Advertisement

Human Genetics

, Volume 117, Issue 1, pp 34–42 | Cite as

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

  • Sean MylesEmail author
  • Nourdine Bouzekri
  • Eden Haverfield
  • Mohamed Cherkaoui
  • Jean-Michel Dugoujon
  • Ryk Ward
Original Investigation
First Online:

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.

Keywords

Lactase Lactose Tolerance Local Ancestry Causal Allele North African Population 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Notes

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.

References

  1. 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, pp348–358Google Scholar
  2. Ammerman A, Cavalli-Sforza LL (1984) The neolithic transition and the genetics of populations in Europe. Princeton University Press, PrincetonGoogle Scholar
  3. 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 75:338–345Google Scholar
  4. 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 95:137–154Google Scholar
  5. 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 151–161Google Scholar
  6. 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, pp149–176Google Scholar
  7. 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 74:1111–1120Google Scholar
  8. Blench RM (2001) Pastoralism in the new millennium. FAO: animal health and production series, No. 150Google Scholar
  9. Blench RM (2001) Types of language spread and their archaeological correlates: the example of Berber. Origini 23:169–189Google Scholar
  10. 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 69:295–311Google Scholar
  11. 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 65:1623–1638CrossRefPubMedGoogle Scholar
  12. 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 8:360–366Google Scholar
  13. 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 68:1019–1029CrossRefPubMedGoogle Scholar
  14. Brett M, Fentress E (1996) The berbers. Blackwell, CambridgeGoogle Scholar
  15. 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, pp548–623Google Scholar
  16. Camps-Fabrer H (1989) Capsien du Maghreb et Natoufien du Proche Orient. Traveaux du LAPMO 1989:1–104Google Scholar
  17. 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, LondonGoogle Scholar
  18. 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 107:312–319Google Scholar
  19. Cordaux R, Deepa E, Vishwanathan H, Stoneking M (2004) Genetic evidence for the demic diffusion of agriculture to India. Science 304:1125Google Scholar
  20. 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 70:1197–1214Google Scholar
  21. Diakonoff I (1998) The earliest semitic society: linguistic data. J Semitic Stud 48:209–219Google Scholar
  22. Diamond J (1998) Guns, germs and steel: a short history of everybody for the last 13,000 years. Vintage, LondonGoogle Scholar
  23. Edmonson MS (1961) Neolithic diffusion rates. Curr Anthropol 2:71–102Google Scholar
  24. 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 26–35Google Scholar
  25. Enattah NS, Sahi T, Savilahti E, Terwilliger JD, Peltonen L, Jarvela I (2002) Identification of a variant associated with adult-type hypolactasia. Nat Genet 30:233–237CrossRefPubMedGoogle Scholar
  26. Flores C, Maca-Meyer N, Gonzalez AM, Cabrera VM (2000a) Northwest African distribution of the CD4/Alu microsatellite haplotypes. Ann Human Genet 64:321–327Google Scholar
  27. 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 33–50Google Scholar
  28. Flores C, Maca-Meyer N, Perez JA, Hernandez M, Cabrera VM (2001) Y-chromosome differentiation in Northwest Africa. Hum Biol 73:513–524Google Scholar
  29. Goudet J, Raymond M, de Meeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940PubMedGoogle Scholar
  30. Greenberg JH (1963) The languages of Africa (Publication No. 25 of the Indiana University Research Center in Anthropology, Folklore, and Linguistics Publications), Bloomington, IndianaGoogle Scholar
  31. 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 3:27–41Google Scholar
  32. 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 62:215–223Google Scholar
  33. 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, pp313–319Google Scholar
  34. Holl AFC (1998) The dawn of African pastoralisms: an introductory note. J Anthropol Archaeol 17:81–96Google Scholar
  35. 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 7:791–800Google Scholar
  36. 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 68:160–172Google Scholar
  37. 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 41–56Google Scholar
  38. 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 64:232–249CrossRefPubMedGoogle Scholar
  39. 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 33–66Google Scholar
  40. McBurney C (1967) The Haua Fteah (Cyrenaica) and the stone age of the south-east Mediterranean. Cambridge University Press, CambridgeGoogle Scholar
  41. McCracken RD (1971) Lactase deficiency: an example of dietary evolution. Curr Anthropol 12:479–500Google Scholar
  42. McEvedy C (1980) The Penguin atlas of African history. Penguin Books, New YorkGoogle Scholar
  43. Menozzi P, Piazza A, Cavalli-Sforza L (1978) Synthetic maps of human gene frequencies in Europeans. Science 201:786–792Google Scholar
  44. 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 135–150Google Scholar
  45. 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 74:1102–1110Google Scholar
  46. 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 12:2333–2340CrossRefPubMedGoogle Scholar
  47. Phillipson D (1993) African archaeology, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  48. 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 67:298–311Google Scholar
  49. 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 62:531–550CrossRefGoogle Scholar
  50. Renfrew C (1991) Before babel: speculations on the origins of linguistic diversity. Camb Archaeol J 1:3–23Google Scholar
  51. Roubet C (1978) Une économie pastorale, pré-agricole en Algérie orientale: le Néolithique de tradition capsienne. Anthropologie 82:583–586Google Scholar
  52. 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, SwitzerlandGoogle Scholar
  53. Simoni L, Gueresi P, Pettener D, Barbujani G (1999) Patterns of gene flow inferred from genetic distances in the Mediterranean region. Hum Biol 71:399–415Google Scholar
  54. 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 15:695–710Google Scholar
  55. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedGoogle Scholar
  56. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989CrossRefPubMedGoogle Scholar
  57. Troelsen J, Olsen J, Moller J, Sjostrom H (2003) An upstream polymorphism associated with lactase persistence has increased enhancer activity. Gastroenterology 125:1686–1694PubMedGoogle Scholar
  58. 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 4:657–662Google Scholar
  59. Zvelebil M, Zvelebil KV (1988) Agricultural transition and Indo-European dispersal. Antiquity 62:574–583 Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Sean Myles
    • 1
    • 2
    Email author
  • Nourdine Bouzekri
    • 1
  • Eden Haverfield
    • 1
    • 3
  • Mohamed Cherkaoui
    • 4
  • Jean-Michel Dugoujon
    • 5
  • Ryk Ward
    • 1
  1. 1.Institute of Biological AnthropologyUniversity of OxfordOxfordUK
  2. 2.Department of Evolutionary GeneticsMax-Planck Institute for Evolutionary AnthropologyGermany
  3. 3.Department of Human GeneticsUniversity of ChicagoChicagoUSA
  4. 4.Laboratoire d’Ecologie Humaine, Faculté des Sciences-SemlaliaUniversité Cadi AyyadMorocco
  5. 5.Centre d’Anthropologie CNRS,University of ToulouseFrance

Personalised recommendations

Cite article

Buy options