Genetic origins of lactase persistence and the spread of pastoralism in africa

American Journal of Human Genetics

Volumn 94, Issue 4, 2014, Pages 496-510

  Ranciaro, Alessia ^a   Campbell, Michael C ^a   Hirbo, Jibril B ^a   Ko, Wen Ya ^a   Froment, Alain ^b   Anagnostou, Paolo ^c,d   Kotze, Maritha J ^e   Ibrahim, Muntaser ^f   Nyambo, Thomas ^g   Omar, Sabah A ^h   Tishkoff, Sarah A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b MUSÉE DE L HOMME   (France)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d Ist Ital di Paleontologia Um   (Italy)

^e STELLENBOSCH UNIVERSITY   (South Africa)

^f UNIVERSITY OF KHARTOUM   (Sudan)

^g MUHIMBILI UNIVERSITY OF HEALTH AND ALLIED SCIENCES   (Tanzania)

^h KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

Author keywords

[No Author keywords available]

Indexed keywords

LACTASE; MINICHROMOSOME MAINTENANCE PROTEIN 6;

AFRICA; ARTICLE; CENTRAL AFRICA; CONTROLLED STUDY; FEMALE; FOOD INTAKE; GENE; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETIC TRAIT; GENETIC VARIABILITY; GENOTYPE; GENOTYPE PHENOTYPE CORRELATION; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE; HUMAN; INTRON; LACTASE PERSISTENCE; LACTOSE TOLERANCE; LCT GENE; MAJOR CLINICAL STUDY; MALE; MCM6 GENE; MICROSATELLITE MARKER; MOLECULAR EVOLUTION; PASTORALISM; PRIORITY JOURNAL; PROMOTER REGION;

AFRICA; HUMANS; INTRONS; LACTASE; LACTASE-PHLORIZIN HYDROLASE; MICROSATELLITE REPEATS; MINICHROMOSOME MAINTENANCE COMPLEX COMPONENT 6; POLYMERASE CHAIN REACTION; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC;

EID: 84897979695     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2014.02.009     Document Type: Article

References (96)

1. A.K. Campbell, J.P. Waud, and S.B. Matthews The molecular basis of lactose intolerance Sci. Prog. 88 2005 157 202
2. G. Cook Hypolactasia: geographical distribution, diagnosis, and pratical significance R.K. Chandra, Critical Reviews in Tropical Medicine Volume 2 1984 Plenum Press New York 117 139
3. A. Holzel, V. Schwarz, and K.W. Sutcliffe Defective lactose absorption causing malnutrition in infancy Lancet 1 1959 1126 1128
4. A. Jacobi Milk-sugar in infant feeding Transactions of the American Pediatric Society 13 1901 150 160
5. N. Kretchmer Lactose and lactase - a historical perspective Gastroenterology 61 1971 805 813
6. T. Sahi Hypolactasia and lactase persistence. Historical review and the terminology Scand. J. Gastroenterol. Suppl. 202 1994 1 6 (Pubitemid 24128389)
7. W. Durham Cultural Mediation: The evolution of adult lactose absorption Coevolution Genes, Culture, and Human Diversity 1992 Stanford University Press Stanford 226 285
8. D.M. Swallow Genetics of lactase persistence and lactose intolerance Annu. Rev. Genet. 37 2003 197 219 (Pubitemid 38041425)
9. J.T. Troelsen Adult-type hypolactasia and regulation of lactase expression Biochim. Biophys. Acta 1723 2005 19 32 (Pubitemid 40744668)
10. H. Arola Diagnosis of hypolactasia and lactose malabsorption Scand. J. Gastroenterol. Suppl. 202 1994 26 35 (Pubitemid 24128392)
11. C.A. Mulcare, M.E. Weale, A.L. Jones, B. Connell, D. Zeitlyn, A. Tarekegn, D.M. Swallow, N. Bradman, and M.G. Thomas The T allele of a single-nucleotide polymorphism 13.9 kb upstream of the lactase gene (LCT) (C-13.9kbT) does not predict or cause the lactase-persistence phenotype in Africans Am. J. Hum. Genet. 74 2004 1102 1110 (Pubitemid 38669309)
12. E.J. Hollox, M. Poulter, M. Zvarik, V. Ferak, A. Krause, T. Jenkins, N. Saha, A.I. Kozlov, and D.M. Swallow Lactase haplotype diversity in the Old World Am. J. Hum. Genet. 68 2001 160 172 (Pubitemid 32048371)
13. Y. Itan, B.L. Jones, C.J. Ingram, D.M. Swallow, and M.G. Thomas A worldwide correlation of lactase persistence phenotype and genotypes BMC Evol. Biol. 10 2010 36
14. S.A. Tishkoff, F.A. Reed, A. Ranciaro, B.F. Voight, C.C. Babbitt, J.S. Silverman, K. Powell, H.M. Mortensen, J.B. Hirbo, and M. Osman et al. Convergent adaptation of human lactase persistence in Africa and Europe Nat. Genet. 39 2007 31 40 (Pubitemid 46026499)
15. C.J. Ingram, M.F. Elamin, C.A. Mulcare, M.E. Weale, A. Tarekegn, T.O. Raga, E. Bekele, F.M. Elamin, M.G. Thomas, N. Bradman, and D.M. Swallow A novel polymorphism associated with lactose tolerance in Africa: multiple causes for lactase persistence? Hum. Genet. 120 2007 779 788 (Pubitemid 46128833)
16. C.J. Ingram, C.A. Mulcare, Y. Itan, M.G. Thomas, and D.M. Swallow Lactose digestion and the evolutionary genetics of lactase persistence Hum. Genet. 124 2009 579 591
17. F. Imtiaz, E. Savilahti, A. Sarnesto, D. Trabzuni, K. Al-Kahtani, I. Kagevi, M.S. Rashed, B.F. Meyer, and I. Järvelä The T/G 13915 variant upstream of the lactase gene (LCT) is the founder allele of lactase persistence in an urban Saudi population J. Med. Genet. 44 2007 e89
18. N.S. Enattah, A. Trudeau, V. Pimenoff, L. Maiuri, S. Auricchio, L. Greco, M. Rossi, M. Lentze, J.K. Seo, and S. Rahgozar et al. Evidence of still-ongoing convergence evolution of the lactase persistence T-13910 alleles in humans Am. J. Hum. Genet. 81 2007 615 625 (Pubitemid 47330220)
19. N.S. Enattah, T.G. Jensen, M. Nielsen, R. Lewinski, M. Kuokkanen, H. Rasinpera, H. El-Shanti, J.K. Seo, M. Alifrangis, and I.F. Khalil et al. Independent introduction of two lactase-persistence alleles into human populations reflects different history of adaptation to milk culture Am. J. Hum. Genet. 82 2008 57 72 (Pubitemid 351735951)
20. N.S. Enattah, T. Sahi, E. Savilahti, J.D. Terwilliger, L. Peltonen, and I. Järvelä Identification of a variant associated with adult-type hypolactasia Nat. Genet. 30 2002 233 237
21. T. Bersaglieri, P.C. Sabeti, N. Patterson, T. Vanderploeg, S.F. Schaffner, J.A. Drake, M. Rhodes, D.E. Reich, and J.N. Hirschhorn Genetic signatures of strong recent positive selection at the lactase gene Am. J. Hum. Genet. 74 2004 1111 1120 (Pubitemid 38669310)
22. M. Coelho, D. Luiselli, G. Bertorelle, A.I. Lopes, S. Seixas, G. Destro-Bisol, and J. Rocha Microsatellite variation and evolution of human lactase persistence Hum. Genet. 117 2005 329 339 (Pubitemid 41194559)
23. R.H. Lewinsky, T.G. Jensen, J. Møller, A. Stensballe, J. Olsen, and J.T. Troelsen T-13910 DNA variant associated with lactase persistence interacts with Oct-1 and stimulates lactase promoter activity in vitro Hum. Mol. Genet. 14 2005 3945 3953 (Pubitemid 43020095)
24. C.J. Ingram, T.O. Raga, A. Tarekegn, S.L. Browning, M.F. Elamin, E. Bekele, M.G. Thomas, M.E. Weale, N. Bradman, and D.M. Swallow Multiple rare variants as a cause of a common phenotype: several different lactase persistence associated alleles in a single ethnic group J. Mol. Evol. 69 2009 579 588
25. B.L. Jones, T.O. Raga, A. Liebert, P. Zmarz, E. Bekele, E.T. Danielsen, A.K. Olsen, N. Bradman, J.T. Troelsen, and D.M. Swallow Diversity of lactase persistence alleles in Ethiopia: signature of a soft selective sweep Am. J. Hum. Genet. 93 2013 538 544
26. â̂ -G DNA polymorphism associated with lactase persistence in Africa interacts with Oct-1 Hum. Genet. 129 2011 111 113
27. â̂ -C variant associated with lactase persistence is located between an Oct-1 and HNF1α binding site and increases lactase promoter activity Hum. Genet. 130 2011 483 493
28. J.T. Troelsen, J. Olsen, J. Møller, and H. Sjöström An upstream polymorphism associated with lactase persistence has increased enhancer activity Gastroenterology 125 2003 1686 1694 (Pubitemid 37500433)
29. S.A. Tishkoff, F.A. Reed, F.R. Friedlaender, C. Ehret, A. Ranciaro, A. Froment, J.B. Hirbo, A.A. Awomoyi, J.-M. Bodo, and O. Doumbo et al. The genetic structure and history of Africans and African Americans Science 324 2009 1035 1044
30. B. Ewing, and P. Green Base-calling of automated sequencer traces using phred. II. Error probabilities Genome Res. 8 1998 186 194 (Pubitemid 28177230)
31. D. Gordon, C. Abajian, and P. Green Consed: a graphical tool for sequence finishing Genome Res. 8 1998 195 202 (Pubitemid 28177231)
32. D.A. Nickerson, V.O. Tobe, and S.L. Taylor PolyPhred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing Nucleic Acids Res. 25 1997 2745 2751 (Pubitemid 27299787)
33. P. Scheet, and M. Stephens A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase Am. J. Hum. Genet. 78 2006 629 644
34. M. Stephens, N.J. Smith, and P. Donnelly A new statistical method for haplotype reconstruction from population data Am. J. Hum. Genet. 68 2001 978 989 (Pubitemid 32289743)
35. M. Stephens, and P. Donnelly A comparison of bayesian methods for haplotype reconstruction from population genotype data Am. J. Hum. Genet. 73 2003 1162 1169 (Pubitemid 37414228)
36. D.C. Crawford, T. Bhangale, N. Li, G. Hellenthal, M.J. Rieder, D.A. Nickerson, and M. Stephens Evidence for substantial fine-scale variation in recombination rates across the human genome Nat. Genet. 36 2004 700 706 (Pubitemid 38886630)
37. J.C. Barrett, B. Fry, J. Maller, and M.J. Daly Haploview: analysis and visualization of LD and haplotype maps Bioinformatics 21 2005 263 265 (Pubitemid 40202029)
38. P.C. Sabeti, S.F. Schaffner, B. Fry, J. Lohmueller, P. Varilly, O. Shamovsky, A. Palma, T.S. Mikkelsen, D. Altshuler, and E.S. Lander Positive natural selection in the human lineage Science 312 2006 1614 1620 (Pubitemid 43902654)
39. B.F. Voight, S. Kudaravalli, X. Wen, and J.K. Pritchard A map of recent positive selection in the human genome PLoS Biol. 4 2006 e72
40. J.P. Jarvis, L.B. Scheinfeldt, S. Soi, C. Lambert, L. Omberg, B. Ferwerda, A. Froment, J.M. Bodo, W. Beggs, and G. Hoffman et al. Patterns of ancestry, signatures of natural selection, and genetic association with stature in Western African pygmies PLoS Genet. 8 2012 e1002641
41. F. Tajima The effect of change in population size on DNA polymorphism Genetics 123 1989 597 601
42. F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism Genetics 123 1989 585 595 (Pubitemid 19274682)
43. P. Librado, and J. Rozas DnaSP v5: a software for comprehensive analysis of DNA polymorphism data Bioinformatics 25 2009 1451 1452
44. R.R. Hudson, M. Slatkin, and W.P. Maddison Estimation of levels of gene flow from DNA sequence data Genetics 132 1992 583 589
45. H.M. Sun, Y.D. Qiao, F. Chen, L.D. Xu, J. Bai, and S.B. Fu The lactase gene -13910T allele can not predict the lactase-persistence phenotype in north China Asia Pac. J. Clin. Nutr. 16 2007 598 601 (Pubitemid 350291890)
46. C.B. Harvey, W.S. Pratt, I. Islam, D.B. Whitehouse, and D.M. Swallow DNA polymorphisms in the lactase gene. Linkage disequilibrium across the 70-kb region Eur. J. Hum. Genet. 3 1995 27 41
47. E.J. Hollox, M. Poulter, Y. Wang, A. Krause, and D.M. Swallow Common polymorphism in a highly variable region upstream of the human lactase gene affects DNA-protein interactions Eur. J. Hum. Genet. 7 1999 791 800 (Pubitemid 29516238)
48. K. Wagh, A. Bhatia, G. Alexe, A. Reddy, V. Ravikumar, M. Seiler, M. Boemo, M. Yao, L. Cronk, and A. Naqvi et al. Lactase persistence and lipid pathway selection in the Maasai PLoS ONE 7 2012 e44751
49. C.M. Schlebusch, P. Sjödin, P. Skoglund, and M. Jakobsson Stronger signal of recent selection for lactase persistence in Maasai than in Europeans Eur. J. Hum. Genet. 21 2013 550 553
50. M. Coelho, F. Sequeira, D. Luiselli, S. Beleza, and J. Rocha On the edge of Bantu expansions: mtDNA, Y chromosome and lactase persistence genetic variation in southwestern Angola BMC Evol. Biol. 9 2009 80
51. S. Torniainen, M.I. Parker, V. Holmberg, E. Lahtela, C. Dandara, and I. Jarvela Screening of variants for lactase persistence/non-persistence in populations from South Africa and Ghana BMC Genet. 10 2009 31
52. H. Wacker, P. Keller, R. Falchetto, G. Legler, and G. Semenza Location of the two catalytic sites in intestinal lactase-phlorizin hydrolase. Comparison with sucrase-isomaltase and with other glycosidases, the membrane anchor of lactase-phlorizin hydrolase J. Biol. Chem. 267 1992 18744 18752
53. J.N. Freund, F. Gossé, and F. Raul Derivatives of plant beta-glucans are hydrolyzed by intestinal lactase-phlorizin hydrolase of mammals Enzyme 45 1991 71 74
54. D.M. Swallow, M. Poulter, and E.J. Hollox Intolerance to lactose and other dietary sugars Drug Metab. Dispos. 29 2001 513 516 (Pubitemid 32275526)
55. B.B. Mishra, and V.K. Tiwari Natural products: an evolving role in future drug discovery Eur. J. Med. Chem. 46 2011 4769 4807
56. J.R. Ehrenkranz, N.G. Lewis, C.R. Kahn, and J. Roth Phlorizin: a review Diabetes Metab. Res. Rev. 21 2005 31 38
57. A. Kumari, R. Catanzaro, and F. Marotta Clinical importance of lactic acid bacteria: a short review Acta Biomed 82 2011 177 180
58. D.M. Saulnier, S. Kolida, and G.R. Gibson Microbiology of the human intestinal tract and approaches for its dietary modulation Curr. Pharm. Des. 15 2009 1403 1414
59. M. de Vrese, A. Stegelmann, B. Richter, S. Fenselau, C. Laue, and J. Schrezenmeir Probiotics - compensation for lactase insufficiency Am. J. Clin. Nutr. 73 Suppl 2001 421S 429S (Pubitemid 32113266)
60. J.K. Pritchard, J.K. Pickrell, and G. Coop The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation Curr. Biol. 20 2010 R208 R215
61. P.S. Pennings, and J. Hermisson Soft sweeps II - molecular population genetics of adaptation from recurrent mutation or migration Mol. Biol. Evol. 23 2006 1076 1084 (Pubitemid 43726073)
62. M. Przeworski, G. Coop, and J.D. Wall The signature of positive selection on standing genetic variation Evolution 59 2005 2312 2323 (Pubitemid 41752645)
63. L.B. Scheinfeldt, and S.A. Tishkoff Recent human adaptation: genomic approaches, interpretation and insights Nat. Rev. Genet. 14 2013 692 702
64. A.D. Cutter, and B.A. Payseur Genomic signatures of selection at linked sites: unifying the disparity among species Nat. Rev. Genet. 14 2013 262 274
65. O. Hanotte, D.G. Bradley, J.W. Ochieng, Y. Verjee, E.W. Hill, and J.E. Rege African pastoralism: genetic imprints of origins and migrations Science 296 2002 336 339 (Pubitemid 34303686)
66. B.M. Henn, L.R. Botigué, S. Gravel, W. Wang, A. Brisbin, J.K. Byrnes, K. Fadhlaoui-Zid, P.A. Zalloua, A. Moreno-Estrada, and J. Bertranpetit et al. Genomic ancestry of North Africans supports back-to-Africa migrations PLoS Genet. 8 2012 e1002397
67. C. Ehret The civilizations of Africa: a history to 1800 2002 University Press of Virginia Charlottesville
68. B. Arredi, E.S. Poloni, S. Paracchini, T. Zerjal, D.M. Fathallah, M. Makrelouf, V.L. Pascali, A. Novelletto, and C. Tyler-Smith A predominantly neolithic origin for Y-chromosomal DNA variation in North Africa Am. J. Hum. Genet. 75 2004 338 345 (Pubitemid 38943878)
69. E. Bosch, F. Calafell, D. Comas, P.J. Oefner, P.A. Underhill, and J. Bertranpetit High-resolution analysis of human Y-chromosome variation shows a sharp discontinuity and limited gene flow between northwestern Africa and the Iberian Peninsula Am. J. Hum. Genet. 68 2001 1019 1029 (Pubitemid 32289745)
70. K. Fadhlaoui-Zid, L. Rodríguez-Botigué, N. Naoui, A. Benammar-Elgaaied, F. Calafell, and D. Comas Mitochondrial DNA structure in North Africa reveals a genetic discontinuity in the Nile Valley Am. J. Phys. Anthropol. 145 2011 107 117
71. N. Maca-Meyer, A.M. González, J. Pestano, C. Flores, J.M. Larruga, and V.M. Cabrera Mitochondrial DNA transit between West Asia and North Africa inferred from U6 phylogeography BMC Genet. 4 2003 15
72. V. Cerný, M. Hájek, M. Bromová, R. Cmejla, I. Diallo, and R. Brdicka MtDNA of Fulani nomads and their genetic relationships to neighboring sedentary populations Hum. Biol. 78 2006 9 27 (Pubitemid 44087144)
73. H.Y. Hassan, P.A. Underhill, L.L. Cavalli-Sforza, and M.E. Ibrahim Y-chromosome variation among Sudanese: restricted gene flow, concordance with language, geography, and history Am. J. Phys. Anthropol. 137 2008 316 323
74. M.C. Campbell, and S.A. Tishkoff African genetic diversity: implications for human demographic history, modern human origins, and complex disease mapping Annu. Rev. Genomics Hum. Genet. 9 2008 403 433
75. J.B. Hirbo, A. Ranciaro, and S.A. Tishkoff Population structure and migration in Africa: correlations between archaeological, linguistic and genetic data M.H. Crawford, Causes and consequences of human migration: An evolutionary perspective, C.B.C 2012 Cambridge University Press Cambridge 135 171
76. A. Smith Origin and spread of pastoralism in Africa Annu. Rev. Anthropol. 21 1992 121 141
77. G.C. Cook Did Persistence of Intestinal Lactase Into Adult Life Originate on the Arabian Peninsula? Man 13 1978 418 427
78. J. Alexander Islam, Archaeology and Slavery in Africa World Archaeol. 33 2001 44 60 (Pubitemid 32635982)
79. T. Levy, and A. Holl Migrations, ethnogenesis and settlement dynamics: Israelites in iron ages Canaan ans Shuaw-Arabs in the Tchad basin Journal of Anthropological Archaeology 21 2002 83 118
80. Vanhove, M. (2006). The Beja language today in Sudan: the state of the art in linguistic. Proceedings of the 7th International Studies Conference.
81. C. Ehret An African classical age: eastern and southern Africa in world history, 1000 B.C. to A.D. 400 1998 University Press of Virginia Charlottesville
82. C. Ehret Linguistic stratigraphies and Holocene history in Northeastern Africa K. Kroeper, M. Chlodnicki, M. Kobusiewicz, Archaeology of Early Northeastern Africa 2006 Poznan Archaeological Museum Poznan 1019 1055
83. S.H. Ambrose Chronology of the Later Stone Age and Food Production in East Africa J. Archaeol. Sci. 25 1998 377 392
84. C. Ehret Southern Nilotic history; linguistic approaches to the study of the past 1971 Northwestern University Press Evanston
85. L. Pagani, T. Kivisild, A. Tarekegn, R. Ekong, C. Plaster, I. Gallego Romero, Q. Ayub, S.Q. Mehdi, M.G. Thomas, and D. Luiselli et al. Ethiopian genetic diversity reveals linguistic stratification and complex influences on the Ethiopian gene pool Am. J. Hum. Genet. 91 2012 83 96
86. C.M. Schlebusch, P. Skoglund, P. Sjödin, L.M. Gattepaille, D. Hernandez, F. Jay, S. Li, M. De Jongh, A. Singleton, and M.G. Blum et al. Genomic variation in seven Khoe-San groups reveals adaptation and complex African history Science 338 2012 374 379
87. J. Denbow A New Look at the Later Prehistory of the Kalahari J. Afr. Hist. 27 1986 3 28
88. L.H. Robbins, A.C. Campbell, M.L. Murphy, G.A. Brook, P. Srivastava, and S. Badenhorst The Advent of Herding in Southern Africa: Early AMS Dates on Domestic Livestock from the Kalahari Desert Curr. Anthropol. 46 2005 671 677 (Pubitemid 44392404)
89. C. Ehret Cattle-Keeping and Milking in Eastern and Southern African History: The Linguistic Evidence J. Afr. Hist. 8 1967 1 17
90. C.F. Hoogendijk, C.L. Scholtz, S.M. Pimstone, E. Ehrenborg, J.J. Kastelein, J.C. Defesche, R. Thiart, L. du Plessis, J.N. de Villiers, and M.G. Zaahl et al. Allelic variation in the promoter region of the LDL receptor gene: analysis of an African-specific variant in the FP2 cis-acting regulatory element Mol. Cell. Probes 17 2003 175 181 (Pubitemid 36999815)
91. H.C. Fleming Asa and Aramanik: Cushitic Hunters in Maasai Land Ethnology 8 1969 1 36
92. D.W. Phillipson The later prehistory of eastern and southern Africa 1977 Africana Pub. Co. New York
93. E.C.D. Carvalho "Traditional" and "Modern" Patterns of Cattle Raising in Southwestern Angola: A Critical Evaluation of Change from Pastoralism to Ranching J. Dev. Areas 8 1974 199 226
94. O. Roland The Nilotic Contribution to Bantu Africa J. Afr. Hist. 23 1982 433 442
95. B.M. Henn, C. Gignoux, A.A. Lin, P.J. Oefner, P. Shen, R. Scozzari, F. Cruciani, S.A. Tishkoff, J.L. Mountain, and P.A. Underhill Y-chromosomal evidence of a pastoralist migration through Tanzania to southern Africa Proc. Natl. Acad. Sci. USA 105 2008 10693 10698
96. J. Newman The Peopling of Africa 1995 Yale Univ. Press New Haven, London