Journal of Human Genetics

, Volume 52, Issue 5, pp 436–447 | Cite as

Mitochondrial DNA geneflow indicates preferred usage of the Levant Corridor over the Horn of Africa passageway

  • D. J. Rowold
  • J. R. Luis
  • M. C. Terreros
  • Rene J. Herrera
Original Article

Abstract

Both the Levantine Corridor and the Horn of Africa route have figured prominently in early hominid migrations from Africa to Eurasia. To gauge the importance of these two African–Asian thoroughfares in the demic movements of modern man, we surveyed the mtDNA control region variation and coding polymorphisms of 739 individuals representing ten African and Middle Eastern populations. Two of these collections, Egypt and Yemen, are geographically close to the Levant and Horn of Africa, respectively. In this analysis, we uncover genetic evidence for the preferential use of the Levantine Corridor in the Upper Paleolithic to Neolithic dispersals of haplogroups H, J*, N1b, and T1, in contrast to an overwhelming preference in favor of the Horn of Africa for the intercontinental expansion of M1 during the Middle to Upper Paleolithic. Furthermore, we also observed a higher frequency of sub-Saharan mtDNA compared to NRY lineages in the Middle Eastern collections, a pattern also seen in previous studies. In short, the results of this study suggest that several migratory episodes of maternal lineages occurred across the African–Asian corridors since the first African exodus of modern Homo sapiens sapiens.

Keywords

Mitochondrial DNA NRY lineages Human phylogeny Middle East Africa 

Notes

Acknowledgments

We are grateful to B. Caeiro for the Benin sample and to M. Tahir for the Jordan sample collections used in this study. We are also indebted to Rachel Chow and Erica Shepard for their work on the RFLP analysis and to Arif Kalantar for performing the HVI and HVII sequencing analysis on the UAE populations. Lastly, we are deeply grateful to all of the people who donated blood specimens for this and other similar projects.

Supplementary material

10038_2007_132_MOESM1_ESM.doc (30 kb)
(Doc 30.5 kb)
10038_2007_132_MOESM2_ESM.doc (68 kb)
(Doc 68.5 kb)
10038_2007_132_MOESM3_ESM.doc (24 kb)
(Doc 23.5 kb)
10038_2007_132_MOESM4_ESM.doc (46 kb)
(Doc 46.0 kb)
10038_2007_132_MOESM5_ESM.doc (48 kb)
(Doc 48.5 kb)
10038_2007_132_MOESM6_ESM.doc (46 kb)
(Doc 48.0 kb)

References

  1. Achilli A, Rengo C, Magri C, Battaglia V, Olivieri A, Scozzari R, Cruciani F (2004) The molecular dissection of mtDNA haplogroup H confirms that the Franco-Cantabrian glacial refuge was a major source for the European gene pool. Am J Hum Genet 75:910–918PubMedCrossRefGoogle Scholar
  2. Alves-Silva J, Santos M, Guimarães P, Ferreira AC, Bandelt HJ, Pena SD, Prado VF (2000) The ancestry of Brazilian mtDNA lineages. Am J Hum Genet 67:444–461PubMedCrossRefGoogle Scholar
  3. Al-Zahery N, Semino O, Benuzzi G, Magri C, Passarino G, Torroni A, Santachiara-Benerecetti AS (2003) Y-chromosome and mtDNA polymorphisms in Iraq, a crossroad of the early human dispersal and of post-Neolithic migrations. Mol Phylogenet Evol 28:458–472PubMedCrossRefGoogle Scholar
  4. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465PubMedCrossRefGoogle Scholar
  5. Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, Howell N (1999) Reanalysis and revision of the Cambridge reference sequence for human mitochondrial. DNA Nat Genet 23:147PubMedCrossRefGoogle Scholar
  6. Antunez de Mayolo A, Antunez de Mayolo G, Thomas E, Reategui EP, Brown MD, Herrera RJ (1999) Worldwide distribution of a polymorphic Alu insertion in the progesterone receptor gene. In: Papiha SS, Deka R (eds) Genomic diversity: applications in human population genetics. Plenum Publishing, New York, pp 213–226Google Scholar
  7. Bandelt HJ, Forster P, Sykes BC, Richards MB (1995) Mitochondrial portraits of human populations using median networks Genetics 141:743–753PubMedGoogle Scholar
  8. Bandelt H-J, Alves-Silva J, Guimaraes P, Santos M, Brehm M, Pereira L, Coppa A, Larruga JM, Rengo C, Scozzari R, Torroni A, Prata MJ, Amorim A, Prado VF, Pena SDJ (2001) Phylogeography of the human mitochondrial L3e: a snapshot of African prehistory and the Atlantic slave trade. Ann Hum Genet 65:549–563PubMedCrossRefGoogle Scholar
  9. 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, pp 548–623Google Scholar
  10. Camps-Fabrer G (1974) Les civilisations préhistoriques de l´Afrique du Nord et du Sahara. Dion, ParísGoogle Scholar
  11. Cavalli-Sforza LL, Piazza A, Menozzi P (1994) The history and geography of human genes. Princeton University Press, PrincetonGoogle Scholar
  12. Chen YS, Torroni A, Excoffier L, Santachiara-Benerecetti AS, Wallace DC (1995) Analysis of mtDNA variation in African populations reveals the most ancient of all human continent-specific haplogroups. Am J Hum Genet 57:133–149PubMedGoogle Scholar
  13. Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112PubMedCrossRefGoogle Scholar
  14. Fadhlaoui-Zid K, Plaza S, Calafell F, Ben Amor M, Comas D, Bennamar El gaaied A (2004) Mitochondrial heterogeneity in Tunisian Berbers. Ann Hum Genet 68:222–233PubMedCrossRefGoogle Scholar
  15. Fagan B (1990) Journey from Eden: the peopling of our world. Thames and Hudson, New YorkGoogle Scholar
  16. Forster P (2004) Ice ages and the mitochondrial DNA chronology of human dispersals: a review. Philos Trans R Soc Lond B Biol Sci 359:255–264PubMedCrossRefGoogle Scholar
  17. Forster P, Harding R, Torroni A, Bandelt H-J (1996) Origin and evolution of Native American mtDNA variation: a reappraisal. Am J Hum Genet 59:935–945PubMedGoogle Scholar
  18. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  19. Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624–626PubMedCrossRefGoogle Scholar
  20. Kimura M (1969) The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics 61:893–903PubMedGoogle Scholar
  21. Kimura M (1971) Theoretical foundation of population genetics at the molecular level. Theor Popul Biol 2:174–208PubMedCrossRefGoogle Scholar
  22. Kivisild T, Reidla M, Metspalu E, Rosa A, Brehm A, Pennarun E, Parik J, Gerberhiwot T, Usanga E, Villems R (2004) Ethiopian mitochondrial DNA heritage: tracking gene flow across and around the Gate of Tears. Am J Hum Genet 75:752–770PubMedCrossRefGoogle Scholar
  23. Lahr M, Foley R (1994) Multiple dispersals and modern human origins. Evol Anthropol 3:48–60CrossRefGoogle Scholar
  24. Lewis B (1992) Race and slavery in the Middle East: an historical enquiry. Oxford University Press, OxfordGoogle Scholar
  25. Luis JR, Rowold DJ, Regueiro M, Caeiro B, Cinnioğlu C, Roseman C, Underhill PA, Cavalli-Sforza LL, Herrera RJ (2004) The Levant versus the Horn of Africa: evidence for bidirectional corridors of human migrations. Am J Hum Genet 74:532–544PubMedCrossRefGoogle Scholar
  26. Maca-Meyer N, Gonzalez A, Larruga J, Flores C, Cabrera V (2001) Major genomic mitochondrial lineages delineate early human expansions. BMC Genetics 2:13PubMedCrossRefGoogle Scholar
  27. Macaulay VA, Richards MB, Hickey E, Vega E, Cruciani F, Guida V, Scozzari R, Bonné-Tamir B, Sykes B, Torroni A (1999) The emerging tree of West Eurasian of West Eurasian mtDNAs: a synthesis of control region sequences and RFLPs. Am J Hum Genet 64:232–249PubMedCrossRefGoogle Scholar
  28. McEvedy C (1980) The penguin atlas of African history. Penguin Books Ltd, LondonGoogle Scholar
  29. Mishmar D, Ruiz-Pesini E, Golik P, Macaulay V, Clark AG, Hosseini S, Brandon M, Easley K, Chen E, Brown MD, Sukernik RI, Olckers A, Wallace DC (2003) Natural selection shaped regional mtDNA variation in humans. Proc Natl Acad Sci USA 100:171–176Google Scholar
  30. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  31. Newman (1995) The peopling of Africa: a geographic interpretation. Yale University Press, New HavenGoogle Scholar
  32. Olivieri A, Achilli A, Pala M, Battaglia V, Fornarino S, Al-Zahery N, Scozzari R, Cruciani F, Behar DM, Dugoujon JM, Coudray C, Santachiara-Benerecetti AS, Semino O, Bandelt HJ, Torroni A (2006) The mtDNA legacy of the Levantine early Upper Paleolithic in Africa. Science 314:1767–1770PubMedCrossRefGoogle Scholar
  33. Oppenheimer S (2003) Out of Eden: the peopling of the world. Constable, LondonGoogle Scholar
  34. Perreira L, Macaulay V, Torroni A, Scozzari R, Prata MJ, Amorim A (2001) Prehistoric and historic traces of mtDNA of Mozambique: insights into the Bantu expansions and the slave trade. Ann Hum Genet 65:439–458CrossRefGoogle Scholar
  35. Quintana-Murci L, Semino O, Bandelt HJ, Passarino G, McElreavey K, Santachiara-Benerecetti AS (1999) Genetic evidence of an early exit of Homo sapiens sapiens from Africa through eastern Africa. Nat Genet 23:437–441PubMedCrossRefGoogle Scholar
  36. Quintana-Murci L, Chaix R, Wells RS, Behar DM, Sayar H, Scozzari R, Rengo C, Al-Zahery N, Semino O, Santachiara-Benerecetti AS, Coppa A, Ayub Q, Mohyuddin A, Tyler-Smith C, Mehdi SQ, Torroni A, McElreavey K (2004) Where West meets East: the complex mtDNA landscape of the southwest and central Asian corridor. Am J Hum Genet 74:827–845PubMedCrossRefGoogle Scholar
  37. Rando JC, Pinto F, Gonzalez AM, Hernadez 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 62:531–550PubMedCrossRefGoogle Scholar
  38. Richards MB, Macaulay V, Bandelt HJ, Sykes BC (1998) Phylogeography of mitochondrial DNA in Western Europe. Ann Hum Genet 62:241–260PubMedCrossRefGoogle Scholar
  39. Richards M, Macaulay V, Hickey E, Vega E, Sykes B, Guida V, Rengo C et al (2000) Tracing European founder lineages in the Eastern mtDNA pool. Am J Hum Genet 67:1251–127PubMedGoogle Scholar
  40. Richards M, Rengo C, Cruciani F, Gratix F, Wilson JF, Scozzari R, Macaulay V, Torroni A (2003) Extensive female lineage-mediated gene flow from sub-Saharan into Near Eastern Arab populations. Am J Hum Genet 72:0158–1064CrossRefGoogle Scholar
  41. Rohlf F (2002) NTSYSpc. Exeter Publishing Ltd, SetauketGoogle Scholar
  42. Rosa A, Brehm A, Kivisild T, Metspalau M, Villems R (2004) MtDNA profile of West Africa Guineans: towards a better understanding of the Senegambia region. Ann Hum Genet 68:340–352PubMedCrossRefGoogle Scholar
  43. Saillard J, Forster P, Lynnerup N, Bandelt H-J, Nørby S (2000) mtDNA variation among Greenland Eskimos: the edge of the Beringian expansion. Am J Hum Genet 67:718–726PubMedCrossRefGoogle Scholar
  44. Salas A, Richards M, De la Fe T, Lareu M-V, Sobrino B, Sanchiz-Diz P, Macaulay V, Carracedo A (2002) The making of the African mtDNA landscape. Am J Hum Genet 71:1082–1111PubMedCrossRefGoogle Scholar
  45. Salas A, Richards M, Lareu M-V, Scozzari R, Coppa A, Torroni A, Macaulay V, Carracedo A (2004) The Africa diaspora: mitochondrial DNA and the Atlantic slave trade. Am J Hum Genet 74:454–465PubMedCrossRefGoogle Scholar
  46. Schneider S, Roessli D, Excoffier L (2000) Arlequin version 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  47. Segal R (2001) Islam’s black slaves. Atlantic, LondonGoogle Scholar
  48. Siddall M, Rohling EJ, Almogi-Labin A, Hemleben C, Meischner D, Schmelzer I, Smeed DA (2003) Sea level fluctuations during the last glacial cycle. Nature 423:853–858PubMedCrossRefGoogle Scholar
  49. Stoneking M, Hedgecock D, Higuch RG, Vigilant L, Erlich HA (1991) population variation of human control region sequences detected by enzymatic amplification and sequence-specific oligonucleotide probes. Am J Hum Genet 48:370–382PubMedGoogle Scholar
  50. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  51. Torroni A, Huoponen K, Francalacci P, Petrozzi M, Morelli L, Scozzari R, Obinu D, Savontaus M-L, Wallace DC (1996) Classification of European mtDNAs from an analysis of three European populations. Genetics 144:1835–1850PubMedGoogle Scholar
  52. Underhill PA, Shen P, Lin AA, Jin L, Passarino G, Yang WH, Kauffman E et al (2000) Y chromosome sequence variation and the history of human populations. Nat Genet 26:358–61PubMedCrossRefGoogle Scholar
  53. Vasina J (1979) Bantu in a crystal ball. Hist Afr 6:287–333CrossRefGoogle Scholar
  54. Watson E, Forster P, Richards M, Bandelt HJ (1997) Mitochondrial footprints of human expansions in Africa. Am J Hum Genet 61:601–704Google Scholar
  55. Watterson G (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276PubMedCrossRefGoogle Scholar
  56. Watterson G (1978) The Homozygosity test of neutrality. Genetics 88:405–417PubMedGoogle Scholar

Copyright information

© The Japan Society of Human Genetics and Springer 2007

Authors and Affiliations

  • D. J. Rowold
    • 1
  • J. R. Luis
    • 1
    • 2
  • M. C. Terreros
    • 1
  • Rene J. Herrera
    • 1
  1. 1.Department of Biological SciencesFlorida International UniversityMiamiUSA
  2. 2.Departamento de Xenetica, Bioquimica e Inmunoloxia, Facultade de BioloxiaUniversidade de VigoGaliciaSpain

Personalised recommendations