Abstract
Arabia has served as a strategic crossroads for human disseminations, providing a natural connection between the distant populations of China and India in the east to the western civilizations along the Mediterranean. To explore this region's critical role in the migratory episodes leaving Africa to Eurasia and back, high-resolution Y-chromosome analysis of males from the United Arab Emirates (164), Qatar (72) and Yemen (62) was performed. The role of the Levant in the Neolithic dispersal of the E3b1-M35 sublineages is supported by the data, and the distribution and STR-based analyses of J1-M267 representatives points to their spread from the north, most likely during the Neolithic. With the exception of Yemen, southern Arabia, South Iran and South Pakistan display high diversity in their Y-haplogroup substructure possibly a result of gene flow along the coastal crescent-shaped corridor of the Gulf of Oman facilitating human dispersals. Elevated rates of consanguinity may have had an impact in Yemen and Qatar, which experience significant heterozygote deficiencies at various hypervariable autosomal STR loci.
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References
Lahr MM, Foley R : Multiple dispersals and modern human origins. Evol Anthropol 1994; 3: 48–60.
Stringer C : Coasting out of Africa. Nature 2000; 405: 24–25,27.
Oppenheimer S : Out of Eden: The Peopling of the World. Constable: London, 2003.
Luis JR, Rowold DJ, Regueiro M et al: The Levant versus the Horn of Africa: evidence for bidirectional corridors of human migrations. Am J Hum Genet 2004; 74: 32–544.
Rowold DJ, Luis JR, Terreros MC, Herrera RJ : Mitochondrial DNA geneflow indicates preferred usage of the Levant corridor over the Horn of Africa. J Hum Genet 2007; 52: 436–447.
Hassan F : Archeology and linguistic diversity in North Africa; In: Bellwood P, Renfrew C (eds): Examining the Farming/Language Dispersal Hypothesis. McDonald Institute for Archaeological Research: Cambridge, 2002, pp 127–133.
Militarev A : 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, 2002, pp 135–150.
Flavin K, Shepherd E : Fishing in the Gulf: preliminary investigations at an Ubaid site, Dalma (UAE). PSAS 1994; 24: 115–134.
Beech M, Elders J : An ‘Ubaid-related settlement on Dalma Island, Abu Dhabi Emirate, United Arab Emirates. Bull Soc Arabian Stud 1999; 4: 17–21.
Beech M, Cuttler R, Moscrop D et al: New evidence for the Neolithic settlement of Marawah Island, Abu Dhabi, United Arab Emirates. PSAS 2005; 35: 37–56.
Cavalli-Sforza LL, Menozzi P, Piazza A : The History and Geography of Human Genes. Princeton University Press: Princeton, 1994.
Cinnioǧlu C, King R, Kvisild T et al: Excavating Y-chromosome haplotype strata in Anatolia. Hum Genet 2004; 114: 127–148.
Nasidze I, Ling EYS, Quinque D et al: Mitochondrial DNA and Y-chromosome variation in the Caucasus. Ann Hum Genet 2004; 68: 205–221.
Regueiro M, Cadenas AM, Gayden T, Underhill PA, Herrera RJ : Iran: Tricontinental nexus for Y-driven migration. Hum Hered 2006; 61: 132–143.
Quintana-Murci L, Chaix R, Wells RS et al: Where west meets east: the complex mtDNA landscape of the southwest and central Asian corridor. Am J Hum Genet 2004; 74: 827–845.
Quintana-Murci L, Krausz C, Zerjal T et al: Y-chromosome lineages trace diffusion of people and languages in southwestern Asia. Am J Hum Genet 2001; 68: 537–542.
Wells RS, Yuldasheva N, Ruzibakiev R et al: The Eurasian heartland: a continental perspective on Y-chromosome diversity. Proc Natl Acad Sci USA 2001; 98: 10244–10249.
Qamar R, Ayub Q, Mohyuddin A et al: Y chromosomal DNA variation in Pakistan. Am J Hum Genet 2002; 70: 1107–1124.
Shepard EM, Herrera RJ : Genetic encapsulation among Near Eastern populations. J Hum Genet 2006; 51: 467–476.
Kivisild T, Reidla M, Metspalu E et al: Ethiopian mitochondrial DNA heritage: tracking gene flow across and around the gate of tears. Am J Hum Genet 2004; 75: 752–770.
Sanchez JJ, Hallenberg C, Borsting C, Hernandez A, Morling N : High frequencies of Y chromosome lineages characterized by E3b1, DYS19-11, DYS392-12 in Somali males. Eur J Hum Genet 2005; 13: 856–866.
Al-Zahery N, Semino O, Benuzzi G et al: Y-chromosome and mtDNA polymorphisms in Iraq, a crossroad of the early human dispersal and of post-Neolithic migrations. Mol Phylogenet Evol 2003; 28: 458–472.
Semino O, Passarino G, Oefner PJ et al: The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: a Y chromosome perspective. Science 2000; 290: 1155–1159.
Thomas MG, Parfitt T, Weiss DA et al: Y chromosomes traveling south: the cohen modal haplotype and the origins of the Lemba-the ‘Black Jews of Southern Africa’. Am J Hum Genet 2000; 66: 674–686.
Shepard EM, Herrera RJ : Iranian STR variation at the fringes of biogeographical demarcation. For Sci Int 2005; 158: 140–148.
Perez-Miranda AM, Alfonso-Sanchez MA, Pena JA, Herrera RJ : Qatari DNA variation at a crossroad of human migrations. Hum Hered 2006; 61: 67–79.
Arredi B, Poloni ES, Paracchini S et al: A predominantly Neolithic origin for Y-chromosomal DNA variation in North Africa. Am J Hum Genet 2004; 75: 338–345.
Semino O, Santachiara-Benerecetti AS, Falaschi F, Cavalli-Sforza LL, Underhill PA : Ethiopians and Khoisan share the deepest clades of the human Y-chromosome phylogeny. Am J Hum Genet 2002; 70: 265–268.
Nasidze I, Sarkisian T, Kerimov A, Stoneking M : Testing hypotheses of language replacement in the Caucasus: evidence from the Y-chromosome. Hum Genet 2003; 112: 255–261.
Sengupta S, Zhivotovsky LA, King R et al: Polarity and temporality of high-resolution Y-chromosome distributions in India identify both indigenous and exogenous expansions and reveal minor genetic influence of Central Asian pastoralists. Am J Hum Genet 2006; 78: 202–221.
Kivisild T, Rootsi S, Metspalu M et al: The genetic heritage of the earliest settlers persists both in Indian tribal and caste populations. Am J Hum Genet 2003; 72: 313–332.
Karafet T, Xu L, Du R et al: Paternal population history of East Asia: sources, patterns, and microevolutionary processes. Am J Hum Genet 2001; 69: 615–628.
Antunez de Mayolo G, Antunez de Mayolo A, Antunez de Mayolo P et al: Phylogenetics of worldwide human populations as determined by polymorphic Alu insertions. Electrophoresis 2002; 23: 3346–3356.
Underhill PA, Passarino G, Lin AA et al: The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations. Ann Hum Genet 2001; 65: 43–62.
Shen P, Lavi T, Kivisild T et al: Reconstruction of patrilineages and matrilineages of Samaritans and other Israeli populations from Y-chromosome and mitochondrial DNA sequence variation. Hum Mutat 2004; 24: 248–260.
Cruciani F, La Fratta R, Torroni A, Underhill PA, Scozzari R : Molecular dissection of the Y chromosome haplogroup E-M78 (E3b1a): a posteriori evaluation of a STR-network-based approach through six new biallelic markers. Hum Mutat 2006; 27: 831–832.
Martinez L, Reategui EP, Fonseca LR et al: Superimposing polymorphism: the case of a point mutation within a polymorphic Alu insertion. Hum Hered 2005; 59: 109–117.
Hammer MF, Horai S : Y chromosomal DNA variation and the peopling of Japan. Am J Hum Genet 1995; 56: 951–962.
Y Chromosome Consortium: A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res 2002; 12: 339–348.
Reynolds J, Weir BS, Cockerham CC : Estimation of the coancestry coefficient: basis for a short term genetic distance. Genetics 1983; 105: 767–779.
SPSS for Windows, Rel. 11.0.1.2001. SPSS Inc: Chicago.
Excoffier L, Smouse PE, Quattro JM : Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 1992; 131: 479–491.
Schneider S, Roessli D, Excoffier L : A software for population genetics data analysis. Arlequin version 2.000. Genetics and Biometry Laboratory, University of Geneva: Switzerland, 2000.
Carmody G : G-test. Carleton University: Ottawa, 1991.
Kimura M, Ohta T : Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA 1978; 75: 2868–2872.
Zhivotovsky LA, Underhill PA, Cinnioǧlu C et al: The effective mutation rate at Y chromosome short tandem repeats, with application to human population-divergence time. Am J Hum Genet 2004; 74: 50–61.
Cruciani F, Santolamazza P, Shen P et al: A back migration from Asia to sub-saharan Africa is supported by high resolution analysis of human Y-chromosome haplotypes. Am J Hum Genet 2002; 70: 1197–1214.
Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB : Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 1994; 91: 3166–3170.
Kittles RA, Perola M, Peltonen L et al: Dual origins of Finns revealed Y chromosome haplotype variation. Am J Hum Genet 1998; 62: 1171–1179.
Kayser M, Krawczak M, Excoffier L et al: An extensive analysis of Y-chromosomal STR haplotypes in globally dispersed human populations. Am J Hum Genet 2001; 68: 990–1018.
Zhivotovsky LA, Goldstein DB, Feldman MW : Genetic sampling error of distance (δμ)2 and variation in mutation rate among STR loci. Mol Biol Evol 2001; 18: 2141–2145.
Raymond M, Rousset F : GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 1995; 86: 248–249.
Rousset F, Raymond M : Testing heterozygote excess and deficiency. Genetics 1995; 140: 1413–1419.
Richards M, Rengo C, Cruciani F et al: Extensive female-mediated gene flow from sub-Saharan Africa into Near Eastern Arab populations. Am J Hum Genet 2003; 72: 1058–1064.
Olivieri A, Achilli A, Pala M et al: The mtDNA legacy of the Levantine early Upper Palaeolithic in Africa. Science 2006; 314: 1767–1770.
Underhill PA, Shen P, Lin AA et al: Y chromosome sequence variation and the history of human populations. Nat Genet 2000; 26: 358–361.
Cruciani F, La Fratta R, Santolamazza P et al: Phylogeographic analysis of haplogroup E3b (E-M215) Y chromosomes reveals multiple migratory events within and out of Africa. Am J Hum Genet 2004; 74: 1014–1022.
Semino O, Magri C, Benuzzi G et al: Origin, diffusion, and differentiation of Y-chromosome haplogroups E and J: inferences on the neolithization of Europe and later migratory events in the Mediterranean area. Am J Hum Genet 2004; 74: 1023–1034.
Gunaid AA, Hummad NA, Tamim KA : Consanguineous marriage in the capital city Sana’a, Yemen. J Biosoc Sci 2004; 36: 111–121.
Hafez M, El-Tahan H, Awadalla M, El-Khayat H, Abdel-Gafar A, Ghoneim M : Consanguineous mating in the Egyptian population. J Med Genet 1983; 20: 58–60.
Basaran N, Sayli BS, Basaran A, Solak M, Artan S, Stevenson JD : Consanguineous marriages in the Turkish population. Clin Genet 1988; 34: 339–341.
Bener A, Alali KA : Consanguineous marriage in a newly developed country: The Qatari population. J Biosoc Sci 2005; 38: 239–246.
Al-Gazali LI, Bener A, Abdulrazzaq YM, Micallef R, Al-Khayat AI, Gaber T : Consanguineous marriages in the United Arab Emirates. J Biosoc Sci 1997; 29: 491–497.
Rajab A, Patton MA : A study of consanguinity in the Sultanate of Oman. Ann Hum Bio 2000; 27: 321–326.
Prothro ET, Diab LN : Changing Family Patterns in the Arab East Beirut. American University: Beirut, 1974.
Khoury SA, Massad D : Consanguineous marriage in Jordan. Am J Med Genet 1992; 43: 769–775.
Sueyoshi S, Ohtsuka R : Effects of polygyny and consanguinity on high fertility in the rural Arab population in South Jordan. J Biosoc Sci 2003; 35: 513–526.
El-Hazmi MAF, Al-Swailem AR, Warsy AS, Al-Swailem AM, Sulaimani R, Al-Meshari AA : Consanguinity among Saudi Arabian population. J Med Genet 1995; 32: 623–626.
Al-Awadi SA, Moussa MA, Naguib KK et al: Consanguinity among the Kuwait population. Clin Genet 1985; 27: 483–486.
Acknowledgements
We gratefully acknowledge Tenzin Gayden and Maria Regueiro for their contributions to this study as well as Sheyla Mirabal for her technical assistance.
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Cadenas, A., Zhivotovsky, L., Cavalli-Sforza, L. et al. Y-chromosome diversity characterizes the Gulf of Oman. Eur J Hum Genet 16, 374–386 (2008). https://doi.org/10.1038/sj.ejhg.5201934
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DOI: https://doi.org/10.1038/sj.ejhg.5201934
