The genomic distribution of intraspecific and interspecific sequence divergence of human segmental duplications relative to human/chimpanzee chromosomal rearrangements

BMC Genomics

Volumn 9, Issue , 2008, Pages

  Marques Bonet, Tomàs ^a,b   Cheng, Ze ^b   She, Xinwei ^b   Eichler, Evan E ^b   Navarro, Arcadi ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ARTICLE; CHIMPANZEE; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DNA SEQUENCE; EVOLUTIONARY RATE; GENE DUPLICATION; HUMAN; HUMAN GENOME; INTERSPECIFIC RELATIONSHIP; INTRASPECIFIC VARIATION; NONHUMAN; PARALOGY; SEQUENCE ANALYSIS; ANIMAL; BIOLOGY; CENTROMERE; COMPARATIVE STUDY; GENE REARRANGEMENT; GENETIC VARIABILITY; GENETICS; GENOME; MOLECULAR EVOLUTION; NUCLEIC ACID DATABASE; PAN TROGLODYTES; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION; TELOMERE;

PAN;

ANIMALS; CENTROMERE; COMPUTATIONAL BIOLOGY; DATABASES, NUCLEIC ACID; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE REARRANGEMENT; GENETIC SPECIATION; GENOME, HUMAN; HUMANS; PAN TROGLODYTES; SPECIES SPECIFICITY; TELOMERE; VARIATION (GENETICS);

EID: 52449113534     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-9-384     Document Type: Article

References (84)

1. Bailey JA Yavor AM Massa HF Trask BJ Eichler EE Segmental duplications: Organization and impact within the current Human Genome Project assembly Genome Research 2001, 11(6):1005-1017 311093 11381028 10.1101/gr.GR-1871R
2. Bailey JA Gu ZP Clark RA Reinert K Samonte RV Schwartz S Adams MD Myers EW Li PW Eichler EE Recent segmental duplications in the human genome Science 2002, 297(5583):1003-1007 10.1126/science.1072047 12169732
3. Cheung J Estivill X Khaja R MacDonald JR Lau K Tsui LC Scherer SW Genome-wide detection of segmental duplications and potential assembly errors in the human genome sequence Genome Biol 2003, 4(4):R25 154576 12702206 10.1186/gb-2003-4-4-r25
4. Linardopoulou EV Williams EM Fan Y Friedman C Young JM Trask BJ Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication Nature 2005, 437(7055):94-100 1368961 16136133 10.1038/nature04029
5. She XW Liu G Ventura M Zhao S Misceo D Roberto R Cardone MF Rocchi M Green ED Archidiacano N Eichler EE A preliminary comparative analysis of primate segmental duplications shows elevated substitution rates and a great-ape expansion of intrachromosomal duplications Genome Research 2006, 16(5):576-583 1457043 16606706 10.1101/gr.4949406
6. Cheng Z Ventura M She XW Khaitovich P Graves T Osoegawa K Church D DeJong P Wilson RK Paabo S Rocchi M Eichler EE A genome-wide comparison of recent chimpanzee and human segmental duplications Nature 2005, 437(7055):88-93 10.1038/nature04000 16136132
7. Sharp AJ Cheng Z Eichler EE Structural Variation of the Human Genome Annu Rev Genomics Hum Genet 2006 16780417
8. Armengol L Pujana MA Cheung J Scherer SW Estivill X Enrichment of segmental duplications in regions of breaks of synteny between the human and mouse genomes suggest their involvement in evolutionary rearrangements Human Molecular Genetics 2003, 12(17):2201-2208 10.1093/ hmg/ddg223 12915466
9. Bailey JA Baertsch R Kent WJ Haussler D Eichler EE Hotspots of mammalian chromosomal evolution Genome Biology 2004, 5(4) 395782 15059256
10. Samonte RV Eichler EE Segmental duplications and the evolution of the primate genome Nature Reviews Genetics 2002, 3(1):65-72 10.1038/nrg705 11823792
11. Sharp AJ Locke DP McGrath SD Cheng Z Bailey JA Vallente RU Pertz LM Clark RA Schwartz S Segraves R Oseroff VV Albertson DG Pinkel D Eichler EE Segmental duplications and copy-number variation in the human genome Am J Hum Genet 2005, 77(1):78-88 15918152 1226196 10.1086/431652
12. Ji Y Eichler EE Schwartz S Nicholls RD Structure of chromosomal duplicons and their role in mediating human genomic disorders Genome Res 2000, 10(5):597-610 10.1101/gr.10.5.597 10810082
13. Coghlan A Eichler EE Oliver SG Paterson AH Stein L Chromosome evolution in eukaryotes: A multi-kingdom perspective Trends Genet 2005, 21(12):673-682 10.1016/j.tig.2005.09.009 16242204
14. Eichler EE Sankoff D Structural dynamics of eukaryotic chromosome evolution Science 2003, 301(5634):793-797 10.1126/science.1086132 12907789
15. Stankiewicz P Shaw CJ Withers M Inoue K Lupski JR Serial segmental duplications during primate evolution result in complex human genome architecture Genome Research 2004, 14(11):2209-2220 525679 15520286 10.1101/gr.2746604
16. Lupski JR Genomic disorders: Structural features of the genome can lead to DNA rearrangements and human disease traits Trends Genet 1998, 14(10):417-422 10.1016/S0168-9525(98)01555-8 9820031
17. Shaw CJ Lupski JR Implications of human genome architecture for rearrangement-based disorders: The genomic basis of disease Human Molecular Genetics 2004, 13:R57-R64 10.1093/hmg/ddh073 14764619
18. Stankiewicz P Lupski JR Genome architecture, rearrangements and genomic disorders Trends in Genetics 2002, 18(2):74-82 10.1016/ S0168-9525(02)02592-1 11818139
19. Courseaux A Nahon JL Birth of two chimeric genes in the Hominidae lineage Science 2001, 291(5507):1293-1297 10.1126/science.1057284 11181993
20. Johnson ME Viggiano L Bailey JA Abdul-Rauf M Goodwin G Rocchi M Eichler EE Positive selection of a gene family during the emergence of humans and African apes Nature 2001, 413(6855):514-519 10.1038/35097067 11586358
21. Eichler EE Segmental duplications: What's missing, misassigned, and misassembled - and should we care? Genome Research 2001, 11(5):653-656 10.1101/gr.188901 11337463
22. Jordan IK Wolf YI Koonin EV Duplicated genes evolve slower than singletons despite the initial rate increase Bmc Evolutionary Biology 2004:4 481058 15238160
23. Conrad DF Andrews TD Carter NP Hurles ME Pritchard JK A high-resolution survey of deletion polymorphism in the human genome Nat Genet 2006, 38(1):75-81 10.1038/ng1697 16327808
24. Sebat J Lakshmi B Troge J Alexander J Young J Lundin P Maner S Massa H Walker M Chi M Navin N Lucito R Healy J Hicks J Ye K Reiner A Gilliam TC Trask B Patterson N Zetterberg A Wigler M Large-scale copy number polymorphism in the human genome Science 2004, 305(5683):525-528 10.1126/ science.1098918 15273396
25. Zhang P Gu ZL Li WH Different evolutionary patterns between young duplicate genes in the human genome Genome Biology 2003, 4(9):R56 193656 12952535 10.1186/gb-2003-4-9-r56
26. Conant GC Wagner A Asymmetric sequence divergence of duplicate genes Genome Res 2003, 13(9):2052-2058 403682 12952876 10.1101/gr.1252603
27. Lynch M Conery JS The evolutionary fate and consequences of duplicate genes Science 2000, 290(5494):1151-1155 10.1126/science.290.5494.1151 11073452
28. Kondrashov FA Rogozin IB Wolf YI Koonin EV Selection in the evolution of gene duplications Genome Biol 2002, 3(2):RESEARCH0008 65685 11864370 10.1186/gb-2002-3-2-research0008
29. Ranz JM Maurin D Chan YS von Grotthuss M Hillier LW Roote J Ashburner M Bergman CM Principles of Genome Evolution in the Drosophila melanogaster Species Group Plos Biology (In press) 2007
30. Casals F Navarro A Inversions - the chicken or the egg? Plos Biology (News & Comments) (In press) 2007
31. Navarro A Barton NH Accumulating postzygotic isolation genes in parapatry: A new twist on chromosomal speciation Evolution 2003, 57(3):447-459 12703935
32. Rieseberg LH Chromosomal rearrangements and speciation Trends in Ecology & Evolution 2001, 16(7):351-358 10.1016/S0169-5347(01)02187-5
33. Noor MAF Grams KL Bertucci LA Reiland J Chromosomal inversions and the reproductive isolation of species P Natl Acad Sci USA P Natl Acad Sci USA 2001, 98(21):12084-12088 10.1073/pnas.221274498
34. Kirkpatrick M Barton N Chromosome inversions, local adaptation and speciation Genetics 2006, 173(1):419-434 1461441 16204214 10.1534/ genetics.105.047985
35. Navarro A Barton NH Chromosomal speciation and molecular divergence - Accelerated evolution in rearranged chromosomes Science 2003, 300(5617):321-324 10.1126/science.1080600 12690198
36. Lu J Li WH Wu CI Comment on "Chromosomal speciation and molecular divergence - Accelerated evolution in rearranged chromosomes" Science 2003, 302(5647):988 10.1126/science.1088277 14605352
37. Navarro A Marques-Bonet T Barton NH Response to comment on "chromosomal speciation and molecular divergence - Accelerated evolution in rearranged chromosomes" Science 2003, 302(5647):988 10.1126/science.1090460 14605352
38. Zhang JZ Wang XX Podlaha O Testing the chromosomal speciation hypothesis for humans and chimpanzees Genome Research 2004, 14(5):845-851 479111 15123584 10.1101/gr.1891104
39. Vallender EJ Lahn BT Effects of chromosomal rearrangements on human-chimpanzee molecular evolution Genomics 2004, 84(4):757-761 10.1016/j.ygeno.2004.07.005 15475253
40. Marques-Bonet T Sànchez-Ruiz J Armengol LL Khaja R Bertranpetit J Rocchi M Gazave E Navarro A On the association between chromosomal rearrangements and genic evolution in humans and chimpanzees. Genome Biol 2007 Oct 30;8 (10):R230 17971225 2007
41. Marques-Bonet T Navarro A Chromosomal rearrangements are associated with higher rates of molecular evolution in mammals Gene 2005, 353(2):147-154 10.1016/j.gene.2005.05.007 15951139
42. Armengol L Marques-Bonet T Cheung J Khaja R Gonzalez JR Scherer SW Navarro A Estivill X Murine segmental duplications are hot spots for chromosome and gene evolution Genomics 2005, 86(6):692-700 10.1016/ j.ygeno.2005.08.008 16256303
43. Lindblad-Toh K Wade CM Mikkelsen TS Karlsson EK Jaffe DB Kamal M Clamp M Chang JL Kulbokas EJ 3rd Zody MC Mauceli E Xie X Breen M Wayne RK Ostrander EA Ponting CP Galibert F Smith DR DeJong PJ Kirkness E Alvarez P Biagi T Brockman W Butler J Chin CW Cook A Cuff J Daly MJ DeCaprio D Gnerre S Grabherr M Kellis M Kleber M Bardeleben C Goodstadt L Heger A Hitte C Kim L Koepfli KP Parker HG Pollinger JP Searle SM Sutter NB Thomas R Webber C Baldwin J Abebe A Abouelleil A Aftuck L Ait-Zahra M Aldredge T Allen N An P Anderson S Antoine C Arachchi H Aslam A Ayotte L Bachantsang P Barry A Bayul T Benamara M Berlin A Bessette D Blitshteyn B Bloom T Blye J Boguslavskiy L Bonnet C Boukhgalter B Brown A Cahill P Calixte N Camarata J Cheshatsang Y Chu J Citroen M Collymore A Cooke P Dawoe T Daza R Decktor K DeGray S Dhargay N Dooley K Dooley K Dorje P Dorjee K Dorris L Duffey N Dupes A Egbiremolen O Elong R Falk J Farina A Faro S Ferguson D Ferreira P Fisher S et al. Genome sequence, comparative analysis and haplotype structure of the domestic dog Nature 2005, 438(7069):803-819 10.1038/nature04338 16341006
44. Cooper DN Youssoufian H The CpG dinucleotide and human genetic disease Hum Genet 1988, 78(2):151-155 10.1007/BF00278187 3338800
45. Sved J Bird A The expected equilibrium of the CpG dinucleotide in vertebrate genomes under a mutation model Proc Natl Acad Sci U S A 1990, 87(12):4692-4696 54183 2352943 10.1073/pnas.87.12.4692
46. Webber C Ponting CP Hotspots of mutation and breakage in dog and human chromosomes Genome Res 2005, 15(12):1787-1797 1356117 16339377 10.1101/ gr.3896805
47. Li WH Yi SJ Makova K Male-driven evolution Curr Opin Genet Dev Curr Opin Genet Dev 2002, 12(6):650-656
48. Wolfe KH Sharp PM Mammalian Gene Evolution - Nucleotide-Sequence Divergence between Mouse and Rat J Mol Evol 1993, 37(4):441-456 8308912 10.1007/BF00178874
49. Rudd MK Willard HF Analysis of the centromeric regions of the human genome assembly Trends in Genetics 2004, 20(11):529-533 10.1016/ j.tig.2004.08.008 15475110
50. She XW Horvath JE Jiang ZS Liu G Furey TS Christ L Clark R Graves T Gulden CL Alkan C Bailey JA Sahinalp C Rocchi M Haussler D Wilson RK Miller W Schwartz S Eichler EE The structure and evolution of centromeric transition regions within the human genome Nature 2004, 430(7002):857-864 10.1038/nature02806 15318213
51. Mikkelsen TS Hillier LW Eichler EE Zody MC Jaffe DB Yang SP Enard W Hellmann I Lindblad-Toh K Altheide TK Archidiacono N Bork P Butler J Chang JL Cheng Z Chinwalla AT deJong P Delehaunty KD Fronick CC Fulton LL Gilad Y Glusman G Gnerre S Graves TA Hayakawa T Hayden KE Huang XQ Ji HK Kent WJ King MC Kulbokas EJ Lee MK Liu G Lopez-Otin C Makova KD Man O Mardis ER Mauceli E Miner TL Nash WE Nelson JO Paabo S Patterson NJ Pohl CS Pollard KS Prufer K Puente XS Reich D Rocchi M Rosenbloom K Ruvolo M Richter DJ Schaffner SF Smit AFA Smith SM Suyama M Taylor J Torrents D Tuzun E Varki A Velasco G Ventura M Wallis JW Wendl MC Wilson RK Lander ES Waterston RH Consortium CSA Initial sequence of the chimpanzee genome and comparison with the human genome Nature 2005, 437(7055):69-87 10.1038/nature04072 16136131
52. Szamalek JM Goidts V Searle JB Cooper DN Hameister H Kehrer-Sawatzki H The chimpanzee-specific pericentric inversions that distinguish humans and chimpanzees have identical breakpoints in Pan troglodytes and Pan paniscus Genomics 2006, 87(1):39-45 10.1016/j.ygeno.2005.09.003 16321504
53. Castresana J Genes on human chromosome 19 show extreme divergence from the mouse orthologs and a high GC content Nucleic Acids Research 2002, 30(8):1751-1756 113201 11937628 10.1093/nar/30.8.1751
54. Castresana J Guigo R Alba MM Clustering of genes coding for DNA binding proteins in a region of atypical evolution of the human genome J Mol Evol 2004, 59(1):72-79 10.1007/s00239-004-2605-z 15383909
55. Newman TL Tuzun E Morrison VA Hayden KE Ventura M McGrath SD Rocchi M Eichler EE A genome-wide survey of structural variation between human and chimpanzee Genome Research 2005, 15(10):1344-1356 1240076 16169929 10.1101/gr.4338005
56. Johnson ME Cheng Z Morrison VA Scherer S Ventura M Gibbs RA Green ED Eichler EE Eukaryotic Transposable Elements and Genome Evolution Special Feature: Recurrent duplication-driven transposition of DNA during hominoid evolution Proc Natl Acad Sci U S A 2006, 103(47):17626-17631 1693797 17101969 10.1073/pnas.0605426103
57. Zody MC Garber M Adams DJ Sharpe T Harrow J Lupski JR Nicholson C Searle SM Wilming L Young SK Abouelleil A Allen NR Bi WM Bloom T Borowsky ML Bugalter BE Butler J Chang JL Chen CK Cook A Corum B Cuomo CA de Jong PJ DeCaprio D Dewar K FitzGerald M Gilbert J Gibson R Gnerre S Goldstein S Grafham DV Grocock R Hafez N Hagopian DS Hart E Norman CH Humphray S Jaffe DB Jones M Kamal M Khodiyar VK LaButti K Laird G Lehoczky J Liu XH Lokyitsang T Loveland J Lui A Macdonald P Major JE Matthews L Mauceli E McCarroll SA Mihalev AH Mudge J Nguyen C Nicol R O'Leary SB Osoegawa K Schwartz DC Shaw-Smith C Stankiewicz P Steward C Swarbreck D Venkataraman V Whittaker CA Yang XP Zimmer AR Bradley A Hubbard T Birren BW Rogers J Lander ES Nusbaum C DNA sequence of human chromosome 17 and analysis of rearrangement in the human lineage Nature 2006, 440(7087):1045-1049 10.1038/nature04689 16625196
58. Zody M Garber M Sharpe T Young S Rowen L O'Neill K Whittaker C Kamal M Chang J Cuomo C Dewar K Fitzgerald M Kodira C Madan A Qin S Yang X Abbasi N Abouelleil A Arachchi H Baradarani L Birditt B Bloom S Bloom T Borowsky M Burke J Butler J Cook A Dearellano K Decaprio D Dorris L Dors M Eichler E Engels R Fahey J Fleetwood P Friedman C Gearin G Hall J Hensley G Johnson E Jones C Kamat A Kaur A Locke D Madan A Munson G Jaffe D Lui A Macdonald P Mauceli E Naylor J Nesbitt R Nicol R O'Leary S Ratcliffe A Rounsley S She X Sneddon K Stewart S Sougnez C Stone S Topham K Vincent D Wang S Zimmer A Birren B Hood L Lander E Nusbaum C Analysis of the DNA sequence and duplication history of human chromosome 15 Nature Nature 2006, 440(7084):671-675 10.1038/nature04601 16572171
59. Navarro A Betran E Barbadilla A Ruiz A Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes Genetics 1997, 146(2):695-709 1208008 9178017
60. Hellmann I Ebersberger I Ptak SE Paabo S Przeworski M A neutral explanation for the correlation of diversity with recombination rates in humans Am J Hum Genet 2003, 72(6):1527-1535 12740762 1180312 10.1086/ 375657
61. Eyrewalker A Recombination and Mammalian Genome Evolution P Roy Soc Lond B Bio 1993, 252(1335):237-243 10.1098/rspb.1993.0071
62. Hardison RC Roskin KM Yang S Diekhans M Kent WJ Weber R Elnitski L Li J O'Connor M Kolbe D Schwartz S Furey TS Whelan S Goldman N Smit A Miller W Chiaromonte F Haussler D Covariation in frequencies of substitution, deletion, transposition, and recombination during eutherian evolution Genome Res 2003, 13(1):13-26 430971 12529302 10.1101/gr.844103
63. Meunier J Duret L Recombination drives the evolution of GC-content in the human genome Mol Biol Evol 2004, 21(6):984-990 10.1093/molbev/msh070 14963104
64. Myers S Bottolo L Freeman C McVean G Donnelly P A fine-scale map of recombination rates and hotspots across the human genome Science 2005, 310(5746):321-324 10.1126/science.1117196 16224025
65. Kong A Gudbjartsson DF Sainz J Jonsdottir GM Gudjonsson SA Richardsson B Sigurdardottir S Barnard J Hallbeck B Masson G Shlien A Palsson ST Frigge ML Thorgeirsson TE Gulcher JR Stefansson K A high-resolution recombination map of the human genome Nature Genetics 2002, 31(3):241-247 12053178
66. Ruiz-Herrera A Garcia F Giulotto E Attolini C Egozcue J Ponsa M Garcia M Evolutionary breakpoints are co-localized with fragile sites and intrachromosomal telomeric sequences in primates Cytogenet Genome Res 2005, 108(1-3):234-247 10.1159/000080822 15545736
67. Nergadze SG Rocchi M Azzalin CM Mondello C Giulotto E Insertion of telomeric repeats at intrachromosomal break sites during primate evolution Genome Res 2004, 14(9):1704-1710 515315 15310657 10.1101/ gr.2778904
68. Murphy WJ Larkin DM Everts-van der Wind A Bourque G Tesler G Auvil L Beever JE Chowdhary BP Galibert F Gatzke L Hitte C Meyers SN Milan D Ostrander EA Pape G Parker HG Raudsepp T Rogatcheva MB Schook LB Skow LC Welge M Womack JE O'Brien S J Pevzner PA Lewin HA Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps Science 2005, 309(5734):613-617 10.1126/science.1111387 16040707
69. Rozen S Skaletsky H Marszalek JD Minx PJ Cordum HS Waterston RH Wilson RK Page DC Abundant gene conversion between arms of palindromes in human and ape Y chromosomes Nature 2003, 423(6942):873-876 10.1038/nature01723 12815433
70. Marques-Bonet T Caceres M Bertranpetit J Preuss TM Thomas JW Navarro A Chromosomal rearrangements and the genomic distribution of gene-expression divergence in humans and chimpanzees Trends in Genetics 2004, 20(11):524-529 10.1016/j.tig.2004.08.009 15475109
71. Browser UCSCG UCSC Genome Browser http://genome.ucsc.edu/
72. Feuk L MacDonald JR Tang T Carson AR Li M Rao G Khaja R Scherer SW Discovery of human inversion polymorphisms by comparative analysis of human and chimpanzee DNA sequence assemblies Plos Genetics 2005, 1(4):489-498 10.1371/journal.pgen.0010056
73. Goidts V Szamalek JM Hameister H Kehrer-Sawatzki H Segmental duplication associated with the human-specific inversion of chromosome 18: A further example of the impact of segmental duplications on karyotype and genome evolution in primates Human Genetics 2004, 115(2):116-122 10.1007/ s00439-004-1120-z 15133654
74. Kehrer-Sawatzki H Sandig C Chuzhanova N Goidts V Szamalek JM Tanzer S Muller S Platzer M Cooper DN Hameister H Breakpoint analysis of the pericentric inversion distinguishing human chromosome 4 from the homologous chromosome in the chimpanzee (Pan troglodytes) Human Mutation 2005, 25(1):45-55 10.1002/humu.20116 15580561
75. Kehrer-Sawatzki H Sandig CA Goidts V Hameister H Breakpoint analysis of the pericentric inversion between chimpanzee chromosome 10 and the homologous chromosome 12 in humans Cytogenetic and Genome Research 2005, 108(1-3):91-97 10.1159/000080806
76. Kehrer-Sawatzki H Schreiner B Tanzer S Platzer M Muller S Hameister H Molecular characterization of the pericentric inversion that causes differences between chimpanzee chromosome 19 and human chromosome 17 Am J Hum Genet 2002, 71(2):375-388 12094327 379169 10.1086/341963
77. Kehrer-Sawatzki H Szamalek JM Tanzer S Platzer M Hameister H Molecular characterization of the pericentric inversion of chimpanzee chromosome 11 homologous to human chromosome 9 Genomics 2005, 85(5):542-550 10.1016/ j.ygeno.2005.01.012 15820305
78. Yunis JJ Prakash O The Origin of Man - a Chromosomal Pictorial Legacy Science 1982, 215(4539):1525-1530 10.1126/science.7063861 7063861
79. Chimpanzee Segmental Duplication Database http://chimpparalogy.gs.washington.edu/
80. Human Segmental Duplication Database http://humanparalogy.gs.washington.edu/
81. Crow JF A new study challenges the current belief of a high human male: female mutation ratio Trends in Genetics 2000, 16(12):525-526 10.1016/ S0168-9525(00)02136-3 11102696
82. Hurst LD Ellegren H Sex biases in the mutation rate Trends in Genetics 1998, 14(11):446-452 10.1016/S0168-9525(98)01577-7 9825672
83. Makova KD Li WH Strong male-driven evolution of DNA sequences in humans and apes Nature 2002, 416(6881):624-626 10.1038/416624a 11948348
84. She XW Jiang ZX Clark RL Liu G Cheng Z Tuzun E Church DM Sutton G Halpern AL Eichler EE Shotgun sequence assembly and recent segmental duplications within the human genome Nature 2004, 431(7011):927-930 10.1038/nature03062 15496912