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Berbers and Arabs: Tracing the Genetic Diversity and History of Southern Tunisia Through Genome Wide Analysis

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Berbers and Arabs: Tracing the Genetic Diversity and History of Southern Tunisia Through Genome Wide Analysis Berbers and Arabs: tracing the genetic diversity and history of Southern Tunisia through genome wide analysis Paolo Anagnostou1,2*, Valentina Dominici1, Cinzia Battaggia1, Nouri Boukhchim3,4, Jaâfar Ben Nasr5, Ridha Boussoffara6, Emanuele Cancellieri7, Marwa Marnaoui7, Meriem Marzouki8, Hedi Bel Haj Brahim9, Mongi Bou Rass10, Savino Di Lernia7,11†and Giovanni Destro Bisol1,2 † 1 Dipartimento di Biologia Ambientale, Università di Roma “La Sapienza”, Roma, Italia 2 Istituto Italiano di Antropologia, Roma, Italia 3 Faculté des Lettres et Sciences Humaines, Université de Kairouan, Kairouan, Tunisia 4 Laboratoire LMAIM, LR99ES01, Université de Tunis 5 Département d’Archéologie, UR 16 ES 01, Université de Kairouan, Tunisia 6 Institut National du Patrimoine, Tunis, Tunisia 7 Dipartimento di Scienze dell'Antichità, Università di Roma “La Sapienza”, Roma, Italia 8 Université de Tunis, Tunis, Tunisia 9 Artisanat du Sahara, Douz, Tunisia 10 Musée Berbère de Tamezret, Tamezret, Tunisia 11 GAES, University of Witwatersrand, Johannesburg, South Africa * Corresponding author email: [email protected] †These authors contributed equally Running title: Genome-wide diversity in Tunisia populations ABSTRACT Objectives Tunisia has been a crossroads for people from Africa, Europe and the Middle East since prehistoric times. At present, it is inhabited by two main ethnic groups, Arabs and Berbers, and several minorities. This study aims to advance knowledge regarding their genetic structure using new population samplings and a genome-wide approach. Materials and Methods We investigated genomic variation, estimated ancestry components and dated admixture events in three Berber and two Arab populations from Southern Tunisia, mining a dataset including Middle Eastern, sub-Saharan and European populations. Results Differences in the proportion of North African, Arabian and European ancestries and the varying impact of admixture and isolation determined significant heterogeneity in the genetic structure of Southern Tunisia populations. Admixture time estimates show a multilayer pattern of admixture events, involving all three ethno-linguistic groups, which started around the mid XI century and lasted for nearly five centuries. Discussion Our study provides evidence that the relationships between genetic and cultural diversity of old and new inhabitants of North Africa follow different patterns. Unlike what has been hypothesized for Algeria and Morocco, the Berbers of southern Tunisia seem to have preserved a significant part of their original genomic heritage despite Islamization and Arab cultural influence. Whereas Berber groups still share a common genetic background regardless of linguistic diversity and differential admixture, Arabs show clearly different genetic structures: the population from Douz bears multiple signatures of stratification and admixture, while the semi-nomad R’Baya, who have maintained their original Bedouin lifestyle, retain most of the genomic background of Arabian populations. Keywords: North Africa, Berbers, population genomics, haplotype, admixture INTRODUCTION Being placed at the centre of North Africa between two permeable barriers, the Sahara Desert to the south and the Mediterranean Sea to the north, the area corresponding to present-day Tunisia is a natural crossroads between Africa, Europe and the Middle East. Due to this strategic location, Tunisia has been witness to a long parade of invaders, settlers and colonizers who have generated a complex and multilayer population history. The most ancient evidence of human presence in this area dates back at least to the late Middle Pleistocene. Over the centuries, Tunisia has been peopled by human groups bearing different cultures, from the Acheulean (Belhouchet 2003; Sahnouni et al., 2013), the Middle Stone Age, dating back to at least 90 Kya (Aouadi-Abdeljaouad et Belhouchet, 2012) up to the Capsian culture (10-4.7 Kya)(Rahmani, 2004; Mulazzani, 2013; Di Lernia et al., 2017). The latter persisted even after the introduction of pastoralism agricultural practices, which took place in North Africa as early as around 7400 kya, likely through contacts and cultural exchanges with different regions and people (Linstädter et al., 2012; Mulazzani et al., 2016). Starting from the second millennium BCE, Tunisia was occupied by the Phoenicians who were succeeded by Romans and, from the 5th century CE by other domains including Vandals, Byzantines, Arabs, Ottomans and finally French (Modéran, 2003; Lassere, 2015). All of these dominations left recognizable traits on the cultural heritage and, possibly, on the genetic makeup of Berbers (Brett et Fentress, 1996), the “autochthonous” inhabitants of North Africa (Collignon, 1886). The most significant and impacting population movement was that involved the Arabic peoples, who converted local populations to their Islamic religion and forced most Berber communities to adopt their Arabic culture and language. Starting in the mid-7th century CE, the Arab invasions initially involved only a few thousand migrants (McEvedy and Jones, 1980). In the 11th century, a considerably larger Arab wave led by Bedouin tribes (Banu Hilal and Banu Sulaym) reached the area of the Maghreb. This event is considered to be the most important of the entire medieval period in the Maghreb (Hess et Julien, 1971), counting from 150,000 to 300,000 Bedouins (El Hareir et Mbaye, 2011). The Arab and Berber dynasties persisted until the 16th century, when the Ottoman took control of the country (Naylor, 2010; Guellouz et al 2010). This complex migratory and cultural history shaped the current ethno-linguistic diversity of today’s Tunisian populations (Leveau, 2018). The two major extant linguistic groups, Arabic and Berbers, are both branches of the Afro-asiatic family (Ruhlen, 1991). A variety of the former, known as Tunsi, is spoken by nearly 99% of the population (Sayahi, 2014; Battenburg, 1999). The latter, or better a series of dialects comprised into the Zenati language branch (Kossmann, 2013), are still spoken in small enclaves concentrated in the southern and southeastern areas of the country which count from 1% to 0.5% of the overall Tunisian population depending on different estimates (Garmadi, 1968, Penchoen 1968, Battenburg, 1999). The cultural diversity is greatest in the northern areas, where the Turco-Tunisians are settled in the coastal cities and on the island of Jerba, which is also home, along with the capital Tunis, of the Jewish community. The southern desertic areas of Tunisia are inhabited by nomadic and semi-nomadic populations of Berber and Bedouin origin (Dupire, 1963). To complete the picture, descendants of the Morisco Andalusians, who were expelled from Spain after the “Reconquista” in 1609, occupy villages and quarters in the capital (Saadaoui, 1996, 2001). While Tunisian populations are known to be characterized by the remarkable cultural diversity outlined above, the structure of their genetic variation studies has yet to be exhaustively investigated. Most of the studies conducted so far have used unilinear polymorphisms, which may help trace specific demographic events but cannot investigate the genetic structure in all its aspects (Fadhlaoui-Zid et al., 2004; Loueslati et al., 2006; Cherni et al., 2009; Fadhlaoui-Zid et Benammar- Elgaaied, 2010; Ennafaa et al., 2011; Kefi et al., 2015; Frigi et al., 2017; Elkamel et al. 2017, Cherni, 2018). Furthermore, genomic approaches, which can define the relationships among individuals and groups more comprehensively, have been limited to Berbers (Henn et al., 2012; Arauna et al., 2017). Finally, some areas, more in particular the southern part of the country, have yet to be adequately investigated. Here we present the results of a new study of genome-wide variation carried out among Arabs, Berbers and R’Baya nomads of Southern Tunisia. Applying an allele and haplotype-based approach, we assess their genomic relationships, reconstruct their admixture history and make inferences on the relationships between genetic and cultural diversity. MATERIALS AND METHODS Populations under study Our dataset includes new data relative to three ethno-linguistic groups of southern Tunisia and literature results pertaining to Berbers and populations from North and sub-Saharan Africa, the Arabian Peninsula, Middle East and Europe (see Supplementary Table S1 and Figure 1). We obtained saliva samples from a total of 80 individuals enrolled following the “grandparents” rule after obtaining informed consent and ethnological, linguistic and familiar information. Thirty- two samples of self-reported Tunisian Arabs were collected in the wider region of the Nefzaoua, mostly in the city of Douz (33° 27′ 0″ N, 9° 1′ 0″ E). Historical sources suggest that this area represents a possible settlement point for the Arab newcomers in the middle ages and also home for Arabized Berber communities (Ellefi, 2016). Fifteen samples of Arab-speaking self-reported Berbers in Matmata (33° 32′ 33.5″ N, 9° 58′ 0.5″ E) and 26 samples of Berber-speaking self-reported Berbers in Nouvelle Zraoua (N=16; 33° 39' 40.1'' N, 9° 47' 34.7'' E ) and Tamezret (N=10; 33° 32' 00" N, 9° 52' 00" E) were sampled. We also gathered saliva samples from seven R’Baya individuals, a small group (nearly 14,000 members) of semi-nomadic herders whose oral chronicles set their origin in the Arabian Peninsula, more precisely in Yemen and their arrival in North Africa between the 11th and the 18th century AC (Dupire, 1963). All experimental protocols were approved
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