A Perspective on the History of the Iberian Gypsies Provided by Phylogeographic Analysis of Y-Chromosome Lineages ∗ A

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A Perspective on the History of the Iberian Gypsies Provided by Phylogeographic Analysis of Y-Chromosome Lineages ∗ A doi: 10.1111/j.1469-1809.2007.00421.x A Perspective on the History of the Iberian Gypsies Provided by Phylogeographic Analysis of Y-Chromosome Lineages ∗ A. Gusmao˜ 1, L. Gusmao˜ 1, , V. Gomes1, C. Alves1, F. Calafell2, A. Amorim1,3 and M. J. Prata1,3 1Ipatimup, Instituto de Patologia e Imunologia da Universidade do Porto. R. Dr. Roberto Frias, s/n. 4200-465 Porto. Portugal 2Unitat de Biologia Evolutiva, Departament de Ciencies` Experimentals i de la Salut, Universitat Pompeu Fabra. 08003 Barcelona, Catalonia, Spain 3Faculty of Sciences, University of Porto, Pr. Gomes Teixeira, 4099-002 Porto. Portugal Summary The European Gypsies, commonly referred to as Roma, are represented by a vast number of groups spread across many countries. Although sharing a common origin, the Gypsy groups are highly heterogeneous as a consequence of genetic drift and different levels of admixture with surrounding populations. With this study we aimed at contributing to the knowledge of the Roma history by studying 17 Y-STR and 34 Y-SNP loci in a sample of 126 Portuguese Gypsies. Distinct genetic hallmarks of their past and migration route were detected, namely: an ancestral component, shared by all Roma groups, that reflects their origin in India (H1a-M82; ∼17%); an influence from their long permanence in the Balkans/Middle-East region (J2a1b-M67, J2a1b1-M92, I-M170, Q-M242; ∼31%); traces of contacts with European populations preceding the entrance in the Iberian Peninsula (R1b1c-M269, J2b1a-M241; ∼10%); and a high proportion of admixture with the non-Gypsy population from Iberia (R1b1c-M269, R1-M173/del.M269, J2a-M410, I1b1b-M26, E3b1b-M81; ∼37%). Among the Portuguese Gypsies the proportion of introgression from host populations is higher than observed in other groups, a fact which is somewhat unexpected since the arrival of the Roma to Portugal is documented to be more recent than in Central or East Europe. Keywords: Portuguese Gypsies, Gypsy diaspora, Roma, Y-chromosome lineages, Y-SNP haplogroups, Y-STR haplo- types Introduction ter entering Iberia they progressively lost the original lan- guage, and while nowadays many Gitanos still speak Calo, Portugal is the westernmost region reached by the Gypsy which is basically Spanish with a large amount of Romani diaspora after the Roma people arrived in Europe 600– loan words, the Ciganos from Portugal speak Portuguese 700 years ago (Liegeois,´ 1989; Fraser, 1998; Kendrick & with the Calo just being a reminiscent reference language Puxon, 1998). The establishment of Gypsy groups in Por- (Fraser, 1998). tugal is recorded since the second half of the 15th century The Roma in Portugal, as indeed the Roma elsewhere, and at present they are estimated to amount to 30–50 thou- are a transnational genetic isolate which fulfil the prop- sand individuals. The Portuguese Gypsies are likely to be erties that make genetic isolates an interesting resource in a branch of the group that crossed the Pyrenees as early genetic epidemiology; namely, they have reduced genetic as the first quarter of the 15th century and rapidly spread diversity and increased linkage disequilibrium (Gonzalez-´ throughout Spain and Portugal. Contrary to many other Neira et al. personal communication). The Roma therefore Roma, the Iberian Gypsies, known as Gitanos in Spain present a particular genetic disease spectrum, with some and Ciganos in Portugal, are non-Romani-speakers. Af- prevalent diseases almost absent, others specific to Gypsies, and others with private Roma mutations (for a review, ∗ Corresponding Author: Leonor Gusmao,˜ Ipatimup Rua Dr. see Kalaydjieva et al. 2001b). Presently in Portugal, Gypsy Roberto Frias, s/n 4200-465 Porto, Portugal. Tel: +351 22 5570700; communities are spread all over the country and represent Fax: +351 22 5570799; E-mail address: [email protected] indeed a conspicuous component of the Portuguese social C 2008 The Authors Annals of Human Genetics (2008) 72,215–227 215 Journal compilation C 2008 University College London A. Gusmao˜ et al. and demographic landscape. Despite that, little is known Y-STR Typing about the Portuguese Gypsies. How are they related with Seventeen Y-STR loci (DYS19, DYS385, DYS389I, DYS389II, other Gypsy groups? Towhat extent interaction with other DYS390, DYS391, DYS392, DYS393, DYS437, DYS438, Portuguese contributed to change the founder gene pool? DYS439, DYS448, DYS456, DYS458, DYS635 and GATA What signs do they still retain from the complex history H4.1) were amplified using the AmpFlSTR Yfiler PCR Am- that pre-dated their entrance in Iberia? plification Kit (AB Applied Biosystems), following the manufac- Such questions cannot be satisfactorily answered by turers’ instructions. Genotypes were produced with a 310 Ge- applying conventional historical approaches, because the netic Analyser (AB Applied Biosystems), and by comparison to proper sources are almost non-existent. As happens with reference sequenced ladders provided with the kit. The nomen- other Roma groups, the Ciganos from Portugal lack a writ- clature was according to the ISFG recommendations (Gusmao˜ ten history of their own and the documentary sources from et al. 2006) and alleles for GATA H4.1 locus were named by non-Gypsies (Coelho, 1996) are limited to episodic refer- adding nine repeats to the allele numbering of the typing kit ences. (Mulero et al. 2006). The absence of records constitutes a major complication in Gypsy studies and explains why the most instructive evidences about the original homeland of the proto- Y-SNP Typing Gypsies have resulted from linguistics and genetics. Lin- Thirty-four Y-SNPmarkers were hierarchically typed, in order to guistics has provided compelling evidence of an ancestral define the major male lineages (Figure 1). All samples were typed origin in the Indian subcontinent (Liegeois,´ 1989; Fraser for the biallelic markers SRY1532, M213, M9, M70, M22, Tat, 1998; Kendrick & Puxon, 1998). Evidence for this hypoth- 92R7, M173 and P25, as previously described by Brion´ et al. esis has been consistently found in genetic analyses (e.g. (2005). For the remaining SNPs, the following typing scheme Gresham et al. 2001; Morar et al. 2004; Malyarchuk et al. was used: 2006), which, although essentially centred in non-Iberian - M201, M170, 12f2, M26, M62 and M172 were typed in samples Gypsies, have further revealed a particular high level of carrying the M213 mutation and lacking M9, as in Brion´ et al. sub-structuring among Gypsy groups, this is in sharp con- (2005); trast to the surrounding relatively uniform European pop- - M96, M35, M78, M81, M123 and M34 were typed in samples ulations. Small population size, strong drift effects, limited carrying only the SRY1532 mutation, as previously described by inter-group gene flow and differential admixture with the Brion´ et al. (2005); host populations, seem to have acted together leading to - M242 was tested in one individual that fell within haplogroup P (xR1). This mutation was typed by SNaPshot according to strong genetic differentiation between Gypsy groups. This Blanco-Verea et al. (2006); means that no group of Gypsies can be representative of - M269, M18 and M73 were screened in all individuals within other groups, which consequently makes the group the R1∗ haplogroup. M18 and M73 were typed by SNaPshot using basic unit of genetic research, as it is of social organisation the primers described in Brion´ et al. (2005). M269 was typed by (Fraser, 1998). In view of this and in order to address the RFLP (Supplementary Table S1); questions raised above about the Portuguese Ciganos,in -F∗ (xGIJK) individuals were screened for M69, M52, M82 this study we firstly examined a sample of 126 unrelated and Apt mutations in a newly implemented multiplex SNaPshot Gypsy males with a high-resolution Y-chromosome STR reaction (Supplementary Table S1); and SNP typing strategy; secondly we exploited the results - Samples carrying M172 were tested for M410, M67, M92, in the context of previously published data on other Gypsy M12 and M241 using also SNaPshot methods (Supplementary groups and respective host populations, and finally we tried Table S1). to unfold layers of genetic male lineages in the Portuguese The YCC (2002) and Jobling & Tyler-Smith (2003) nomen- Gypsies to retrieve information about major events in their clature was updated according to Cruciani et al. (2004); Sengupta demographic history. et al. (2006); Semino et al. (2004) and Cinnioglu˘ et al. (2004). Material and Methods Data Analysis Sample Collection Haplotype diversity, mean number of pairwise differences and pairwise genetic distances (Rst, for STR-haplotypes and Fst for Blood samples were taken under informed consent from 126 SNP-haplogroups) were calculated using the Arlequin software unrelated Gypsy males, from 18 different communities in 11 dif- ver. 3.01 (Excoffier & Scheinder, 2005). In genetic distance ferent Portuguese districts. Personal inquiries were made to each analyses, DYS385 was not considered, and the number of re- individual in order to avoid close kinship. Genomic DNA was peats in DYS389I was subtracted from DYS389II. Haplogroup extracted according to standard phenol-chloroform method. frequencies were estimated by direct counting. 216 Annals of Human Genetics (2008) 72,215–227 C 2008 The Authors Journal compilation C 2008 University College London A Perspective on the History of the Iberian Gypsies Figure 1 Phylogenetic network of Y-SNP haplogroups, indicating the biallelic markers typed in the present work and their absolute frequencies in a sample of 126 Portuguese
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