Distribution of Y chromosome lineages in Jerba island population

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1 Forensic Science International 148 (2005) Distribution of Y chromosome lineages in Jerba island population Houssein Khodjet el Khil a,*, Raja Triki Marrakchi a, Besma Yacoubi Loueslati a, André Langaney b, Marc Fellous c,1, Amel BenAmmar Elgaaied a a Laboratoire de Génétique moléculaire, Immunologie et Biotechnologie, Faculté des Sciences de Tunis, Campus Universitaire 2092 Manar II, Tunisia b Laboratoire d Anthropologie Biologique, Musée de l Homme, Paris, France c Unité d Immunogénétique Humaine, INSERM E 21, Institut Pasteur, Paris, France Received 5 December 2003; received in revised form 14 May 2004; accepted 18 May 2004 Available online 26 August 2004 Abstract We have analysed Y chromosome polymorphism on six STR markers (DYS19, DYS389I, DYS390, DYS391, DYS392, and DYS393) and eight classical UEP markers (SRY10831a, YAP, SRY4064, M2, 92R7, M9, SRY2627 and 12f2) in three distinct ethnical, linguistic and cultural groups of Jerba island (Berbers, Arabs and a Jerban group of Sub-Saharan origin). F st genetic distance and principal co-ordinate analysis based on STR haplotype frequencies, showed a genetic differentiation between the three Jerban groups and a genetic relationship between Jerban Berbers and Mozabites (a well defined Berber group in Algeria). Compound use of UEP and STR markers have increased discriminatory capacity. The detection of the most common haplotype (H9) in both Berbers and Mozabites may be useful in forensic special cases. # 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Forensic science; Y chromosome; Microsatellites; UEP markers; Jerba island 1. Introduction The non-recombining region of human Y chromosome (NRY) is strictly paternally transmitted unchanged from father to son except by the accumulation of mutations. Markers on this region will be therefore inherited within a haploid state which makes them powerful tools to trace easily paternal lineages. This, makes Y chromosome, a very important system to use in human population evolutionary studies [1]. Furthermore, Y chromosome exhibits two kind of polymorphism markers: (a) biallelic markers with a low mutation rate representing a near unique mutation events (UMEs) in human evolution such as single base-pair substitutions [2,3] * Tel.: þ x361; fax: þ addresses: Houssein.KhodjetElKhil@fst.rnu.tn (H. Khodjet el Khil), Amel.BenAmmar@mes.rnu.tn (A. BenAmmar Elgaaied). 1 Present address: Pavillon Baudelocque, Inserm U361, Hôpital Cochin, 123, Boulevard de Port-Royal 75014, Paris, France. and insertion/deletions [4,5]; (b) mutiallelic markers with high mutation rate of 6 11% per generation for the minisatellite locus MSY1 [6] and of 0.2% per generation for microsatellites [7,8]. Currently one of the most important goal of both forensic and anthropological geneticists is the development of population databases which is crucial to establish an ethnical and geographical stratification of Y chromosome haplotype frequencies, to trace different population moving and to evaluate geographical, cultural and linguistic effects on human evolution. In the present study, we typed DNA from 135 Jerban males belonging to three ethnic groups of Jerba island: Berbers, Arabs and Jerbans with Sub-Saharan origin for six microsatellite and eight biallelic Y chromosome markers and we compared them to North African, African and Euro- Mediterranean populations data available from the literature. According to the population history of Jerba island, situated in the South-East of Tunisia, Berbers belong to the most ancient group which seems to have Capsians as local ancestors ( B.C.) [9] /$ see front matter # 2004 Elsevier Ireland Ltd. All rights reserved. doi: /j.forsciint

2 212 H. Khodjet el Khil et al. / Forensic Science International 148 (2005) Anthropological and linguistic studies on Jerban Berbers reported that this group belongs to the Ibadhite religious community and has its distinct Berber language [10]. Arab reached the island with the Muslim invasions to North Africa in the 7th century. No demographic information about their number at this period are available, but this group has certainly imposed its language and religion on Berbers. Jerban group of Sub-Saharan origin seems to be descendent of Sudanese or Nigerian slaves who came in the 18th century [10].The goal of this study is to define a Y chromosome lineage database in Jerba island groups, and to compare them to some North African and European populations in order to better appreciate their haplotype distribution and genetic relationship which are very important for forensic applications. 2. Materials and methods 2.1. Population samples Jerban samples analysed in the present study, include 47 Berbers, 46 Arabs and 42 Jerbans of Sub-Saharan origin. They were collected from different locations of the island. Information about geographic origin and native language of their four grandparents was obtained. DNA was extracted from fresh blood using standard phenol chloroform methods from all the 135 unrelated donors STR typing Six Y linked STR loci were amplified from genomic DNA (DYS19, DYS389I, DYS390, DYS391, DYS392 and DYS393). Polymerase chain reactions (PCR) were performed using primer sequences given by Kayser et al. [11], and cycling conditions previously described by Hurles et al. [12] with the presence of fluorescently labelled dctp derivative (RGG, Applied Biosystems) with respect to dctp present in the reaction mixture. Amplified DNA for each sample and each locus was run in standard 6% denaturing sequence gel using an ABI 373 A sequencer in the presence of GS500 (Applied Biosystems) as a size standard. Data were collected and alleles at each locus were determined using Gen Scan Software (Applied Biosystems). Primers for DYS389 generate two PCR fragments [11], only variability of the short fragment (DYS389I) was considered. Allele nomenclature was as proposed by Kayser et al. [11] with the exception of the DYS389I locus. The nomenclature of this locus was according to Gill et al. [13], considering that the sum of p and q stretches corresponds to DYS389I [14] UEP markers typing Among the 135 samples screened for microsatellite markers, 128 were typed for eight biallelic UEP markers. Six from the eight UEP analysed correspond to base-pair substitution and typed by PCR RFLP method: SRY-10831a [15,16]; SRY-4064 [15,17]; SRY-2627 [12]; 92R7 [18]; M9 [2]; M2[19]. The two other UEP markers where typed by PCR amplifications: YAP insertion [4,20] and 12f2 deletion [21]. All markers were typed using the experimental conditions reported by Rosser et al. [21]. UEP-defined haplogroups were assigned using the nomenclature proposed in the Y chromosome consortium [22,23] Statistical analysis For each Jerban group, haplotypes were constructed for the six STR loci analysed and their frequencies were computed by simple gene counting. Haplotype diversity was calculated according to the formula D ¼ 1 P P 2 i where p i is the frequency of ith haplotype frequency. Discriminatory capacity were estimated according to Kayser et al. [24]. Based on haplotype frequencies, F st genetic distances [25], were computed between each pair of populations (Jerban groups and available North African, African and European population data analysed for the same six STR loci), and their significance was tested using ARLEQUIN 2.0 package. Principal Coordinate analysis (PCa) was performed on the F st genetic distance matrix computed between pair of populations, using SAS 6.2 package. 3. Results and discussion One hundred and thirty five Jerban males were analysed for six Y STR loci. Sixty-seven distinct haplotypes were observed (Table 1) and distributed as following: 18 haplotypes among 47 Berbers, 27 haplotypes among 46 Arabs and 33 haplotypes among 42 Jerban of Sub-Saharan (Table 2). Haplotype diversity values range from to (Table 2). Berbers show the lowest value, whereas, Jerban of Sub-Saharan origin show the highest one. These informations are totally in agreement with a previous report in which only allele frequencies are considered [26], and point out the great genetic homogeneity of Berber group, since 18 out of 47 individuals analysed have the same STR haplotype, H9. This Berber group has most likely undergone in a recent past a genetic drift that has reduced its genetic diversity [26]. Unlike Berbers, Jerban of Sub-Saharan origin show a high diversity level and since this group settled in the island no far than three centuries, its diversity level was most probably present before it comes to the island. From the 67 observed STR haplotypes, ten were shared between Arabs and Berbers (Table 1) suggesting therefore their genetic relationship, but only one H14 is shared between the three Jerban groups. Interestingly, H9, is the most frequent common STR haplotype observed in Jerba population and particularly in Arab and Berber groups. Comparison to data available from the analysis of the six microsatellite loci in some other populations, shows that H9 was absent in many European populations: 56 Andalusians,

3 H. Khodjet el Khil et al. / Forensic Science International 148 (2005) Table 1 Y chromosome STR and UEP haplotypes for the three groups of Jerba island JSO: Jerban of Sub-Saharan origin. ND: not determined. The same STR haplotypes with different or not determined UEP Haplogroups are indicated by the letters a or b added to the correspondant haplotype number DYS19 DYS389I DYS390 DYS39I DYS392 DYS393 UEP Arabs Berbers J.S.O Total H E*(xE3a) H E*(xE3a) H E*(xE3a) H J H4a E*(xE3a) H E*(xE3a) H E*(xE3a) H6a P*(R1b3f,R1a) H E*(xE3a) H E*(xE3a) H8a J H E*(xE3a) H9a R1a H9b K*(xP) H E*(xE3a) H E*(xE3a) H E*(xE3a) H E*(xE3a) H E*(xE3a) H14a ND I 0 0 I H E*(xE3a) H E*(xE3a) H E*(xE3a) H E*(xE3a) H18a R1a H E*(xE3a) H E*(xE3a) H E*(xE3a) H ND H E*(xE3a) H E*(xE3a) H E*(xE3a) H E*(xE3a) H26a J H E*(xE3a) H J H E*(xE3a) H E*(xE3a) H ND H P*(R1b3f;R1a) H ND H P*(R1b3f,R1a) H BR*(xDE,JK) H P*(R1b3f,R1a) H P*(R1b3f,R1a) H E*(xE3a) H BR*(xDE,JK) H P*(R1b3f,R1a) H E*(xE3a) H E3a H E3a H E3a H Y*(xBR) H E*(xE3a) H P*(R1b3f;R1a)

4 214 H. Khodjet el Khil et al. / Forensic Science International 148 (2005) Table 1 (Continued ) DYS19 DYS389I DYS390 DYS39I DYS392 DYS393 UEP Arabs Berbers J.S.O Total H ND H BR*(xDE,JK) H P*(R1b3f;R1a) H P*(R1b3f,R1a) H P*(R1b3f,R1a) H ND H E*(xE3a) H E*(xE3a) H E*(xE3a) H E3a H P*(R1b3f,R1a) 0 0 I 1 H E3a H E3a H E3a H E3a H E3a H E3a I H64a ND H E3a H E*(xE3a) H E*(xE3a) Galicians and 31 Valencians [27]; 27 Sardinians [28]; 49 Basques and 22 Catalans [29] and 984 male individuals from 20 globally dispersed human populations [30], but is only present in one out of 100 Italians [31,30], 55 Portugueses [27] and 88 Germans [30]. It was also absent in African populations: 84 Ethiopians, 31 Malians, 29 males from Central Africa and 85 males from South Africa [32]. However, H9 was fully observed in North African populations: 44 Morocco Arabs, 44 Berbers of the South of Morocco, 29 Saharawi and 68 Mozabites from Algeria [33]. Furthermore, H9, which is the most frequent haplotype observed in Jerban Berbers is also the most frequent haplotype detected in Mozabites according to data reported by Bosch et al. [33], who analysed eight STR loci (DYS19, DYS388, DYS389I DYS389II, DYS390, DYS391, DYS392 and Table 2 Y STR Haplotype characteristics in three groups of Jerba Island Arabs Berbers J.S.O STR typed samples Number of ditinct STR haplotypes STR haplotype diversity Discriminatory capacity a UEPþSTR typed samples Number of ditinct UEPþ STR haplotypes Discriminatory capacity b J.S.O: Jerban of Sub-Saharan origin. a On the basis of STR markers. b On the basis of UEP þ STR markers. DYS393). Therefore, H9 which is considered as the core of two sub-haplotypes referred to H21 and H27 and observed in 24 and 4 individuals out of 44 Mozabites respectively [33], seems likely specific to Jerban Berbers and Mozabites, even though it is present at a frequency of 15% in Jerban Arabs. The presence of such characteristic haplotype at a high frequency in a population has been previously observed when reduced and isolated populations were analysed [28,29]. In these conditions drift acts strongly and particularly on the Y chromosome and this is what seemed to happened in Mozabite and Jerban Berber populations. Such feature reduces intra-population diversity, increases differentiation among them and gives rise to a clearer Y chromosome haplotype stratification. F st genetic distances based on STR haplotype frequencies were computed for our samples and for Euro-Mediterranean, North African and African populations which are typed for the same six Y chromosome microsatellite loci and sharing haplotypes with Jerban groups. A significant genetic differentiation has been found between the three Jerban groups, as well as, between Jerban groups and the other compared populations (Table 3). Principal coordinate analysis (PCa) was performed on the base of F st distance matrix. The two-dimensional plot of the first two PC axes which accounts for 74.6% of the variance, showed several clusters among which one can distinguish Jerban Berbers Mozabites grouping (Fig. 1). This result is of great interest since both populations belong to the Ibadhite religion community and have the same cultural practices and Berber language [10]. Hence, our genetic analysis is in agreement with historical data indicating, a relationship

5 H. Khodjet el Khil et al. / Forensic Science International 148 (2005) Table 3 Population pairwise F st statistics calculated from STR haplotype frequencies in Jerban, African and Italian populations Jber Jara JSO Ara SOB SAH MZA ITA Eth Mal CAF SAF Jber Jara JSO Ara * SOB SAH MZA ITA Eth Mal CAF * SAF F st distance matrix (below diagonal) a,f st probability values (1000 permutations, above diagonal). Jber: Jerban Berbers; Jara: Jerban Arabs and JSO: Jerban of Sub-Saharan origin (present study); ARA: Moroccan Arabs; SOB: Southern Moroccan Berbers; SAH: Saharawis; MZA: Mzabites [33]; Eth: Ethiopians; Mal: Malians; CAF: Central-Africans and Zaîrians; SAF: Southern-Africans [32]; Ita: Italians [31]. *Asterisk indicates non significant F st P values (significance level ¼ 0.05). Only P values > were noted. between Mozabites and Jerban Berbers which seem to belong to a same Berber group settled in Tahert, West Algeria in the 8th century [10]. Interestingly, the plot shows that the Jerban Arabs are close to Morrocan Arabs and Berbers of South Morroco and an intermediate position between Italians and Sub-Saharan African cluster of the Jerban group of Sub-Saharan origin. In order to better investigate genetic relationship between our Jerban groups and other North African and Mediterranean populations, we typed eight Y chromosome UEPs on 128 from the 135 Jerban samples in which we defined eight different haplogroups (Table 4). Five different haplogroups were observed in Jerban group of Sub-Saharan origin, whereas, they were observed respectively four and three haplogroups in Jerban Arabs and Jerban Berbers (Table 4). The most frequent haplogroup detected in all the Jerban samples analysed and particularly in both Berbers (93.62%) and Arabs (84.1%) is Hg E*(xE3a). This is not surprising since this haplogroup has a large African distribution [3], with some lineages are specially frequent in North Africa [33]. However, Jerban Arabs with their presumed origin from the Middle East, show a low frequency of HgJ (9.1%). This was not expected since it has been observed that HgJ has its highest frequencies in populations of Central Asia and Fig. 1. Principal coordinate analysis (PCa) of 12 populations. The first axis accounts for 47.6% of the total variance. The second axis accounts for 26.9% of the total variance. Population represented are: JBer, Jerban Berbers; JAra, Jerban Arabs and JSO, Jerban of Sub-Saharan origin (present study); ARA, Moroccan Arabs; SOB, Southern Moroccan Berbers; SAH, Saharawis; MZA, Mozabites [33]; Eth, Ethiopians; Mal, Malians; CAF, Central-Africans and Zaîrians; SAF, Southern-Africans [32]; Ita, Italians [31].

6 216 H. Khodjet el Khil et al. / Forensic Science International 148 (2005) Table 4 UEPs haplogroup definition and their frequencies in three groups of Jerba Island Allele state (0: ancestral; 1: derived) Frequency (%) SRY-10831a YAP SRY-4064 M2 12f2a M9 92R7 SRY-2627 Berbers (47) Arabs (44) J.S.O (37) Total (128) Y*(xBR) , 7 0, 78 BR*(xDE,JK) , 25 10, 81 4, 68 J , 1 3, 12 K*(xP) , 13 0, 78 P*(R1b3f,R1a) , 26 40, 54 12, 5 R1a , 54 1, 56 E*(xE3a) , 62 84, 1 13, 51 67, 18 E3a , 44 9, 37 J.S.O: Jerban of Sub-Saharan origin. Middle East [3,35]. Furthermore, HgJ includes lineages such as what is referred to H71 or E10 [34,36], that were specially detected with high frequencies in Middle East and it has been suggested that their presence in European and North West African populations was the consequence of a Neolithic diffusion with the farmers as reported by the same authors. Moreover, the presence of these lineages in North West African populations has also been suggested to be the result of a recent gene flow caused by the migration of Arabian tribes in the first millennium [37,38]. In our case, we suggest that the detection of HgJ in Jerban Arabs is the consequence of their recent coming in the 7th Century with the Muslim army as reported by historians [10]. Interestingly, the presence in this group of high frequencies of Hg E*(xE3a) (84.1%) rather than HgJ (9.1%) can be the consequence of Arabization and Islamization of Berber population, as a strong cultural phenomena that resulted in a new ethnocultural entity as reported in Nebel et al. [39], and which made more difficult the cultural differentiation between Berbers and Arabs. In the Jerban group of Sub- Saharan origin, the most frequent haplogroups oberved were Hg E3a and Hg P*(R1b8,R1a) with the frequency of (32.41%) and (40.54%) respectively. The detection of HgE3a in this group is quite expected since this haplogroup which is also referred to Hg8 [40,21], was found with high frequencies in Central and South African populations [3], and considered of Sub-Saharan origin [41,35]. However, the detection of high frequencies of Hg P*(R1b8,R1a) in this group is with great interest since lineages of this clade showed an Eurasian distribution [3,35]. The four remained haplogroups were observed with low frequency: Hg Y*(xBR) is observed in only 1/37 Jerban male of Sub- Saharan origin; Hg R1a is observed in only 2/44 Jerban Arabs; Hg BR*(xDE,JK) is observed in 2/47 Jerban Berbers and 4/37 Jerban males of Sub-Saharan origin and finely, Hg K*(xP) observed in only 1/47 Berbers (Table 4). In conclusion, for local forensic purposes, our data based on STR markers is not enough informative to be used in inclusion cases or paternity testing since low values of discriminatory capacity were obtained (Table 2), except for Jerban of Sub-Saharan origin where, 62% of the individuals analysed have their own haplotype. In this case more STR loci should be typed. However, analysis of microsatellite haplotype frequencies for the 128 individuals typed for UEP markers show that homoplasy of STR haplotypes across UEP haplogroups was high: 10.14% (7/68 compound UEP-STR haplotypes). This is what, have increased the number of haplotypes/jerban group and consequently gives higher discriminatory capacities (Table 2). Therefore, even if this was clear just for Jerban Arabs, combined use of UEP and STR markers can be useful for forensic analysis not only for predicting population of origin, but also for providing in some cases more precise male identifications. Nevertheless, the common Y chromosome haplotype (H9) of Jerban Berbers and Mozabites can be used with much care, (i) in constructing ethnic and geographic stratification of Y chromosome haplotypes and (ii) in some forensic special cases, particularly out of Jerba island. Acknowledgements We would like to thank all the DNA donors who made this study possible. We are grateful to Dr. Reiner Veitia for technical help and advice concerning microsatellite typing. This work was supported by the Tunisian Ministry of Higher Education and a French Tunisian cooperation. References [1] M.A. Jobling, C. Tyler-Smith, Fathers and sons, the Y chromosome and human evolution, Trends Genet. 11 (1995) [2] P.A. Underhill, L. Jin, A.A. Lin, S. Q Mehdi, T. Jenkins, D. Vollrath, R.W. Davis, L.L. Cavalli-Sforza, P.J. Oefner, Detection of numerous Y chromosome biallelic polymorphisms by denaturating high-performance liquid chromatography, Genome Res. 7 (1997) [3] P.A. Underhill, P. Shen, A.A. Lin, L. Jin, G. Passarino, W.H. Yang, E. Kauffman, B. Bonne -Tamir, J. Bertranpetit, P.

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