroup, avoid sequencing errors, and verify statistical methods. Our results show that the number of positively selected genes is substantially smaller in humans than in chimps, despite a generally higher nonsynonymous substitution rate in humans. These observations are explainable by the reduced efficacy of natural selection in humans because of their smaller long-term effective population size but refute the anthropocentric view that a grand enhancement in Darwinian selection underlies human origins. Although human and chimp positively selected genes have different molecular functions and participate in different biological processes, the differences do not ostensibly correspond to the widely assumed adaptations of these species, suggesting how little is currently known about which traits have been under positive selection. Our analysis of the identified positively selected genes lends support to the association between human Mendelian diseases and past adaptations but provides no evidence for either the chromosomal speciation hypothesis or the widespread brain-gene acceleration hypothesis of human origins.

MeSH Terms
Animals Disease Evolution, Molecular Gene Expression Regulation Humans Pan troglodytes/genetics Selection, Genetic
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bakewell Margaret A
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA.
Shi Peng
Zhang Jianzhi
References (68)
68 references, click to expand
  1. Large-scale recombination rate patterns are conserved among human populations.
    Genome Res. 2005 Nov;15(11):1547-52 PMID: 16251464
  2. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level.
    Mol Biol Evol. 2005 Dec;22(12):2472-9 PMID: 16107592
  3. Molecular signatures of natural selection.
    Annu Rev Genet. 2005;39:197-218 PMID: 16285858
  4. Comparing the human and chimpanzee genomes: searching for needles in a haystack.
    Genome Res. 2005 Dec;15(12):1746-58 PMID: 16339373
  5. High genomic deleterious mutation rates in hominids.
    Nature. 1999 Jan 28;397(6717):344-7 PMID: 9950425
  6. Diabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"?
    Am J Hum Genet. 1962 Dec;14:353-62 PMID: 13937884
  7. The PANTHER database of protein families, subfamilies, functions and pathways.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D284-8 PMID: 15608197
  8. Accelerated evolution of nervous system genes in the origin of Homo sapiens.
    Cell. 2004 Dec 29;119(7):1027-40 PMID: 15620360
  9. Extensive nuclear DNA sequence diversity among chimpanzees.
    Science. 1999 Nov 5;286(5442):1159-62 PMID: 10550054
  10. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees.
    Am J Hum Genet. 2001 Feb;68(2):444-56 PMID: 11170892
  11. Great ape DNA sequences reveal a reduced diversity and an expansion in humans.
    Nat Genet. 2001 Feb;27(2):155-6 PMID: 11175781
  12. High levels of Y-chromosome nucleotide diversity in the genus Pan.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):43-8 PMID: 11756656
  13. Genomewide comparison of DNA sequences between humans and chimpanzees.
    Am J Hum Genet. 2002 Jun;70(6):1490-7 PMID: 11992255
  14. Molecular evolution of FOXP2, a gene involved in speech and language.
    Nature. 2002 Aug 22;418(6900):869-72 PMID: 12192408
  15. Divergence between samples of chimpanzee and human DNA sequences is 5%, counting indels.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13633-5 PMID: 12368483
  16. The origin and evolution of model organisms.
    Nat Rev Genet. 2002 Nov;3(11):838-49 PMID: 12415314
  17. Sequencing the chimpanzee genome: insights into human evolution and disease.
    Nat Rev Genet. 2003 Jan;4(1):20-8 PMID: 12509750
  18. Accelerated protein evolution and origins of human-specific features: Foxp2 as an example.
    Genetics. 2002 Dec;162(4):1825-35 PMID: 12524352
  19. Estimating ancestral population sizes and divergence times.
    Genetics. 2003 Jan;163(1):395-404 PMID: 12586724
  20. Estimation of divergence times for major lineages of primate species.
    Mol Biol Evol. 2003 Mar;20(3):424-34 PMID: 12644563
  21. Chromosomal speciation and molecular divergence--accelerated evolution in rearranged chromosomes.
    Science. 2003 Apr 11;300(5617):321-4 PMID: 12690198
  22. Patterns of transitional mutation biases within and among mammalian genomes.
    Mol Biol Evol. 2003 Jun;20(6):988-93 PMID: 12716982
  23. Implications of natural selection in shaping 99.4% nonsynonymous DNA identity between humans and chimpanzees: enlarging genus Homo.
    Proc Natl Acad Sci U S A. 2003 Jun 10;100(12):7181-8 PMID: 12766228
  24. Statistical significance for genomewide studies.
    Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9440-5 PMID: 12883005
  25. Comment on "Chromosomal speciation and molecular divergence-accelerated evolution in rearranged chromosomes".
    Science. 2003 Nov 7;302(5647):988; author reply 988 PMID: 14605352
  26. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios.
    Science. 2003 Dec 12;302(5652):1960-3 PMID: 14671302
  27. Evolution of the human ASPM gene, a major determinant of brain size.
    Genetics. 2003 Dec;165(4):2063-70 PMID: 14704186
  28. Elevated rates of protein secretion, evolution, and disease among tissue-specific genes.
    Genome Res. 2004 Jan;14(1):54-61 PMID: 14707169
  29. Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans.
    Hum Mol Genet. 2004 Mar 1;13(5):489-94 PMID: 14722158
  30. Evidence for a complex demographic history of chimpanzees.
    Mol Biol Evol. 2004 May;21(5):799-808 PMID: 14963091
  31. A gene atlas of the mouse and human protein-encoding transcriptomes.
    Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):6062-7 PMID: 15075390
  32. Testing the chromosomal speciation hypothesis for humans and chimpanzees.
    Genome Res. 2004 May;14(5):845-51 PMID: 15123584
  33. DNA sequence and comparative analysis of chimpanzee chromosome 22.
    Nature. 2004 May 27;429(6990):382-8 PMID: 15164055
  34. Frequent false detection of positive selection by the likelihood method with branch-site models.
    Mol Biol Evol. 2004 Jul;21(7):1332-9 PMID: 15014150
  35. Positive selection on the human genome.
    Hum Mol Genet. 2004 Oct 1;13 Spec No 2:R245-54 PMID: 15358731
  36. Ancient and recent positive selection transformed opioid cis-regulation in humans.
    PLoS Biol. 2005 Dec;3(12):e387 PMID: 16274263
  37. Differential susceptibility to hypertension is due to selection during the out-of-Africa expansion.
    PLoS Genet. 2005 Dec;1(6):e82 PMID: 16429165
  38. Variable molecular clocks in hominoids.
    Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1370-5 PMID: 16432233
  39. Should the draft chimpanzee sequence be finished?
    Trends Genet. 2006 Mar;22(3):122-5 PMID: 16406850
  40. Gene losses during human origins.
    PLoS Biol. 2006 Mar;4(3):e52 PMID: 16464126
  41. The effect of gene flow on the coalescent time in the human-chimpanzee ancestral population.
    Mol Biol Evol. 2006 May;23(5):1040-7 PMID: 16495349
  42. Positive selection, relaxation, and acceleration in the evolution of the human and chimp genome.
    PLoS Comput Biol. 2006 Apr;2(4):e38 PMID: 16683019
  43. Positive selection on gene expression in the human brain.
    Curr Biol. 2006 May 23;16(10):R356-8 PMID: 16618540
  44. Positive natural selection in the human lineage.
    Science. 2006 Jun 16;312(5780):1614-20 PMID: 16778047
  45. Genetic evidence for complex speciation of humans and chimpanzees.
    Nature. 2006 Jun 29;441(7097):1103-8 PMID: 16710306
  46. Did brain-specific genes evolve faster in humans than in chimpanzees?
    Trends Genet. 2006 Nov;22(11):608-13 PMID: 16978728
  47. Accelerated evolution of conserved noncoding sequences in humans.
    Science. 2006 Nov 3;314(5800):786 PMID: 17082449
  48. Analysis of one million base pairs of Neanderthal DNA.
    Nature. 2006 Nov 16;444(7117):330-6 PMID: 17108958
  49. Rate of evolution in brain-expressed genes in humans and other primates.
    PLoS Biol. 2007 Feb;5(2):e13 PMID: 17194215
  50. Chromosomal rearrangements and the genomic distribution of gene-expression divergence in humans and chimpanzees.
    Trends Genet. 2004 Nov;20(11):524-9 PMID: 15475109
  51. The effect of linkage on limits to artificial selection.
    Genet Res. 1966 Dec;8(3):269-94 PMID: 5980116
  52. Evolution at two levels in humans and chimpanzees.
    Science. 1975 Apr 11;188(4184):107-16 PMID: 1090005
  53. Extensive polymorphism in the mitochondrial DNA of apes.
    Proc Natl Acad Sci U S A. 1981 Oct;78(10):6319-23 PMID: 6273863
  54. The origin of man: a chromosomal pictorial legacy.
    Science. 1982 Mar 19;215(4539):1525-30 PMID: 7063861
  55. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  56. 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
  57. Synonymous and nonsynonymous substitutions in mammalian genes and the nearly neutral theory.
    J Mol Evol. 1995 Jan;40(1):56-63 PMID: 7714912
  58. Divergence time and population size in the lineage leading to modern humans.
    Theor Popul Biol. 1995 Oct;48(2):198-221 PMID: 7482371
  59. Genetic and morphological records of the Hominoidea and hominid origins: a synthesis.
    Mol Phylogenet Evol. 1996 Feb;5(1):155-68 PMID: 8673283
  60. Molecular phylogeny of the hominoids: inferences from multiple independent DNA sequence data sets.
    Mol Biol Evol. 1997 Mar;14(3):248-65 PMID: 9066793
  61. PAML: a program package for phylogenetic analysis by maximum likelihood.
    Comput Appl Biosci. 1997 Oct;13(5):555-6 PMID: 9367129
  62. Positive Darwinian selection after gene duplication in primate ribonuclease genes.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3708-13 PMID: 9520431
  63. Base-calling of automated sequencer traces using phred. I. Accuracy assessment.
    Genome Res. 1998 Mar;8(3):175-85 PMID: 9521921
  64. Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence.
    Mol Phylogenet Evol. 1998 Jun;9(3):585-98 PMID: 9668008
  65. Inferring the mode of speciation from genomic data: a study of the great apes.
    Genetics. 2005 Jan;169(1):259-64 PMID: 15677748
  66. Evidence for widespread degradation of gene control regions in hominid genomes.
    PLoS Biol. 2005 Feb;3(2):e42 PMID: 15678168
  67. Initial sequence of the chimpanzee genome and comparison with the human genome.
    Nature. 2005 Sep 1;437(7055):69-87 PMID: 16136131
  68. Natural selection on protein-coding genes in the human genome.
    Nature. 2005 Oct 20;437(7062):1153-7 PMID: 16237444
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2007-05-01
Epub
2007-00-20
Pages
7489-94
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1863478
Subset
IM
Grants
NIGMS NIH HHS · R01 GM067030 · United States
NHGRI NIH HHS · T32 HG000040 · United States
NIGMS NIH HHS · GM67030 · United States
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]