Abstract
The complex demographic history of human populations in North Africa has resulted in a high degree of genetic heterogeneity across the region. However, little is known about the pattern of these genetic variations in its current populations. The present study provides new data on the genetic background of Chaouia, an Arabic-speaking North African population in the western center of Morocco. A random sample of 150 unrelated healthy individuals from Chaouia was assessed using the AmpFLSTR Identifiler kit. The most polymorphic markers were D21S11 and D18S51, with 23 and 22 alleles, respectively. After Bonferroni’s correction, two loci (TH01 and D18S51) deviated from Hardy–Weinberg equilibrium. The phylogeny analysis separated North African populations into northeastern and northwestern groups. The Chaouia population was clustered with northwestern Africans. It was the closest to the Berbers of Azrou. The Chaouia shared close genetic affinities with populations from North Africa, the Middle East, and Europe, particularly Iberians, and to a lesser extent with sub-Saharan populations. The pattern of genetic admixture varied across North African populations without a clear correlation between their geographic (northeastern or northwestern) or linguistic identities (Arab or Berber), however, genetic heterogeneity among Berbers was observed. These findings suggest that the diversity observed in North African populations extends geographical and linguistic boundaries. It is further linked to each population's unique and complex demographic history. Human North African population genetics seems to present an intriguing landscape for future studies in the region and its surrounding populations to trace the origins of the genetic heterogeneity observed in these populations.
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The data supporting the findings of this study are submitted as supplementary materials. The genotypic data are available upon request from the corresponding author.
References
Abdeli A, Benhassine T (2020) Genetic diversity of 15 autosomal STRs in a sample of Berbers from Aurès region in the Northeast of Algeria and genetic relationships with other neighbouring samples. Ann Hum Biol 47(3):284–293. https://doi.org/10.1080/03014460.2020.1736628
Alenizi M, Goodwin W, Ismael S, Hadi S (2008) STR data for the AmpFℓSTR® Identifiler® loci in Kuwaiti population. Leg Med 10(6):321–325. https://doi.org/10.1016/j.legalmed.2008.05.003
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(3):458–472. https://doi.org/10.1016/s1055-7903(03)00039-3
Amir N, Sahnoune M, Chikhi L, Atmani D (2015) STR-based genetic structure of the Berber population of Bejaia (Northern Algeria) and its relationships to various ethnic groups. Gene 574(1):140–148. https://doi.org/10.1016/j.gene.2015.08.002
Arauna LR, Comas D (2017) Genetic heterogeneity between Berbers and Arabs. ELS. https://doi.org/10.1002/9780470015902.a0027485
Arauna LR, Mendoza-Revilla J, Mas-Sandoval A, Izaabel H, Bekada A, Benhamamouch S, Fadhlaoui-Zid K, Zalloua P, Hellenthal G, Comas D (2017) Recent historical migrations have shaped the gene pool of Arabs and Berbers in North Africa. Mol Biol Evol 34(2):318–329. https://doi.org/10.1093/molbev/msw218
Babiker HMA, Schlebusch CM, Hassan HY, Jakobsson M (2011) Genetic variation and population structure of Sudanese populations as indicated by 15 Identifiler sequence-tagged repeat (STR) loci. Investig Genet. https://doi.org/10.1186/2041-2223-2-12
Barni F, Berti A, Pianese A, Boccellino A, Miller MP, Caperna A, Lago G (2007) Allele frequencies of 15 autosomal STR loci in the Iraq population with comparisons to other populations from the middle-eastern region. Forensic Sci Int 167(1):87–92. https://doi.org/10.1016/j.forsciint.2006.03.005
Bosch E, Calafell F, Pérez-Lezaun A, Comas D, Mateu E, Bertranpetit J (1997) Population history of north Africa: evidence from classical genetic markers. Hum Biol 69(3):295–311
Bosch E, Calafell F, Pérez-Lezaun A, Clarimón J, Comas D, Mateu E, Martínez-Arias R, Morera B, Brakez Z, Akhayat O, Sefiani A, Hariti G, Cambon-Thomsen A, Bertranpetit J (2000) Genetic structure of north-west Africa revealed by STR analysis. Eur J Hum Genet 8(5):360–366. https://doi.org/10.1038/sj.ejhg.5200464
Bosch E, Calafell F, Comas D, Oefner PJ, Underhill PA, Bertranpetit J (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(4):1019–1029. https://doi.org/10.1086/319521
Botigué LR, Henn BM, Gravel S, Maples BK, Gignoux CR, Corona E, Atzmon G, Burns E, Ostrer H, Flores C, Bertranpetit J, Comasa D, Bustamante CD (2013) Gene flow from North Africa contributes to differential human genetic diversity in southern europe. Proc Natl Acad Sci USA 110(29):11791–11796. https://doi.org/10.1073/pnas.1306223110
Butler JM (2006) Genetics and genomics of core short tandem repeat loci used in human identity testing. J Forensic Sci 51(2):253–265. https://doi.org/10.1111/j.1556-4029.2006.00046.x
Cadenas AM, Zhivotovsky LA, Cavalli-Sforza LL, Underhill PA, Herrera RJ (2008) Y-chromosome diversity characterizes the Gulf of Oman. Eur J Hum Genet 16(3):374–386. https://doi.org/10.1038/sj.ejhg.5201934
Camacho MV, Benito C, Figueiras AM (2007) Allelic frequencies of the 15 STR loci included in the AmpFlSTR® Identifiler™ PCR amplification kit in an autochthonous sample from Spain. Forensic Sci Int 173(2–3):241–245. https://doi.org/10.1016/j.forsciint.2007.02.006
Canossi A, Piancatelli D, Aureli A, Oumhani K, Ozzella G, Del Beato T, Liberatore G, El Aouad R, Adorno D (2010) Correlation between genetic HLA class i and II polymorphisms and anthropological aspects in the Chaouya population from Morocco (Arabic speaking). Tissue Antigens. https://doi.org/10.1111/j.1399-0039.2010.01498.x
Cheffi K, Dahbi N, El Khair A, Stambouli H, Elbouri A, Talbi J, Hilali A, El Ossmani H (2022) Consanguinity in the Chaouia population (Morocco): prevalence, trends, determinants, fertility, and spontaneous abortions. Egypt J Med Hum Genet 23(1):128. https://doi.org/10.1186/s43042-022-00337-2
Coudray C, Guitard E, El-Chennawi F, Larrouy G, Dugoujon JM (2007a) Allele frequencies of 15 short tandem repeats (STRs) in three Egyptian populations of different ethnic groups. Forensic Sci Int 169(2–3):260–265. https://doi.org/10.1016/j.forsciint.2006.03.017
Coudray C, Guitard E, Keyser-Tracqui C, Melhaoui M, Cherkaoui M, Larrouy G, Dugoujon JM (2007b) Population genetic data of 15 tetrameric short tandem repeats (STRs) in Berbers from Morocco. Forensic Sci Int 167(1):81–86. https://doi.org/10.1016/j.forsciint.2006.01.003
Coudray C, Olivieri A, Achilli A, Pala M, Melhaoui M, Cherkaoui M, El-chennawi F, Kossmann M, Torroni A, Dugoujon JM (2009) The complex and diversified mitochondrial gene pool of Berber populations. Ann Hum Genet 73(2):196–214. https://doi.org/10.1111/j.1469-1809.2008.00493.x
Cruciani F, Dugoujon JM, Coudray C, Louali N, Kossmann M, Torroni A, Moral P, Scozzari R (2009) The berber and the berbers: genetic and linguistic diversities. John Benjamins Publishing Company, Amsterdam
El Ossmani H, Bouchrif B, Aboukhalid R, Bouabdillah M, Gazzaz B, Zaoui D, Chafik A, Talbi J (2010) Assessment of phylogenetic structure of Berber-speaking population of Azrou using 15 STRs of Identifiler kit. Legal Med. https://doi.org/10.1016/j.legalmed.2009.10.004
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10(3):564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fadhlaoui-Zid K, Martinez-Cruz B, Khodjet-el-khil H, Mendizabal I, Benammar-Elgaaied A, Comas D (2011) Genetic structure of Tunisian ethnic groups revealed by paternal lineages. Am J Phys Anthropol 146(2):271–280. https://doi.org/10.1002/ajpa.21581
Gaibar M, Esteban E, Moral P, Gómez-Gallego F, Santiago C, Bandrés F, Luna F, Fernández-Santander A (2010) STR genetic diversity in a Mediterranean population from the south of the Iberian Peninsula. Ann Hum Biol 37(2):254–267. https://doi.org/10.3109/03014460903341851
Gaibar M, Esteban ME, Via M, Harich N, Kandil M, Fernández-Santander A (2012) Usefulness of autosomal STR polymorphisms beyond forensic purposes: data on Arabic- and Berber-speaking populations from central Morocco. Ann Hum Biol 39(4):297–304. https://doi.org/10.3109/03014460.2012.697578
Garcia-Bertrand R, Simms TM, Cadenas AM, Herrera RJ (2014) United Arab Emirates: phylogenetic relationships and ancestral populations. Gene 533(1):411–419. https://doi.org/10.1016/j.gene.2013.09.092
Gourjon G, Degioanni A (2009) AdFiT v1.7 (Admixture Files Tool): input files creating tool for population genetic admixture estimation software. Bulletins et Mémoires de La Société d’anthropologie de Paris 21(3–4):223–229. https://doi.org/10.4000/bmsap.6586
Gouy A, Zieger M (2017) STRAF-A convenient online tool for STR data evaluation in forensic genetics. Forensic Sci Int Genet 30:148–151. https://doi.org/10.1016/j.fsigen.2017.07.007
Hamamy H, Antonarakis SE, Cavalli-Sforza LL, Temtamy S, Romeo G, Ten Kate LP, Bennett RL, Shaw A, Megarbane A, van Duijn C, Bathija H, Fokstuen S, Engel E, Zlotogora J, Dermitzakis E, Bottani A, Dahoun S, Morris MA, Arsenault S, Bittles AH (2011) Consanguineous marriages, pearls and perils: Geneva International Consanguinity Workshop Report. Genet Med 13(9):841–847. https://doi.org/10.1097/GIM.0b013e318217477f
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9
Harich N, Costa MD, Fernandes V, Kandil M, Pereira JB, Silva NM, Pereira L (2010) The trans-Saharan slave trade—clues from interpolation analyses and high-resolution characterization of mitochondrial DNA lineages. BMC Evol Biol 10(1):1–18. https://doi.org/10.1186/1471-2148-10-138
Henn BM, Botigué LR, Gravel S, Wang W, Brisbin A, Byrnes JK, Fadhlaoui-Zid K, Zalloua PA, Moreno-Estrada A, Bertranpetit J, Bustamante CD, Comas D (2012) Genomic ancestry of North Africans supports back-to-Africa migrations. PLoS Genet. https://doi.org/10.1371/journal.pgen.1002397
Howard-Johnston J (2010) The middle east in the seventh century: Arab conquests. In: Howard-Johnston J (ed) Witnesses to a world crisis: historians and histories of the middle east in the seventh century. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:oso/9780199208593.003.0016
Khodjet-El-Khil H, Fadhlaoui-Zid K, Gusmão L, Alves C, Benammar-Elgaaied A, Amorim A (2008) Substructure of a Tunisian berber population as inferred from 15 autosomal short tandem repeat loci. Hum Biol 80(4):435–448. https://doi.org/10.3378/1534-6617-80.4.435
Khodjet-El-Khil H, Fadhlaoui-Zid K, Gusmão L, Alves C, Benammar-Elgaaied A, Amorim A (2012) Allele frequencies for 15 autosomal STR markers in the Libyan population. Ann Hum Biol 39(1):80–83. https://doi.org/10.3109/03014460.2011.630678
Khubrani YM, Hallast P, Jobling MA, Wetton JH (2019) Massively parallel sequencing of autosomal STRs and identity-informative SNPs highlights consanguinity in Saudi Arabia. Forensic Sci Int. https://doi.org/10.1016/j.fsigen.2019.102164
Khubrani YM, Wetton JH, Jobling MA (2019b) Analysis of 21 autosomal STRs in Saudi Arabia reveals population structure and the influence of consanguinity. Forensic Sci Int Genet 39:97–102. https://doi.org/10.1016/j.fsigen.2018.12.006
Lucas-Sánchez M, Serradell JM, Comas D (2021) Population history of North Africa based on modern and ancient genomes. Hum Mol Genet 30(R1):R17–R23. https://doi.org/10.1093/hmg/ddaa261
Lucas-Sánchez M, Fadhlaoui-Zid K, Comas D (2022) The genomic analysis of current-day North African populations reveals the existence of trans-Saharan migrations with different origins and dates. Hum Genet 142(2):305–320. https://doi.org/10.1007/s00439-022-02503-3
Luna-Vazquez A, Vilchis-Dorantes G, Aguilar-Ruiz MO, Bautista-Rivas A, Rojo-Nava AL, Rios-Barrios E, Rangel-Villalobos H (2005) Population data for 15 loci (Identifiler® Kit) in a sample from the Valley of Mexico. Leg Med 7(5):331–333. https://doi.org/10.1016/j.legalmed.2005.06.002
Marian C, Anghel A, Bel SM, Ferencz BK, Ursoniu S, Dressler M, Popescu O, Budowle B (2007) STR data for the 15 AmpFlSTR identifiler loci in the Western Romanian population. Forensic Sci Int 170(1):73–75. https://doi.org/10.1016/j.forsciint.2006.04.011
Martinez GG, Schaller LC, Brondani A, Bolea M, Martinez-Jarreta B (2011) Allele frequencies of 15 STRs in a representative sample of Entre Ríos province of Argentina population. Forensic Sci Int 3(1):e81–e82. https://doi.org/10.1016/j.fsigss.2011.08.040
Melo MM, Carvalho M, Lopes V, Anjos MJ, Serra A, Vieira DN, Sequeiros J, Corte-Real F (2010) Genetic study of 15 STRs loci of Identifiler system in Angola population. Forensic Sci Int 4(5):e153–e157. https://doi.org/10.1016/j.fsigen.2010.03.010
Mission Scientifique du Maroc. (1915). Villes et tribus du Maroc. Documents et renseignements publiés sous les auspices de la Résidence générale. Casablanca et les Chaouïa: Vol. I. E. Leroux, Paris.
Muñoz P, Pinto de Erazo EL, Baeza C, Arroyo-Pardo E, López-Parra AM (2015) Genetic polymorphism of 15 STR loci in El Salvador. Int J Legal Med 129(5):991–993. https://doi.org/10.1007/s00414-015-1148-8
Omran GA, Rutty GN, Jobling MA (2009) Genetic variation of 15 autosomal STR loci in Upper (Southern) Egyptians. Forensic Sci Int 3(2):e39–e44. https://doi.org/10.1016/j.fsigen.2008.05.007
Ossmani, H. El, Bouchrif, B., Talbi, J., Amri, H. El, & Chafik, A. (2007). La diversité génétique de 15 STR chez la population arabophone de Rabat-Salé-Zemmour-Zaer. Population (English Edition), 55–62.
Ossmani HE, Talbi J, Bouchrif B, Chafik A (2009) Allele frequencies of 15 autosomal STR loci in the southern Morocco population with phylogenetic structure among worldwide populations. Leg Med 11(3):155–158. https://doi.org/10.1016/j.legalmed.2009.01.053
Pérez-Miranda AM, Alfonso-Sánchez MA, Peña JA, Herrera RJ (2006) Qatari DNA variation at a crossroad of human migrations. Hum Hered 61(2):67–79. https://doi.org/10.1159/000092648
Semo AC, Carvalho MR, Bogas V, Serra A, Lopes V, Brito P, Sá FB, Porto MJ, Gonçalves IMT, Corte-Real F (2017) Allelic frequencies of 15 autosomal STRs from two main population groups (Makua and Changana) in Mozambique. Forensic Sci Int 6(September):e286–e288. https://doi.org/10.1016/j.fsigss.2017.09.139
Serra-Vidal G, Lucas-Sanchez M, Fadhlaoui-Zid K, Bekada A, Zalloua P, Comas D (2019) Heterogeneity in palaeolithic population continuity and neolithic expansion in North Africa. Curr Biol 29(22):3953-3959.e4. https://doi.org/10.1016/j.cub.2019.09.050
Shepard EM, Herrera RJ (2006) Iranian STR variation at the fringes of biogeographical demarcation. Forensic Sci Int 158(2–3):140–148. https://doi.org/10.1016/j.forsciint.2005.05.012
Shrivastava P, Jain T, Trivedi VB (2015) Genetic polymorphism study at 15 autosomal locus in central Indian population. Springerplus 4(1):1–12. https://doi.org/10.1186/s40064-015-1364-1
Srithawong S, Muisuk K, Srikummool M, Kampuansai J, Pittayaporn P, Ruangchai S, Liu D, Kutanan W (2021) Close genetic relationship between central Thai and Mon people in Thailand revealed by autosomal microsatellites. Int J Legal Med 135(2):445–448. https://doi.org/10.1007/s00414-020-02290-4
Takezaki N, Nei M (2008) Empirical tests of the reliability of phylogenetic trees constructed with microsatellite DNA. Genetics 178(1):385–392. https://doi.org/10.1534/genetics.107.081505
Takezaki N, Nei M, Tamura K (2014) POPTREEW: Web version of POPTREE for constructing population trees from allele frequency data and computing some other quantities. Mol Biol Evol 31(6):1622–1624. https://doi.org/10.1093/molbev/msu093
Tau T, Wally A, Fanie TP, Ngono GL, Mpoloka SW, Davison S, D’Amato ME (2017) Genetic variation and population structure of Botswana populations as identified with AmpFLSTR Identifiler short tandem repeat (STR) loci. Sci Rep 7(1):6768. https://doi.org/10.1038/s41598-017-06365-y
Tokdemir M, Tunçez FT, Vicdanli NH (2016) Population genetic data for 15 autosomal STR markers in Eastern Turkey. Gene 586(1):36–40. https://doi.org/10.1016/j.gene.2016.03.014
Verzeletti A, Cerri N, Gasparini F, Poglio A, Mazzeo E, De Ferrari F (2009) Population data for 15 autosomal STRs loci and 12 Y chromosome STRs loci in a population sample from the Sardinia island (Italy). Leg Med 11(1):37–40. https://doi.org/10.1016/j.legalmed.2008.06.003
Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10(4):506–513
Wang J (2003) Maximum-likelihood estimation of admixture proportions from genetic data. Genetics 164(2):747–765. https://doi.org/10.1093/genetics/164.2.747
Weisgerber, F. (1935). Casablanca et les Châouïa en 1900. Préface du général d’Amade, avec un plan de Casablanca et une carte des Châouïa, des reproductions d’aquarelles de E. W. Soudan et de photographies de l’auteur et de G. L. Tricot.
Yao J, Wang BJ (2016) Genetic variation of 25 Y-chromosomal and 15 autosomal STR loci in the Han Chinese population of Liaoning Province, northeast China. PLoS ONE 11(8):1–11. https://doi.org/10.1371/journal.pone.0160415
Zlojutro M, Roy R, Palikij J, Crawford MH (2006) Autosomal STR variation in a Basque population: Vizcaya Province. Hum Biol 78(5):599–618. https://doi.org/10.1353/hub.2007.0007
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The authors thank Professor Jinliang Wang for his assistance with the LEADMIX software.
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All authors contributed to the study’s conception and design. Sample collection, material preparation, data collection and analysis were performed by KC. AE and ND were involved in sample collection. HE helped with the experimental work. The first draft of the manuscript was written by KC and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. JT, AH and HE created the initial concept for this study and guided through each step of the process.
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Cheffi, K., El Khair, A., Dahbi, N. et al. Genetic analysis based on 15 autosomal short tandem repeats (STRs) in the Chaouia population, western center Morocco, and genetic relationships with worldwide populations. Mol Genet Genomics 298, 931–941 (2023). https://doi.org/10.1007/s00438-023-02028-y
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DOI: https://doi.org/10.1007/s00438-023-02028-y