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Cited by 52Forensic and Genetic ResearchGenetic diversity and population structurePleistocene-Era Hominins and Archaeology

Genome-Wide and Paternal Diversity Reveal a Recent Origin of Human Populations in North Africa

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Fadhlaoui-Zid, Karima, Haber, Marc, Martínez-Cruz, Begoña, Zalloua, Pierre, Benammar Elgaaied, Amel, Comas, David·2013·PLoS ONE
DOI 10.1371/journal.pone.0080293PMC PMC3842387
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Abstract

The geostrategic location of North Africa as a crossroad between three continents and as a stepping-stone outside Africa has evoked anthropological and genetic interest in this region. Numerous studies have described the genetic landscape of the human population in North Africa employing paternal, maternal, and biparental molecular markers. However, information from these markers which have different inheritance patterns has been mostly assessed independently, resulting in an incomplete description of the region. In this study, we analyze uniparental and genome-wide markers examining similarities or contrasts in the results and consequently provide a comprehensive description of the evolutionary history of North Africa populations. Our results show that both males and females in North Africa underwent a similar admixture history with slight differences in the proportions of admixture components. Consequently, genome-wide diversity show similar patterns with admixture tests suggesting North Africans are a mixture of ancestral populations related to current Africans and Eurasians with more affinity towards the out-of-Africa populations than to sub-Saharan Africans. We estimate from the paternal lineages that most North Africans emerged ∼15,000 years ago during the last glacial warming and that population splits started after the desiccation of the Sahara. Although most North Africans share a common admixture history, the Tunisian Berbers show long periods of genetic isolation and appear to have diverged from surrounding populations without subsequent mixture. On the other hand, continuous gene flow from the Middle East made Egyptians genetically closer to Eurasians than to other North Africans. We show that genetic diversity of today's North Africans mostly captures patterns from migrations post Last Glacial Maximum and therefore may be insufficient to inform on the initial population of the region during the Middle Paleolithic period.

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  • Craniometric analyses have suggested an affinity between the Natufians and populations of north or sub-Saharan Africa.

    “Craniometric analyses have suggested an affinity between the Natufians and populations of north or sub-Saharan Africa24,25”

    From Genomic insights into the origin of farming in the ancient Near East (2016) · cites this paper as [25]

    The Introduction discusses genetic affinities of present-day North Africans, and the Discussion mentions lithic similarities between North Africa and the Middle East. Neither addresses Natufians or craniometric affinity. Searches for Natufians and cranial morphology found no passage supporting the attributed claim. (LLM, conf=0.76)

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  1. [3]Garcea EAA (2010) The spread of Aterian peoples in North Africa. In: GarceaEAA, editor. South-Eastern Mediterranean Peoples Between 130,000 and 10,000 years ago. Oxford: Oxbow Books.
  2. [6]Camps G (1982) Beginnings of pastoralism and cultivation in north-west Africa and the Sahara: origins of the Berbers. In: The Cambridge History of Africa Vol1: from the earliest times to c500 BC, JD Clark, ed Cambridge: Cambridge University Press: 548–612.
  3. [7]Murdock GP (1959) Africa, Its Peoples and their Culture History. New York, Toronto, London: McGraw-Hill Book Company.
  4. [9]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– 154. 7802092
  5. [10]Bosch E, Calafell F, Perez-Lezaun A, Comas D, Mateu E, et al (1997) Population history of north Africa: evidence from classical genetic markers. Hum Biol 69: 295– 311. 9164042
  6. [11]Chaabani H, Helal AN, van Loghem E, Langaney A, Benammar Elgaaied A, et al (1984) Genetic study of Tunisian Berbers. I. Gm, Am and Km immunoglobulin allotypes and ABO blood groups. J Immunogenet 11: 107– 113. 6427354
  7. [12]Loveslati BY, Sanchez-Mazas A, Ennafaa H, Marrakchi R, Dugoujon JM, et al (2001) A study of Gm allotypes and immunoglobulin heavy gamma IGHG genes in Berbers, Arabs and sub-Saharan Africans from Jerba Island, Tunisia. Eur J Immunogenet 28: 531– 538. 11881820
  8. [13]Fadhlaoui-Zid K, Dugoujon JM, Elgaaied A, Amor MB, Yacoubi B, et al (2004a) Genetic diversity in Tunisia: a study based on the GM polymorphism of human immunoglobulins. Hum Biol 76: 559– 567. 15754972
  9. [14]Abdennaji Guenounou B, Loueslati BY, Buhler S, Hmida S, Ennafaa H, et al (2006) HLA class II genetic diversity in southern Tunisia and the Mediterranean area. Int J Immunogenet 33: 93– 103. 16611253
  10. [15]Fadhlaoui-Zid K, Buhler S, Dridi A, Benammar El Gaaied A, Sanchez-Mazas A (2010) Polymorphism of HLA class II genes in Berbers from Southern Tunisia. Tissue Antigens 76: 416– 420. 20670354
  11. [16]Bosch E, Calafell F, Perez-Lezaun A, Clarimon J, Comas D, et al (2000) Genetic structure of north-west Africa revealed by STR analysis. Eur J Hum Genet 8: 360– 366. 10854096
  12. [17]Cherni L, Loueslati Yaacoubi B, Pereira L, Alves C, Khodjet-El-Khil H, et al (2005a) Data for 15 autosomal STR markers (Powerplex 16 System) from two Tunisian populations: Kesra (Berber) and Zriba (Arab). Forensic Sci Int 147: 101– 106. 15541599
  13. [18]Coudray C, Calderon R, Guitard E, Ambrosio B, Gonzalez-Martin A, et al (2007) Allele frequencies of 15 tetrameric short tandem repeats (STRs) in Andalusians from Huelva (Spain). Forensic Sci Int 168: e21– 24. 17337332
  14. [19]Khodjet-El-Khil H, Fadhlaoui-Zid K, Gusmao L, Alves C, Benammar-Elgaaied A, et al (2008) Substructure of a Tunisian Berber population as inferred from 15 autosomal short tandem repeat loci. Hum Biol 80: 435– 448. 19317598
  15. [20]Comas D, Calafell F, Benchemsi N, Helal A, Lefranc G, et al (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– 319. 11129330
  16. [21]Flores C, Maca-Meyer N, Gonzalez AM, Cabrera VM (2000) Northwest African distribution of the CD4/Alu microsatellite haplotypes. Ann Hum Genet 64: 321– 327. 11415516
  17. [22]Gonzalez-Perez E, Via M, Esteban E, Lopez-Alomar A, Mazieres S, et al (2003) Alu insertions in the Iberian Peninsula and north west Africa—genetic boundaries or melting pot? Coll Antropol 27: 491– 500. 14746135
  18. [23]Ennafaa H, Amor MB, Yacoubi-Loueslati B, Khodjet el-khil H, Gonzalez-Perez E, et al (2006) Alu polymorphisms in Jerba Island population (Tunisia): comparative study in Arab and Berber groups. Ann Hum Biol 33: 634– 640. 17381061
  19. [24]Frigi S, Ennafaa H, Ben Amor M, Cherni L, Ben Ammar-Elgaaied A (2011) Assessing human genetic diversity in Tunisian Berber populations by Alu insertion polymorphisms. Ann Hum Biol 38: 53– 58. 20545473
  20. [25]Henn BM, Botigue LR, Gravel S, Wang W, Brisbin A, et al (2012) Genomic ancestry of North Africans supports back-to-Africa migrations. PLoS Genet 8: e1002397. 22253600 PMC3257290
  21. [26]Haber M, Gauguier D, Youhanna S, Patterson N, Moorjani P, et al (2013) Genome-wide diversity in the levant reveals recent structuring by culture. PLoS Genet 9: e1003316. 23468648 PMC3585000
  22. [27]Botigué LR, Henn BM, Gravel S, Maples BK, Gignoux CR, et al.. (2013) Gene flow from North Africa contributes to differential human genetic diversity in Southern Europe. Proceedings of the National Academy of Sciences USA: in press. PMC3718088 23733930
  23. [28]Bosch E, Calafell F, Comas D, Oefner PJ, Underhill PA, et al (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– 1029. 11254456 PMC1275654
  24. [29]Arredi B, Poloni ES, Paracchini S, Zerjal T, Fathallah DM, et al (2004) A predominantly neolithic origin for Y-chromosomal DNA variation in North Africa. Am J Hum Genet 75: 338– 345. 15202071 PMC1216069
  25. [30]Cruciani F, La Fratta R, Santolamazza P, Sellitto D, Pascone R, et al (2004) Phylogeographic analysis of haplogroup E3b (E-M215) y chromosomes reveals multiple migratory events within and out of Africa. Am J Hum Genet 74: 1014– 1022. 15042509 PMC1181964
  26. [31]Cruciani F, La Fratta R, Trombetta B, Santolamazza P, Sellitto D, 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. Mol Biol Evol 24: 1300– 1311. 17351267
  27. [32]Cruciani F, Trombetta B, Sellitto D, Massaia A, Destro-Bisol G, et al (2010) Human Y chromosome haplogroup R-V88: a paternal genetic record of early mid Holocene trans-Saharan connections and the spread of Chadic languages. Eur J Hum Genet 18: 800– 807. 20051990 PMC2987365
  28. [33]Semino O, Magri C, Benuzzi G, Lin AA, Al-Zahery N, et al (2004) 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 74: 1023– 1034. 15069642 PMC1181965
  29. [34]Ottoni C, Larmuseau MH, Vanderheyden N, Martinez-Labarga C, Primativo G, et al (2011) Deep into the roots of the Libyan Tuareg: a genetic survey of their paternal heritage. Am J Phys Anthropol 145: 118– 124. 21312181
  30. [35]Pereira L, Cerny V, Cerezo M, Silva NM, Hajek M, et al (2010) Linking the sub-Saharan and West Eurasian gene pools: maternal and paternal heritage of the Tuareg nomads from the African Sahel. Eur J Hum Genet 18: 915– 923. 20234393 PMC2987384
  31. [36]Zalloua PA, Xue Y, Khalife J, Makhoul N, Debiane L, et al (2008) Y-chromosomal diversity in Lebanon is structured by recent historical events. Am J Hum Genet 82: 873– 882. 18374297 PMC2427286
  32. [37]Haber M, Platt DE, Badro DA, Xue Y, El-Sibai M, et al (2011) Influences of history, geography, and religion on genetic structure: the Maronites in Lebanon. Eur J Hum Genet 19: 334– 340. 21119711 PMC3062011
  33. [38]Zalloua PA, Platt DE, El Sibai M, Khalife J, Makhoul N, et al (2008) Identifying genetic traces of historical expansions: Phoenician footprints in the Mediterranean. Am J Hum Genet 83: 633– 642. 18976729 PMC2668035
  34. [39]Fadhlaoui-Zid K, Martinez-Cruz B, Khodjet-el-khil H, Mendizabal I, Benammar-Elgaaied A, et al (2011b) Genetic structure of Tunisian ethnic groups revealed by paternal lineages. Am J Phys Anthropol 146: 271– 280. 21915847
  35. [40]Ennafaa H, Fregel R, Khodjet-El-Khil H, Gonzalez AM, Mahmoudi HA, et al (2011) Mitochondrial DNA and Y-chromosome microstructure in Tunisia. J Hum Genet 56: 734– 741. 21833004
  36. [41]Fadhlaoui-Zid K, Plaza S, Calafell F, Ben Amor M, Comas D, et al (2004b) Mitochondrial DNA heterogeneity in Tunisian Berbers. Ann Hum Genet 68: 222– 233. 15180702
  37. [42]Plaza S, Calafell F, Helal A, Bouzerna N, Lefranc G, et al (2003) Joining the Pillars of Hercules: mtDNA sequences show multidirectional gene flow in the western Mediterranean. Ann Hum Genet 67: 312– 328. 12914566
  38. [43]González AM, Cabrera VM, Larruga JM, Tounkara A, Noumsi G, et al (2006) Mitochondrial DNA variation in Mauritania and Mali and their genetic relationship to other Western Africa populations. Ann Hum Genet 70: 631– 657. 16907709
  39. [44]Harich N, Costa MD, Fernandes V, Kandil M, Pereira JB, et al (2010) The trans-Saharan slave trade-clues from interpolation analyses and high resolution characterization of mitochondrial DNA lineages. BMC Evol Biol 10: 138– 156. 20459715 PMC2875235
  40. [45]Fadhlaoui-Zid K, Rodriguez-Botigue L, Naoui N, Benammar-Elgaaied A, Calafell F, et al (2011a) Mitochondrial DNA structure in North Africa reveals a genetic discontinuity in the Nile Valley. Am J Phys Anthropol 145: 107– 117. 21312180
  41. [46]Badro DA, Douaihy B, Haber M, Youhanna SC, Salloum A, et al (2013) Y-chromosome and mtDNA genetics reveal significant contrasts in affinities of modern Middle Eastern populations with European and African populations. PLoS One 8: e54616. 23382925 PMC3559847
  42. [47]Karafet TM, Mendez FL, Meilerman MB, Underhill PA, Zegura SL, et al (2008) New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree. Genome Res 18: 830– 838. 18385274 PMC2336805
  43. [48]Gill P, Jeffreys AJ, Werrett DJ (1985) Forensic application of DNA ‘fingerprints’. Nature 318: 577– 579. 3840867
  44. [49]Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37– 48. 10331250
  45. [50]Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564– 567. 21565059
  46. [52]Jolliffe I (1986) Principal Coponents Analysis. Second Edition New York, NY: Springer.
  47. [53]Wilson IJ, Weale ME, Balding DJ (2003) Inferences from DNA data: population histories, evolutionary processes and forensic match probabilities. Journal of the Royal Statistical Society A 166, part 2.
  48. [54]Balaresque P, Bowden GR, Adams SM, Leung HY, King TE, et al (2010) A predominantly neolithic origin for European paternal lineages. PLoS Biol 8: e1000285. 20087410 PMC2799514
  49. [55]Weale ME, Weiss DA, Jager RF, Bradman N, Thomas MG (2002) Y chromosome evidence for Anglo-Saxon mass migration. Mol Biol Evol 19: 1008– 1021. 12082121
  50. [56]Rebala K, Martinez-Cruz B, Tonjes A, Kovacs P, Stumvoll M, et al.. (2012) Contemporary paternal genetic landscape of Polish and German populations: from early medieval Slavic expansion to post-World War II resettlements. Eur J Hum Genet. PMC3598329 22968131
  51. [59]Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, et al (2008) Worldwide human relationships inferred from genome-wide patterns of variation. Science 319: 1100– 1104. 18292342
  52. [60]Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559– 575. 17701901 PMC1950838
  53. [61]Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2: e190. 17194218 PMC1713260
  54. [64]Brovkin V, Claussen M (2008) Comment on “Climate-driven ecosystem succession in the Sahara: the past 6000 years”. Science 322: 1326; author reply 1326. 19039121
  55. [65]Kropelin S, Verschuren D, Lezine AM, Eggermont H, Cocquyt C, et al (2008) Climate-driven ecosystem succession in the Sahara: the past 6000 years. Science 320: 765– 768. 18467583
  56. [66]Bar-Yosef O (1987) Pleistocene Connexions between Africa and Southwest Asia: An Archaeological Perspective. The African Archaeological Review 5: 29– 38.
  57. [67]Balter M (2011) Was North Africa The Launch Pad For Modern Human Migrations? Science 331: 20– 23. 21212332

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Authors
Fadhlaoui-Zid, K., Haber, M., Martínez-Cruz, B., Zalloua, P., Benammar Elgaaied, A., & Comas, D.
Affiliations
  • Consejo Superior de Investigaciones Científicas (ES)
  • Lebanese American University (LB)
Corresponding author
Comas, David
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2013-11-27
Volume
8
Issue
11
Pages
e80293
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0080293
PMC
PMC3842387
OpenAlex
W2097341043
Cited by
52
References
4
Citations by year
2026: 1 · 2025: 3 · 2024: 3 · 2023: 2 · 2022: 1 · 2021: 6 · 2020: 2 · 2019: 8 · 2018: 7 · 2017: 5 · 2016: 6 · 2015: 5 · 2014: 3
FWCI
3.10
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RECERCAT (Consorci de Serveis Universitaris de Catalunya) (publishedVersion, other-oa)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • University of Birmingham Research Portal (University of Birmingham) (submittedVersion, other-oa)
  • Repositori digital de la UPF (Universitat Pompeu Fabra) (submittedVersion, cc-by)
Funders
Ministerio de Asuntos Exteriores y de Cooperación
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Forensic and Genetic Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
  • Social Sciences › Anthropology › Pleistocene-Era Hominins and Archaeology
Keywords
North African populations, population structure, paternal lineages, maternal lineage, genome-wide variation, Berbers, Egyptians, Last Glacial Maximum, out-of-Africa migration, human evolutionary history, uniparental markers
MeSH terms
Africa, Northern, Genetics, Population, Humans, Genetic Linkage, Male, Genetic Variation, Genome, Human, Cluster Analysis, Evolution, Molecular, Chromosomes, Human, Y, Genome-Wide Association Study

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