Common 5′ β-globin RFLP haplotypes harbour a surprising level of ancestral sequence mosaicism

Abecasis GR, Noguchi E, Heinzmann A, Traherne JA, Bhattacharyya S, Leaves NI, Anderson GG, Zhang Y, Lench NJ, Carey A, Cardon LR, Moffatt MF, Cookson WO (2001) Extent and distribution of linkage disequilibrium in three genomic regions. Am J Hum Genet 68:191–197 Boyer SH, Crosby EF, Noyes AN, Fuller GF, Leslie SE, Donaldson LJ, Vrablik GR, Schaefer EW Jr, Thurmon TF (1970) Primate hemoglobins: some sequences and some proposals concerning the character of evolution and mutation. Biochem Genet 5:405–448 Calzolari R, McMorrow T, Yannoutsos N, Langeveld A, Grosveld F (1999) Deletion of a region that is a candidate for the difference between the deletion forms of hereditary persistence of fetal hemoglobin and δβ-thalassemia affects β- but not γ-globin gene expression. EMBO J 18:949–958 Cargill M, Altshuler D, Ireland J, Sklar P, Ardlie K, Patil N, Shaw N, Lane CR, Lim EP, Kalayanaraman N, Nemesh J, Ziaugra L, Friedland L, Rolfe A, Warrington J, Lipshutz R, Daley GQ, Lander ES (1999) Characterization of single-nucleotide polymorphisms in coding regions of human genes. Nat Genet 22:231–238 Chakravarti A, Buetow KH, Antonarakis SE, Waber PG, Boehm CD, Kazazian HH Jr (1984) Nonuniform recombination within the human β-globin gene cluster. Am J Hum Genet 36:1239–1258 Chen FC, Li WH (2001) Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 68:444–456 Clark AG (1987) Neutrality tests of highly polymorphic restriction-fragment-length polymorphisms. Am J Hum Genet 41:948–956 Clark AG, Weiss KM, Nickerson DA, Taylor SL, Buchanan A, Stengård J, Salomaa V, Vartiainen E, Perola M, Boerwinkle E, Sing CF (1998) Haplotype structure and population genetic inferences from nucleotide-sequence variation in human lipoprotein lipase. Am J Hum Genet 63:595–612 Collins A, Lonjou C, Morton NE (1999) Genetic epidemiology of single-nucleotide polymorphisms. Proc Natl Acad Sci USA 96:15173–15177 Currat M, Trabuchet G, Rees D, Perrin P, Harding RM, Clegg JB, Langaney A, Excoffier L (2002) Molecular analysis of the beta-globin gene cluster in the Niokholo Mandenka population reveals a recent origin of the beta(S) Senegal mutation. Am J Hum Genet 70:207–223 Daly MJ, Rioux JD, Schaffner SF, Hudson TJ, Lander ES (2001) High-resolution haplotype structure in the human genome. Nat Genet 29:229–232 Dawson E, Abecasis GR, Bumpstead S, Chen Y, Hunt S, Beare DM, Pabial J, Dibling T, Tinsley E, Kirby S, Carter D, Papaspyridonos M, Livingstone S, Ganske R, Lõhmussaar E, Zernant J, Tõnisson N, Remm M, Mägi R, Puurand T, Vilo J, Kurg A, Rice K, Deloukas P, Mott R, Metspalu A, Bentley DR, Cardon LR, Dunham I (2002) A first-generation linkage disequilibrium map of human chromosome 22. Nature 418:544–548 Fearnhead P, Donnelly P (2001) Estimating recombination rates from population genetic data. Genetics 159:1299–1318 Flint J, Harding RM, Boyce AJ, Clegg JB (1998) The population genetics of the haemoglobinopathies. Baillieres Clin Haematol 11:1-51 Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709 Fullerton SM, Harding RM, Boyce AJ, Clegg JB (1994) Molecular and population genetic analysis of allelic sequence diversity at the human β-globin locus. Proc Natl Acad Sci USA 91:1805–1809 Fullerton SM, Clark AG, Weiss KM, Nickerson DA, Taylor SL, Stengård JH, Salomaa V, Vertiainen E, Perola M, Boerwinkle E, Sing CF (2000) Apolipoprotein E variation at the sequence haplotype level: implications for the origin and maintenance of a major human polymorphism. Am J Hum Genet 67:881–900 Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, Higgins J, DeFelice M, Lochner A, Faggart M, Liu-Cordero SN, Rotimi C, Adeyemo A, Cooper R, Ward R, Lander ES, Daly MJ, Altshuler D (2002) The structure of haplotype blocks in the human genome. Science 296:2225–2229 Gribnau J, Diderich K, Pruzina S, Calzolari R, Fraser P (2000) Intergenic transcription and developmental remodeling of chromatin subdomains in the human β-globin locus. Mol Cell 5:377–386 Goldstein DB (2001) Islands of linkage disequilibrium. Nat Genet 29:109–111 Halushka MK, Fan J-B, Bentley K, Hsie L, Shen N, Weder A, Cooper R, Lipshutz R, Chakravarti A (1999) Patterns of single-nucleotide polymorphisms in candidate genes for blood-pressure homeostasis. Nat Genet 22:239–247 Harding RM, Fullerton SM, Griffiths RC, Bond J, Cox MJ, Schneider JA, Moulin DS, Clegg JB (1997) Archaic African and Asian lineages in the genetic ancestry of modern humans. Am J Hum Genet 60:772–789 Harris EE, Hey J (1999) X chromosome evidence for ancient human histories. Proc Natl Acad Sci USA 96:3320–3324 Harris S, Barrie PA, Weiss ML, Jeffreys AJ (1984) The primate ψβ1 gene. An ancient β-globin pseudogene. J Mol Biol 180:785–801 Hudson RR, Kreitman M, Aguadé M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159 Huttley GA, Smith MW, Carrington M, O'Brien SJ (1999) A scan for linkage disequilibrium across the human genome. Genetics 152:1711–1722 Jeffreys AJ, Kauppi L, Neumann R (2001) Intensely punctate meiotic recombination in the class II region of the major histocompatibility complex. Nat Genet 29:217–222 Johnson GCL, Esposito L, Barratt BJ, Smith AN, Heward J, Di Genova G, Ueda H, Cordell HJ, Eaves IA, Dudbridge F, Twells RCJ, Payne F, Hughes W, Nutland S, Stevens H, Carr P, Tuomilehto-Wolf E, Tuomilehto J, Gough SCL, Clayton DG, Todd JA (2001) Haplotype tagging for the identification of common disease genes. Nat Genet 29:233–237 Kreitman M (2000) Methods to detect selection in populations with applications to the human. Annu Rev Genomics Hum Genet 1:539–559 Kruglyak L (1999) Prospects for whole-genome linkage disequilibrium mapping of common disease genes. Nat Genet 22:139–144 Laan M, Pääbo S (1997) Demographic history and linkage disequilibrium in human populations. Nat Genet 17:435–438 Li WH, Sadler LA (1991) Low nucleotide diversity in man. Genetics 129:513–523 Maeda N, Bliska JB, Smithies O (1983) Recombination and balanced chromosome polymorphism suggested by DNA sequences 5′ to the human δ-globin gene. Proc Natl Acad Sci USA 80:5012–5016 Maniatis N, Collins A, Xu CF, McCarthy LC, Hewett DR, Tapper W, Ennis S, Ke X, Morton NE (2002) The first linkage disequilibrium (LD) maps: delineation of hot and cold blocks by diplotype analysis. Proc Natl Acad Sci USA 99:2228–2233 Nakajima T, Jorde LB, Ishigami T, Umemura S, Emi M, Lalouel JM, Inoue I (2002) Nucleotide diversity and haplotype structure of the human angiotensinogen gene in two populations. Am J Hum Genet 70:108–123 Newman JL (1995) The peopling of Africa: a geographic interpretation. Yale University Press, New Haven Newton CR, Graham A, Heptinstall LE, Powell SJ, Summers C, Kalsheker N, Smith JC, Markham AF (1989) Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS). Nucleic Acids Res 17:2503–2516 Nordborg M, Tavaré S (2002) Linkage disequilibrium: what history has to tell us. Trends Genet 18:83–90 Orkin SH, Kazazian HH Jr (1984) The mutation and polymorphism of the human β-globin gene and its surrounding DNA. Annu Rev Genet 18:131–171 Patil N, Berno AJ, Hinds DA, Barrett WA, Doshi JM, Hacker CR, Kautzer CR, Lee DH, Marjoribanks C, McDonough DP, Nguyen BT, Norris MC, Sheehan JB, Shen N, Stern D, Stokowski RP, Thomas DJ, Trulson MO, Vyas KR, Frazer KA, Fodor SP, Cox DR (2001) Blocks of limited haplotype diversity revealed by high-resolution scanning of human chromosome 21. Science 294:1719–1723 Pritchard JK, Przeworski M (2001) Linkage disequilibrium in humans: models and data. Am J Hum Genet 69:1-14 Przeworski M, Hudson RR, Di Rienzo A (2000) Adjusting the focus on human variation. Trends Genet 16:296–302 Quintana-Murci L, Semino O, Bandelt HJ, Passarino G, McElreavey K, Santachiara-Benerecetti AS (1999) Genetic evidence of an early exit of Homo sapiens sapiens from Africa through eastern Africa. Nat Genet 23:437–441 Reich DE, Cargill M, Bolk S, Ireland J, Sabeti PC, Richter DJ, Lavery T, Kouyoumjian R, Farhadian SF, Ward R, Lander ES (2001) Linkage disequilibrium in the human genome. Nature 411:199–204 Reich DE, Schaffner SF, Daly MJ, McVean G, Mullikin JC, Higgins JM, Richter DJ, Lander ES, Altshuler D (2002) Human genome sequence variation and the influence of gene history, mutation and recombination. Nat Genet 32:135–142 Rieder MJ, Taylor SL, Clark AG, Nickerson DA (1999) Sequence variation in the human angiotensin converting enzyme. Nat Genet 22:59–62 Schneider JA, Peto TE, Boone RA, Boyce AJ, Clegg JB (2002) Direct measurement of the male recombination fraction in the human β-globin hot spot. Hum Mol Genet 11:207–215 Schneider S, Roessli D, Excoffier L (2000) Arlequin version 2.000: a software for population genetic data analysis. University of Geneva, Geneva Service SK, Ophoff RA, Freimer NB (2001) The genome-wide distribution of background linkage disequilibrium in a population isolate. Hum Mol Genet 10:545–551 Steinberg MH, Adams JG III (1991) Hemoglobin A2: origin, evolution, and aftermath. Blood 78:2165–2177 Strobeck C, Morgan K (1978) The effect of intragenic recombination on the number of alleles in a finite population. Genetics 88:829–844 Taillon-Miller P, Bauer-Sardina I, Saccone NL, Putzel J, Laitinen T, Cao A, Kere J, Pilia G, Rice JP, Kwok PY (2000) Juxtaposed regions of extensive and minimal linkage disequilibrium in human Xq25 and Xq28. Nat Genet 25:324–328 Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595 Tishkoff SA, Williams SM (2002) Genetic analysis of African populations: human evolution and complex disease. Nat Rev Genet 3:611–621 Tishkoff SA, Pakstis AJ, Stoneking M, Kidd JR, Destro-Bisol G, Sanjantila A, Lu RB, Deinard AS, Sirugo G, Jenkins T, Kidd KK, Clark AG (2000) Short tandem-repeat polymorphism/Alu haplotype variation at the PLAT locus: implications for modern human origins. Am J Hum Genet 67:901–925 Wall JD, Przeworski M (2000) When did the human population size start increasing? Genetics 155:1865–1874 Weatherall DJ (1987) Common genetic disorders of the red cell and the "malaria hypothesis". Ann Trop Med Parasitol 81:539–548 Weatherall DJ, Clegg JB (2000) The thalassaemia syndromes. Blackwell Science, Oxford Webster MT, Wells RS, Clegg JB (2002) Analysis of variation in the human β-globin gene cluster using a novel DHPLC technique. Mut Res 501:99–103 Wiuf C, Hein J (1997) On the number of ancestors to a DNA sequence. Genetics 147:1459–1468 Yu N, Fu YX, Sambuughin N, Ramsay M, Jenkins T, Leskinen E, Patthy L, Jorde LB, Kuromori T, Li WH (2001) Global patterns of human DNA sequence variation in a 10-kb region on chromosome 1. Mol Biol Evol 18:214–222