A Genetic Study of Nine Populations from the Region Of

ANTHROPOLOGICAL SCIENCE Advance Publication Vol. advpub(0), 000–000, 2012

A genetic study of nine populations from the region of Tlemcen in Western Algeria: a comparative analysis on the Mediterranean scale Ammaria Aouar METRI1, Adel SIDI-YAKHLEF2,3*, Christian BIÉMONT4, Mohamed SAÏDI2, Okacha CHAÏF2, Sid Ahmed OURAGHI2

1Laboratoire de valorisation de l’action de l’homme pour la protection de l’environnement et application en santé publique (équipe environnement et santé), Faculté des Sciences, Université Abou Bakr Belkaïd de Tlemcen, 13000, Algeria 2Laboratoire d’Anthropologie des Religions et comparaison, Faculté des Sciences Humaines et Sociales, Université Abou Bakr Belkaïd de Tlemcen, 13000, Algeria 3Centre de Recherches Comparatives en Ethnologie (CERCE/EA 3532), Université Paul Valéry, route de Mende, 34199 Montpellier Cedex 5, France 4Laboratoire de Biométrie et Biologie Évolutive, UMR 5558, CNRS, Université de Lyon, Université Lyon 1, 69622 Villeurbanne cedex, France

Received 13 June 2011; accepted 18 June 2012

Abstract We characterized 2005 individuals from nine populations in the region of Tlemcen in Western Algeria for the ABO, rhesus, MNSs, and Duffy blood groups, in association with genetic traits. The results were compared to those for other populations in Algeria, North Africa, and Southern Europe, in order to situate and clarify the genetic status of this region. Principal-component analyses and phylogenetic trees of the matrices of the genetic distances, on the regional and Mediterranean scales, reveal strong homogeneity at the regional level and convergence between North African populations. This indicates high genetic affinities among these populations. This study highlights the dif- ferences between the two sides of the Mediterranean, probably due to the independent peopling history of these populations after they had settled. The resulting genetic structure of these populations is best explained by a combination of gene flow, ecology, and history.

Key words: population, north-western Algeria, anthropogenetics, polymorphism, blood groups

Introduction pleted because of the disruption associated with World War II. However, Benabadji and Chamla (1971) resumed the ge- The genetic diversity of human populations reflects the netic studies of this region by examining the ABO and D/d routes followed by our ancestors during their migrations rhesus alleles in a large sample of Algerian blood donors. throughout the world. In the Mediterranean region, and in The results indicated the predominance of genetic homoge- North Africa in particular, the data suggest a complex pat- neity due to gene flow between different regions of Algeria, tern of human movements. Archaeological data and histori- but with some migration emanating from sub-Saharan cal accounts provide evidence of relationships between the Africa and Mediterranean Europe. Since 1964, multidisci- different Mediterranean peoples since ancient times. How- plinary studies have been conducted on sedentary and no- ever, the dates and the geographical locations of their expan- madic populations of the Algerian Sahara, mostly on Tuareg sion are debatable (Stringer, 2000). In this regard, North tribes in the central region. Over a period of 30 years, more African populations probably played an important role in the than 10000 samples have been examined for an ever- early migrations of modern populations. It has been demon- increasing number of red cell and serum genetic polymor- strated that there were links between sub-Saharan popula- phisms (Benabadji et al., 1969; Ruffle and Lefevre-Witier, tions and those of Western Europe until the recent past. 1972; Lefevre-Witier, 1974, 1996; Constans et al., 1980; Contacts between different civilizations, migrations, and the Aireche et al., 1982; Aireche and Benabadji, 1986). spread of successive cultures, which reveal the tracks of his- A number of recent studies have also surveyed North tory, may also have determined the genetic relationships be- African populations on the basis of non-recombining Y, tween the different populations. single-nucleotide polymorphisms, and mitochondrial DNA Many of the investigations started in Tunisia, Algeria, and (mtDNA). The mtDNA analysis of a sample of west Algeri- Morocco in the late 1930s and early 1940s could not be com- an students from the wilaya of Oran concluded that Algeri- ans are genetically close to an Israeli-Arab population and have less affinity to the Mediterranean populations of Sicily, * Correspondence to: Adel Sidi-Yakhlef, 715 Avenue de l’Abbé Paul Parguel, 34090, Montpellier, France. Majorca, Calabria, and Sardinia (Ivanova et al., 1999). Sim- E-mail: [email protected] ilarly, Bosch et al. (2000) sampled Moroccans from north- Published online 21 August 2012 western Africa, including northern, central, and southern in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.120618 Berbers, Saharawis, and Mozabites. They tested DNA

Figure 1. Map showing the region of Tlemcen and the surrounding areas. samples with two panels of autosomal STRs, and compared Materials and Methods them to reference populations. The North African groups clustered with an Arab sample (Lefevre et al., 2006). The region of Tlemcen has very ancient human origins. It One of the largest population movements on both sides of carries vivid traces of various ages, which today make it of the Mediterranean was the conquest of the Iberian Peninsula archaeological importance. Bordering on Morocco, and by North Africans. The Arabs came from the East to West, occupying the western zone of the region of Oran (western bringing their religion and language. One of the most impor- Algeria), it extends over an area of more than 907000 ha of tant passages of Arabs to the Iberian Peninsula occurred the littoral region in the north with the steppe in the south from the region of north-west Algeria (Lethielleux, 1974), constituting a diversified landscape where four distinct suggesting the existence of an important migratory flow, ge- physical landscapes occur (Figure 1). Its ancient past is at- netic admixture, and cultural diversity within the region. tested by the existence of numerous monuments from the In view of the rarity of anthropogenetic data on several pre-Roman, Roman, and Arab eras. The Arabo-Muslim civ- Algerian populations, especially those of the western re- ilization has without any doubt marked this region for a long gions, we analyzed the genetic polymorphism of the ABO, time, which was a crossroads during the reign of the power- rhesus, Duffy, and MNSs blood groups of nine Arab-Berber ful Idrisid, Almoravid, and Almohad Arab dynasties that populations (Oulhaça, Honaine, Ghazaouet, M’sirda, Be- governed the Maghreb in the Middle Ages (Lethielleux, niouerssous, Nadrouma, Benisnouss, Sabra, and Sidi El 1974; Hassar, 2000). Djilali) in the region of Tlemcen in north-western Algeria, The nine populations selected (Oulhaça, Honaine, Ghaza- whose anthropogenetic characterization has never previous- ouet, M’sirda, Beniouerssous, Nadrouma, Benisnouss, Sa- ly been reported. We compared our findings with previous bra, and Sidi El Djilali) have the peculiarity of having been studies of several populations of the Mediterranean basin. considerably enriched genetically and culturally by the vari- We identified a high degree of genetic homogeneity among ous invasions they have undergone (Phoenicians, Carthagin- these populations due to the long history of autochthonous ians, Romans, Arabs, etc.) and by their geographic location populations spreading into this region. The analysis also re- in the Tlemcen region, which was one of the main departure veals the genetic relationship between populations from the points for Arabs from the East crossing over to the Iberian opposite sides of the Mediterranean Sea. peninsula (Carette, 1853). At the same time, these populations have remained highly conserved and isolated because Vol. 120, 2012 ANTHROPO-GENETIC ANALYSIS OF NINE POPULATIONS IN THE ALGERIAN WEST 3

Table 1. Populations used for the comparative study of the blood groups Code Population Reference Tlm-1 Oulhaça Current study Tlm-2 Honaine Current study Tlm-3 Ghazaouet Current study Tlm-5 Nadrouma Current study Tlm-4 M’sirda Current study Tlm-7 Sabra Current study Tlm-6 Beniouerssous Current study Tlm-8 Benisnous Current study Tlm-9 Sidi El Jilali Current study Alg-1 Algiers (Algeria) Lefevre-Witier et al., 2006 Alg-2 Annaba (Algeria) Lefevre-Witier et al., 2006 Alg-3 Laghouat (Algeria) Lefevre-Witier et al., 2006 Mar-1 Al-hoceima berbers (Morroco) Afkir, 2004 Mar-2 Berbers of the middle Atlas (Morocco) Harich et al., 2002 Mar-3 Meridionaus Arabs (Morocco) Kandil, 1999 Lib Libya Walter et al., 1975a Egy Egypt Bonné et al., 1970a Cat Catalonia (Spain) Moreno and Moral, 1983a Basq Basque Country (Spain) Manzano et al., 1996a Por Portugal Roychoudhury and Nei, 1988a Fr-c Corsica (France) Memmi et al., 1998 Ita-s Sardinia (Italy) Piazza et al., 1989 Gre Continental Greece Tsiakalos et al., 1980a Mal Malta Ikin, 1963a Chyp Cyprus Poumpourido and Scheil, 1995 Turk Turkey Atasoy and Abaci-Kalfoglu, 1995 a Cited by Afkir (2004). of their geographical location (mountains, cliffs, steppes, tibodies to determine the blood group. Each antigen was etc.), and by their tribal structures. Virtually all the first fam- determined twice, using two different batches (or two clones ilies that founded these populations came from the Maghreb. for monoclonal reagents). The reagents were used according Over time, these families settled and formed tribes and to the manufacturer’s instructions. douars (Desanges, 1980; Churchill, 1981). Statistical analyses Sampling Allele and haplotype frequencies were estimated ac- This study was conducted from July 2008 to December cording to the maximum-likelihood method using 2009. The individuals analyzed came from nine populations Bernstein’s method to estimate ABO allele prevalences, located in the region of Tlemcen according to the geograph- then checked for Hardy–Weinberg equilibrium by compar- ical gradient: littoral (Oulhaça, Honaïne, Ghazaouet, ing the absolute observed frequencies with the theoretical M’sirda), hills (Nadrouma, Beniouerssous, Benisnous, frequencies. The Bernstein estimates of p, q, and r are Sabra), and high plateau (Sidi El Djilali). Informed consent given by: p = 1 − (F[B] + F[O])1/2, q = 1 − (F[A] + F[O])1/2, was sought and obtained from all donors (Executive Decree r = (F[O])1/2, where F[ ] indicates the phenotypic frequency No 276 of 6 July 1992 concerning Medical Code of Ethics). (Nan Juan and Gart, 1976). The validity of the results was verified by determining the Sample collection chi-square of the observed values. Results with P < 0.05 The blood groups were determined from samples taken were considered statistically significant. The biological rela- from 2005 unrelated individuals belonging to the nine popu- tionships between the populations analyzed (Table 1) were lations. Approximately 10 ml of blood were collected per in- represented by a two-dimensional diagram obtained by a dividual. The blood grouping was performed within a few principal-component analysis using ADE-4 software hours of taking the samples. (Chessel et al., 2004). The genetic distances between the We cleared the plasma surrounding the red blood cells by populations were estimated from the genetic frequencies washing the blood before determining the phenotypes. data as the Reynolds coefficient of coancestry (Reynolds et 0.5 ml samples were placed in hemolysis tubes filled with al., 1983), using the Phylip 3.5C program. The degrees of saline (0.9%). After suspension by gentle stirring, they were similarity between the populations were estimated from the centrifuged at 1000 rpm for 1 minute, and the supernatant genetic distance matrices using the neighbor-joining method was removed. This procedure was repeated twice. The third (Saitou and Nei, 1987) with the Phylip 3.5C program. pellet of red blood cells was resuspended (5%) to be used for The relative rate of genetic flow between populations was blood grouping. We observed the presence or absence of an- estimated by tracing the average distance from the center of tigens on the surface of red blood cells by using specific an- the allele frequencies for each region against the degree of 4 A.A. METRI ET AL. ANTHROPOLOGICAL SCIENCE

Table 2. Allelic and haplotypic frequencies of the ABO, rhesus, MNSs and Duffy blood groups in the nine studied populations

Blood Blood Populations system group Tlm-1 Tlm-2 Tlm-3 Tlm-5 Tlm-4 Tlm-6 Tlm-7 Tlm-8 Tlm-9 ABO A 0.251 0.271 0.199 0.202 0.181 0.209 0.261 0.192 0.180 B 0.111 0.053 0.091 0.120 0.112 0.105 0.122 0.092 0.082 O 0.639 0.670 0.705 0.678 0.712 0.682 0.616 0.741 0.742 Rhesus CDE 0 0 0 0.126 0 0 0 0 0.041 CDe 0.365 0.291 0.41 0.189 0.390 0.420 0.530 0.41 0.273 cDE 0.130 0.092 0.13 0.172 0.121 0.161 0.122 0.096 0.071 cDe 0.211 0.280 0.158 0.258 0.373 0.186 0.156 0.291 0.312 CdE000000000 Cde 0 0 0.010 0.005 0 0 0 0 0 cdE 0 0 0.011 0.030 0 0 0 0 0 cde 0.294 0.340 0.284 0.231 0.121 0.244 0.202 0.224 0.310 MNSs MS 0.166 0.121 0.142 0.201 0.200 0.144 0.210 0.212 0.133 Ms 0.333 0.227 0.238 0.375 0.275 0.421 0.211 0.260 0.271 NS 0.095 0.152 0.144 0.075 0.131 0.041 0.120 0.105 0.130 Ns 0.405 0.503 0.477 0.353 0.402 0.399 0.472 0.425 0.471 Duffy Fya 0.244 0.293 0.225 0.399 0.175 0.334 0.368 0.180 0.232 Fyb + o 0.756 0.71 0.775 0.6 0.825 0.666 0.632 0.821 0.771 Total 294 200 200 260 250 203 200 170 228

heterozygosity for each locus (Harpending and Ward, 1982). A simple linear regression was then traced between the heterozygosity level of a population and its distance, defined as the arithmetic average of the gene frequencies. The bibliographic database used for the comparative study (frequency distributions and allele haplotype) appears in the various publications cited in Table 1 and in the bibli- ography.

Results and Discussion Allele and haplotype frequencies of blood groups The frequencies of the ABO, rhesus, MNSs, and Duffy blood groups in the nine populations are summarized in Table 2. The chi-square test values show that these frequencies did not deviate from the Hardy–Weinberg equilibrium Figure 2. Principal-component analysis based on allele frequen- for the four groups in any of the populations. cies of the nine populations studied (for abbreviations, see Table 2).

Inter-population affinities At the regional level Figure 2 and Figure 3 represent the projections on the first two axes (which contribute 57% of the total variability) of the principal-component analysis of the nine populations and the blood groups, respectively. The first axis (35.6% of variance) separates the haplotype frequencies (cDe, CdE, cde, NS, and NS) and the alleles (ABO*O and Fy b + o), which appears to distinguish the populations of Honaïne, Nadrouma, M’sirda, Benisnouss, and Sid-Djilali from those of Oulhaça, Gahzaouet, Beniouerssous, and Sabra. The second axis (21.4% of variance) separates the populations of M’sirda, Benisnous, and Sid El Djilali, which correlate with the haplotypes cDe and CdE and the ABO*O and Fy b + o alleles, from the remaining populations. The phylogenetic tree (Figure 4) based on hierarchical Figure 3. Contribution of the allele and haplotype frequencies of classifications of neighbor-joining (Saitou and Nei, 1987) the blood systems in Figure 2 (for abbreviations, see Table 2). Vol. 120, 2012 ANTHROPO-GENETIC ANALYSIS OF NINE POPULATIONS IN THE ALGERIAN WEST 5

Figure 4. Neighbor-joining tree of the genetic distances estimated from the blood group allele frequencies of the nine populations. Statis- tical support at the internodes on the trees was assessed by 1000 boot- Figure 6. Principal-component analysis based on allele frequen- strap replications employing the Consense programme included in the cies of the nine populations studied and other North Africa and North- Phylip package (for abbreviations, see Table 2). ern Mediterranean populations (for abbreviations, see Table 2).

regression line, with the exception of the population of Sid- El-Djilali. The low heterozygosity level of this population could be due to its geographical isolation and the frequent practice of endogamy.

At the Mediterranean level We compared the distribution of gene frequencies of the blood groups in our nine populations with those in some other North African and northern Mediterranean populations. Figure 6 shows the distribution of the blood groups after principal-component analysis. The first two axes account for 54.6% of the total variability. The first axis (28.1% of the variability) separates the majority of the North African pop- Figure 5. Regression chart among the heterozygosity level aver- ulations, including our nine populations, from the popula- ages by locus (H) and the central distance of the distribution of the nine studied populations (D) (for abbreviations, see Table 2). tions of the northern Mediterranean coast, according to the allele frequencies of the group NS and Fy b + o. The second axis (21.4% of variability) separates the populations of Nadroma, Middle Atlas, and southern Arabs from all the was constructed from a matrix consisting of Reynolds dis- other populations, suggesting the existence of genetic simi- tances (Reynolds et al., 1983). This tree confirms the results larity between these three populations. obtained from the principal-component analysis. It distin- The phylogenetic tree (Figure 7) obtained from the matrix guishes three population clusters. The first cluster includes of the genetic distances of the Mediterranean basin popula- the populations of Oulhaça, Ghazaouet, Sabra, and Be- tions also distinguishes two major clusters, reflecting the ge- niouerssous; the second cluster includes those of Sid-El- netic affinity between the populations. The first cluster Djilali and M’sirda, and the third cluster includes Nadrouma includes all the northern Mediterranean populations, while Honaïne and Bnisnous. However, we can observe in this plot the second, which includes all the North African populations that the three clusters are closer, probably due to the insig- with the exclusion of that of Libya, is divided into two nificant difference between the genetic distances. Therefore, branches. The first branch includes the populations of neither of these two analyses (the principal-component anal- Nadroma, Middle Atlas, the southernmost Arabs, Be- ysis and the phylogenetic tree) shows any significant differ- niouerssous, and Sabra, and the second branch includes all ence between the nine populations studied on the the remaining populations. geographical level, which suggests a high degree of homogeneity between these populations. This could be explained Conclusion by the long history of autochthonous populations spreading into this region, and their particular coastal environment and Our anthropogenetic analysis of nine Arab-Berber popu- political history, especially during the Ottoman period. lations from the region of Tlemcen, shows that these popula- The regression analysis of the heterozygosity level of tions display a high degree of genetic similarity, but differ populations over the distance of the distribution center of the from a larger group of populations in other Mediterranean allele and haplotype frequencies (Figure 5) shows that most countries. The analyses reveal genetic difference of these of the nine populations are situated near the theoretical populations from the opposite sides of the Mediterranean 6 A.A. METRI ET AL. ANTHROPOLOGICAL SCIENCE

postulates the existence of pre-Neolithic relations between North Africa and Spain. However, the historical depth of these relations remains controversial (Barbujani et al., 1994; Fernandez-Santander et al., 1999; Ennafaa et al., 2009). More genetic data will be required to date the relationships between the northern and southern shores of the Mediterra- nean before we can make a more precise dating of these relationships to about 10000 years before the present, the current limit of linguistic reconstruction. Our study is com- plementary to those of Mourant et al. (1976), Cavalli-Sforza et al. (1994), and Bosch et al. (1997), but we also need a more precise characterization by other markers for a better illustration of the ethnohistorical events specific to this vast Mediterranean region.

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