DNA history of Egypt

The genetic history of the demographics of Egypt reflects Egypt's geographical location at the crossroads of several major cultural areas: Northeast Africa, the Sahara, Sub-Saharan Africa, the Middle East, and the Mediterranean.

In general, various DNA studies have found that the gene frequencies of present Egyptian populations are intermediate between those of the Middle East, the Horn of Africa, southern Europe and Sub-Saharan Africa,[1] though NRY frequency distributions of the modern Egyptian population appear to be much more similar to those of the Middle East than to any Sub-Saharan African or European population, suggesting a much larger Middle Eastern genetic component.[2][3][3][4][5][6][7]

Ancient DNA

Contamination from handling and intrusion from microbes create obstacles to the recovery of Ancient DNA.[8] Consequently most DNA studies have been carried out on modern Egyptian populations with the intent of learning about the influences of historical migrations on the population of Egypt.[9][10][11][12] One successful study was performed on ancient mummies of the 12th Dynasty, by Paabo and Di Rienzo, which identified multiple lines of descent, some of which originated in Sub-Saharan Africa.[13]

Blood typing and DNA sampling on ancient Egyptian mummies is scant; however, blood typing of dynastic mummies found ABO frequencies to be most similar to modern Egyptians,[14] and some also to Northern Haratin populations. ABO blood group distribution shows that the Egyptians form a sister group to North African populations, including Berbers, Nubians and Canary Islanders.[15]

A DNA study Hawass at al. (2012) of two male mummies, Ramesses III and the other possibly his son Pentawere, from the 20th dynasty of the New Kingdom found that they carried the haplogroup E1b1a.[16]

In 2013, Nature announced the publication of the first genetic study utilizing next-generation sequencing to ascertain the ancestral lineage of an Ancient Egyptian individual. The research was led by Carsten Pusch of the University of Tübingen in Germany and Rabab Khairat, who released their findings in the Journal of Applied Genetics. DNA was extracted from the heads of five Egyptian mummies that were housed at the institution. All the specimens were dated between 806 BC and 124 AD, a timeframe corresponding with the late Dynastic period. The researchers observed that one of the mummified individuals likely belonged to the mtDNA haplogroup I2, a maternal clade that is believed to have originated in Western Asia.[17]

DNA studies on modern Egyptians

Egypt has experienced several invasions during its history. However, these do not seem to account for more than about 10% overall of current Egyptians ancestry when the DNA evidence of the ancient mitochondrial DNA and modern Y chromosomes is considered.

In general, various DNA studies have found that the gene frequencies of modern North African populations are intermediate between those of the Horn of Africa and Eurasia,[18] though possessing a greater genetic affinity with the populations of Eurasia than they do with Africa.[3][3][4] The present population of the Sahara is Caucasoid in the extreme north, with a fairly gradual increase of Negroid component as one goes south.[6][19][20] The results of these genetic studies is consistent with the historical record, which records significant bidirectional contact between Egypt and Nubia, and the Levant/Middle East within the last few thousand years, but with general population continuity from the Early Dynastic Period of Egypt up to the modern day era.[21][22]

Genetic analysis of modern Egyptians reveals that they have paternal lineages common to indigenous North-East African populations primarily (Algeria, Tunisia, Morocco), and to Middle Eastern peoples to a lesser extent—these lineages would have spread during the Neolithic and were maintained by the predynastic period.[23][24]

A study by Krings et al. (1999) on mitochondrial DNA clines along the Nile Valley found that a Eurasian cline runs from Northern Egypt to Southern Sudan and a Sub-Saharan cline from Southern Sudan to Northern Egypt.[25] Another mtDNA study of modern Egyptians from the Gurna region near Thebes in Southern Egypt by Stevanovitch et al. 2004 revealed that Eurasian Out of Africa haplogroups represented 61.8% of the population, with the remainder being of Sub-Saharan (20.6%) and with a high frequency (17.6%) of haplogroup M1. According to the authors "This sedentary population presented similarities to the Ethiopian population by the L1 and L2 macrohaplogroup frequency (20.6%), by the West Eurasian component (defined by haplogroups H to K and T to X) and particularly by a high frequency (17.6%) of haplogroup M1... Our results suggest that the Gurna population has conserved the trace of an ancestral genetic structure from an ancestral East African population, characterized by a high M1 haplogroup frequency". The oral tradition of the Gurna people indicates that they, like most modern day Egyptians, descend from the Ancient Egyptians [26]

Luis et al. (2004) found that the male haplogroups in a sample of 147 Egyptians were E1b1b (36.1%, predominantly E-M78), J (32.0%), G (8.8%), T(8.2%), and R (7.5%). E1b1b and its subclades are characteristic of some Afro-Asiatic speakers and are believed to have originated in either the Middle East, North Africa, or the Horn of Africa. Cruciani et al. (2007) suggests that E-M78, E1b1b predominant subclade in Egypt, originated in "Northeastern Africa", which in the study refers specifically to Egypt and Libya [2][27]

Other studies have shown that modern Egyptians have genetic affinities primarily with populations of Asia, North and Northeast Africa,[28][29][30][31] and to a lesser extent Middle Eastern and European populations.[32]

Some genetic studies done on modern Egyptians suggest that they are not closely related to most Sub Saharan Africans.[33] Other studies suggest that they are instead mostly closely related to other North Africans.[30] In addition, some studies suggest lesser ties with populations in the Middle East, as well as some groups in southern Europe.[31] A 2004 mtDNA study of upper Egyptians from Gurna found a genetic ancestral heritage to modern Northeast Africans, characterized by a high M1 haplotype frequency and a comparatively low L1 and L2 macrohaplogroup frequency of 20.6%. Another study links Egyptians in general with people from modern Eritrea and Ethiopia.[29][34] Though there has been much debate of the origins of haplogroup M1 a recent 2007 study had concluded that M1 has West Asia origins not a Sub Saharan African origin[35] Origin A 2003 Y chromosome study was performed by Lucotte on modern Egyptians, with haplotypes V, XI, and IV being most common. Haplotype V is common in Berbers and has a low frequency outside North Africa. Haplotypes V, XI, and IV are all predominantly North African/Horn of African haplotypes, and they are far more dominant in Egyptians than in Middle Eastern or European groups.[36]

Y-DNA haplogroups

A study using the Y-chromosome of modern Egyptian males found similar results, namely that North East African haplogroups are predominant in the South but the predominant haplogroups in the North are characteristic of North African and Eurasian populations.[22]

Population Nb A/B E1b1a E1b1b1 (M35) E1b1b1a (M78) E1b1b1b (M81) E1b1b1c (M123) F K G I J1 J2 R1a R1b Other Study
1 Egyptians 1472.7%2.7%018.4%8.2%9.5%07.5%9.5%019.7%12.2%3.4% 4.1%2.1%Luis et al. (2004)[37]
2 Egyptians from El-Hayez Oasis (Western Desert)3505.70%5.7%28.6%28.6%0000031.4%0000Kujanová et al. (2009)[38]
3 Egyptians from Siwa Oasis (Western Desert)9328.0%6.5%2.2%6.5%1.1%2.2%003.2%07.5% 6.5%028.0%8.3%Dugoujon et al. (2009)[39]
4 Northern Egyptians 442.3%04.5%27.3%11.4%9.1%6.8%2.3%009.1%9.1%2.3%9.9%6.8%Arredi et al. (2004)
5 Southern Egyptians 290.0%0017.2%6.9%6.9%17.2%10.3%03.4%20.7%3.4%013.8%0Arredi et al. (2004)
Distribution of E1b1b1a (E-M78) and its subclades
Population N E-M78 E-M78* E-V12* E-V13 E-V22 E-V32 E-V65 Study
Southern Egyptians7950.6%44.3%1.3%3.8%1.3% Cruciani et al. (2007)[40]
Egyptians from Bahari4141.4%14.6%2.4%21.9%2.4% Cruciani et al. (2007)
Northern Egyptians (Delta)7223.6%5.6%1.4%13.9%2.8% Cruciani et al. (2007)
Egyptians from Gurna Oasis3417.6%5.9%8.8%2.9% Cruciani et al. (2007)
Egyptian from Siwa Oasis936.4%2.1%4.3% Cruciani et al. (2007)

Autosomal DNA

In 13 January 2012, an exhaustive genetic study of North Africa's human populations was published.[41] The researchers analyzed around 800,000 genetic markers, distributed throughout the entire genome in 125 North African individuals belonging to seven representative populations in the whole region (Saharawi, South Moroccans, North Moroccans, Algerians, Tunisians Berbers, Libyans and Egyptians) and the information obtained was compared with the information from the neighbouring populations. The results of this study show that there is a native genetic component ("Maghrebi") which defines North Africans. The study identified mainly two distinct, opposite gradients of ancestry: an east-to-west increase of this native North African ancestry and an east-to-west decrease in likely Middle Eastern Arab ancestry.

The study also reveals that the genetic composition of North Africa's human populations is very complex and is the result of five distinct ancestries : a local component (Maghrebi) dating back thirteen thousand years and the varied genetic influence of neighbouring populations on North African groups during successive migrations (European, Middle Eastern, eastern and western Sub-Saharan Africa). According to the authors, the people inhabiting North Africa today are not descendants of either the earliest occupants of this region fifty thousand years ago, or descendants of the most recent Neolithic populations. The data shows that the ancestors of today's North Africans were a group of populations which already lived in the region around thirteen thousand years ago. Furthermore, this local North African genetic component is very different from the one found in the populations in the south of the Sahara, which shows that the ancestors of today's North Africans were members of a subgroup of humanity who left Africa to conquer the rest of the world and who subsequently returned to the north of the continent to settle in the region. As well as this local component, North African populations were also observed to share genetic markers with all the neighbouring regions, as a result of more recent migrations, although these appear in different proportions. There is an influence from the Middle East, which becomes less marked as the distance from the Arabian Peninsula increases, similar proportions of European influence in all North African populations, and, in some populations (South Moroccans, Saharawi...), there are even individuals who present a large proportion of recent influence from the South of the Sahara in their genome.

Admixture analysis

Recent genetic analysis of North African populations have found that, despite the complex admixture genetic background, there is an autochthonous genomic component which is likely derived from "back-to-Africa" gene flow older than 12,000 years ago (ya) (i.e., prior to the Neolithic migrations). This local population substratum seems to represent a genetic discontinuity with the earliest modern human settlers of North Africa (those with the Aterian industry) given the estimated ancestry is younger than 40,000 years ago. North Morocco, Libya and Egypt carry high proportions of European and Middle Eastern ancestral components, whereas Tunisian Berbers and Saharawi are those populations with highest autochthonous North African component.[42]

Average ancestry proportions in North African populations estimated by ADMIXTURE for k = 4 different ancestries (October 2012)
Population N Maghreb Europe Near East Sub-Saharan Africa
Tunisia (Berbers)1893%4%2%1%
Saharawi1855%17%10%18%
Morocco North1844%31%14%11%
Morocco South1644%13%10%33%
Algeria1939%27%16%18%
Libya1731%28%25%16%
Egypt1919%37%30%14%

Copts

A 2008 study of a Copts group in Sudan found relatively high frequencies of the Sub-Saharan Haplogroup B. The Sudanese Copts are converts to Egyptian Christianity and are not ethnically closely related to Egyptian Copts. According to the study, the presence of Sub-Saharan haplogroups may also be consistent with the historical record in which southern Egypt was colonized by Nilotic populations during the early state formation.[43]

See also

References

  1. ↑ Cavalli-Sforza, History and Geography of Human Genes, The intermediacy of North Africa and to a lesser extent Europe is apparent
  2. ↑ 2.0 2.1 Luis, J. R. et al. (2004). "The Levant versus the Horn of Africa: Evidence for Bidirectional Corridors of Human Migrations" (PDF). American Journal of Human Genetics 74 (3): 532–544. doi:10.1086/382286. PMC 1182266. PMID 14973781.
  3. ↑ 3.0 3.1 3.2 3.3 Cavalli-Sforza, L.L., P. Menozzi, and A. Piazza. 1994. The History and Geography of Human Genes. Princeton: Princeton University Press.
  4. ↑ 4.0 4.1 Bosch, E.; Calafell, F; Pérez-Lezaun, A; Comas, D; Mateu, E; Bertranpetit, J (1997). "Population history of north Africa: evidence from classical genetic markers". Human Biology 69 (3): 295–311. PMID 9164042.
  5. ↑ Arredi B, Poloni E, Paracchini S, Zerjal T, Fathallah D, Makrelouf M, Pascali V, Novelletto A, Tyler-Smith C; Poloni; Paracchini; Zerjal; Fathallah; Makrelouf; Pascali; Novelletto; Tyler-Smith (2004). "A predominantly Nilo Saharan origin for Y-chromosomal DNA variation in North Africa". Am J Hum Genet 75 (2): 338–45. doi:10.1086/423147. PMC 1216069. PMID 15202071.
  6. ↑ 6.0 6.1 Manni F, Leonardi P, Barakat A, Rouba H, Heyer E, Klintschar M, McElreavey K, Quintana-Murci L; Leonardi; Barakat; Rouba; Heyer; Klintschar; McElreavey; Quintana-Murci (2002). "Y-chromosome analysis in Egypt suggests a genetic regional continuity in Northeastern Africa". Hum Biol 74 (5): 645–58. doi:10.1353/hub.2002.0054. PMID 12495079.
  7. ↑ Cavalli-Sforza. "Synthetic maps of Africa". The History and Geography of Human Genes. ISBN 978-0-691-08750-4.The present population of the Sahara is Sudan in the extreme north, with an increase of Negroid component as one goes south
  8. ↑ Encyclopedia of the Archaeology of Ancient Egypt By Kathryn A. Bard, Steven Blake Shubert pp 278-279
  9. ↑ S.O.Y. Keita & A. J. Boyce, S. O. Y.; Boyce, A. J. (Anthony J.) (June 2009). "Genetics, Egypt, and History: Interpreting Geographical Patterns of Y Chromosome Variation". History in Africa 32 (1): 221. doi:10.1353/hia.2005.0013. Check date values in: |year= / |date= mismatch (help)
  10. ↑ Shomarka Keita (2005), S. O. Y. (2005). "Y-Chromosome Variation in Egypt". African Archaeological Review 22 (2): 61. doi:10.1007/s10437-005-4189-4.
  11. ↑ Keita, S.O.Y. (2005). "History in the Interpretation of the Pattern of p49a,f TaqI RFLP Y-Chromosome Variation in Egypt". American Journal of Human Biology 17 (5): 559–67. doi:10.1002/ajhb.20428. PMID 16136533.
  12. ↑ Shomarka Keita: What genetics can tell us
  13. ↑ Paabo, S., and A. Di Rienzo, A molecular approach to the study of Egyptian history. In Biological Anthropology and the Study of Ancient Egypt. V. Davies and R. Walker, eds. pp. 86-90. London: British Museum Press. 1993
  14. ↑ Borgognini Tarli, S.M.; Paoli, G. (1982). "Survey on paleoserological studies". Homo 33: 69–89.
  15. ↑ Cavalli-Sforza, L.L., P. Menozzi, and A. Piazza. 1994. The History and Geography of Human Genes. Princeton: Princeton University Press, 169-174
  16. ↑ Hawass, Z.; Ismail, S.; Selim, A.; Saleem, S. N.; Fathalla, D.; Wasef, S.; Gad, A. Z.; Saad, R.; Fares, S.; Amer, H.; Gostner, P.; Gad, Y. Z.; Pusch, C. M.; Zink, A. R. (2012). "Revisiting the harem conspiracy and death of Ramesses III: anthropological, forensic, radiological, and genetic study". BMJ 345: e8268. doi:10.1136/bmj.e8268. PMID 23247979. Genetic kinship analyses revealed identical haplotypes in both mummies; using the Whit Athey’s haplogroup predictor, we determined the Y chromosomal haplogroup E1b1a. The testing of polymorphic autosomal microsatellite loci provided similar results in at least one allele of each marker (table 2⇓). Although the mummy of Ramesses III’s wife Tiy was not available for testing, the identical Y chromosomal DNA and autosomal half allele sharing of the two male mummies strongly suggest a father-son relationship.
  17. ↑ Marchant, Jo (12 April 2013). "Egyptian mummies yield genetic secrets". Nature. Retrieved 13 January 2014.
  18. ↑ Cavalli-Sforza, History and Geography of Human Genes, The intermediacy of North Africa and to lesser extent East Africa between Africa and Europe is apparent
  19. ↑ Arredi B, Poloni E, Paracchini S, Zerjal T, Fathallah D, Makrelouf M, Pascali V, Novelletto A, Tyler-Smith C; Poloni; Paracchini; Zerjal; Fathallah; Makrelouf; Pascali; Novelletto; Tyler-Smith (2004). "A predominantly neolithic origin for Y-chromosomal DNA variation in North Africa". Am J Hum Genet 75 (2): 338–45. doi:10.1086/423147. PMC 1216069. PMID 15202071.
  20. ↑ Cavalli-Sforza. "Synthetic maps of Africa". The History and Geography of Human Genes. ISBN 978-0-691-08750-4.The present population of the Sahara is Caucasoid in the extreme north, with a fairly gradual increase of Negroid component as one goes south
  21. ↑ Krings, T; Salem, AE; Bauer, K; Geisert, H; Malek, AK; Chaix, L; Simon, C; Welsby, D et al. (1992). "mtDNA Analysis of Nile River Valley Populations: Genetic Corridor or a Barrier to Migration?" (PDF). Am J Hum Genet. 64 (5): 1116–76. doi:10.1086/302314. PMC 1377841. PMID 10090902.
  22. ↑ 22.0 22.1 Lucotte, G.; Mercier, G. (2001). "Brief communication: Y-chromosome haplotypes in Egypt". American Journal of Physical Anthropology 121 (1): 63–6. doi:10.1002/ajpa.10190. PMID 12687584.
  23. ↑ Arredi B, Poloni E, Paracchini S, Zerjal T, Fathallah D, Makrelouf M, Pascali V, Novelletto A, Tyler-Smith C; Poloni; Paracchini; Zerjal; Fathallah; Makrelouf; Pascali; Novelletto; Tyler-Smith (2004). "A Predominantly Neolithic Origin for Y-Chromosomal DNA Variation in North Africa". Am J Hum Genet 75 (2): 338–45. doi:10.1086/423147. PMC 1216069. PMID 15202071.
  24. ↑ Manni F, Leonardi P, Barakat A, Rouba H, Heyer E, Klintschar M, McElreavey K, Quintana-Murci L; Leonardi; Barakat; Rouba; Heyer; Klintschar; McElreavey; Quintana-Murci (2002). "Y-chromosome analysis in Egypt suggests a genetic regional continuity in Northeastern Africa". Hum Biol 74 (5): 645–58. doi:10.1353/hub.2002.0054. PMID 12495079.
  25. ↑ Kings, T; Salem, AE; Bauer, K; Geisert, H; Malek, AK; Chaix, L; Simon, C; Welsby, D et al. (1992). "mtDNA Analysis of Nile River Valley Populations: Genetic Corridor or a Barrier to Migration?" (PDF). Am J Hum Genet. 64 (5): 1116–76. doi:10.1086/302314. PMC 1377841. PMID 10090902.
  26. ↑ Stevanovitch, A.; Gilles, A.; Bouzaid, E.; Kefi, R.; Paris, F.; Gayraud, R. P.; Spadoni, J. L.; El-Chenawi, F.; Beraud-Colomb, E. (2004). "Mitochondrial DNA Sequence Diversity in a Sedentary Population from Egypt". Annals of Human Genetics 68 (Pt 1): 23–39. doi:10.1046/j.1529-8817.2003.00057.x. PMID 14748828.
  27. ↑ Underhill (2002), Bellwood and Renfrew, ed., Inference of Neolithic Population Histories using Y-chromosome Haplotypes, Cambridge: McDonald Institute for Archaeological Research, ISBN 978-1-902937-20-5.
  28. ↑ Kivisild T, Reidla M, Metspalu E et al. (2004). "Ethiopian mitochondrial DNA heritage: tracking gene flow across and around the gate of tears". Am. J. Hum. Genet. 75 (5): 752–70. doi:10.1086/425161. PMC 1182106. PMID 15457403.
  29. ↑ 29.0 29.1 Stevanovitch A, Gilles A, Bouzaid E et al. (2004). "Mitochondrial DNA sequence diversity in a sedentary population from Egypt". Ann. Hum. Genet. 68 (Pt 1): 23–39. doi:10.1046/j.1529-8817.2003.00057.x. PMID 14748828.
  30. ↑ 30.0 30.1 Arredi B, Poloni E, Paracchini S, Zerjal T, Fathallah D, Makrelouf M, Pascali V, Novelletto A, Tyler-Smith C; Poloni; Paracchini; Zerjal; Fathallah; Makrelouf; Pascali; Novelletto; Tyler-Smith (2004). "A predominantly neolithic origin for Y-chromosomal DNA variation in North Africa". Am J Hum Genet 75 (2): 338–45. doi:10.1086/423147. PMC 1216069. PMID 15202071.
  31. ↑ 31.0 31.1 Manni F, Leonardi P, Barakat A, Rouba H, Heyer E, Klintschar M, McElreavey K, Quintana-Murci L; Leonardi; Barakat; Rouba; Heyer; Klintschar; McElreavey; Quintana-Murci (2002). "Y-chromosome analysis in Egypt suggests a genetic regional continuity in Northeastern Africa". Hum Biol 74 (5): 645–58. doi:10.1353/hub.2002.0054. PMID 12495079.
  32. ↑ Luca Cavalli-Sforza, Luigi; Paolo Menozzi; Alberto Piazza (1996-08-05). The History and Geography of Human Genes. Princeton University Press. ISBN 978-0-691-02905-4.
  33. ↑ Cavalli-Sforza, L.L., P. Menozzi, and A. Piazza. 1994, The History and Geography of Human Genes. Princeton:Princeton University Press.
  34. ↑ Kivisild T, Reidla M, Metspalu E, Rosa A, Brehm A, Pennarun E, Parik J, Geberhiwot T, Usanga E et al. (2004). "Ethiopian mitochondrial DNA heritage: tracking gene flow across and around the gate of tears". Am J Hum Genet 75 (5): 752–70. doi:10.1086/425161. PMC 1182106. PMID 15457403.
  35. ↑ González, A. M.; Larruga, J. M.; Abu-Amero, K. K.; Shi, Y; Pestano, J; Cabrera, V. M. (2007). "Mitochondrial lineage M1 traces an early human backflow to Africa". BMC Genomics 8: 223. doi:10.1186/1471-2164-8-223. PMC 1945034. PMID 17620140.
  36. ↑ Keita, S.O. (2005). "History in the interpretation of the pattern of p49a, f TaqI RFLP Y-chromosome variation in Egypt: a consideration of multiple lines of evidence". Am J Hum Biol 17 (5): 559–67. doi:10.1002/ajhb.20428. PMID 16136533.
  37. ↑ Luis, JR; Rowold, DJ; Regueiro, M; Caeiro, B; Cinnioglu, 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 (3): 532–544. doi:10.1086/382286. PMC 1182266. PMID 14973781.
  38. ↑ Martina Kujanová, Luísa Pereira, Verónica Fernandes, Joana B. Pereira, Viktor Černý, Near Eastern Neolithic genetic input in a small oasis of the Egyptian Western Desert, American Journal of Physical Anthropology, Volume 140, Issue 2, pages 336–346, October 2009
  39. ↑ Dugoujon J.M., Coudray C., Torroni A., Cruciani F., Scozzari F., Moral P., Louali N., Kossmann M. The Berber and the Berbers: Genetic and linguistic diversities
  40. ↑ Cruciani, F.; La Fratta, R.; Trombetta, B.; Santolamazza, P.; Sellitto, D.; Colomb, E. B.; Dugoujon, J.-M.; Crivellaro, F. et al. (2007). "Tracing Past Human Male Movements in Northern/Eastern Africa and Western Eurasia: New Clues from Y-Chromosomal Haplogroups E-M78 and J-M12" (PDF). Molecular Biology and Evolution 24 (6): 1300–1311. doi:10.1093/molbev/msm049. PMID 17351267.
  41. ↑ Henn, BM; Botigué, LR; Gravel, S; Wang, W; Brisbin, A et al. (2012). "Genomic Ancestry of North Africans Supports Back-to-Africa Migrations". PLoS Genet 8 (1): e1002397. doi:10.1371/journal.pgen.1002397. PMC 3257290. PMID 22253600.
  42. ↑ North African Populations Carry the Signature of Admixture with Neandertals. Sánchez-Quinto F, Botigué LR, Civit S, Arenas C, Ávila-Arcos MC, et al. (2012) North African Populations Carry the Signature of Admixture with Neandertals" PLoS ONE 7(10) e47765. doi:10.1371/journal.pone.0047765
  43. ↑ Hassan, Hisham Y.; Underhill, Peter A.; Cavalli-Sforza, Luca L.; Ibrahim, Muntaser E. (2008). "Y-Chromosome Variation Among Sudanese:Restricted Gene Flow, Concordance With Language, Geography, and History" (PDF). American Journal of Physical Anthropology 137 (3): 316–23. doi:10.1002/ajpa.20876. PMID 18618658.