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Genetic Structure of Tunisian Ethnic Groups Revealed by Paternal Lineages

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Genetic Structure of Tunisian Ethnic Groups Revealed by Paternal Lineages AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 146:271–280 (2011) Genetic Structure of Tunisian Ethnic Groups Revealed by Paternal Lineages Karima Fadhlaoui-Zid,1 Begon˜ a Martinez-Cruz,2 Houssein Khodjet-el-khil,1 Isabel Mendizabal,2 Amel Benammar-Elgaaied,1 and David Comas2* 1Laboratory of Genetics, Immunology and Human Pathology, Faculty of Sciences of Tunis, University Tunis El Manar, 1068 Tunis, Tunisia 2Institut de Biologia Evolutiva (CSIC-UPF), Department de Cie`ncies Experimentals i de la Salut, Universitat Pompeu Fabra, 08003 Barcelona, Spain KEY WORDS Tunisia; Berbers; Andalusians; binary markers; SNP; STR; Y-chromosome haplogroups; Y-chromosome phylogeography; human population genetics ABSTRACT Tunisia has experienced a variety of lineage was the North African haplogroup E-M81 (71%), human migrations that have modeled the myriad cul- being fixed in two Berber samples (Chenini–Douiret and tural groups inhabiting the area. Both Arabic and Ber- Jradou), suggesting isolation and genetic drift. Differen- ber-speaking populations live in Tunisia. Berbers are tial levels of paternal gene flow from the Near East were commonly considered as in situ descendants of peoples detected in the Tunisian samples (J-M267 lineage over who settled roughly in Palaeolithic times, and posterior 30%); however, no major sub-Saharan African or Euro- demographic events such as the arrival of the Neolithic, pean influence was found. This result contrasts with the the Arab migrations, and the expulsion of the ‘‘Moors’’ high amount of sub-Saharan and Eurasian maternal lin- from Spain, had a strong cultural influence. Nonetheless, eages previously described in Tunisia. Overall, our the genetic structure and the population relationships of results reveal a certain genetic inter-population diver- the ethnic groups living in Tunisia have been poorly sity, especially among Berber groups, and sexual asym- assessed. In order to gain insight into the paternal metry, paternal lineages being mostly of autochthonous genetic landscape and population structure, more than origin. In addition, Andalusians, who are supposed to be 40 Y-chromosome single nucleotide polymorphisms and migrants from southern Spain, do not exhibit any sub- 17 short tandem repeats were analyzed in five Tunisian stantial contribution of European lineages, suggesting a ethnic groups (three Berber-speaking isolates, one Anda- North African origin for this ethnic group. Am J Phys lusian, and one Cosmopolitan Arab). The most common Anthropol 146:271–280, 2011. VC 2011 Wiley-Liss, Inc. Because of its strategic geographic location, Tunisia language (Ibn Khaldoun, 1968). The only populations has been a crossroads of multiple civilizations and a that escaped this influence were some tribes that were point of contact for many human migrations during suc- forced back to the mountains or settled in remote vil- cessive historical periods. At present, both Arabic and lages located in the north and south of Tunisia and Berber-speaking populations live in Tunisia. Arab origins maintained their tribal structures (e.g., Jradou, Sened, in Tunisia can be traced back to the Islamic expansions Matmata, and Chenini–Douiret). In more recent times, of the 7th century AD, but the origin of the Berbers, the most important population movement from Iberia to both within and outside of Tunisia, is a matter of debate. Berbers are commonly considered as in situ descendants of local Palaeolithic and/or Mesolithic populations, and Additional Supporting Information may be found in the online archaeological data points to a human occupation of version of this article. North Africa since at least 45,000 years ago, as attested Grant sponsor: Direccio´n General de Investigacio´n, Ministerio de by the Aterian industry (Garcea and Giraudi, 2006) and Ciencia e Innovacio´n, Spain; Grant number: CGL2010-14944/BOS. subsequent cultures until the Neolithic (the adoption of Grant sponsor: Tunisian Ministry of High Education and Scientific agriculture and husbandry), which began around 5,500 Research; Programa de Cooperacio´n Interuniversitaria e Investiga- years ago in the region (Camps, 1974; Camps, 1982). As cio´n Cientı´fica (AECI), Ministerio de Asuntos Exteriores y Coopera- a result, the current Tunisian population is composed of cio´n, Spain; Grant numbers: A/5180/06, A/8394/07, and B/018514/08. an ancient Berber background together with influences Grant sponsor: Direccio´ General de Recerca, Generalitat de Catalu- from the different civilizations settled in this region in nya; Grant number: 2009SGR1101. historical times: Phoenicians (814–146 B.C.), Romans (146–439 B.C.), Vandals (439–534 B.C.), and Byzantines *Correspondence to: David Comas, Institut de Biologia Evolutiva (CSIC-UPF), Department de Cie`ncies Experimentals i de la Salut, (534–647 B.C.). By the end of the 7th century, Arab Universitat Pompeu Fabra, 08003 Barcelona, Spain. armies migrated from the Arabian Peninsula to expand E-mail: [email protected] the Islamic religion and Arabic language into North Africa, and the late 10th century saw an important Received 25 March 2011; accepted 24 May 2011 movement of Arab populations within North Africa, mostly Bedouins (Murdock, 1959; Hiernaux, 1975). DOI 10.1002/ajpa.21581 These latter inter-African migrations had a strong cul- Published online 16 August 2011 in Wiley Online Library tural importance on Berber customs, religion, and (wileyonlinelibrary.com). VC 2011 WILEY-LISS, INC. 272 K. FADHLAOUI-ZID ET AL. North Africa resulted from the expulsion of the ‘‘Moors’’ known sub-Saharan origin of Jerbans, the paternal line- residing in Andalusia (in southern Spain) after Grana- age results revealed a quite homogeneous pattern of da’s capitulation (in 1492 A.D.). Tunisia received a large diversity among Tunisians with a high frequency of the number of immigrants, estimated to have been over autochthonous North African haplogroup E-M81 80,000 ‘‘Andalusians’’ (Abdul-Wahab, 1917), who settled (E1b1b1b, following the nomenclature by Karafet et al., in the north of the country in dispersed, small isolated 2008). However, up to now, no Y-chromosome high villages like Zaghouan village. ‘‘Andalusian’’ villages resolution analyses in well-defined Tunisian ethnic were similar to ancient Arabic towns in Spain (Latham, groups (Berbers, Arabs, and Andalusians) have been 1957), recognized in the many archaeological and cul- carried out. tural imprints, such as the architecture of houses and In order to fill this void and to unravel the genetic mosques (Marcias, 1942; Saadani, 1990), Arab–Andalu- structure of male lineages in Tunisian ethnic groups, we sian music (Marzouki, 1994), marital clothes, and culi- have performed the first high resolution Y-chromosome nary traditions (DeEpalza, 1980; Skhiri, 1968; Skhiri, lineage analysis of Berber-speaking isolates from the 1969). Nowadays, ‘‘Andalusian’’ families are often identi- north and south of Tunisia (Jradou, Sened, and Chenini– fiable by their surnames, such as Zbiss, Marco, and Douiret), Andalusians from Zaghouan, and Cosmopolitan Blanco, which are very different from Arabic ones Arabs from Tunis. In addition, 17 Y-STR loci were typed (Marcias, 1942). to determine the lineage diversity of these ethnic groups. Many studies have attempted to describe the genetic The aim of this work is to evaluate the possible popu- structure of Tunisian populations using different autoso- lation diversity of Tunisians, previously described for the mal markers: the GM and KM allotypes (Chaabani mtDNA, and to analyze the genetic relationships et al., 1984; Loueslati et al., 2001; Fadhlaoui-Zid et al., between different ethnic groups. Overall, these compari- 2004a), HLA class II polymorphisms (Guenounou et al., sons should give us a better understanding of the Tuni- 2006; Fadhlaoui-Zid et al., 2010), autosomal short tan- sian paternal genetic structure and in turn help us to dem repeats (STRs) (Bosch et al., 2001a; Khodjet-El-Khil understand the intricate history of this region. et al., 2008), and polymorphic Alu insertions (Ennafaa et al., 2006; Frigi et al., 2010). These results have sug- gested a certain inter-population diversity in Tunisia MATERIALS AND METHODS compared with Europe and sub-Saharan Africa, with migrations from both neighboring regions but with a Population samples greater Eurasian contribution. Concerning uniparental Blood samples were collected from 159 unrelated markers, mitochondrial DNA analyses have been per- healthy men belonging to the following communities: an formed on different populations from Tunisia (Berbers, urban sample of Arab speakers from the capital Tunis (n Arabs, and Andalusians), showing that Tunisian Berber 5 33); one ‘‘Andalusian’’ community (Zaghouan n 5 32); groups present a remarkable genetic inter-population di- and four small Berber communities (Sened n 5 35; Jra- versity (Fadhlaoui-Zid et al., 2004b; Cherni et al., 2005a; dou n 5 32; Chenini–Douiret n 5 27). Samples from Frigi et al., 2006a; Loueslati et al., 2006). Small effective Chenini and Douiret, two neighboring villages 20 km sizes, founder effects, and isolation processes followed by apart, were pooled in the analyses. Their geographic genetic drift have been postulated as the main factors location is shown in Figure 1. The sampling in the ‘‘An- contributing to current population differentiation of dalusian’’ community was based on a patronymic crite- these Berber samples. Compared with Arab and Andalu- rion, whereas Berbers were Berber Chelha speakers sian groups in Tunisia, Berbers are genetically more
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