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Genetic evidence in support of a shared Eurasian-North African dairying origin

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Abstract

The process by which pastoralism and agriculture spread from the Fertile Crescent over the past 10,000 years has been the subject of intense investigation by geneticists, linguists and archaeologists. However, no consensus has been reached as to whether this Neolithic transition is best characterized by a demic diffusion (with a significant genetic input from migrating farmers) or a cultural diffusion (without substantial migration of farmers). Milk consumption and thus lactose tolerance are assumed to have spread with pastoralism and we propose that by looking at the relevant mutations in and around the lactase gene in human populations, we can gain insight into the origin(s) and spread of dairying. We genotyped the putatively causal allele for lactose tolerance (−13910T) and constructed haplotypes from several polymorphisms in and around the lactase gene (LCT) in three North African Berber populations and compared our results with previously published data. We found that the frequency of the −13910T allele predicts the frequency of lactose tolerance in several Eurasian and North African Berber populations but not in most sub-Saharan African populations. Our analyses suggest that contemporary Berber populations possess the genetic signature of a past migration of pastoralists from the Middle East and that they share a dairying origin with Europeans and Asians, but not with sub-Saharan Africans.

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References

  • Ammerman A, Cavalli-Sforza LL (1973) A population model for the diffusion of early farming in Europe. In: Renfrew C (ed) The explanation of culture change: models in prehistory. Duckworth, London, pp348–358

  • Ammerman A, Cavalli-Sforza LL (1984) The neolithic transition and the genetics of populations in Europe. Princeton University Press, Princeton

    Google Scholar 

  • Arredi B, Poloni ES, Paracchini S, Zerjal T, Fathallah DM, Makrelouf M, Pascali VL, Novelletto A, Tyler-Smith C (2004) A predominantly neolithic origin for Y-chromosomal DNA variation in North Africa. Am J Hum Genet 75:338–345

    Google Scholar 

  • Barbujani G, Pilastro A, De Domenico S, Renfrew C (1994) Genetic variation in North Africa and Eurasia: neolithic demic diffusion vs. paleolithic colonisation. Am J Phys Anthropol 95:137–154

    Google Scholar 

  • Barker G (2003) Transitions to farming and pastoralism in North Africa. In: Bellwood P, Renfrew C (eds) Examining the farming/language dispersal hypothesis. McDonald Institute for Archaeological Research, Cambridge, pp 151–161

  • Bernus E (1990) Dates, dromedaries, and drought: diversification in tuareg pastoral systems. In: Galaty JG, Johnson DL (eds) The world of pastoralism: herding systems in comparative perspective. Belhaven Press, London, pp149–176

  • 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

    Google Scholar 

  • Blench RM (2001) Pastoralism in the new millennium. FAO: animal health and production series, No. 150

  • Blench RM (2001) Types of language spread and their archaeological correlates: the example of Berber. Origini 23:169–189

    Google Scholar 

  • Bosch E, Calafell F, Perez-Lezaun A, Comas D, Mateu E, Bertranpetit J (1997) Population history of North Africa: evidence from classical genetic markers. Hum Biol 69:295–311

    Google Scholar 

  • Bosch E, Calafell F, Santos FR, Perez-Lezaun A, Comas D, Benchemsi N, Tyler-Smith C, Bertranpetit J (1999) Variation in short tandem repeats is deeply structured by genetic background on the human Y chromosome. Am J Hum Genet 65:1623–1638

    Article  CAS  PubMed  Google Scholar 

  • Bosch E, Calafell F, Perez-Lezaun A, Clarimon J, Comas D, Mateu E, Martinez-Arias R, Morera B, Brakez Z, Akhayat O et al (2000) Genetic structure of north-west Africa revealed by STR analysis. Eur J Hum Genet 8:360–366

    Google Scholar 

  • Bosch E, Calafell F, Comas D, Oefner PJ, Underhill PA, Bertranpetit J (2001) 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 68:1019–1029

    Article  CAS  PubMed  Google Scholar 

  • Brett M, Fentress E (1996) The berbers. Blackwell, Cambridge

  • Camps G (1982) Beginnings of pastoralism and cultivation in North-West Africa and the Sahara: origins of the berbers. In: Clark JD (ed) The Cambridge History of Africa, vol 1. Cambridge University Press, Cambridge, pp548–623

  • Camps-Fabrer H (1989) Capsien du Maghreb et Natoufien du Proche Orient. Traveaux du LAPMO 1989:1–104

    Google Scholar 

  • Clutton-Brock J (1993) The spread of domestic animals in Africa. In: Shaw T, Sinclair P, Andah B, Okpoko A (eds) The archaeology of Africa: food, metals and towns. Routledge, London

  • Comas D, Calafell F, Benchemsi N, Helal A, Lefranc G, Stoneking M, Batzer M, Bertranpetit J, Sajantila A (2000) Alu insertion polymorphisms in NW Africa and the Iberian Peninsula: evidence for a strong genetic boundary through the Gibraltar Straits. Hum Genet 107:312–319

    Google Scholar 

  • Cordaux R, Deepa E, Vishwanathan H, Stoneking M (2004) Genetic evidence for the demic diffusion of agriculture to India. Science 304:1125

    Google Scholar 

  • Cruciani F, Santolamazza P, Shen P, Macaulay V, Moral P, Olckers A, Modiano D, Holmes S, Destro-Bisol G, Coia V, Wallace DC, Oefner PJ, Torroni A, Cavalli-Sforza LL, Scozzari R, Underhill PA (2002) A back migration from Asia to sub-Saharan Africa is supported by high-resolution analysis of human Y-chromosome haplotypes. Am J Hum Genet 70:1197–1214

    Google Scholar 

  • Diakonoff I (1998) The earliest semitic society: linguistic data. J Semitic Stud 48:209–219

    Google Scholar 

  • Diamond J (1998) Guns, germs and steel: a short history of everybody for the last 13,000 years. Vintage, London

    Google Scholar 

  • Edmonson MS (1961) Neolithic diffusion rates. Curr Anthropol 2:71–102

    Google Scholar 

  • Ehret C (1984) Historical/linguistic evidence for early African food production. In: Clark JD, Brandt SA (eds) From hunters to farmers: the causes and consequences of food production in Africa. University of California Press, Berkeley, pp 26–35

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Flores C, Maca-Meyer N, Gonzalez AM, Cabrera VM (2000a) Northwest African distribution of the CD4/Alu microsatellite haplotypes. Ann Human Genet 64:321–327

    Google Scholar 

  • Flores C, Hernandez M, Gonzalez AM, Cabrera VM (2000b) Genetic affinities among human populations inhabiting the subsaharan area, northwest Africa, and the Iberian peninsula. In: Arnaiz-Villena A (ed) Prehistoric Iberia: genetics, anthropology and linguistics. Kluwer/Plenum, New York, pp 33–50

  • Flores C, Maca-Meyer N, Perez JA, Hernandez M, Cabrera VM (2001) Y-chromosome differentiation in Northwest Africa. Hum Biol 73:513–524

    Google Scholar 

  • Goudet J, Raymond M, de Meeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940

    CAS  PubMed  Google Scholar 

  • Greenberg JH (1963) The languages of Africa (Publication No. 25 of the Indiana University Research Center in Anthropology, Folklore, and Linguistics Publications), Bloomington, Indiana

  • Harvey CB, Pratt WS, Islam I, Whitehouse DB, Swallow DM (1995) DNA polymorphisms in the lactase gene: linkage disequilibrium across the 70 kb region. Eur J Hum Genet 3:27–41

    Google Scholar 

  • Harvey CB, Hollox EJ, Poulter M, Wang Y, Rossi M, Auricchio S, Iqbal TH, Cooper BT, Barton R, Sarner M, Korpela R, Swallow DM (1998) Lactase haplotype frequencies in Caucasians: association with the lactase persistence/non-persistence polymorphism. Ann Hum Genet 62:215–223

    Google Scholar 

  • Higgs E (1967) Domestic animals. In: McBurney C (ed) The Haua Fteah (Cyrenaica) and the stone age of the south-east Mediterranean. Cambridge University Press, Cambridge, pp313–319

  • Holl AFC (1998) The dawn of African pastoralisms: an introductory note. J Anthropol Archaeol 17:81–96

    Google Scholar 

  • Hollox EJ, Poulter M, Wang Y, Krause A, Swallow DM (1999) Common polymorphism in a highly variable region upstream of the human lactase gene affects DNA-protein interactions. Eur J Hum Genet 7:791–800

    Google Scholar 

  • 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

    Google Scholar 

  • Lubell D (1984) Paleoenvironments and epi-paleolithic economies in the maghreb (ca. 20,000 to 5000 BP). In: Clark JD, Brandt SA (eds) From hunters to farmers: the causes and consequences of food production in Africa. University of California Press, Berkeley, pp 41–56

  • Macaulay V, Richards M, Hickey E, Vega E, Cruciani F, Guida V, Scozzari R, Bonne-Tamir B, Sykes B, Torroni A (1999) The emerging tree of west Eurasian mtDNAs: a synthesis of control-region sequences and RFLPs. Am J Hum Genet 64:232–249

    Article  CAS  PubMed  Google Scholar 

  • MacDonald KC (1998) Archaeology, language and the peopling of West Africa: a consideration of the evidence. In: Blench RM, Spriggs M (eds) Archaeology and language II: correlating archaeological and linguistic hypotheses. Routledge, London, pp 33–66

  • McBurney C (1967) The Haua Fteah (Cyrenaica) and the stone age of the south-east Mediterranean. Cambridge University Press, Cambridge

  • McCracken RD (1971) Lactase deficiency: an example of dietary evolution. Curr Anthropol 12:479–500

    Google Scholar 

  • McEvedy C (1980) The Penguin atlas of African history. Penguin Books, New York

    Google Scholar 

  • Menozzi P, Piazza A, Cavalli-Sforza L (1978) Synthetic maps of human gene frequencies in Europeans. Science 201:786–792

    Google Scholar 

  • Militarev A (2003) The prehistory of a dispersal: the proto-Afrasian (Afroasiatic) farming lexicon. In: Bellwood P, Renfrew C (eds) Examining the farming/language dispersal hypothesis. McDonald Institute for Archaeological Research, Cambridge, pp 135–150

  • 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 lactase-persistence phenotype in Africans. Am J Hum Genet 74:1102–1110

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Phillipson D (1993) African archaeology, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • 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

    Google Scholar 

  • Rando JC, Pinto F, Gonzalez AM, Hernandez M, Larruga JM, Cabrera VM, Bandelt HJ (1998) Mitochondrial DNA analysis of northwest African populations reveals genetic exchanges with European, near-eastern, and sub-Saharan populations. Ann Hum Genet 62:531–550

    Article  Google Scholar 

  • Renfrew C (1991) Before babel: speculations on the origins of linguistic diversity. Camb Archaeol J 1:3–23

    Google Scholar 

  • Roubet C (1978) Une économie pastorale, pré-agricole en Algérie orientale: le Néolithique de tradition capsienne. Anthropologie 82:583–586

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: A software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland

  • Simoni L, Gueresi P, Pettener D, Barbujani G (1999) Patterns of gene flow inferred from genetic distances in the Mediterranean region. Hum Biol 71:399–415

    Google Scholar 

  • 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

    Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    CAS  PubMed  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed  Google Scholar 

  • Troelsen J, Olsen J, Moller J, Sjostrom H (2003) An upstream polymorphism associated with lactase persistence has increased enhancer activity. Gastroenterology 125:1686–1694

    CAS  PubMed  Google Scholar 

  • Wang Y, Harvey CB, Pratt WS, Sams VR, Sarner M, Rossi M, Auricchio S, Swallow DM (1995) The lactase persistence/nonpersistence polymorphism is controlled by a cis-acting element. Hum Mol Genet 4:657–662

    Google Scholar 

  • Zvelebil M, Zvelebil KV (1988) Agricultural transition and Indo-European dispersal. Antiquity 62:574–583

    Google Scholar 

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Acknowledgements

We are grateful to all of the participants who donated blood samples, and to the people who aided in sample collection. In particular we would like to thank M. Abdellatif Baali and M. Kamel Hilali for the samples from Amizmiz; M. Pedro Moral, Mostafa Kandil and Nourdin Harich for the samples from Middle Atlas; Ms. Anne Cambon-Thomsen, Ghania Hariti and M.S. Issad for the samples from Ghardaia. This research received partial support within the framework of the OMLL (The Origin of Man, Language and Languages, EUROCORES Program) and benefited from funding from the CNRS (Centre National de la Recherche Scientifique, France). We thank Mark Stoneking and Dallas Swallow for helpful comments and Nic Timpson for technical assistance. SM was supported by a Wüest-Zirfass scholarship and a grant from the Deutscher Akademischer Austauschdienst (DAAD). This paper is presented in memory of Ryk Ward.

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Authors and Affiliations

  1. Institute of Biological Anthropology, University of Oxford, Oxford, UK

    Sean Myles, Nourdine Bouzekri, Eden Haverfield & Ryk Ward

  2. Department of Evolutionary Genetics, Max-Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany

    Sean Myles

  3. Department of Human Genetics, University of Chicago, 920 East 58th Street, Chicago, IL, 60637, USA

    Eden Haverfield

  4. Laboratoire d’Ecologie Humaine, Faculté des Sciences-Semlalia, Université Cadi Ayyad, Morocco

    Mohamed Cherkaoui

  5. Centre d’Anthropologie CNRS,, University of Toulouse, UMR 8555, France

    Jean-Michel Dugoujon

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  1. Sean Myles
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Correspondence to Sean Myles.

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Myles, S., Bouzekri, N., Haverfield, E. et al. Genetic evidence in support of a shared Eurasian-North African dairying origin. Hum Genet 117, 34–42 (2005). https://doi.org/10.1007/s00439-005-1266-3

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