HLA affinities of Iyers, a Brahmin population of Tamil Nadu, South India
Balakrishnan, K
Abstract Seventy-four randomly sampled Iyers, a Brahmin population of Tamil Nadu and preachers and followers of the Advaita philosophy, living in Madurai, were studied for their HLA-A, HLA-B, HLAC, HLA-DR, HLA-DQ, C4A, C4B, and BF polymorphisms and compared with other populations. HLA alleles A1, Al 1.1, A24, A33, B35, B44, B51, B52, B57, Cw4, Cw6, Cw7, DR4, DR7, DR8, DR]0, DR]], DR15, and DQ] and C4A*3, C4A*4, C4A*6, C4A*QO, C4B*1, and BF*S were represented in 15% of the samples studied. HLA alleles A25, A69, Cw3, Cw8, B45, B14, B39, B18, B50, and B56 were not identified. Various populations of Tamil Nadu were compared, but the Iyers of Madurai formed a separate cluster with Sourashtrans of Madurai and major group 4 (various Brahmin populations of Tamil Nadu); hill tribes (Irulas, Malayalis, and Badagas) and caste groups in the plains (Kallars and Nadars) formed distinct clusters. Comparison of the Iyers with other Indian and world populations revealed that Iyers form a distinct branch of the IndoEuropean and Central Asian tree. The Bhargavas of Lucknow, another Brahmin caste group from Uttar Pradesh, did not cluster with the yers but clustered with Central Asian populations. The Punjabis of Delhi clustered with European and Middle Eastern populations. Studies on twolocus haplotypes of Iyers revealed unique haplotypes in them (A26-B8, A33-B44, A33-Cw7, Al-B57, B8-DR3, B44-DR7, DR7-DQ2, C4A*32C4B*QO, and C4A*6-C4B*2), most of which were not identified in the Bhargavas of Lucknow and the Punjabis of Delhi. Thus it is possible that various Brahmin populations of India differ in their origin, migration, and settlement, although all of them adopted Hinduism in ancient times. A comparison of haplotypes in Iyers with the world population reveals a sharing of haplotypes with Southeast Asian populations. This implies that the ancestors of the Iyers of Madurai, who originated in the Eurasian steppes or Central Asia, might have migrated to India through Southeast Asia, thus developing the prevalent haplotypes en route.
HLA Affinities of Iyers, a Brahmin Population of Tamil Nadu, South India K. BALAKRISHNAN,1 R.M. PITCHAPPAN,1 K. SUZUKI,2 U. SANKAR KUMAR,1 R. SANTHAKUMARI,2 AND K. TOKUNAGA3
The ancestral history of South India and modern studies on the genetics of its inhabitants are still relatively new subjects (Nilakanta Sastry 1955; Singh 1993; Joshi et al. 1993; Reddy et al. 1993). The population of Tamil Nadu can be divided into four social strata that correlate well with the migrational history, genetics, and anthropology of Tamil Nadu [see Balakrishnan and Sanghvi (1981)]. Language may not have a good relation to ethnic group, but it may be of value in the study of cultural history. This leaves us with biological (genetic) diversity as a reliable tool to decipher demic spread (CavalliSforza et al. 1993). Indeed, genetic differences between the different caste groups of Tamil Nadu are as high as that of two major ethnic groups of the world (Sanghvi et al. 1981; Pitchappan 1988). This may not be surprising, considering the origin and characteristics of the caste system, viz., migration, miscegenation, endogamy, inbreeding, and sympatric isolation [see Sunder Rao (1984)].
To understand the distribution of HLA antigens in South India, we study various populations (castes) and correlate them with various diseases (Pitchappan et al. 1984, 1986, 1989; Rajasekar et al. 1987; Pitchappan 1988; Brahmajothi et al. 1991; Balakrishnan 1993). Here, we present the HLA and complement polymorphism results in Iyers, a Brahmin caste group living in Tamil Nadu, and compare them with results from other caste groups of Tamil Nadu and selected populations of India and the world.
Brahmins everywhere in India enjoy the highest social status in Hindu society and claim that they are the descendants of one of the seven rishis (saints) (Nilakanta Sastry 1955; Sanghvi and Balakrishnan 1981). Brahmins from different parts of India have adopted the local languages and customs of their place of settlement (e.g., first-cousin and uncle-niece marriages in South India but not in North India), although their ideologies, profession, and major language (Sanskrit) remained the same. However, they can be heterogeneous in their origin and genetic profile.
Brahmins of Tamil Nadu are divided into two main sects: Saivites (Shiva worshippers) and Vaishnavites (Vishnu worshippers). The Smartha sect of Saivism (Advaita philosophy) was founded by Adi Sankara, a Nambudri Brahmin of Kerala (A.D. 788-820). The yers of Tamil Nadu and nearby states of Kerala and Karnataka are the preachers and followers of the Advaita philosophy.
Previous studies on the Iyers of Tamil Nadu brought out their genetic and anthropological profile and distinguished them from other caste groups of Tamil Nadu (Balakrishnan and Sanghvi 1981; Undevia et al. 1981; Malhotra et al. 1981). The genetic profile revealed that the Iyers have a higher frequency of blood group A than of blood group B and high frequencies of ABH secretors, PTC tasters, and color-blind individuals (Undevia et al.1981). The Iyers learned and adopted many local customs. For example, uncle-niece marriages and first-cousin marriages, local practices of consanguinity in Tamil Nadu, are prevalent in the Iyers but are unknown in Brahmins of other states in India. As a result, the inbreeding coefficient of the Iyers was 0.019 in the 1960s (Balakrishnan and Sanghvi 1981). Thus, it is interesting to study such a sympatrically isolated, endogamous population with such a polymorphic tool as the HLA system, which encompasses the immune response genes, and to compare the population with other populations of Tamil Nadu, India, and nearby regions.
Materials and Methods
Volunteers. Seventy-four unrelated individuals belonging to the Iyers, a subgroup of Brahmins living in Madurai, were enrolled at random and studied. They were students and staff members of Madura College, run by Brahmins. The ages of the subjects ranged from 17 to 50 years; 55.4% of the subjects belonged to the age group 17-19 years, and the male:female ratio was 6.4:1.
Sampling. Five to seven samples of blood per day were obtained over a period of 1 month. Details on the subsect and gothram (patrilineal clan) of both parents and the parents’ nativity, address, and other details were obtained from a precoded questionnaire. Ten milliliters of blood was obtained from each volunteer using sterile disposable syringes and needles. Seven milliliters of blood was defibrinated, and 3 ml of blood was dispensed to 0.3 ml of EDTA in a vial and refrigerated. The samples were taken to the laboratory (16 km away) and processed the same day.
HLA Typing. HLA typing was performed by two-stage microlymphocytotoxicity assay (Terasaki and McClelland 1964), and two-color fluorescence was used to read the results (van Rood et al. 1976). Lymphocytes were isolated from defibrinated blood samples on a Ficoll-Conray density solution (Boyum 1968). HLA class II typing for HLA-DR and HLA-DQ were performed on B lymphocytes isolated using a miniature nylon wool column (Manickasundari et al. 1984) and a long incubation period.
Two hundred ninety-nine samples of sera for HLA-A, HLA-B, and HLA-C loci and 239 samples of sera for HLA-DR and HLA-DQ loci provided by the IHWC XI (llth International Histocompatibility Workshop and Conference; Tsuji et al. 1992) were used. In addition, 58 samples of sera for HLAA and HLA-B specificities and 58 samples of sera for HLA-DR specificities, obtained locally and characterized in our screening program, were used to assign the HLA antigens (Balakrishnan 1993; Pitchappan et al. 1993). Thus 16 alleles of HLA-A, 27 alleles of HLA-B, 8 alleles of HLA-C, 13 alleles of HLA-DR, and 5 alleles of HLA-DQ were defined. The nomenclature used to define these alleles serologically has been reported by Bodmer et al. (1992). The allele frequencies of the HLA loci were obtained from the phenotypes using Bernstein’s formula, and hence only the nomenclature of the serological definition has been used to describe various alleles.
Results of HLA typing were read in a Leitz-Patimed system and stored in a database (Pitchappan and Arulraj 1989). The score data were analyzed for the behavior of the applied reagents using our computer program and the quality of antigen assignment (Pitchappan and Arulraj 1989; Balakrishnan 1993). Most of the antisera gave a serum versus serum correlation coefficient greater than 0.8, with another antiserum reacting to the same specificity. A serum versus antigen correlation gave a coefficient greater than 0.9.
Complement Typing. Plasma in an EDTA solution for complement studies was processed and frozen at – 80degC within 4 hours of obtaining the blood. Plasma was separated using a refrigerated centrifuge (set at 100C), divided into aliquots, and frozen. The plasma was sent to Japan within two months of collection and typed for BF, C4A, and C4B polymorphisms (Tokunaga et al. 1992). The allele frequencies of BF, C4A, and C4B were calculated from phenotype frequencies by the direct gene counting method.
Statistical Analysis. The frequencies of HLA alleles and haplotypes were estimated and their standard errors were calculated using standard methods [Mattiuz et al. 1970; see also Baur and Danilovs (1980)]. A dedicated computer database and software developed for HLA studies were used to analyze the data (Pitchappan and Arulraj 1989). The SPSS PC + (version 2.0) statistics package was used to compare various populations; a squared Euclidean measure was used to calculate the genetic distance, and the dendrogram was drawn using complete linkage.
Other Population Comparisons. Data on other populations used for comparison were from published sources and from IHWC XI (Tsuji et al. 1992). Details are given in the figure legends and tables.
Results
HLA Polymorphism in the Iyers. Table 1 presents the phenotype and allele frequencies of the various HLA and complement loci studied. The phenotype percentages of HLA Al, A24, A33, Cw4, Cw6, Cw7, B5, DR4, DR7, DQ1 and DQ3 were greater than or equal to 30%. HLA A25, A69, Cw3, Cw8, B45, B 14, B39, B 18, B50, and B56 were not represented in this sample; HLA A23, All.2, A36, A43, CwS, B16, B38, B58, B27, B70, and B78 were rare (1/148 alleles each). Many new splits, described at IHWC XI (Tsuji et al. 1992), such as HLA B5.35 (B*5102), B78, B75, B70, B67, B68, and A43, were also identified in the Iyers (Table 1). Most of the HLA All alleles identified in Iyers were of the All.1 subtype (12/13). Although HLA A19
Table omitted
was present in 54% of the phentotypes, A33 was the major split (29.7%) followed by A31 (10.8%). Among HLA DR2 specificities DR15 was the most common allele (16/20),, and among HLA DR5 specificities DR11 was the most common allele (11/15); DR14 was rare, but DR10 was quite common (10.8% phenotype frequency).
Allele frequencies for the BF, C4A, and C4B loci among the Iyers (Table 2) revealed that BF*S, C4A*3, and C4B*1 were the major alleles present in this population, with frequencies of 0.75, 0.69, and 0.817, respectively. Many rare alleles of the complement loci C4A*55 and C4B*35 were also identified in the Iyers. A new allele, C4B*18, was found in one Iyer sample (Mauff et al. 1992).
Table 3 lists two-locus calculated haplotypes identified in the Iyers of Madurai. A33-B44, Al-B57, A33-Cw7, B44-DR7, B8-DR3, and DR7-DQ2 were the most frequent.
Comparison of the Iyers with Other Populations. HLA-A and HLA-B allele frequency estimates of various population and caste groups studied hitherto in our laboratory were compared with the Iyers. Figure 1 presents the dendrogram derived from the genetic distance analysis; three clusters are apparent among the populations. The first cluster is formed by the Iyers, major group IV [various Brahmin populations of Tamil Nadu considered together; see Pitchappan et al. (1984)], and the Sourashtrans of Madurai (a migrant group from Gujarat) (Sethuraman 1977; Pitchappan et al. 1986). The second cluster is composed of Kallars, Nadars [an ancient population of Tamil Nadu; see Sanghvi et al. (1981)], and major group III [a cluster of Vellalas, i.e., artisan-related caste groups; see Pitchappan et al. (1984) and Rajasekar et al. (1987)]. The third cluster is formed by the three hill tribes Badagas (Selvakumar et al. 1987), Irulas of Nilgiri, and Malayalis of Shevroy (Balakrishnan 1993).
Figure 2 presents the relationship of the Iyers with various other Indian populations and populations from Southeast Asia, the Far East, Central Asia, the Middle East, and Europe, studied at the IHWC XI (Tsuji et al. 1992). Data on HLA-A, HLA-B, HLA-C, HLA-DR, and HLA-DQ loci were considered and compared. The following observations can be made: (1) The Iyers of Madurai and Indians (a mixture of Indian immigrant samples studied by various laboratories around the world and data submitted to IHWC XI) along with Spanish Gypsies form a distinct cluster that in turn joins the European and Central Asian clusters. (2) Various populations of India studied at the IHWC XI and compared here, namely, the Bhargavas of Lucknow (another Brahmin population from Uttar Pradesh) and the Punjabis of Delhi, do not fall into the same cluster with the yers of Madurai. (3) Although the Bharagavas of Lucknow cluster with Uzbekis, Ukrainians, and Portuguese, the Punjabis of Delhi cluster with Armenians, Iranians, Iraqis, and other European populations. (4) The Far Eastern and Southeast Asian populations form another major subdivision of the tree, and none of the Indian populations considered in the present study fall into this cluster.
Discussion
We have described the presence of many newly defined alleles, such as HLA A11.1, B5.35, B70, B75, and B78, and a few highly significant twolocus haplotypes in the Iyers of Madurai. The genetic distance and cluster analyses place the Iyers closer to the Sourashtrans of Madurai (Figure 1) and distinguish them from the Bhargavas and the Punjabis (Figure 2). This suggests that various Brahmin populations of India might be different in their origin, although they all have adopted the same ideology and philosophy. The Iyers of Madurai are distinct from other populations of Tamil Nadu and India. The Iyers cluster with the Sourashtrans of Madurai (Pitchappan et al. 1986), a population with a known history of migration from Kutch of Bujarat. The Sourashtrans started their migration by A.D. 1024, following the fall of the Somnath Empire to Ghazani Mohamed (Sethuraman 1977), and continued until the Vijaya Nagar Empire. They were further settled in Madurai by A.D. 1600. They claim that they are Brahmins, and the present study (Figure 1, Table 4) places them closer to the Iyers of Madurai, a Brahmin group, than to other caste groups of Tamil Nadu.
The Iyers, however, were quite distant from two other population clusters of Tamil Nadu (Figure 1). The first cluster includes the Kallars, earlier settlers of Tamil Nadu (Balakrishnan and Sanghvi 1981); the Nadars, another ancient population of Tamil Nadu; and major group III (the Vellalas, i.e., artisan-related caste groups, thought to be immigrant communities). The second cluster includes the hill tribes, presumably the earliest settlers in this region who are thought to have been marginalized by subsequent waves of migration [see Sanghvi and Balakrishnan (1981)]. The present study has brought out that various caste groups and populations of Tamil Nadu are distinct from one another in their HLA polymorphisms and that the Iyers of Madurai are unique in their HLA gene pool. This compares well with earlier studies on Tamil Nadu [see Balakrishnan and Sanghvi (1981), Malhotra et al. (1981), and Undevia et al. (1981)].
A comparison of the yers with other world populations at the HLA-A, HLA-B, HLA-C, HLA-DR, and HLA-DQ loci revealed that the Iyers, the Bhargavas, and the Punjabis do not cluster together, although they are included in the same major tree (Figure 2). The Bhargavas cluster with Central Asian populations and the Punjabis cluster with Middle Eastern and European populations. The Iyers, however, form a separate cluster distinct from these two, suggesting that they are distant from the present-day European, Central Asian, and Middle Eastern populations. It is possible that the Iyers and the Bhargavas, the two Brahmin populations, settled in different regions of India during different time periods and remained isolated. A study on the origin and migration of various Brahmin populations in India might give better insight into the origin and settlement of Brahmin populations in India and also into the origin of Vedas and Hinduism.
Origin of the Iyers. In light of the data on MHC allele and haplotype polymorphisms presented here, it is interesting to discuss the origin of the Iyers. The origin of Brahminism and the Vedas, which correlate to the advent of social stratification and the caste system in India, dates back to the existence of human societies in the Eurasian steppes. A recent analysis of genetic data suggests that the inhabitants of the western part of the Eurasian steppes, originally settled by Caucasoid people speaking Indo-European languages, migrated in various directions, including Iran and India (Cavalli-Sforza et al. 1993). It is believed that these pastoral nomads often generated hierarchical societies and introduced the caste system to the Indian subcontinent (CavalliSforza et al. 1993). Cavalli-Sforza et al. (1993) also suggested another route of migration through China and Southeast Asia to India.
The dendrogram analysis presented here places the Iyers of Madurai in a separate cluster, joining the European and Central Asian clusters, that is distinct from Far Eastern populations. A comparison of the two-locus haplotypes revealed that the Iyers share a classical haplotype, A33-B44, with high frequency and linkage disequilibrium (Table 4) and extended haplotypes [A33-Cw7-B44-DR7-DQw2 (5.4/100) and A33-B44-BF*S-C4A*3-C4B*1 (8.7/100)] (Mariapia et al. 1992) with adjacent Asian populations, such as Thais, Thai Chinese, and Koreans (data not shown). Furthermore, a new complement allele C4B*18 was described in an Iyer and in Thai samples during the IHWC XI (Mauff et al. 1992). It is known that the HLA haplotypes between various ethnic groups can be vastly different and it is thought that migration and miscegenation are the major factors influencing the spread of various haplotypes. It is interesting to note that Hinduism has preached the Anuloma and Pratiloma concepts, permitting a woman of lower social status to marry a man of higher social status but not vice versa. In terms of genetics, this is one-way gene flow from a lower social stratum to a higher stratum. Thus it is possible that the ancestors of the yers migrated to India through Southeast Asia, acquiring the haplotype in question en route. This might explain the sharing of a haplotype with another population (e.g., A33-B44 with Thais; see Table 4) and clustering with another population in the place of origin (see Figure 2, Central Asian and European populations).
Apparently, the Iyers of Madurai originated from either the Eurasian steppes or Central Asia.
Conclusion. The present study, based on HLA polymorphism, separates the Iyers of Madurai from other tribes and caste groups of Tamil Nadu. The results suggest that not all Brahmin populations of India are the same in their HLA profile, thus suggesting a difference in their origin. The Iyers of Madurai may be distantly related to present-day European or Central Asian and Middle Eastern populations but not to Far Eastern or Southeast Asian populations. However, the sharing of some haplotypes between the Iyers and some Southeast Asian populations suggests a migration through Southeast Asia to India.
Acknowledgments We acknowledge the financial assistance received from the University Grants Commission, Government of India (awarded to K. Balakrishan), the Government of Tamil Nadu, Education Ministry (grant MS 1024/Education/7/7/ 87), and the Tissue Typing Services, Madurai Kamaraj University. We thank the authorities of Madurai College, Madurai, and the faculty of the Department of Zoology for their permission and assistance in sampling; and Partha Majumdar, of the Indian Statistical Institute, Calcutta, and J. Muthukrishnan, of the School of Biological Sciences, Madurai Kamaraj University, for their suggestions and critical comments on the manuscript. We also thank P. Selvaraj, a statistician at the Aravind Eye Hospital, Madurai, for the use of the SPSS statistics package to draw the dendrograms and V. Mahendran and R. Jeyamahendran for preparing the manuscript.
Received 22 August 1994; final revision received 25 September 1995.
1 Unit of Immunogenetics, HLA Building, School of Biological Sciences, Madurai Kamaraj University, Madurai 625 021, India.
2 Department of Legal Medicine, Osaka University Medical School, 1-1-5 Fukushima, Fukushimaku, Osaka-shi, Osaka 553, Japan.
3 Japanese Red Cross Central Blood Centre, 4-1-31 Hiroo, Shibuya-ku, Tokyo 150, Japan.
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