The origins of lactase persistence in Europe

PLoS Computational Biology

Volumn 5, Issue 8, 2009, Pages

  Itan, Yuval ^a   Powell, Adam ^a   Beaumont, Mark A ^b   Burger, Joachim ^c   Thomas, Mark G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BAYESIAN NETWORKS;

APPROXIMATE BAYESIAN; BAYESIAN COMPUTATION; CENTRAL EUROPE; COEVOLUTIONARY MODELS; COMPUTER SIMULATION MODELING; FRESH MILKS; GENETIC MARKERS; GEOGRAPHICS; HAPLOTYPES; POSITIVE SELECTION;

GENES;

LACTASE; LACTOSE; VITAMIN D;

AGRICULTURAL WORKER; ARTICLE; CULTURAL PERIOD; DAIRYING; DEMOGRAPHY; EUROPE; GENE FREQUENCY; GENE POOL; GEOGRAPHIC DISTRIBUTION; HUMAN; MOLECULAR EVOLUTION; SIMULATION; ALLELE; BAYES THEOREM; BIOLOGY; CHEMISTRY; COMPUTER SIMULATION; DIET; GENETIC MARKER; GENETIC POLYMORPHISM; GENETICS; GEOGRAPHY; HAPLOTYPE; METABOLISM; METHODOLOGY; PHYSIOLOGY;

ALLELES; BAYES THEOREM; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; DIET; EUROPE; EVOLUTION, MOLECULAR; GENE FREQUENCY; GENETIC MARKERS; GEOGRAPHY; HAPLOTYPES; HUMANS; LACTASE; LACTOSE; POLYMORPHISM, GENETIC; VITAMIN D;

EID: 70149112524     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000491     Document Type: Article

References (82)

1. Swallow DM (2003) Genetics of lactase persistence and lactose intolerance. Annu Rev Genet 37: 197-219.
2. Ingram CJ, Elamin MF, Mulcare CA, Weale ME, Tarekegn A, et al. (2007) A novel polymorphism associated with lactose tolerance in Africa: multiple causes for lactase persistence? Hum Genet 120: 779-788.
3. Mulcare CA, Weale ME, Jones AL, Connell B, Zeitlyn D, et al. (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 lactase-persistence phenotype in Africans. Am J Hum Genet 74: 1102-1110. (Pubitemid 38669309)
4. Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC, et al. (2007) Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet 39: 31-40. (Pubitemid 46026499)
5. Enattah NS, Sahi T, Savilahti E, Terwilliger JD, Peltonen L, et al. (2002) Identification of a variant associated with adult-type hypolactasia. Nat Genet 30: 233-237. (Pubitemid 34887722)
6. Lewinsky RH, Jensen TG, Moller J, Stensballe A, Olsen J, et al. (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)
7. Mulcare CA (2006) The Evolution of the Lactase Persistence Phenotype. London: University of London. 311 p.
8. Bersaglieri T, Sabeti PC, Patterson N, Vanderploeg T, Schaffner SF, et al. (2004) Genetic signatures of strong recent positive selection at the lactase gene. Am J Hum Genet 74: 1111-1120. (Pubitemid 38669310)
9. Ingram CJ, Mulcare CA, Itan Y, Thomas MG, Swallow DM (2008) Population and molecular genetics of lactase persistence. Journal of Human Genetics In Press.
10. Enattah NS, Jensen TG, Nielsen M, Lewinski R, Kuokkanen 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)
11. Enattah NS, Trudeau A, Pimenoff V, Maiuri L, Auricchio S, et al. (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)
12. Coelho M, Luiselli D, Bertorelle G, Lopes AI, Seixas S, et al. (2005) Microsatellite variation and evolution of human lactase persistence. Hum Genet 117: 329-339. (Pubitemid 41194559)
13. Kretchmer N (1972) Lactose and lactase. Sci Am 227: 71-78.
14. Simoons FJ (1970) 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.
15. McCracken RD (1971) Origins and implications of the distribution of adult lactase deficiency in human populations. J Trop Pediatr Environ Child Health 17: 7-10.
16. Aoki K (1986) A stochastic model of gene-culture coevolution suggested by the "culture historical hypothesis" for the evolution of adult lactose absorption in humans. Proc Natl Acad Sci U S A 83: 2929-2933.
17. Bayless TM, Paige DM, Ferry GD (1971) Lactose intolerance and milk drinking habits. Gastroenterology 60: 605-608.
18. Nei M, Saitou N (1986) Genetic relationship of human populations and ethnic differences in reaction to drugs and food. Prog Clin Biol Res 214: 21-37.
19. McCracken RD (1971) Lactase Deficiency: An Example of Dietary Evolution. Current Anthropology 12: 497-517.
20. Flatz G, Rotthauwe HW (1973) Lactose nutrition and natural selection. Lancet 2: 76-77.
21. Vigne JD, Helmer D (2007) Was milk a "secondary product" in the Old World Neolithisation process? Its role in the domestication of cattle, sheep and goats. Anthropozoologica 42: 9.
22. Bartosiewicz L (2007) Mammalian Bone. In: Whittle A, ed. The early Neolithic on the Great Hungarian plain Investigations of the Körös culture site of Ecsegfalva 23, County Békés. Budapest.
23. Craig OE, J. C, Heron CP, Willis LH, Taylor G, et al. (2005) Did the first farmers of central and eastern Europe produce dairy foods? Antiquity 79: 882-894.
24. Copley MS, Berstan R, Dudd SN, Docherty G, Mukherjee AJ, et al. (2003) Direct chemical evidence for widespread dairying in prehistoric Britain. Proc Natl Acad Sci U S A 100: 1524-1529. (Pubitemid 36254480)
25. Copley MS, Berstan R, Mukherjee AJ, Dudd SN, Straker V, et al. (2005) Dairying in antiquity. III. Evidence from absorbed lipid residues dating to the British Neolithic. Journal of Archaeological Science 32: 523-546. (Pubitemid 40335047)
26. Evershed RP, Payne S, Sherratt AG, Copley MS, Coolidge J, et al. (2008) Earliest date for milk use in the Near East and southeastern Europe linked to cattle herding. Nature 455: 528-531.
27. Burger J, Kirchner M, Bramanti B, HaakW, 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)
28. Vigne J-D (2006) Maîtrise et usages de l'élevage et des animaux domestiques au Néolithique: quelques illustrations au Proche-Orient et en Europe. In: Guilaine J, ed. Populations néolithiques et environnements. Paris: Errance éd. pp 87-114.
29. Edmonds CA, Lillie AS, Cavalli-Sforza LL (2004) Mutations arising in the wave front of an expanding population. Proc Natl Acad Sci U S A 101: 975-979.
30. Klopfstein S, Currat M, Excoffier L (2006) The fate of mutations surfing on the wave of a range expansion. Mol Biol Evol 23: 482-490. (Pubitemid 43278259)
31. Pinhasi R, Fort J, Ammerman AJ (2005) Tracing the origin and spread of agriculture in Europe. PLoS Biol 3: e410. (Pubitemid 41796342)
32. Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162: 2025-2035. (Pubitemid 36114682)
33. Barbujani G, Sokal RR, Oden NL (1995) Indo-European origins: a computer-simulation test of five hypotheses. Am J Phys Anthropol 96: 109-132.
34. Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20: 76-86. (Pubitemid 36077902)
35. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13: 853-864.
36. Currat M, Excoffier L (2005) The effect of the Neolithic expansion on European molecular diversity. Proc Biol Sci 272: 679-688. (Pubitemid 41411125)
37. Bellwood PS (2005) The first farmers : the origins of agricultural societies. Malden, MA: Blackwell Pub.
38. Colledge S, Conolly J, Shennan S (2004) Archaeobotanical evidence for the spread of farming in the Eastern Mediterranean. Curr Anthropol 45: S35-S58.
39. Hassan FA (1981) Demographic Archaeology. New York: Academic Press. 298 p.
40. Beja-Pereira A, Luikart G, England PR, Bradley DG, Jann OC, et al. (2003) Gene-culture coevolution between cattle milk protein genes and human lactase genes. Nat Genet 35: 311-313. (Pubitemid 37486911)
41. Simoons F (1980) Effects of culture: geographical and historical approaches. Int J Obes 4: 387-394.
42. Simoons FJ (1978) The geographic hypothesis and lactose malabsorption. A weighing of the evidence. Am J Dig Dis 23: 963-980.
43. Bloom G, Sherman P (2005) Dairying barriers affect the distribution of lactose malabsorption. Evolution and Human Behavior 26: 301.e301-301.e333. (Pubitemid 40912069)
44. Simoons FJ (2001) Persistence of lactase activity among northern europeans: A weighing of the evidence for the calcium absorption hypothesis. Ecology of Food and Nutrition 40: 397-469.
45. Röhrs M, Herre W (1961) Zur Frühentwicklung der Haustiere. Die Tierreste der Neolithischen Siedlung Fikirtepe am Kleinasiatischen Gestade des Bosporus. Zeitschrift für Tierzüchtung und Züchtungsbiologie. pp 110-127.
46. Boessneck JVD, Driesch A (1979) Die Tierknochenfunde aus der Neolithischen Siedlung auf dem Fikirtepe bei Kadiköy am Marmarameer. Munich: Munich, Inst. für Domestikationsforschung.
47. Buttenhuis H (1995) The Faunal Remains. In: Roodenberg J, ed. The Ilipinar Excavations I, Five Seasons of Fieldwork in NW Anatolia, 1987-91. Istanbul: Nederlands Historisch-Archaeologisch Instituut. pp 151-156.
48. Benecke N (1998) Animal Remains From the Neolithic and Bronze Age Settlements at Kirklareli (Turkish Thrace). In: Buitenhuis H, ed. Archaeozoology of the Near East III: Groningen ARC Publicaties. pp 172-179.
49. Bartosiewicz L (2005) Animals, environment, and culture in the Neolithic of the Carpathian Basin and adjacent areas. In: Bailey D, Whittle A, Cummings V, eds. (un)settling the Neolithic: Oxbow 2005. pp 51-63.
50. Benecke N (1994) Der Mensch und seine Haustiere. Stuttgart: Theiss.
51. Arbogast RM (1994) Premiers élevages néolithqiues du Nord-Est de la France. Liège: Ètudes et Rech.Arch.Univ. Liège.
52. Balasse M, Tresset A (2002) Early weaning of Neolithic domestic cattle (Bercy, France) revealed by intra-tooth variation in nitrogen isotope ratios. Journal of Archaeological Science 29: 853-859. (Pubitemid 34949626)
53. Tresset A (1996) Le rôle des relations homme/animal dans l'évolution économique et culturelle des sociétés des V-VI millénaires en Bassin Parisien [Thèse Doc.]. Paris: Université de Paris I, Panthéon- Sorbonne.
54. Tresset A (1997) L'approvisionnement carné Cerny dans le contexte néolithique du Bassin Parisien. In: Constatin C, Mordant D, Simonin D, eds. La Culture de Cerny: Nouvelle économie, nouvelle société au Néolithique. Nemours: Actes du colloque de Nemours. pp 299-314.
55. Benecke N (1994) Archäozoologische Studien zur Entwicklung der Haustierhaltung in Mitteleuropa und Südskandinavien von den Anfängen bis zum ausgehenden Mittelalter. Berlin.
56. Cribb RLD (1987) The Logic of the herd: A computer simulation of archaeological herd structure. Journal AnthrArch 6: 367.
57. Vigne JD, Helmer D (2007) Was milk a "secondary product" in the Old World Neolithisation process? Its role in the domestication of cattle, sheep and goats. Anthropozoologica 42: 9-40.
58. Strabo (1969) The Geography of Strabo in eight volumes with an English translation of H.L.Jones. London, Cambridge, Mass.: Henry G. Bohn.
59. Pavúk J (2005) Typologische Geschichte der Linearbandkeramik. In: Lüning J, Friedrich C, Zimmermann A, eds. Die Bandkeramik im 21 Jahrhundert: Symposium in der Abtei Brauweiler bei Köln. pp 17-39.
60. Bánffy E (2004) The 6th Millennium BC boundary in Western Transdanubia and its role in the Central European Neolithic transition (The Szentgyörgyvölgy-Pityerdomb Settlement). Budapest: Varia Arch. Hungarica.
61. Baldia MO. Breaking unnatural barriers: Comparative archaeology, climate, and culture change in Central and Northern Europe (6000-2000 BC). Paper presented in the Session "Comparative archeology and paleoclimatology: sociocultural responses to a changing world" under the theme "Past human environments in modern contexts" at the Fifth World Archaeology Congress, June 23, 2003, Washington DC, USA; 2003; Washington DC, USA.
62. Lüning J (2005) Bandkeramische Hofplätze und absolute Chronologie der Bandkeramik. In: Lüning J, Friedrich C, Zimmermann A, eds. Die Bandkeramik im 21 Jahrhundert: Symposium in der Abtei Brauweiler bei Köln. pp 49-74.
63. Weiss KM (2004) The unkindest cup. Lancet 363: 1489-1490.
64. Hollox EJ, Poulter M, Zvarik M, Ferak V, Krause A, et al. (2001) Lactase haplotype diversity in the Old World. Am J Hum Genet 68: 160-172. (Pubitemid 32048371)
65. Akey JM, Eberle MA, Rieder MJ, Carlson CS, Shriver MD, et al. (2004) Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol 2: e286.
66. Özdogan M, Basgelen N (1999) Neolithic in Turkey. The cradle of civilization. Istanbul: Ancient Anatolians Civilizations Series 3.
67. Cavalli-Sforza LL, Menozzi P, Piazza A (1994) The history and geography of human genes. Princeton, N.J.: Princeton University Press.
68. Özdogan M (2007) Von Zentralanatolien nach Europa. Die Ausbreitung der neolithischen Lebensweise. In: Landesmuseum B, ed. Vor 12000 Jahren in Anatolien- Die ältesten Monumente der Menschheit. Stuttgart: Konrad Theiss Verlag. pp 177-189.
69. Troy CS, MacHugh DE, Bailey JF, Magee DA, Loftus RT, et al. (2001) Genetic evidence for Near-Eastern origins of European cattle. Nature 410: 1088-1091. (Pubitemid 32391038)
70. Bollongino R, Edwards CJ, Alt KW, Burger J, Bradley DG (2006) Early history of European domestic cattle as revealed by ancient DNA. Biol Lett 2: 155-159. (Pubitemid 43384699)
71. Edwards CJ, Bollongino R, Scheu A, Chamberlain A, Tresset A, et al. (2007) Mitochondrial DNA analysis shows a Near Eastern Neolithic origin for domestic cattle and no indication of domestication of European aurochs. Proc Biol Sci 274: 1377-1385. (Pubitemid 47056686)
72. Achilli A, Olivieri A, Pellecchia M, Uboldi C, Colli L, et al. (2008) Mitochondrial genomes of extinct aurochs survive in domestic cattle. Curr Biol 18: R157-158. (Pubitemid 351258346)
73. Achilli A, Bonfiglio S, Olivieri A, Malusa A, Pala M, et al. (2009) The multifaceted origin of taurine cattle reflected by the mitochondrial genome. PLoS One 4: e5753.
74. Spielmann KA, Eder JF (1994) Hunters and Farmers : Then and Now. Annu Rev Anthropol 23: 303-323.
75. Mace R (1993) Transitions Between Cultivation and Pastoralism in Sub-Saharan Africa. Current Anthropology 34: 363-382.
76. Weale ME, Yepiskoposyan L, Jager RF, Hovhannisyan N, Khudoyan A, et al. (2001) Armenian Y chromosome haplotypes reveal strong regional structure within a single ethno-national group. Hum Genet 109: 659-674. (Pubitemid 34051421)
77. Thomas MG, Barnes I, Weale ME, Jones AL, Forster P, et al. (2008) New genetic evidence supports isolation and drift in the Ladin communities of the South Tyrolean Alps but not an ancient origin in the Middle East. Eur J Hum Genet 16: 124-134. (Pubitemid 350269246)
78. Clark JGD (1965) Radiocarbon dating and the expansion of farming culture from the Near East over Europe. Proc Prehist Soc 31: 57-73.
79. Haldane JBS (1927) The mathematical theory of natural and artificial selection. Part V. Selection and mutation. Proc Camb Phil Soc 23.
80. Maynard Smith J (1998) Evolutionary genetics. Oxford; New York: Oxford University Press. pp xiv, 330.
81. Thomas MG, Stumpf MP, Harke H (2006) Evidence for an apartheid-like social structure in early Anglo-Saxon England. Proc Biol Sci 273: 2651-2657.
82. Tremblay M, Vezina H (2000) New estimates of intergenerational time intervals for the calculation of age and origins of mutations. Am J Hum Genet 66: 651-658. (Pubitemid 30468841)