Extensive Female-Mediated Gene Flow from Sub-Saharan Africa Into Near Eastern Arab Populations
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Edinburgh Research Explorer Extensive female-mediated gene flow from sub-Saharan Africa into near eastern Arab populations Citation for published version: Richards, M, Rengo, C, Cruciani, F, Gratrix, F, Wilson, JF, Scozzari, R, Macaulay, V & Torroni, A 2003, 'Extensive female-mediated gene flow from sub-Saharan Africa into near eastern Arab populations', American Journal of Human Genetics, vol. 72, no. 4, pp. 1058-64. https://doi.org/10.1086/374384 Digital Object Identifier (DOI): 10.1086/374384 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: American Journal of Human Genetics Publisher Rights Statement: Copyright © 2003 by The American Society of Human Genetics. All rights reserved. General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 29. Sep. 2021 Am. J. Hum. Genet. 72:1058–1064, 2003 Report Extensive Female-Mediated Gene Flow from Sub-Saharan Africa into Near Eastern Arab Populations Martin Richards,1 Chiara Rengo,2,3 Fulvio Cruciani,2 Fiona Gratrix,4 James F. Wilson,5 Rosaria Scozzari,2 Vincent Macaulay,6 and Antonio Torroni7 1Department of Chemical and Biological Sciences, University of Huddersfield, Huddersfield, United Kingdom; 2Dipartimento di Genetica e Biologia Molecolare, Universita` di Roma “La Sapienza,” and 3Istituto di Medicina Legale, Universita` Cattolica del Sacro Cuore, Rome; 4Department of Biological Sciences, Imperial College, and 5Department of Biology, University College London, London; 6Department of Statistics, University of Oxford, Oxford, United Kingdom; and 7Dipartimento di Genetica e Microbiologia, Universita` di Pavia, Pavia, Italy We have analyzed and compared mitochondrial DNA variation of populations from the Near East and Africa and found a very high frequency of African lineages present in the Yemen Hadramawt: more than a third were of clear sub-Saharan origin. Other Arab populations carried ∼10% lineages of sub-Saharan origin, whereas non-Arab Near Eastern populations, by contrast, carried few or no such lineages, suggesting that gene flow has been preferentially into Arab populations. Several lines of evidence suggest that most of this gene flow probably occurred within the past ∼2,500 years. In contrast, there is little evidence for male-mediated gene flow from sub-Saharan Africa in Y- chromosome haplotypes in Arab populations, including the Hadramawt. Taken together, these results are consistent with substantial migration from eastern Africa into Arabia, at least in part as a result of the Arab slave trade, and mainly female assimilation into the Arabian population as a result of miscegenation and manumission. Contacts between eastern Africa and Arabia have existed and Ethiopia were gradually incorporated into the area since the establishment of obsidian exchange networks of Arab influence. These contacts crystallized in the for- as early as the 7th millennium B.C. They were stimulated mation of the Ethio-Sabean state of Daamat on the Ti- by the growth of the Egyptian state from the 4th mil- grean plateau in ∼600 B.C. The archaeological evidence lennium onward, with possible settlements of people from suggests that this is likely to have been the result of small- Arabia in the Horn of Africa as early as the 3rd and 2nd scale colonization by several Arabian groups (including millennia B.C. The Afro-Arabian Tihama cultural com- Sabeans) and acculturation of the indigenous population plex, for which an African origin seems most likely, arose (Fattovich 1997). This was succeeded, following the de- in the mid-2nd millennium. In addition to the coastal site cline of Saba and Daamat and several centuries of iso- ∼ of Adulis in Eritrea and sites farther inland in Eritrea, lation, by the kingdom of Aksum in A.D. 100, which Ethiopia, and Sudan, it is represented on the Saudi coastal formed as part of the Roman exchange network ex- plains and the western and southern coasts of Yemen. tending from Egypt as far as India, trading via the Red Other traditions appear to have spread in the opposite Sea port of Adulis. Aksum survived for 800 years and direction (Fattovich 1997). occupied southern Arabia for part of this period. Util- Southern Arabs gained control of the Red Sea trade itarian Aksumite pottery has been found in large quan- tities in deposits from the 5th and 6th centuries in the routes in the 12th century B.C., and the first kingdom, Yemen Hadramawt, suggesting that there may have been Saba, arose in Yemen in ∼800 B.C. As a result, Eritrea substantial immigration during that period. From the 7th century onward, with the rise of Islam, Muslim com- Received December 2, 2002; accepted for publication January 21, 2003; electronically published March 10, 2003. munities became established along the coast of Eritrea Address for correspondence and reprints: Dr. Martin Richards, De- and Somalia, spreading inland from the late 1st millen- partment of Chemical and Biological Sciences, University of Hudders- nium onward (Fattovich 1997). Concomitantly, the Arab field, Queensgate, Huddersfield, HD1 3DH, United Kingdom. E-mail: slave trade, operating from pre-Islamic times but at its [email protected] ᭧ 2003 by The American Society of Human Genetics. All rights reserved. height between A.D. 650 and 1900, carried millions of 0002-9297/2003/7204-0030$15.00 men and women from the Nile Valley, the Horn of Africa, 1058 Reports 1059 and the eastern African coast across the Red Sea to Arabia Table 1 and many more millions across the Sahara (Segal 2001). Percentages of mtDNA Haplogroups L1–L3A, U6, M1, and To evaluate the extent and nature of gene flow between (pre-HV)1 in Near Eastern and African Populations Africa and the Near East, we have examined mtDNA HAPLOGROUP FREQUENCIES variation in numerous populations from the two geo- (%) graphic areas and compared it with that observed in the GROUP AND POPULATION/REGION N L1–L3A U6 M1 (pre-HV)1 Y chromosome. These genetic systems are uniparentally transmitted and trace out the female and male geneal- Arab Near East: a ogies. Moreover, their sequence variation has been sub- Iraqis 116 9 1 1 4 Bedouinb 29 10 7 7 17 divided into a number of clades, termed “haplogroups,” Palestiniansa 117 15 1 2 3 each of which has originated at one time and place and Syriansa 69 9 4 0 6 been subsequently dispersed by the movement of people. Jordaniansa 146 14 0 2 0 Thus, haplogroups tend to be geographically restricted Yemen Hadramawtb 56 34 0 4 7 and are particularly informative for detecting gene flow Non-Arab Near East: Georgiansc 105 0 0 0 2 between continents. The haplogroup profiles of Africans Armeniansa 192 0 0 0 1 and Eurasians are sufficiently distinct to allow us to ad- Azerbaijanisa 48 0 0 0 0 dress the question of historical gene flow between eastern Turksa 218 1 0 0 1 Africa and Arabia and whether the same patterns are seen Kurdsa 53 4 0 0 2 in both female and male lines of descent. Near Eastern Jews: Iraqi Jewsc 56 0 0 7 0 We studied the variation in the first hypervariable seg- Iranian Jewsc 75 0 0 1 1 ment (HVS-I) of the mtDNA control region (encompass- Ashkenazi Jewsc 78 0 3 0 3 ing at minimum nps 16090–16365 but as much as nps Georgian Jewsc 70 0 0 0 0 16017–16497 in many cases; numbering as per Ander- Yemen Jewsc 65 11 0 0 17 a son et al. [1981]) in 533 subjects from Arabic-speaking Yemen Jews 38 5 0 0 26 East Africa: communities and 960 from non-Arabic–speaking com- Ethiopiansc 74 55 3 10 8 munities in the Near East, including 344 Near Eastern Ethiopian Jewsc 46 52 0 15 15 Jews (table 1). (An additional set of 38 Yemeni Jews [Rich- Somaliansd 27 70 0 11 11 ards et al. 2000] was also included but was kept distinct, Nubianse 80 58 0 10 9 e since some members may be from the same sample as Southern Sudanese 76 92 0 4 0 Kenyansd 63 95 3 2 0 those reported by Thomas et al. [2002].) We compared West Africa: these with 74 Ethiopians and 46 Ethiopian Jews, 246 Overalld,f,g,h 447 89 3 0 0 additional East Africans, 447 West Africans, 132 Central Central Africa: Africans, and 98 Khoisan and 416 Mozambican Bantu Mbuti and Biakaf 37 100 0 0 0 i speakers from southern Africa (table 1). Haplogroup Equatorial Guineans 95 99 1 0 0 Southern Africa: affiliation was defined primarily on the basis of the ob- Kung and Khwef,j 98 100 0 0 0 served HVS-I motif, with some additional testing of di- Mozambicansk,l 416 100 0 0 0 agnostic RFLP markers to ensure that misassignments a Richards et al. (2000). were avoided. These were: haplogroups H (Ϫ7025 AluI), b Di Rienzo and Wilson (1991). HV (Ϫ14766 MseI), V (Ϫ4577 NlaIII), U (ϩ12308 c Thomas et al. (2002). HinfI), K (Ϫ9052 HaeII), JT (ϩ4216 NlaIII), T (ϩ15606 d Watson et al. (1997). Ϫ ϩ e Krings et al. (1999). AluI), F1 ( 12406 HincII), R ( 12703 MboII), M f ϩ ϩ Ϫ Vigilant et al.