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Positive Darwinian selection in human population: A review

  • Review
  • Genetics
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Chinese Science Bulletin

Abstract

This paper reviews a large number of genes under positive Darwinian selection in modern human populations, such as brain development genes, immunity genes, reproductive related genes, perception receptors. The research on the evolutionary property of these genes will provide important insight into human evolution and disease mechanisms. With the increase of population genetics and comparative genomics data, more and more evidences indicate that positive Darwinian selection plays an indispensable role in the origin and evolution of human beings. This paper will also summarize the methods to detect positive selection, analyze the interference factors faced and make suggestions for further research on positive selection.

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References

  1. Darwin C, Wallace A R. On the tendency of the species to form varieties and on the perpetuation of the species by natural means of selection. J Proc Linnaean Soc London (Zoology), 1858, 3: 45–62

    Google Scholar 

  2. Nei M. Selectionism and neutralism in molecular evolution. Mol Biol Evol, 2005, 22: 2318–2342

    Article  PubMed  CAS  Google Scholar 

  3. Nei M, Kumar S. Molecular Evolution and Phlogenetics. New York: Oxiford University, 2000

    Google Scholar 

  4. Kimura M. Evolutionary rate at the molecular level. Nature, 1968, 217: 624–626

    Article  PubMed  CAS  Google Scholar 

  5. King J L, Jukes T H. Non-Darwinian evolution. Science, 1969, 164: 788–798

    Article  PubMed  CAS  Google Scholar 

  6. Eyre-Walker A. The genomic rate of adaptive evolution. Trends Ecol Evol, 2006, 21(10): 569–575

    Article  PubMed  Google Scholar 

  7. Smith N G, Eyre-Walker A. Adaptive protein evolution in Drosophila. Nature, 2002, 415: 1022–1024

    Article  PubMed  CAS  Google Scholar 

  8. Fay J C, Wyckoff G J, Wu C I. Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature, 2002, 415: 1024–1026

    Article  PubMed  CAS  Google Scholar 

  9. Ohta T. Near-neutrality in evolution of genes and gene regulation. Proc Natl Acad Sci USA, 2002, 99: 16134–16137

    Article  PubMed  CAS  Google Scholar 

  10. Ohta T. The nearly neutral theory of molecular evolution. Annu Rev Ecol Syst, 1992, 23: 263–286

    Article  Google Scholar 

  11. Ohta T. Population size and rate of evolution. J Mol Evol, 1972, 1: 305–314

    Article  Google Scholar 

  12. Wang E T, Kodama G, Baldi, P, et al. Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc Natl Acad Sci USA, 2006, 103: 135–140

    Article  PubMed  CAS  Google Scholar 

  13. Voight B F, Kudaravalli S, Wen X, et al. A map of recent positive selection in the human genome. PLoS Biol, 2006, 4(3): e72

    Article  PubMed  Google Scholar 

  14. Sabeti P C, Schaffner S F, Fry B, et al. Positive natural selection in the human lineage. Science, 2006, 312: 1614–1620

    Article  PubMed  CAS  Google Scholar 

  15. Nielsen R, Bustamante C, Clark A G, et al. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol, 2005, 3: e170

    Article  PubMed  Google Scholar 

  16. Nielsen R. Molecular signatures of natural selection. Annu Rev Genet, 2005, 39: 197–218

    Article  PubMed  CAS  Google Scholar 

  17. Bustamante C D, Fledel-Alon A, Williamson S, et al. Natural selection on protein-coding genes in the human genome. Nature, 2005, 437: 1153–1157

    Article  PubMed  CAS  Google Scholar 

  18. Mekel-Bobrov N, Gilbert S L, Evans P D, et al. Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens. Science, 2005, 309: 1720–1722

    Article  PubMed  CAS  Google Scholar 

  19. Evans P D, Anderson J R, Vallender E J, et al. Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans. Hum Mol Genet, 2004, 13: 489–494

    Article  PubMed  CAS  Google Scholar 

  20. Zhang J. Evolution of the human ASPM gene, a major determinant of brain size. Genetics, 2003, 165: 2063–2070

    PubMed  CAS  Google Scholar 

  21. Kouprina N, Pavlicek A, Mochida G H, et al. Accelerated evolution of the ASPM gene controlling brain size begins prior to human brain expansion. PLoS Biol, 2004, 2: e126

    Article  PubMed  Google Scholar 

  22. Wang Y, Su B. Molecular evolution of microcephalin, a gene determining human brain size. Hum Mol Genet, 2004, 13: 1131–1137

    Article  PubMed  CAS  Google Scholar 

  23. Evans P D, Anderson J R, Vallender E J, et al. Reconstructing the evolutionary history of microcephalin, a gene controlling human brain size. Hum Mol Genet, 2004, 13: 1139–1145

    Article  PubMed  CAS  Google Scholar 

  24. Evans P D, Gilbert S L, Mekel-Bobrov N, et al. Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science, 2005, 309: 1717–1720

    Article  PubMed  CAS  Google Scholar 

  25. Zhang J, Webb D M, Podlaha O. Accelerated protein evolution and origins of human-specific features FOXP2 as an example. Genetics, 2002, 162: 1825–18352

    PubMed  CAS  Google Scholar 

  26. Enard W, Przeworski M, Fisher SE, et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature, 2002, 418: 869–872

    Article  PubMed  CAS  Google Scholar 

  27. Clark A G, Glanowski S, Nielsen R, et al. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science, 2003, 302: 1960–1963

    Article  PubMed  CAS  Google Scholar 

  28. Wang Y Q, Qian Y P, Yang S, et al. Accelerated evolution of the pituitary adenylate cyclase-activating polypeptide precursor gene during human origin. Genetics, 2005, 170: 801–806

    Article  PubMed  CAS  Google Scholar 

  29. Hughes A L, Nei M, Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature, 1988, 335: 167–170

    Article  PubMed  CAS  Google Scholar 

  30. van Valen L. A new evolutionary law. Evol Theory, 1973, 1: 1–30

    Google Scholar 

  31. Zhang J, Webb D M. Rapid evolution of primate antiviral enzyme APOBEC3G. Hum Mol Genet, 2004, 13: 1785–1791

    Article  PubMed  CAS  Google Scholar 

  32. Sawyer S L, Emerman M, Malik H S. Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol, 2004, 2: e275

    Article  PubMed  Google Scholar 

  33. Sabeti P C, Walsh E, Schaffner S F, et al. The case for selection at CCR5-Δ32. PLoS Biol, 2005, 3: e378

    Article  PubMed  Google Scholar 

  34. Bamshad M J, Mummidi S, Gonzalez E, et al. A strong signature of balancing selection in the 5′ cis-regulatory region of CCR5. Proc Natl Acad Sci USA, 2002, 99: 10539–10544

    Article  PubMed  CAS  Google Scholar 

  35. Maayan S, Zhang L, Shinar E, et al. Evidence for recent selection of the CCR5-Δ32 deletion from differences in its frequency between Ashkenazi and Sephardi Jews. Genes Immun, 2000, 1: 358–361

    Article  PubMed  CAS  Google Scholar 

  36. Wooding S, Stone A C, Dunn D M, et al. Contrasting effects of natural selection on human and chimpanzee CC chemokine receptor 5. Am J Hum Genet, 2005, 76: 291–301

    Article  PubMed  CAS  Google Scholar 

  37. Zhang Y W, Oliver A, Ryder, et al. Intra-and interspecific variation of the CCR5 gene in higher primates. Mol Biol Evol, 2003, 20(10): 1722–1729

    Article  PubMed  CAS  Google Scholar 

  38. Li H P, Zhang Y W, Zhang Y P, et al. Neutrality tests using DNA polymorphism from multiple samples. Genetics, 2003, 163: 1147–1151

    PubMed  Google Scholar 

  39. Swanson W J, Yang Z, Wolfner M F, et al. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc Natl Acad Sci USA, 2001, 98: 2509–2514

    Article  PubMed  CAS  Google Scholar 

  40. Swanson W J, Vacquier V D. The rapid evolution of reproductive proteins. Nat Rev Genet, 2002, 3: 137–144

    Article  PubMed  CAS  Google Scholar 

  41. Wyckoff G J, Wang W, Wu C I. Rapid evolution of male reproductive genes in the descent of man. Nature, 2000, 403: 261–263

    Article  Google Scholar 

  42. Shi P, Zhang J, Yang H, et al. Adaptive diversification of bitter taste receptor genes in mammalian evolution. Mol Biol Evol, 2003, 20: 805–814

    Article  PubMed  CAS  Google Scholar 

  43. Soranzo N, Bufe B, Sabeti P C, et al. Positive selection on a high-sensitivity allele of the human bitter-taste receptor TAS2R16. Curr Biol, 2005, 15: 1257–1265

    Article  PubMed  CAS  Google Scholar 

  44. Wooding S, Kim U K, Bamshad M J, et al. Natural selection and molecular evolution in PTC, a bitter-taste receptor gene. Am J Hum Genet, 2004, 74: 637–646

    Article  PubMed  CAS  Google Scholar 

  45. Gilad Y, Bustamante C D, Lancet D, et al. Natural selection on the olfactory receptor gene family in humans and chimpanzees. Am J Hum Genet, 2003, 73: 489–501

    Article  PubMed  CAS  Google Scholar 

  46. Yu F, Sabeti PC, Hardenbol P, et al. Positive selection of a pre-expansion CAG repeat of the human SCA2 gene. PLoS Genet, 2005, 1(3): e41

    Article  PubMed  Google Scholar 

  47. Nachman M W, Crowell S L. Contrasting evolutionary histories of two introns of the duchenne muscular dystrophy gene, Dmd, in Humans. Genetics, 2000, 155: 1855–1864

    PubMed  CAS  Google Scholar 

  48. Huttley G A, Easteal S, Southey M C, et al. Adaptive evolution of the tumour suppressor BRCA1 in humans and chimpanzees. Nat Genet, 2000, 25: 410–413

    Article  PubMed  CAS  Google Scholar 

  49. Fleming M A, Potter J D, Ramirez C J, et al. Understanding missense mutations in the BRCA1 gene: An evolutionary approach. Proc Natl Acad Sci USA, 2003, 100: 1151–1156

    Article  PubMed  CAS  Google Scholar 

  50. Wang X, Zhang J, Zhang Y P. Erratic evolution of SRY in higher primates. Mol Biol Evol, 2002, 19: 582–584

    PubMed  CAS  Google Scholar 

  51. Kwiatkowski D P. How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet, 2005, 77: 171–192

    Article  PubMed  CAS  Google Scholar 

  52. Ruwende C, Hill A. Glucose-6-phosphate dehydrogenase deficiency and malaria. J Mol Med, 1998, 76: 581–588

    Article  PubMed  CAS  Google Scholar 

  53. Sabeti P C, Usen S, Farhadian S, et al. CD40L association with protection from severe malaria. Genes Immun, 2002, 3: 286–291

    Article  PubMed  CAS  Google Scholar 

  54. Baum J, Ward R H, Conway D J. Natural selection on the erythrocyte surface. Mol Biol Evol, 2002, 19: 223–229

    PubMed  CAS  Google Scholar 

  55. Zimmerman P A, Woolley I, Masinde G L, et al. Emergence of FY*A null in a plasmodium vivax-endemic region of Papua New Guinea. Proc Natl Acad Sci USA, 1999, 96: 13973–13977

    Article  PubMed  CAS  Google Scholar 

  56. Hamblin M T, Thompson E E, Rienzo A D. Complex signatures of natural selection at the duffy blood group locus. Am J Hum Genet, 2002, 70: 369–383

    Article  PubMed  Google Scholar 

  57. Hamblin M T, Rienzo A D. Detection of the signature of natural selection in humans: Evidence from the Duffy blood group Locus. Am J Hum Genet, 2000, 66: 1669–1679

    Article  PubMed  CAS  Google Scholar 

  58. Clark N L, Swanson W J. Pervasive adaptive evolution in primate seminal proteins. PLoS Genet, 2005 1(3): e35

    Article  PubMed  Google Scholar 

  59. Ding Y C, Chi H C, Grady D L, et al. Evidence of positive selection acting at the human dopamine receptor D4 gene locus. Proc Natl Acad Sci USA, 2002, 99(1): 309–314

    Article  PubMed  CAS  Google Scholar 

  60. Harpending H, Gregory C. In our genes. Proc Natl Acad Sci USA, 2002, 99(1): 10–12

    Article  PubMed  CAS  Google Scholar 

  61. Hughes A L. Strength in numbers. Nature, 2002, 417: 795

    Article  PubMed  CAS  Google Scholar 

  62. Bamshad M, Wooding S. Signature of natural selection in the human genome. Nat Rev Genet, 2003, 4: 99–111

    Article  PubMed  CAS  Google Scholar 

  63. Ewens W J. The sampling theory of selectively neutral alleles. Theor Popul Biol, 1972, 3: 87–112

    Article  PubMed  CAS  Google Scholar 

  64. Watterson G A. Heterosis or neutrality? Genetics, 1977, 85: 789–814

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  66. Nielsen R, Williamson S, Kim Y, et al. Genomic scans for selective sweeps using SNP data. Genome Res, 2005, 15: 1566–1575

    Article  PubMed  CAS  Google Scholar 

  67. Fu Y X, Li W H. Statistical tests of neutrality of mutations. Genetics, 1993, 133: 693–709

    PubMed  CAS  Google Scholar 

  68. Fu Y X. New statistical tests of neutrality for DNA samples from a population. Genetics, 1996, 143: 557–570

    PubMed  CAS  Google Scholar 

  69. Fu Y X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 1997, 147: 915–925

    PubMed  CAS  Google Scholar 

  70. Fay J C, Wu C I. Hitchhiking under positive darwinian selection. Genetics, 2000, 155: 1405–1413

    PubMed  CAS  Google Scholar 

  71. Lewontin R C, Krakauer J. Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphism. Genetics, 1973, 74: 175–195

    PubMed  CAS  Google Scholar 

  72. Akey J M, Zhang G, Zhang K, et al. Interrogating a high-density SNP Map for signatures of natural selection. Genome Res, 2002, 12: 1805–1814

    Article  PubMed  CAS  Google Scholar 

  73. Rockman M V, Hahn M W, Soranzo N, et al. Positive selection on a human-specific transcription factor binding site regulating IL4 expression. Curr Biol, 2003, 13: 2118–2123

    Article  PubMed  CAS  Google Scholar 

  74. Sabeti P C, Reich D E, Higgins J M, et al. Detecting recent positive selection in the human genome from haplotype structure. Nature, 2002, 419: 832–837

    Article  PubMed  CAS  Google Scholar 

  75. Hanchard N A, Rockett K A, Spencer C, et al. Screening for recently selected alleles by analysis of human haplotype similarity. Am J Hum Genet, 2006, 78: 153–159

    Article  PubMed  CAS  Google Scholar 

  76. Nielsen R, Yang Z. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics, 1998, 148: 929–936

    PubMed  CAS  Google Scholar 

  77. Yang Z. Maximum likelihood estimation on large phylogenies and analysis of adaptive evolution in human influenza virus A. J Mol Evol, 2000, 51: 423–432

    PubMed  CAS  Google Scholar 

  78. Yang Z. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol, 1998, 15: 568–573

    PubMed  CAS  Google Scholar 

  79. Yang Z. Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol, 1998, 46: 409–418

    Article  PubMed  CAS  Google Scholar 

  80. Yang Z, Nielsen R. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol, 2002, 19: 908–917

    PubMed  CAS  Google Scholar 

  81. Yang Z, Nielsen R, Goldman N, et al. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics, 2000, 155: 431–449

    PubMed  CAS  Google Scholar 

  82. Yang Z, Wong W, Nielsen R. Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol, 2005, 22: 1107–1118

    Article  PubMed  CAS  Google Scholar 

  83. Zhang J, Nielsen R, Yang Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol, 2005, 22: 2472–2479

    Article  PubMed  CAS  Google Scholar 

  84. Anisimova M, Bielawski J P, Yang Z. Accuracy and power of bayes prediction of amino acid sites under positive selection. Mol Biol Evol, 2002, 19: 950–958

    PubMed  CAS  Google Scholar 

  85. Anisimova M, Bielawski J P, Yang Z. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol, 2001, 18: 1585–1592

    PubMed  CAS  Google Scholar 

  86. Wang H Y, Chien H C, Osada N, et al. Rate of evolution in brain-expressed genes in humans and other primates. PLoS Biol, 2007, 5(2): e13

    Article  PubMed  Google Scholar 

  87. Xia X. What amino acid properties affect protein evolution? J Mol Evol, 1998, 47: 557–564

    Article  PubMed  CAS  Google Scholar 

  88. McClellan D A, McCracken K G. Estimating the influence of selection on the variable amino acid sites of the cytochrome b protein functional domains. Mol Biol Evol, 2001, 18: 917–925

    PubMed  CAS  Google Scholar 

  89. Woolley S, Johnson J, Smith M J, et al. TreeSAAP: Selection on amino acid properties using phylogenetic trees. Bioinformatics, 2003, 19: 671–672

    Article  PubMed  CAS  Google Scholar 

  90. McDonald J, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature, 1991, 351: 652–654

    Article  PubMed  CAS  Google Scholar 

  91. Hudson R, Kreitman M, Aguade M. A Test of neutral molecular evolution based on nucleotide data. Genetics, 1987, 116: 153–159

    PubMed  CAS  Google Scholar 

  92. Currat M, Excoffier L, Maddison W, et al. Comment on “ongoing adaptive evolution of ASPM, a brain size determinant in homo sapiens” and “Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans”. Science, 2006, 313: 172a

    Article  Google Scholar 

  93. Mekel-Bobrov N, Posthuma D, Gilbert S L, et al. Response to comment on “Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens” and “Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans”. Science, 2006, 313: 172b

    Article  Google Scholar 

  94. McVean G A, Myers S R, Hunt S, et al. The fine-scale structure of recombination rate variation in the human genome. Science, 2004, 304: 581–584

    Article  PubMed  CAS  Google Scholar 

  95. Crawford D C, Bhangale T, Li N, et al. Evidence for substantial fine-scale variation in recombination rates across the human genome. Nat Genet, 2004, 36: 700–706

    Article  PubMed  CAS  Google Scholar 

  96. Reed F A, Tishkoff S A. Positive selection can create false hotspots of recombination. Genetics, 2006, 172: 2011–2014

    Article  PubMed  CAS  Google Scholar 

  97. Nielsen R. Population genetic analysis of ascertained SNP data. Hum Genomics, 2004, 1: 218–224

    PubMed  CAS  Google Scholar 

  98. Haygood R, Fedrigo O, Hanson B, et al. Promoter regions of many neural-and nutrition-related genes have experienced positive selection during human evolution. Nat Genet, 2007, 39(9): 1140–1144

    Article  PubMed  CAS  Google Scholar 

  99. Chen K, Rajewsky N. Natural selection on human microRNA binding sites inferred from SNP data. Nat Genet, 2006, 38: 1452–1456

    Article  PubMed  CAS  Google Scholar 

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Correspondence to YaPing Zhang.

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Supported by the National Natural Science Foundation of China (Grant Nos. 30621092 and 30430110), and Bureau of Science and Technology of Yunnan Province

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Wu, D., Zhang, Y. Positive Darwinian selection in human population: A review. Chin. Sci. Bull. 53, 1457–1467 (2008). https://doi.org/10.1007/s11434-008-0202-z

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