Herders of indian and european cattle share their predominant allele for lactase persistence

Molecular Biology and Evolution

Volumn 29, Issue 1, 2012, Pages 249-260

  Romero, Irene Gallego ^a,j   Mallick, Chandana Basu ^b   Liebert, Anke ^c   Crivellaro, Federica ^a   Chaubey, Gyaneshwer ^b   Itan, Yuval ^c,k   Metspalu, Mait ^b   Eaaswarkhanth, Muthukrishnan ^d,l   Pitchappan, Ramasamy ^e   Villems, Richard ^b   Reich, David ^f,g   Singh, Lalji ^d,h   Thangaraj, Kumarasamy ^d   Thomas, Mark G ^c,i   Swallow, Dallas M ^c   Lahr, Marta Mirazón ^a   Kivisild, Toomas ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF TARTU   (Estonia)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^e CHETTINAD HOSPITAL AND RESEARCH INSTITUTE   (India)

^f HARVARD MEDICAL SCHOOL   (United States)

^g BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^h Genome Foundation   (India)

ⁱ UPPSALA UNIVERSITY   (Sweden)

^j UNIVERSITY OF CHICAGO   (United States)

^k ROCKEFELLER UNIVERSITY   (United States)

^l WADSWORTH CENTER   (United States)

more..

Author keywords

Haplotype; India; Lactase persistence; Pastoralism; Positive selection

Indexed keywords

DNA; LACTASE;

ANIMAL HUSBANDRY; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; CATTLE; ENHANCER REGION; EUROPE; GENE FREQUENCY; GENE IDENTIFICATION; GENE LOCUS; GENE MUTATION; GENE SEQUENCE; GENETIC TRAIT; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC DISTRIBUTION; GOAT; HAPLOTYPE; HUMAN; INDIA; LINGUISTICS; MILK; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMAL HUSBANDRY; ANIMALS; CATTLE; EUROPEAN CONTINENTAL ANCESTRY GROUP; EVOLUTION, MOLECULAR; GENE FREQUENCY; HAPLOTYPES; HUMANS; INDIA; LACTASE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC;

BOS;

EID: 84856757955     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr190     Document Type: Article

References (73)

1. Babu J, Kumar S, Babu P, Prasad JH, Ghoshal UC. 2010. Frequency of lactose malabsorption among healthy southern and northern Indian populations by genetic analysis and lactose hydrogen breath and tolerance tests. Am J Clin Nutr. 91:140-146.
2. Baig M, Beja-Pereira A, Mohammad R, Kulkarni K, Farah S, Luikart G. 2005. Phylogeography and origin of Indian domestic cattle. Curr Sci 89:38-40. (Pubitemid 41666046)
3. Balaresque P, Bowden GR, Adams SM, et al. (16 co-Authors). 2010. A predominantly neolithic origin for European paternal lineages. PLoS Biol. 8:e1000285.
4. Bandelt HJ, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 16:37-48. (Pubitemid 29024937)
5. Barendse W, Reverter A, Bunch RJ, Harrison BE, Barris W, Thomas MB. 2007. A validated whole-genome association study of efficient food conversion in cattle. Genetics 176:1893-1905. (Pubitemid 47105241)
6. Barrett JC, Fry B, Maller J, Daly MJ. 2005. Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics 21:263-265. (Pubitemid 40202029)
7. Bayless TM, Rosensweig NS. 1966. A racial difference in incidence of lactase deficiency. A survey of milk intolerance and lactase deficiency in healthy adult males. JAMA. 197:968-972.
8. Bersaglieri T, Sabeti PC, Patterson N, Vanderploeg T, Schaffner SF, Drake JA, Rhodes M, Reich DE, Hirschhorn JN. 2004. Genetic signatures of strong recent positive selection at the lactase gene. Am J Hum Genet. 74:1111-1120. (Pubitemid 38669310)
9. Browning SR, Browning BL. 2007. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering.AmJHumGenet. 81:1084-1097. (Pubitemid 47580259)
10. Buller HA, Kothe MJ, Goldman DA, Grubman SA, Sasak WV, Matsudaira PT, Montgomery RK, Grand RJ. 1990. Coordinate expression of lactase-phlorizin hydrolase mRNA and enzyme levels in rat intestine during development. J Biol Chem. 265:6978-6983.
11. Burger J, Kirchner M, Bramanti B, Haak W, Thomas MG. 2007. Absence of the lactase-persistence-Associated allele in early Neolithic Europeans. Proc Natl Acad Sci U S A. 104:3736-3741. (Pubitemid 47181524)
12. Chen S, Lin BZ, Baig M, et al. (23 co-Authors). 2010. Zebu cattle are an exclusive legacy of the South Asia Neolithic. Mol Biol Evol. 27:1-6.
13. Clutton-Brock J. 1999. A natural history of domesticated mammals. Cambridge (MA): Cambridge University Press.
14. Coelho M, Luiselli D, Bertorelle G, Lopes AI, Seixas S, Destro-Bisol G, Rocha J. 2005. Microsatellite variation and evolution of human lactase persistence. Hum Genet. 117:329-339. (Pubitemid 41194559)
15. Copley MS, Berstan R, Dudd SN, Aillaur S, Mukherjee AJ, Straker V, Payne S, Evershed RP. 2005a. Processing of milk products in pottery vessels through British prehistory. Antiquity 79: 895-908.
16. Copley MS, Berstan R, Dudd SN, Docherty G, Mukherjee AJ, Straker V, Payne S, Evershed RP. 2003. Direct chemical evidence for widespread dairying in prehistoric Britain. Proc Natl Acad Sci U S A. 100:1524-1529. (Pubitemid 36254480)
17. Copley MS, Berstan R, Mukherjee AJ, Dudd SN, Straker V, Payne S, Evershed RP. 2005b. Dairying in antiquity. III. Evidence from absorbed lipid residues dating to the British Neolithic. J Archaeol Sci. 32:523-546. (Pubitemid 40335047)
18. Cuatrecasas P, Lockwood DH, Caldwell JR. 1965. Lactase deficiency in the adult. A common occurrence. Lancet. 1:14-18.
19. Davey Smith G, Lawlor DA, Timpson NJ, Baban J, Kiessling M, Day IN, Ebrahim S. 2009. Lactase persistence-related genetic variant: Population substructure and health outcomes. Eur J Hum Genet. 17:357-367.
20. Desai HG, Gupte UV, Pradhan AG, Thakkar KD, Antia FP. 1970. Incidence of lactase deficiency in control subjects from India. Role of hereditary factors. Indian J Med Sci. 24:729-736.
21. Durham WH. 1991. Cultural mediation: The evolution of adult lactose absorption. In: Coevolution: Genes, culture and human diversity. Stanford (CA): Stanford University Press. p 629.
22. Eaaswarkhanth M, Haque I, Ravesh Z, et al. (12 co-Authors). 2010. Traces of sub-Saharan and Middle Eastern lineages in Indian Muslim populations. Eur J Hum Genet. 18:354-363.
23. Enattah NS, Jensen TG, Nielsen M, et al. 2008. Independent introduction of two lactase-persistence alleles into human populations reflects different history of adaptation to milk culture. Am J Hum Genet. 82:57-72. (Pubitemid 351735951)
24. Enattah NS, Sahi T, Savilahti E, Terwilliger JD, Peltonen L, Jarvela I. 2002. Identification of a variant associated with adult-Type hypolactasia. Nat Genet. 30:233-237.
25. Enattah NS, Trudeau A, Pimenoff V, et al. (22 co-Authors). 2007. Evidence of still-ongoing convergence evolution of the lactase persistence T-13910 alleles in humans. Am J Hum Genet. 81:615-625. (Pubitemid 47330220)
26. Food and Agriculture Organization of the United Nations. 2009.
27. FAO statistical yearbook. Rome (Italy): Food and Agriculture Organization of the United Nations.
28. Fuller D. 2003. An agricultural perspective on dravidian historical linguistics: Archaeological crop packages, livestock and dravidian crop vocabulary. In: Bellwood P, Renfrew C, editors. Assessing the languaging/farming dispersal hypothesis. Cambridge (MA): McDonald Institute for Archaeological Research Monographs.
29. Gerbault P, Moret C, Currat M, Sanchez-Mazas A. 2009. Impact of selection and demography on the diffusion of lactase persistence. PLoS One. 4:e6369.
30. Gibbs RA, Taylor JF, Van Tassell CP, et al. (91 co-Authors). 2009.
31. Gupta PS, Misra RC, Ramachandran KA, Sarin GS, Chutani HK. 1971. Intestinal disaccharidases activity in normal adult population in tropics. J Trop Med Hyg. 74:225-229.
32. Hanotte O, Bradley DG, Ochieng JW, Verjee Y, Hill EW, Rege JE. 2002. African pastoralism: Genetic imprints of origins and migrations. Science 296:336-339. (Pubitemid 34303686)
33. Hollox EJ, Poulter M, Zvarik M, Ferak V, Krause A, Jenkins T, Saha N, Kozlov AI, Swallow DM. 2001. Lactase haplotype diversity in the Old World. Am J Hum Genet. 68:160-172. (Pubitemid 32048371)
34. Ingram CJ, Elamin MF, Mulcare CA, et al. (11 co-Authors). 2007. A novel polymorphism associated with lactose tolerance in Africa: Multiple causes for lactase persistence? Hum Genet. 120:779-788. (Pubitemid 46128833)
35. Ingram CJ, Mulcare CA, Itan Y, Thomas MG, Swallow DM. 2009a. Lactose digestion and the evolutionary genetics of lactase persistence. Hum Genet. 124:579-591.
36. Ingram CJ, Raga TO, Tarekegn A, Browning SL, Elamin MF, Bekele E, Thomas MG, Weale ME, Bradman N, Swallow DM. 2009b. Multiple rare variants as a cause of a common phenotype: Several different lactase persistence associated alleles in a single ethnic group. J Mol Evol. 69:579-588.
37. Itan Y, Jones BL, Ingram CJ, Swallow DM, Thomas MG. 2010. A worldwide correlation of lactase persistence phenotype and genotypes. BMC Evol Biol. 10:36.
38. Itan Y, Powell A, Beaumont MA, Burger J, Thomas MG. 2009. The origins of lactase persistence in Europe. PLoS Comput Biol. 5:e1000491.
39. Jensen RG. 1995. Handbook of milk composition. San Diego (CA): Academic Press.
40. Johnson JD, Kretchmer N, Simoons FJ. 1974. Lactose malabsorption: Its biology and history. Adv Pediatr. 21:197-237.
41. Kivisild T, Rootsi S, Metspalu M, et al. (18 co-Authors). 2003. The genetic heritage of the earliest settlers persists both in Indian tribal and caste populations. Am J Hum Genet. 72:313-332. (Pubitemid 36194241)
42. Kumar S, Nagarajan M, Sandhu JS, Kumar N, Behl V. 2007.Phylogeography and domestication of Indian river buffalo. BMC Evol Biol. 7:186.
43. Lacey SW, Naim HY, Magness RR, Gething MJ, Sambrook JF. 1994. Expression of lactase-phlorizin hydrolase in sheep is regulated at the RNA level. Biochem J. 302(Pt 3):929-935. (Pubitemid 24289335)
44. Lewinsky RH, Jensen TG, Moller J, Stensballe A, Olsen J, Troelsen JT. 2005. T-13910 DNA variant associated with lactase persistence interacts with Oct-1 and stimulates lactase promoter activity in vitro. Hum Mol Genet. 14:3945-3953. (Pubitemid 43020095)
45. Li JZ, Absher DM, Tang H, et al. (11 co-Authors). 2008. Worldwide human relationships inferred from genome-wide patterns of variation. Science 319:1100-1104. (Pubitemid 351300793)
46. Loftus RT, MacHugh DE, Bradley DG, Sharp PM, Cunningham P. 1994. Evidence for two independent domestications of cattle. Proc Natl Acad Sci U S A. 91:2757-2761. (Pubitemid 24139427)
47. McCracken RD. 1971. Lactase. deficiency: An example of dietary evolution. Curr Anthropol. 12:479-517.
48. Meadow RH. 1993. Animal domestication in the Middle East: A revised view from the eastern margin. In: Possehl G, editor. Harappan civilization. New Delhi (India): Oxford University Press and India Book House. p 295-320.
49. Metspalu M, Kivisild T, Metspalu E, et al. (16 co-Authors). 2004. Most of the extant mtDNA boundaries in south and southwest Asia were likely shaped during the initial settlement of Eurasia by anatomically modern humans. BMC Genet. 5:26.
50. Mulcare CA, Weale ME, Jones AL, Connell B, Zeitlyn D, Tarekegn A, Swallow DM, Bradman N, Thomas MG. 2004. 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 lactasepersistence phenotype in Africans. Am J Hum Genet. 74:1102-1110. (Pubitemid 38669309)
51. Olds LC, Sibley E. 2003. Lactase persistence DNA variant enhances lactase promoter activity in vitro: Functional role as a cis regulatory element. Hum Mol Genet. 12:2333-2340. (Pubitemid 37160877)
52. Plimmer RH. 1906. On the presence of lactase in the intestines of animals and on the adaptation of the intestine to lactose. J Physiol. 35:20-31.
53. Possehl GL. 1997. The transformation of the Indus Civilization. J World Prehistory. 11:425-472.
54. Poulter M, Hollox E, Harvey CB, Mulcare C, Peuhkuri K, Kajander K, Sarner M, Korpela R, Swallow DM. 2003. The causal element for the lactase persistence/non-persistence polymorphism is located in a 1 Mb region of linkage disequilibrium in Europeans. Ann Hum Genet. 67:298-311. (Pubitemid 38312835)
55. R Core Development Team. 2009. R: A language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing.
56. Reddy V, Pershad J. 1972. Lactase deficiency in Indians. Am J Clin Nutr. 25:114-119.
57. Reich D, Thangaraj K, Patterson N, Price AL, Singh L 2009. Reconstructing Indian population history. Nature 461:489-494.
58. Sabeti PC, Reich DE, Higgins JM, et al. (17 co-Authors). 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832-837. (Pubitemid 35238568)
59. Sabeti PC, Varilly P, Fry B, et al. (247 co-Authors). 2007. Genomewide detection and characterization of positive selection in human populations. Nature 449:913-918. (Pubitemid 47598625)
60. Sahi T, Isokoski M, Jussila J, Launiala K, Pyorala K. 1973. Recessive inheritance of adult-Type lactose malabsorption. Lancet 2:823-826.
61. Sahoo S, Singh A, Himabindu G, et al. (12 co-Authors). 2006. A prehistory of Indian Y chromosomes: Evaluating demic diffusion scenarios. Proc Natl Acad Sci U S A. 103:843-848. (Pubitemid 43212185)
62. Sebastio G, Villa M, Sartorio R, Guzzetta V, Poggi V, Auricchio S, Boll W, Mantei N, Semenza G. 1989. Control of lactase in human adult-Type hypolactasia and in weaning rabbits and rats. Am J Hum Genet. 45:489-497. (Pubitemid 19261436)
63. Simoons FJ. 1970a. Primary adult lactose intolerance and the milking habit: A problem in biologic and cultural interrelations. II. A culture historical hypothesis. Am J Dig Dis. 15:695-710.
64. Simoons FJ. 1970b. The traditional limits of milking and milk use in southern Asia. Anthropos 65:547-593.
65. Simoons FJ. 1978. The geographic hypothesis and lactose malabsorption. A weighing of the evidence. Am J Dig Dis. 23: 963-980. (Pubitemid 9067097)
66. Swaminathan N, Mathan VI, Baker SJ, Radhakrishnan AN. 1970. Disaccharidase levels in jejunal biopsy specimens from American and south Indian control subjects and patients with tropical sprue. Clin Chim Acta. 30:707-712.
67. Tandon RK, Joshi YK, Singh DS, Narendranathan M, Balakrishnan V, Lal K. 1981. Lactose intolerance in North and South Indians. Am J Clin Nutr. 34:943-946. (Pubitemid 11077932)
68. Thangaraj K, Singh L, Reddy AG, Rao VR, Sehgal SC, Underhill PA, Pierson M, Frame IG, Hagelberg E. 2003. Genetic affinities of the Andaman Islanders, a vanishing human population. Curr Biol. 13:86-93. (Pubitemid 36154335)
69. Tishkoff SA, Reed FA, Ranciaro A, et al. (19 co-Authors). 2007. Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet. 39:31-40. (Pubitemid 46026499)
70. Troelsen JT, Olsen J, Moller J, Sjostrom H. 2003. An upstream polymorphism associated with lactase persistence has increased enhancer activity. Gastroenterology 125:1686-1694. (Pubitemid 37500433)
71. Troy CS, MacHugh DE, Bailey JF, Magee DA, Loftus RT, Cunningham P, Chamberlain AT, Sykes BC, Bradley DG. 2001.Genetic evidence for Near-Eastern origins of European cattle. Nature 410:1088-1091. (Pubitemid 32391038)
72. Voight BF, Kudaravalli S, Wen X, Pritchard JK. 2006. A map of recent positive selection in the human genome. PLoS Biol. 4:e72.
73. Wa19281165106 Wigginton JE, Cutler DJ, Abecasis GR. 2005. A note on exact tests of Hardy-Weinberg equilibrium. Am J Hum Genet. 76:887-893. (Pubitemid 40563110)