Reconstructing the Demographic History of the Himalayan and Adjoining Populations
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Human Genetics https://doi.org/10.1007/s00439-018-1867-2 ORIGINAL INVESTIGATION Reconstructing the demographic history of the Himalayan and adjoining populations Rakesh Tamang1,2,3,4 · Gyaneshwer Chaubey5,6 · Amrita Nandan4 · Periyasamy Govindaraj4,7 · Vipin Kumar Singh4 · Niraj Rai4,8 · Chandana Basu Mallick5,9 · Vishwas Sharma4 · Varun Kumar Sharma4 · Anish M. Shah4 · Albert Lalremruata4 · Alla G. Reddy4 · Deepa Selvi Rani4 · Pilot Doviah4 · Neetu Negi10 · Yarin Hadid11 · Veena Pande10 · Satti Vishnupriya2 · George van Driem12 · Doron M. Behar5 · Tikaram Sharma13 · Lalji Singh4,14 · Richard Villems3,5 · Kumarasamy Thangaraj4 Received: 15 September 2017 / Accepted: 6 January 2018 © Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract The rugged topography of the Himalayan region has hindered large-scale human migrations, population admixture and assimilation. Such complexity in geographical structure might have facilitated the existence of several small isolated com- munities in this region. We have genotyped about 850,000 autosomal markers among 35 individuals belonging to the four major populations inhabiting the Himalaya and adjoining regions. In addition, we have genotyped 794 individuals belonging to 16 ethnic groups from the same region, for uniparental (mitochondrial and Y chromosomal DNA) markers. Our results in the light of various statistical analyses suggest a closer link of the Himalayan and adjoining populations to East Asia than their immediate geographical neighbours in South Asia. Allele frequency-based analyses likely support the existence of a specifc ancestry component in the Himalayan and adjoining populations. The admixture time estimate suggests a recent westward migration of populations living to the East of the Himalaya. Furthermore, the uniparental marker analysis among the Himalayan and adjoining populations reveal the presence of East, Southeast and South Asian genetic signatures. Interest- ingly, we observed an antagonistic association of Y chromosomal haplogroups O3 and D clines with the longitudinal distance. Thus, we summarise that studying the Himalayan and adjoining populations is essential for a comprehensive reconstruction of the human evolutionary and ethnolinguistic history of eastern Eurasia. Introduction region (van Driem 2001). The number of individuals liv- ing in the whole area is small due to the cold climate and The Himalayan mountain ranges extend from Pakistan in the some inhospitable alpine habitats. It has been estimated that West to the northeastern Indian states and northern Burma the population size of the Himalayas tripled only in recent in the East. More than three hundred distinct ethnic groups times, i.e., from 1901 to 1980 (Nandy and Rao 2001). Trans- and language communities have been documented in this Himayalan is the second most populous language family in the world, comprising more than 300 diferent languages, which can be divided into 42 subgroups (van Driem 2001). Deceased: Lalji Singh. Out of the 42 major linguistic subgroups, 30 live to the south of the Himalayas, 7 to the North and East, and the remaining Rakesh Tamang and Gyaneshwer Chaubey contributed equally. 5 are distributed over both the southern and northern fanks Electronic supplementary material The online version of this (van Driem 2001). article (https://doi.org/10.1007/s00439-018-1867-2) contains The prehistoric human settlement in this region remains supplementary material, which is available to authorized users. poorly studied. It is still unclear when the frst human activi- ties occurred in this region. The archaeological record in * Gyaneshwer Chaubey [email protected] Nepal suggests a long prehistory of human habitation, with abundant lithic material from the Early, Middle and Late * Kumarasamy Thangaraj [email protected] Palaeolithic periods as well as through the Mesolithic and Neolithic periods (Corvinus and Erlangen Institut für Ur-und Extended author information available on the last page of the article Vol.:(0123456789)1 3 Human Genetics Frühgeschichte 2007). An Early Palaeolithic presence of share the closest genetic afnity with the HAAPs? Do the the Acheulian tradition in the Early Middle Pleistocene is HAAPs have any specifc ancestry component? Since we indicated by Acheulian bifacial sand fake tools industry, included large number of populations from a diverse region with Levallois technology appearing in the Middle Palaeo- of Himalaya, we also addressed whether we see any genetic lithic. Further, archaeological record suggest an increase in cline of HAAPs? Is there any sex-specifc admixture pattern, population density at the end of the last glacial maximum as we see among Indian Austroasiatic speakers? (Field et al. 2007). The foothills of the central Himalayas straddle the so-called Movius line, represent a transition zone between two traditions of lithic expression and show Results and discussion afnity with coetaneous Occidental technocomplexes as well as with technocomplexes in Southeast Asia (Schick 1994). HAAP’s specifc ancestry and genetic cline The Acheulian artefacts in the Śivālik region were made by archaic humans about 0.7 Ma (Khanduri 2002; Ganjoo and First, we merged the high-quality autosomal SNP data of 35 Ota 2012; Leipe et al. 2014). samples from this study with the available published data. The Tibetan plateau was likewise occupied by modern The combined data was thereafter used in all our autoso- humans during their frst arrival in Asia (Qiu 2015), and the mal analyses (Supplementary Table 1b and Supplementary Neolithic presence of modern humans both North and South Text). To have an insight at the inter- and intra-population of the Himalayas is archaeologically widely attested (Khanduri variation among the HAAPs, we computed the Fst distances 2002; Tewari 2007; Ganjoo and Ota 2012; Wang et al. 2012; (Supplementary Fig. 1 and Supplementary Table 2). The Leipe et al. 2014). During the Neolithic time, many pastoralist HAAPs showed closest and largely similar genetic distances communities have made permanent settlements in this region. with the East Asian and Southeast Asian populations, fol- One such pastoral community, the Changpa tribe in Ladakh, lowed by the Central Asians. When we compared the intra- were thought to have originated from the ancient tribes on the population distances among the HAAPs; Kusunda, Khasi Tibetan Plateau (Ganjoo and Ota 2012; Leipe et al. 2014). and Sherpa showed larger distances, likely due to drift and, Genetic studies so far, have suggested two diferent schools in the case of Kusunda and Khasi, perhaps due to linguis- of thoughts (Torroni et al. 1994; Su et al. 2000; Gayden et al. tic isolation (Supplementary Table 3). Highlander Ladakh 2007; Qin et al. 2010; Wang et al. 2012; Huerta-Sánchez et al. (India) pastoral population Changpa was closest to Tibetan 2014; Bhandari et al. 2015; Zhang et al. 2017). Some studies followed by Subba and Sherpa populations. Among the have suggested that the Himalayan border formed a natural South Asian populations, apart from Tibeto-Burman speak- barrier for migratory animals including humans (Papiha et al. ers, Munda speakers showed the closest afnity to the stud- 1989; Aggarwal et al. 2003; Gayden et al. 2007). However, ied groups, probably due to the shared East/Southeast Asian there is also evidence supporting the Himalaya as a corri- ancestry (Chaubey et al. 2011). The principle component dor for human migrations (Debnath et al. 2011; Wang et al. (PC) analysis of Eurasian groups placed the HAAPs closer 2012; Bhandari et al. 2015; Kang et al. 2016). These studies to the East/Southeast Asians (Fig. 2a), supporting the Fst were mainly based on a limited number of samples as well analysis. To see the placement of the HAAPs within the as low-resolution markers. Moreover, to explore a detailed East/Southeast Asian cluster, we ran a separate PC analysis genomic ancestry of this region, one needs to cover the wider among the HAAPs along with the East and Southeast Asian geographic region as well as populations, whereas previous populations (Supplementary Fig. 2). It is interesting to note studies were largely inclined towards Tibetan and Sherpa that the HAAPs do not assemble in the defned East and populations. Thus, to establish the temporal and spatial origin Southeast Asian cline, instead they form their own cline. of Himalayan and adjoining populations (HAAPs) and their In the wider picture of a Eurasian PC plot, this cline is also afnity with East and South Asians, we have undertaken an visible and we see that it is stretched between East/Southeast extensive study with more than 790 samples from the politi- Asia and South Asia (Fig. 2). This suggests that the HAAPs cal boarders of India, however, their geographical spread is are admixed populations with higher East Asian-like and across the Himalayas (Fig. 1; Supplementary Table 1a; and lower South Asian-like ancestries, whereas, the admixture Supplementary Text). Additionally, we have also assayed two observed in South Asian Munda (Austroasiatic) populations phenotype markers, the 1540C variant in EDAR, known to is characterised by the opposite pattern i.e., higher South be positively selected among East Asians (Bryk et al. 2008) Asian-like and lower East Asian-like ancestries (Chaubey and rs1426654 pigmentation gene SLC24A5 associated with et al. 2011). lighter skin colour among South Asians (Jonnalagadda et al. To gain a better understanding of ancestral components 2011; Basu Mallick et al. 2013; Mishra et