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Genetic Heterogeneity Advanced article Article Contents between Berbers and • Introduction • Genetic Diversity in Berber and Arab Groups Arabs • Related Articles

Lara R Arauna, Institut de Biologia Evolutiva (CSIC-UPF), Departament de Ciències Online posting date: 15th September 2017 Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona, Spain David Comas, Institut de Biologia Evolutiva (CSIC-UPF), Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona, Spain

The human population history of North Africa ∼45 000 ya) (Smith et al., 2007). The Aterian is the first prehis- has been different from the rest of the conti- toric industry characterised in North Africa (Barton et al., 2009), nent, and it has been characterised by population which has been suggested to have started around 120 000 ya. replacements, extensive continuous gene ﬂow, Although paradoxical, the Sahara desert has been reported to be a corridor for the movement of people during the ‘green Sahara’ and differential admixture from neighbouring periods thanks to its watercourses. The old dates of AMH remains regions. This complex demographic landscape has and the Sahara corridor leave many open questions about the role yielded a large degree of genetic heterogeneity of North Africa in the origin of modern humans and their disper- among North African populations. Recent histori- sal out of the continent. Different hypotheses have been proposed: cal admixture processes have been inferred from Was North Africa just a stop on the road out of Africa, or did it genome-wide data; no correlation between genet- play a more important role in the evolution of modern humans? ics and ethnic groups has been described, pointing No clear connections have been established between this first to a lack of genetic differentiation between Berber human industry and subsequent cultures in the region, such as the and Arab groups in North Africa. This complex Iberomaurusian industry (22 000–9500 ya) (Newman, 1995). The genetic population structure should be taken into prefix ‘Ibero-’ refers to the ancient presumption that this culture extended into Iberia, although an origin in the Nile River valley is account when designing biomedical approaches in widely accepted (Camps, 1995). The Iberomaurusian culture was North African groups. followed by the Capsian industry (10 000–4700 ya) (Newman, 1995) that persisted well into the Neolithic, which began around 5500 ya in the region. The prehistoric cultural changes in North Africa were independent of the change dynamics on the European Introduction shores of the Mediterranean. Based on archaeology and linguistics, it has been argued Little is known about the initial human settlement in North that the peopling of North Africa has not been continuous and Africa, the movements during the Upper Paleolithic (known as that population replacements may have occurred in different the ‘Late Stone Age’ in the study of African prehistory) and moments. Genetic data (Henn et al., 2012) has supported this the possible introgression from archaic humans, such as Nean- population replacement hypothesis in North Africa, suggesting a derthals (Green et al., 2010) and Denisovans (Reich et al., 2010) back-to-Africa migration from the Middle East in pre-Holocene or other unknown African hominins (Hammer et al., 2011), to times, older than 12 000 ya. The ancestors of today’s North the populations inhabiting this area. Recent description of forms African populations derive at least partially from this migration of Homo sapiens with a mosaic of modern and primitive char- wave; however, it is not clear if this replacement was complete acteristics in North Africa dated back to ∼300 000 ya (years or there might be some traces of ancient continuity in the region. ago) has even challenged the geographical origins of our species Therefore, many open questions remain about the demography of (Hublin et al., 2017). However, the first presence of anatomi- the region in relation to the demographic continuity of humans cally modern humans (AMHs) in North Africa has been estimated since the first occupation of North Africa by modern humans, 190 000–130 000 ya by archaeological studies (much older than such as how many times a population replacement took place and previous estimates that dated the first occupation of the region which are the demographic parameters such as population size of the migrants and where did they come from. eLS subject area: Evolution and Diversity of Life The challenges of the understanding of North African pop- How to cite: ulations are not limited to prehistoric times: in historic times, Arauna, Lara R and Comas, David (September 2017) Genetic North Africa has also experienced a very complex history that is Heterogeneity between Berbers and Arabs. In: eLS. John Wiley reflected in its human demography. Historical records document & Sons, Ltd: Chichester. trade routes across the Sahara and contacts between both Mediter- DOI: 10.1002/9780470015902.a0027485 ranean shores and the Middle East. Phoenicians (814 B.C.) and

Romans (146 B.C.) occupied part of coastal North Africa with this classification is not free of caveats, and populations identi- limited population contributions, which were even less signifi- fied as Arabs or non-Berbers could in fact have a large Berber cant for Vandals (A.D. 429) and Byzantines (A.D. 533) (New- genetic ancestry. It is important to emphasise that the purpose of man, 1995). One of the major historical events in the region this classification is to understand the genetics of North African that changed the cultural and demographic landscape of North populations and in any case to establish socio-cultural groups, Africa is the Arabisation. The first Arab invasion, initially con- which should take into consideration many other aspects (tradi- fined to Egypt, started in A.D. 643 and may have involved onlya tions, identity, etc.). few thousand individuals (McEvedy, 1995). The Arabs began to Despite the scanty genetic data on North African groups, pop- impose their religion and language over the Berber autochthonous ulation genetics might shed some light on the genetic structure of population, a process that culminated with a second and larger Berbers and Arabs, trying to establish the demographic scenarios Arab wave in which the Bedouin reached the Maghreb (northwest that have modelled the current genetic landscape in North Africa. Africa) in the eleventh century. The Islamic expansion even went on to engulf the Iberian Peninsula (A.D. 711). The later arrivals to North Africa in colonial times include Europeans and Ottoman Genetic Diversity in Berber and Turks, mainly in Egypt. Nowadays in North Africa, two main groups of languages are Arab Groups spoken: Berber and Arab dialects. Both belong to the Afroasiatic family, which is a group of languages that might have originated The human genetic data of North Africa is scarce compared to in the Mesolithic, between 15 000 and 10 000 ya. Although it is other regions of the African continent, and most of the African not clear, one of the most plausible places of origin of Afroasiatic genetic diversity studies have been focused on the origin of our languages is the ‘grassland east of the Nile Valley’ (Newman, species and the first dispersions out of Africa (see, for instance, 1995). However, it is unknown if the arrival of the Afroasiatic Tishkoff et al., 2009), the genetic diversity of North African languages was mainly a cultural diffusion process or it also populations and surrounding groups being poorly characterised. implied a relevant demographic movement. The analyses based on frequencies of classical genetic poly- The Berbers (Amazighen, as they call themselves) are con- morphisms (blood groups, red cell enzymes and serum proteins) sidered the autochthonous people of North Africa. As can be have shown that the genetic landscape in North Africa presents an elucidated from the complex and unsolved prehistory and his- east-west pattern of variation without differences between Arabs tory of North Africa, it is difficult to establish an origin for the and Berbers, pointing to a sizeable Upper Paleolithic component Berbers, and many hypotheses have been proposed. Historical in current North African populations, whereas the Neolithic dif- records reveal their presence before the Phoenician arrival to fusion in the region was more a cultural than a demic process the region (Camps, 1998), and archaeologically, it has been sug- (Barbujani et al., 1994;Boschet al., 1997). These classical stud- gested a link between the Capsian culture and the Berber people ies showed little contribution from sub-Saharan populations in (Camps, 1995). However, the Berbers might not have been a uni- North Africans and genetic differentiation from southern Euro- form and homogeneous group, since it has been known that the peans, including Iberians (Bosch et al., 1997). However, the anal- populations that inhabited North Africa by the time of the Phoeni- ysis of mtDNA lineages has shown an important sub-Saharan cian arrival were a composite group known as Libyco-Berbers, contribution, although most haplogroups in North Africa are of where we find the Garamantes, Bavares, Mauri, Gaetuli, among west-Eurasian origin (Fadhlaoui-Zid et al., 2004, 2011b; Krings many others (Newman, 1995). In addition to the uncertainties et al., 1999;Plazaet al., 2003; Rando et al., 1998). Some of about the origins of the Berbers, the arrival of other people in them can be traced to ancient Paleolithic times (such as hap- the region, especially the influence of Arabs, makes the under- logroups U6, M1, which are almost specific of North African standing of the population history of Berbers more challenging. populations); however, some maternal lineages have been the Considering these previous points, the population genetics def- result of a more recent acquisition from Europe or the Mid- inition of today’s Berber and Arab groups is a complex task. dle East (such as haplogroups U5, V, R0a, J1b, U3) (González Different points of view can be considered to determine whether et al., 2007; Maca-Meyer et al., 2003; Olivieri et al., 2006) a population is considered as Berber or not. Berbers can be under- (Figure 1). In addition, a large degree of genetic heterogene- stood as non-Semitic autochthonous populations in North Africa, ity has been shown in North African maternal and paternal lin- although it is challenging to determine which current populations eages compared to other geographical regions such as Europe derive from an ancestral autochthonous group in North Africa. (Fadhlaoui-Zid et al., 2004, 2011a; Plaza et al., 2003). The anal- Another way to identify Berbers and Arabs is regarding their cul- ysis of Y-chromosome lineages has shown a high frequency of tural characteristics, but again, the cultural exchange in recent two specific North African haplogroups (E-M81 and E-M78) history of North Africa has been common, and it is difficult to (Figure 1), although their origins have been controversial since differentiate, for example, an Arabised Berber society from an some analyses have suggested a Paleolithic component (Bosch Arab population in North Africa, among many other combina- et al., 2001), whereas others have pointed to a Neolithic ori- tions. Given this combination of circumstances, the best option gin (Arredi et al., 2004; Cruciani et al., 2004, 2007; Semino for a classification may be based on linguistics, Berber popula- et al., 2004). The data on autosomal markers in North African tions being those who speak Berber languages and Arabs being populations based on some short tandem repeats (STRs) (Bosch those speaking Arab (Dugoujon et al., 2009). This classifica- et al., 2000) and Alu polymorphisms (Comas et al., 2000; Flo- tion could be the way of having less ‘false positives’; however, res et al., 2000; González-Pérez et al., 2010) has been analysed

Mt DNA haplogroups M iwa orocc L0 U* 100 S ans L1 U6 S ite a L2 K b ha za ra o w L3 HV 75 i M s L4NAL5 H M1 HV0 M Other 50 A l d g e e N1/N2 n r i e a I S n 25 s X J/T

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0 t J

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s Arabs M

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Ychr haplogroups ans Mor 100 eri occ A3b2* J2f1 Alg an s E3a* J2* E1 J2a s 75 n E3b3a* F*(xH.I.J.K) a c S c E3b3* J* o a r h o a r E3b1* O*(xO1.O2a.O3) M a w 50 h E3b* K*(xK2.K3.L.M.N1.N3.O.P) t i s u o E3b2a K2 S E3b2* R1b8 25 E3b2b R1*(xR1a1.R1b1-R1b8) I1b2* R1a1*

A I*(xI1a2.I1a3.I1b2) P*(xP1.Q1.Q2.Q3.R1)

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Figure 1 Haplogroup frequencies for different Berber and Arab populations for (a) mitochondrial DNA (data from Coudray et al., 2009 and Plaza et al., 2003) and (b) Y chromosome (data from Arredi et al., 2004).

eLS © 2017, John Wiley & Sons, Ltd. www.els.net 3 Genetic Heterogeneity between Berbers and Arabs in few North African samples pointing to a closer genetic affin- is correlated with a specific pattern of admixture proportions. A ity to West Eurasian populations. Y-chromosome lineages and completely different scenario was shown when analysing North autosomal markers show a clear differentiation of North African African Jews, who are genetically closer to other Jewish popula- populations with some sub-Saharan gene flow and almost negli- tions than to their geographic neighbours (Campbell et al., 2012). gible European contact (Bosch et al., 2000, 2001; Comas et al., There are many possible scenarios that might explain the dif- 2000; González-Pérez et al., 2010). Nonetheless, the contribution ferential admixture in North Africa, socio-cultural structure and of North African female and male lineages in the Iberian Penin- historical events being the main reasons. However, more com- sula (Adams et al., 2008;Plazaet al., 2003) should be stressed. plex socio-cultural scenarios, including socio-economic factors, Genome-wide analyses have recently become the most pow- a more precise ethnic or linguistic definition, particularities of erful tool to unravel the genetic history of populations. The first the history of each local area and rural versus urban lifestyles, large genome-wide study in North Africa analysing several North should be considered in order to find a correlation with the com- African and surrounding populations (Henn et al., 2012) sug- plex genetic pattern observed (Arauna et al., 2017). gested the existence of an autochthonous North African compo- Concerning the genetic differences between Berber and Arab nent whose origin is located out of Africa before the Holocene groups, classical and uniparental markers have highlighted the > ( 12 000 years ago) and a complex admixture from the Mid- lack of a genetic structure that could differentiate Berber and dle East, Europe and sub-Saharan Africa. This autochthonous Arab populations (Bekada et al., 2015; Fadhlaoui-Zid et al., 2004; North African component was found in high frequencies in the Harich et al., 2001;Kefiet al., 2015). Most of these authors have only Berber sample (Berber Tunisian from Chenini) analysed in agreed on a cultural rather than a demographic impact of the the study, suggesting that Berbers might be responsible for this Arabisation after the Arab expansion (Bosch et al., 2000, 2001; autochthonous component in North African samples. However, Ennafaa et al., 2011; Flores et al., 2011). However, as stated ear- recent genome-wide data with additional Berber samples have lier, an East-to-West genetic gradient of a Middle Eastern compo- shown a different scenario, with some Berber groups present- nent has been described in genome-wide analyses, and admixture ing less frequencies of the autochthonous component compared events have been dated to the Arabisation period (Arauna et al., et al to some Arab groups (Arauna ., 2017). In addition to the 2017;Hennet al., 2012), suggesting that the Arabisation might autochthonous component in North Africa, it has been possible to have had more demographic impact than previously thought. quantify and estimate the recent dates of the sub-Saharan admix- The first widespread genome-wide study in North Africa (Henn ture in North Africa (Henn et al., 2012) as well as the genetic et al., 2012) suggested that the single Berber sample analysed contacts from North Africa mainly restricted to south-western (Tunisian Berber from Chenini) presented high frequencies of an Europe (Botigué et al., 2013). Concerning the introgression of autochthonous North African component (named in the study the archaic hominins into North Africans, some Neanderthal admix- ‘Maghrebi’ component) and negligible presence of the Middle ture is detected in these groups independent of their European Eastern component. This lack of Middle Eastern component in component (Sánchez-Quinto et al., 2012). Berbers and its higher frequencies in Arabs pointed to a genome Most of the genetic studies in North African populations agree differentiation between both North African groups. However, the with a limited or non-existent correlation between genetics and posterior genome-wide analysis of additional Berber samples has geography, and therefore, they show a high population heterogeneity in the region (Bosch et al., 2000; Fadhlaoui-Zid et al., challenged this genetic differentiation idea (Arauna et al., 2017). 2004; Flores et al., 2011; González-Pérez et al., 2010). How- This study has corroborated the lack of genetic differentiation ever, an east-west genetic pattern of variation has been observed between Berbers and Arabs; however, it has shown that the Arabi- (Arauna et al., 2017;Boschet al., 1997; Harich et al., 2001; Henn sation had also a demographic impact in North Africa (Figure 2). et al., 2012), which has been explained by Middle Eastern gene It is difficult to exactly quantify the magnitude of the Arab genetic flow towards North Africa according to genome-wide analyses contribution during the Arab expansion in the seventh century, (Arauna et al., 2017;Hennet al., 2012). The genetic heterogene- among other reasons because the influence from Middle East has ity is not only due to the wide extension of North Africa, since it been continuous into North Africa (Camps, 1995). Therefore, this is also found at microgeographical level when considering more data supports the lack of significant differences between Berber restricted areas, such as Algeria (Bekada et al., 2015) or Tunisia and Arabs, but points to a new explanation: a high and differential (Fadhlaoui-Zid et al., 2011a;Kefiet al., 2015), for instance. level of admixture since the Arab expansion that has affected most Regardless of the genetic markers analysed, North African popu- North African groups regardless of their Berber or Arab identity. lations have been described as a mosaic of North African, Middle The other genetic components that are present in North African Eastern, European and sub-Saharan ancestries. The differential populations also contribute to the heterogeneity between Berber admixture with these four ancestry sources explains the current and Arabs. Both peoples have admixed with sub-Saharan popula- genetic structure in North Africa, characterised by diverse and tions in the last two millennia regardless of their ethnicity, which heterogeneous populations. This differential admixture explains has contributed to the lack of differentiation between both groups why nearby populations or even individuals inhabiting the same (Flores et al., 2000; Harich et al., 2010;Hennet al., 2012). How- location might be genetically more distant than groups of peo- ever, it has been shown that the sub-Saharan admixture is most ple in geographically distant populations. For instance, North frequent in the southern groups, and in fact, a South-North gradi- African individuals with similar amounts of sub-Saharan admix- ent of sub-Saharan admixture has been described in North Africa ture present high genetic similarities regardless of their geograph- (Comas et al., 2000;Plazaet al., 2003), which sometimes can ical origin. Neither geography, linguistics nor ethnic affiliation mimic differences between Arab and Berber populations that are

Morocco S. Morocco N. Sahara Algeria Libya Egypt Ancestry Basque Syria Arabs Tun. Chen. Ber. Tunisia Sened Morocco Tiznit Morocco Err. Algeria Tim. Berbers YRI

Figure 2 Analyses of autosomal markers. Each bar shows the proportion of the genome that each individual share with each of the four ancestral populations according to ChromoPainter analyses (Lawson et al., 2012). The separation between bars within each population represents clusters of individuals with similar ancestry proportions. Source: Arauna et al. (2017). mainly explained by a differential sub-Saharan contribution (Flo- notice the wide extension and fragmentation of the territory where res et al., 2011). the Berbers live, which could lead to population differentiation The high heterogeneity found in North African populations because of many reasons apart from ethnicity (simply by isolation is also present within ethnic groups. Berbers are a composite by distance or differential gene flow). Then, it is important to of groups with very different demographic characteristics, and compare the Berber groups to geographically close populations some Berber groups are genetic outliers compared to other Berber in order to make inferences of genetic distances. or North African populations. This is the case of the Tunisian The genetic heterogeneity of North African samples, the com- Berber population from Chenini, which has been analysed for plex population admixture patterns and the lack of correla- uniparental and genome-wide markers, and in both cases, it has tion between genetics and ethnic groups should be taken into been described as an outlier group compared to their North account when addressing biomedical approaches in North Africa. African populations (Ennafaa et al., 2011; Fadhlaoui-Zid et al., Ignoring these population aspects might lead to artefacts and 2004, 2011a;Hennet al., 2012). This genetic singularity is false-positive results when searching for associations between not exclusive of this group since other Tunisian Berber groups genetic markers and biomedical phenotypes, including disease have also shown similar outlier characteristics (Ennafaa et al., association studies. Furthermore, population genetic studies in 2011; Fadhlaoui-Zid et al., 2004, 2011a). Another example are North Africa should also take this diversity into account. It is the Mozabite, an Algerian Berber group included in the Human important to trace many different variables when studying North Genome Diversity Panel (HGDP) (Cann et al., 2002), which African populations, such as the social and demographic char- have been extensively analysed in many genetic studies and have acteristics of the studied groups (if it is urban or rural, if it is also been described as an outlier group within North Africa and geographically isolated, etc.) and their history (the Arab influence also within Berbers (Bekada et al., 2015;Plazaet al., 2003). in the region, slave trade routes, etc.). The genetic structure of It is important to note that Mozabite have been considered as North African population is determined by many different factors the representative North African group in a large number of apart from a simple ethnic dichotomy Arab–Berber, and including studies due to the fact that they are the only North African those variables sheds lights in the understanding of the popula- group in the HGDP, which should be taken with caution given tions. their genetic outlier characteristics. Furthermore, the Siwa Berber population from Egypt is genetically distant from other Berber groups from West North Africa (Coudray et al., 2009), suggesting a differentiation between Egyptian Berbers and Western Berbers. Related Articles However, there are many other Berber groups that are closely related between them and to other North African groups. All these Reconstructing Human History Using Autosomal, Y-Chro- evidences support a high diversity within Berbers, which could mosomal and Mitochondrial Markers be explained by isolation processes and inbreeding. For example, Gene Flow, Haplotype Patterns and Modern Human Origins the Chenini population is an isolated population that shows high Genetic Diversity in Africa levels of inbreeding (Arauna et al., 2017;Hennet al., 2012). It has Humans: Demographic History been described that some of the diversity observed within Berbers is due to the belonging to an urban or rural area. Rural areas favour Glossary isolation leading to genetic differentiated populations (Brakez et al., 2001; Ennafaa et al., 2011;Frigiet al., 2006). On the Admixture The process of mixing of different populations other hand, urban areas that are less isolated are more favourable within a species. to high admixture levels and lead to the lack of differentiation Cultural diffusion The spread of cultural practices from between Berber and Arab groups. Finally, it is important to another group of people without genetic exchange.

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