Indian Siddis: African Descendants with Indian Admixture
2011; Elsevier BV; Volume: 89; Issue: 1 Linguagem: Inglês
10.1016/j.ajhg.2011.05.030
ISSN1537-6605
AutoresAnish M. Shah, Rakesh Tamang, Priya Moorjani, Deepa Selvi Rani, Periyasamy Govindaraj, Gururaj D. Kulkarni, Tanmoy Bhattacharya, Mohammed S. Mustak, L.V.K.S. Bhaskar, Alla G. Reddy, Dharmendra Gadhvi, Pramod B. Gai, Gyaneshwer Chaubey, Nick Patterson, David Reich, Chris Tyler‐Smith, Lalji Singh, Kumarasamy Thangaraj,
Tópico(s)Colonialism, slavery, and trade
ResumoThe Siddis (Afro-Indians) are a tribal population whose members live in coastal Karnataka, Gujarat, and in some parts of Andhra Pradesh. Historical records indicate that the Portuguese brought the Siddis to India from Africa about 300–500 years ago; however, there is little information about their more precise ancestral origins. Here, we perform a genome-wide survey to understand the population history of the Siddis. Using hundreds of thousands of autosomal markers, we show that they have inherited ancestry from Africans, Indians, and possibly Europeans (Portuguese). Additionally, analyses of the uniparental (Y-chromosomal and mitochondrial DNA) markers indicate that the Siddis trace their ancestry to Bantu speakers from sub-Saharan Africa. We estimate that the admixture between the African ancestors of the Siddis and neighboring South Asian groups probably occurred in the past eight generations (∼200 years ago), consistent with historical records. The Siddis (Afro-Indians) are a tribal population whose members live in coastal Karnataka, Gujarat, and in some parts of Andhra Pradesh. Historical records indicate that the Portuguese brought the Siddis to India from Africa about 300–500 years ago; however, there is little information about their more precise ancestral origins. Here, we perform a genome-wide survey to understand the population history of the Siddis. Using hundreds of thousands of autosomal markers, we show that they have inherited ancestry from Africans, Indians, and possibly Europeans (Portuguese). Additionally, analyses of the uniparental (Y-chromosomal and mitochondrial DNA) markers indicate that the Siddis trace their ancestry to Bantu speakers from sub-Saharan Africa. We estimate that the admixture between the African ancestors of the Siddis and neighboring South Asian groups probably occurred in the past eight generations (∼200 years ago), consistent with historical records. Siddis, or Habshis, are a unique tribe that has African ancestry and lives in South Asia. They are mainly found in three Indian states—Gujarat, Karnataka, and Andhra Pradesh—and according to the latest census, their total population size is about 0.25 million.1Lodhi A. African settlements in India.Nordic Journal of African Studies. 1992; 1: 83-86Google Scholar The first documented record of Siddis in India dates to 1100 AD, when the Siddis settled in Western India.2Bhattacharya D. Indians of African origin.Cah. Etud. Afr. 1970; 10: 579-582Crossref Google Scholar, 3Gauniyal M. Chahal S.M. Kshatriya G.K. Genetic affinities of the Siddis of South India: an emigrant population of East Africa.Hum. Biol. 2008; 80: 251-270Crossref PubMed Scopus (15) Google Scholar By the thirteenth century, substantial numbers of Siddis were being imported by the Nawabs and the Sultans of India to serve as soldiers and slaves. The major influx of Siddis occurred during the 17th–19th centuries, when the Portuguese brought them as slaves to India.2Bhattacharya D. Indians of African origin.Cah. Etud. Afr. 1970; 10: 579-582Crossref Google Scholar Previous genetic studies have shown that the Siddis have ancestry from up to three continental groups: Africans, Europeans, and South Asians.2Bhattacharya D. Indians of African origin.Cah. Etud. Afr. 1970; 10: 579-582Crossref Google Scholar, 4Thangaraj K. Ramana G.V. Singh L. Y-chromosome and mitochondrial DNA polymorphisms in Indian populations.Electrophoresis. 1999; 20: 1743-1747Crossref PubMed Scopus (39) Google Scholar, 5Ramana G.V. Su B. Jin L. Singh L. Wang N. Underhill P. Chakraborty R. Y-chromosome SNP haplotypes suggest evidence of gene flow among caste, tribe, and the migrant Siddi populations of Andhra Pradesh, South India.Eur. J. Hum. Genet. 2001; 9: 695-700Crossref PubMed Scopus (67) Google Scholar Some genetic studies have suggested that they are most closely related to Africans.3Gauniyal M. Chahal S.M. Kshatriya G.K. Genetic affinities of the Siddis of South India: an emigrant population of East Africa.Hum. Biol. 2008; 80: 251-270Crossref PubMed Scopus (15) Google Scholar, 6Gauniyal M. Aggarwal A. Kshatriya G.K. Genomic Structure of the Immigrant Siddis of East Africa to Southern India: A Study of 20 Autosomal DNA Markers.Biochem. Genet. 2011; (Published online January 28, 2011)https://doi.org/10.1007/s10528-011-9419-7Crossref PubMed Scopus (6) Google Scholar However, the specific African group to which the Siddis trace their ancestry remains unknown. To obtain a high-resolution genome-wide perspective of ancestry, we analyzed data from three Siddi groups (from Karnataka and Gujarat) by genotyping them with ∼850,000 autosomal and sex-linked markers. Applying statistical methods, we have estimated the contributions of various continental ancestries to the Siddis genome and investigated the likely source of the ancestral populations and the timing of the admixture events. Blood samples (about 10 ml from each individual) were collected from Gujarat and Karnataka in India. Specifically, we collected samples from 60 Siddis (unrelated and healthy males) and 90 individuals belonging to the nearby tribal populations (Charan and Bharwad) of the Junagarh district of Gujarat and from 94 Siddis (65 males and 29 females) and 178 individuals belonging to neighboring tribal populations (Medar, Gram Vokkal, Kare Vokkal, and Korova) from the Uttara Kannad district of Karnataka. Informed written consent was obtained from all the donors. This project was approved by the Institutional Ethical Committee of the Centre for Cellular and Molecular Biology, Hyderabad, India. We genotyped 16 Siddi samples on Affymetrix (SNP 6.0) arrays by using standard protocols. We removed four duplicate samples and restricted the analysis to SNPs that had > 25), but the genetic variation in Africans does not fully explain the underlying genetic data in the Siddis (Table S2A). Next, we assessed whether a two-way model or three-way mixture model provides a better fit to the data. Table S2B shows that a two-way model of African + Portuguese or African + Mala (or any other group that has high ASI ancestry) provides a poor fit to the data. However, the model of African + Vaish (or any other group that has high ANI ancestry) provides just as good a fit to the data as a three-way model of African + any Indian population + Portuguese (Table S2B). This suggests that the Siddis have some West-Eurasian-related (ANI or Portuguese) ancestry, in addition to their African and ASI ancestry. However, the size of our dataset prevents our methods from being sensitive enough to differentiate between ANI and Portuguese ancestry. To represent the ancestral non-African population of the Siddis, we combined the data from 16 Indian groups and the Portuguese (“ICP”). To test the robustness of our models, we analyzed Siddi Karnataka samples with the models built from the Siddi Gujarat samples and showed that the models provided a good fit to the data (Table S2C). Applying the regression-style method to all three Siddi groups with YRI and ICP as the ancestral populations, we estimated that the Siddis have on average ∼67% African ancestry (Table 1). We obtained qualitatively similar results when we used East Africans (HapMap Luhya [LWK]) in place of YRI (Table 1 and Table S2D).Table 1Estimation of Ancestry Proportions in the SiddisAfrican AncestryNon-African AncestryAfrican Ancestral Population = West Africans (YRI)Siddi_Gujarat66.90% ± 0.59%33.10% ± 0.59%Siddi_Karnataka-170.90% ± 0.65%29.10% ± 0.65%Siddi_Karnataka-262.30% ± 0.99%37.70% ± 0.99%African Ancestral Population = East Africans (LWK)Siddi_Gujarat70.50% ± 0.66%29.50% ± 0.66%Siddi_Karnataka-174.40% ± 0.71%25.60% ± 0.71%Siddi_Karnataka-264.80% ± 1.11%35.20% ± 1.11%Admixture proportion estimates are based on a regression-style method11Patterson N. Petersen D.C. van der Ross R.E. Sudoyo H. Glashoff R.H. Marzuki S. Reich D. Hayes V.M. Genetic structure of a unique admixed population: Implications for medical research.Hum. Mol. Genet. 2010; 19: 411-419Crossref PubMed Scopus (88) Google Scholar for which the ancestral populations shown in the table were used. ICP includes combined data from 16 Indian groups and the Portuguese and represents the ancestral non-African population. Open table in a new tab Admixture proportion estimates are based on a regression-style method11Patterson N. Petersen D.C. van der Ross R.E. Sudoyo H. Glashoff R.H. Marzuki S. Reich D. Hayes V.M. Genetic structure of a unique admixed population: Implications for medical research.Hum. Mol. Genet. 2010; 19: 411-419Crossref PubMed Scopus (88) Google Scholar for which the ancestral populations shown in the table were used. ICP includes combined data from 16 Indian groups and the Portuguese and represents the ancestral non-African population. To characterize the temporal impact of admixture and to develop a historical interpretation of the results, we needed not only to qualitatively demonstrate a history of admixture but also to quantitatively estimate a date for the admixture event. We applied the ROLLOFF method,12Moorjani P. Patterson N. Hirschhorn J.N. Keinan A. Hao L. Atzmon G. Burns E. Ostrer H. Price A.L. Reich D. The history of african gene flow into southern europeans, levantines, and jews.PLoS Genet. 2011; 7: e1001373Crossref PubMed Scopus (165) Google Scholar which utilizes information related to admixture linkage disequilibrium (LD) to estimate the time since admixture. This method capitalizes on the fact that the genome of an admixed population contains chromosomal segments from ancestral populations, whose length is inversely proportional to the date of admixture. By modeling the decay of the LD in the admixed individuals and weighting it by the allele frequency differentiation in the ancestral populations (such that the statistics are only sensitive to admixture LD), we can precisely estimate the time since the admixture event. Simulations have suggested that this method is robust for data from poor surrogates of ancestral populations and can estimate the date of admixture up to 300 generations ago.12Moorjani P. Patterson N. Hirschhorn J.N. Keinan A. Hao L. Atzmon G. Burns E. Ostrer H. Price A.L. Reich D. The history of african gene flow into southern europeans, levantines, and jews.PLoS Genet. 2011; 7: e1001373Crossref PubMed Scopus (165) Google Scholar Applying ROLLOFF to the Siddis (combining data from all three groups—Siddi_Karnataka-1, Siddi_Karnataka-2, and Siddi_Gujarat—to increase the power), we observed an approximately exponential decay of the weighted correlation with distance, which provides strong evidence of admixture (Figure 2). By using the least-squares method to fit an exponential distribution to this pattern, we estimated an average date of ∼eight generations, or 200 years (if one assumes a generation size of 25 years13Rootsi S. Zhivotovsky L.A. Baldovic M. Kayser M. Kutuev I.A. Khusainova R. Bermisheva M.A. Gubina M. Fedorova S.A. Ilumae M.A. et al.A counter-clockwise northern route of the Y-chromosome haplogroup N from Southeast Asia towards Europe.Eur. J. Hum. Genet. 2008; 15: 204-221Crossref Scopus (119) Google Scholar). This approximately coincides with the historical date of arrival of most African ancestors of the Siddis to India. To show that combining the data from the admixed group does not substantially change the results, we ran ROLLOFF separately for each admixed group and obtained qualitatively similar results (within two standard errors) for Siddi_Gujarat and Siddi_Karnataka-1. Because of the limited number of samples, we were not able to perform analysis for the Siddi_Karnataka-2 group (ROLLOFF analysis requires at least four samples). In addition, changing the African ancestral group to East African Luhya did not change the estimated date of admixture (Figure S1). To gain insight into the most likely source of the African ancestry in Siddis, we examined paternally inherited Y-chromosomal biallelic markers as well as maternally inherited mtDNA markers. Analysis of data from uniparentally inherited markers can provide information about population genetic relatedness, including probable ancestral source populations and information related to admixture events. We genotyped 32 Y-chromosomal biallelic markers (viz. M94, M60, M182, M168, M130, M145, M96, M75, M2, M89, M82, M304, M172, M9, M70, M11, M45, M207, M173, M17, M124, M201, M170, M70, M147, M189, M214, M52, M33, M356, P36, and P2) in 125 Siddis and 268 individuals (all males) from nearby Indian groups. We combined our data with published data from 2,301 individuals belonging to 56 different groups from the African subcontinent and 667 individuals from 16 populations from Gujarat, Karnataka, Maharashtra, and Andhra-Pradesh in India (Document S2).14Scozzari R. Torroni A. Semino O. Cruciani F. Spedini G. Santachiara Benerecetti S.A. Genetic studies in Cameroon: Mitochondrial DNA polymorphisms in Bamileke.Hum. Biol. 1994; 66: 1-12PubMed Google Scholar, 15Scozzari R. Cruciani F. Santolamazza P. Sellitto D. Cole D.E. Rubin L.A. Labuda D. Marini E. Succa V. Vona G. Torroni A. mtDNA and Y chromosome-specific polymorphisms in modern Ojibwa: implications about the origin of their gene pool.Am. J. Hum. Genet. 1997; 60: 241-244PubMed Google Scholar, 16Scozzari R. Cruciani F. Pangrazio A. Santolamazza P. Vona G. Moral P. Latini V. Varesi L. Memmi M.M. Romano V. et al.Human Y-chromosome variation in the western Mediterranean area: Implications for the peopling of the region.Hum. Immunol. 2001; 62: 871-884Crossref PubMed Scopus (72) Google Scholar, 17Cruciani F. Santolamazza P. Shen P. Macaulay V. Moral P. Olckers A. Modiano D. Holmes S. Destro-Bisol G. Coia V. et al.A back migration from Asia to sub-Saharan Africa is supported by high-resolution analysis of human Y-chromosome haplotypes.Am. J. Hum. Genet. 2002; 70: 1197-1214Abstract Full Text Full Text PDF PubMed Scopus (282) Google Scholar, 18Luis J.R. Rowold D.J. Regueiro M. Caeiro B. Cinnioğlu C. Roseman C. Underhill P.A. Cavalli-Sforza L.L. Herrera R.J. The Levant versus the Horn of Africa: Evidence for bidirectional corridors of human migrations.Am. J. Hum. Genet. 2004; 74: 532-544Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar, 19Semino O. Santachiara-Benerecetti A.S. Falaschi F. Cavalli-Sforza L.L. Underhill P.A. Ethiopians and Khoisan share the deepest clades of the human Y-chromosome phylogeny.Am. J. Hum. Genet. 2002; 70: 265-268Abstract Full Text Full Text PDF PubMed Scopus (137) Google Scholar, 20Semino O. Magri C. Benuzzi G. Lin A.A. Al-Zahery N. Battaglia V. Maccioni L. Triantaphyllidis C. Shen P. Oefner P.J. et al.Origin, diffusion, and differentiation of Y-chromosome haplogroups E and J: Inferences on the neolithization of Europe and later migratory events in the Mediterranean area.Am. J. Hum. Genet. 2004; 74: 1023-1034Abstract Full Text Full Text PDF PubMed Scopus (319) Google Scholar, 21Underhill P.A. Shen P. Lin A.A. Jin L. Passarino G. Yang W.H. Kauffman E. Bonné-Tamir B. Bertranpetit J. Francalacci P. et al.Y chromosome sequence variation and the history of human populations.Nat. Genet. 2000; 26: 358-361Crossref PubMed Scopus (768) Google Scholar, 22Plaza S. Salas A. Calafell F. Corte-Real F. Bertranpetit J. Carracedo A. Comas D. Insights into the western Bantu dispersal: mtDNA lineage analysis in Angola.Hum. Genet. 2004; 115: 439-447Crossref PubMed Scopus (69) Google Scholar, 23Kivisild T. Rootsi S. Metspalu M. Mastana S. Kaldma K. Parik J. Metspalu E. Adojaan M. Tolk H.V. Stepanov V. et al.The genetic heritage of the earliest settlers persists both in Indian tribal and caste populations.Am. J. Hum. Genet. 2003; 72: 313-332Abstract Full Text Full Text PDF PubMed Scopus (289) Google Scholar, 24Thanseem I. Thangaraj K. Chaubey G. Singh V.K. Bhaskar L.V.K.S. Reddy B.M. Reddy A.G. Singh L. Genetic affinities among the lower castes and tribal groups of India: Inference from Y chromosome and mitochondrial DNA.BMC Genet. 2006; 7: 42Crossref PubMed Scopus (82) Google Scholar, 25Trivedi R. Sahoo S. Singh A. Bindu G. Banerjee J. Tandon M. Gaikwad S. Rajkumar R. Sitalaximi T. Ashma R. Genetic imprints of Pleistocene origin of Indian populations: A comprehensive phylogeographic sketch of Indian Y-chromosomes.Int. J. Hum. Genet. 2008; 8: 97-118Google Scholar, 26Thangaraj K. Naidu B.P. Crivellaro F. Tamang R. Upadhyay S. Sharma V.K. Reddy A.G. Walimbe S.R. Chaubey G. Kivisild T. Singh L. The influence of natural barriers in shaping the genetic structure of Maharashtra populations.PLoS ONE. 2010; 5: e15283Crossref PubMed Scopus (25) Google Scholar We observed that the Y-chromosomal haplogroups B2-M182 and E1b1a-M2, which are characteristic of African ancestry, were present at high frequencies in the Siddis but not in other Indians. Moreover, about 70% of the Siddi male lineages fall into haplogroups generally characteristic of African populations (Figure 3A ), thus confirming the results from the autosomal DNA markers (Figure 1B). The remaining 30% were C∗-M130- and M89-derived Indian or Near-Eastern lineages (H1a-M82, H2-Apt-H2, J2-M172, L-M11, and P∗-M45). The populations neighboring the Siddis were found to harbor only these Asian-specific haplogroups. It is interesting to note that none of the African paternal lineages were observed among the neighboring Indian groups, whereas Indian-specific lineages were detected in Siddi individuals. This suggests primarily unidirectional paternal gene flow from Indian populations to the Siddis (Figure 2B). To learn more about the source of the African paternal lineages, we performed PCA with a merge of our Y-chromosomal dataset (Siddis and neighboring Indian groups) with data from 2,301 individuals from 56 African populations (Document S2). A plot of the first and second PCs showed that the Siddis cluster with Bantu-speaking populations of sub-Saharan Africa (Figure S2A). Previous studies have proposed that the E3a (currently known as E1b1a), E2, and B2 haplogroups are associated with the Bantu expansions within Africa.21Underhill P.A. Shen P. Lin A.A. Jin L. Passarino G. Yang W.H. Kauffman E. Bonné-Tamir B. Bertranpetit J. Francalacci P. et al.Y chromosome sequence variation and the history of human populations.Nat. Genet. 2000; 26: 358-361Crossref PubMed Scopus (768) Google Scholar, 22Plaza S. Salas A. Calafell F. Corte-Real F. Bertranpetit J. Carracedo A. Comas D. Insights into the western Bantu dispersal: mtDNA lineage analysis in Angola.Hum. Genet. 2004; 115: 439-447Crossref PubMed Scopus (69) Google Scholar, 27Brehm A. Pereira L. Bandelt H.J. Prata M.J. Amorim A. Mitochondrial portrait of the Cabo Verde archipelago: The Senegambian outpost of Atlantic slave trade.Ann. Hum. Genet. 2002; 66: 49-60Crossref PubMed Scopus (60) Google Scholar The presence of these haplogroups in the Siddis suggests that their ancestors might have been part of this expansion. To investigate this possibility, we typed 17 Y-STRs by using multiplex PCR and the Y-filer kit (Applied Biosystems, Foster City, USA) in reaction volumes of 10 μl with 1U of AmpliTaq Gold DNA polymerase (Applied Biosystems, Foster City, USA), 10 mM Tris-HCl (pH 8.3), 50 mM KCl, 1.5 mM MgCl2, 250 μM dNTPs, 3.0 μM of each primer (forward primers were fluorescently labeled), and 1 ng of DNA template. Thermal cycling conditions were as follows: (1) 95°C for 11 min, (2) 30 cycles as follows: 94°C for 1 min, 61°C for 1 min, and 72°C for 1 min, (3) 60°C for 80 min, and (4) 25°C hold. The PCR amplicons along with GS500 LIZ (as a size standard) were run in the ABI 3730 DNA Analyzer (Applied Biosystems, Foster City, USA). The raw data were analyzed with the GeneMapper v4.0 software program (Applied Biosystems, Foster City, US). We excluded two DYS385 loci from the current analyses because they could not be distinguished via the typing method employed, and we renamed locus DYS389I as DYS389b, whereas we calculated DYS389a by subtracting DYS389I from DYS389II. We constructed median-joining networks with ten common loci (Figure S3) for the two major African haplogroups (E1b1a-M2 and B2-M182) that are present at high frequencies in Siddis. We supplemented our dataset with other published data that included African samples.28Berniell-Lee G. Calafell F. Bosch E. Heyer E. Sica L. Mouguiama-Daouda P. van der Veen L. Hombert J.M. Quintana-Murci L. Comas D. Genetic and demographic implications of the Bantu expansion: Insights from human paternal lineages.Mol. Biol. Evol. 2009; 26: 1581-1589Crossref PubMed Scopus (92) Google Scholar, 29Tofanelli S. Bertoncini S. Castrì L. Luiselli D. Calafell F. Donati G. Paoli G. On the origins and admixture of Malagasy: New evidence from high-resolution analyses of paternal and maternal lineages.Mol. Biol. Evol. 2009; 26: 2109-2124Crossref PubMed Scopus (83) Google Scholar The TMRCA (time to most recent common ancestor) was estimated with the ρ statistic (the mean number of mutations from the assumed root), for which a 25-year generation time was used, and the TD statistic (for both, a mutation rate of 6.9 × 10−4 per STR per generation was assumed),30Zhivotovsky L.A. Underhill P.A. Cinnioğlu C. Kayser M. Morar B. Kivisild T. Scozzari R. Cruciani F. Destro-Bisol G. Spedini G. et al.The effective mutation rate at Y chromosome short tandem repeats, with application to human population-divergence time.Am. J. Hum. Genet. 2004; 74: 50-61Abstract Full Text Full Text PDF PubMed Scopus (333) Google Scholar The majority of the Siddis haplotypes were found shared on otherwise Bantu-specific branches and were present all over the tree (Figure S3). In addition, the Gujarat and Karnataka Siddis were highly diverged and did not share any haplotypes. These results support the autosomal observation of high Fst differentiation among Siddis from Gujarat and Karnataka. Although the majority of the Siddi haplotypes were scattered in the network, we found that all haplogroup B2 Gujarat Siddis formed a cluster and coalesced to their most recent common ancestor 2.4 ± 1 Kya (thousand years ago). The sharing of haplotypes suggests relatedness among the samples. This is similar to the results seen in the autosomal analyses of the Siddi_Gujarat and Siddi_Karnataka-2 samples. The male effective population size was estimated with BATWING31Beerli P. Felsenstein J. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach.Proc. N
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