The Himalayas as a Directional Barrier to Gene Flow
2007; Elsevier BV; Volume: 80; Issue: 5 Linguagem: Inglês
10.1086/516757
ISSN1537-6605
AutoresTenzin Gayden, Alicia M. Cadenas, María Regueiro, Nanda Bahadur Singh, Lev A. Zhivotovsky, Peter A. Underhill, Luigi Luca Cavalli-Sforza, René J. Herrera,
Tópico(s)Genetically Modified Organisms Research
ResumoHigh-resolution Y-chromosome haplogroup analyses coupled with Y–short tandem repeat (STR) haplotypes were used to (1) investigate the genetic affinities of three populations from Nepal—including Newar, Tamang, and people from cosmopolitan Kathmandu (referred to as “Kathmandu” subsequently)—as well as a collection from Tibet and (2) evaluate whether the Himalayan mountain range represents a geographic barrier for gene flow between the Tibetan plateau and the South Asian subcontinent. The results suggest that the Tibetans and Nepalese are in part descendants of Tibeto-Burman–speaking groups originating from Northeast Asia. All four populations are represented predominantly by haplogroup O3a5-M134–derived chromosomes, whose Y-STR–based age (±SE) was estimated at 8.1±2.9 thousand years ago (KYA), more recent than its Southeast Asian counterpart. The most pronounced difference between the two regions is reflected in the opposing high-frequency distributions of haplogroups D in Tibet and R in Nepal. With the exception of Tamang, both Newar and Kathmandu exhibit considerable similarities to the Indian Y-haplogroup distribution, particularly in their haplogroup R and H composition. These results indicate gene flow from the Indian subcontinent and, in the case of haplogroup R, from Eurasia as well, a conclusion that is also supported by the admixture analysis. In contrast, whereas haplogroup D is completely absent in Nepal, it accounts for 50.6% of the Tibetan Y-chromosome gene pool. Coalescent analyses suggest that the expansion of haplogroup D derivatives—namely, D1-M15 and D3-P47 in Tibet—involved two different demographic events (5.1±1.8 and 11.3±3.7 KYA, respectively) that are more recent than those of D2-M55 representatives common in Japan. Low frequencies, relative to Nepal, of haplogroup J and R lineages in Tibet are also consistent with restricted gene flow from the subcontinent. Yet the presence of haplogroup O3a5-M134 representatives in Nepal indicates that the Himalayas have been permeable to dispersals from the east. These genetic patterns suggest that this cordillera has been a biased bidirectional barrier. High-resolution Y-chromosome haplogroup analyses coupled with Y–short tandem repeat (STR) haplotypes were used to (1) investigate the genetic affinities of three populations from Nepal—including Newar, Tamang, and people from cosmopolitan Kathmandu (referred to as “Kathmandu” subsequently)—as well as a collection from Tibet and (2) evaluate whether the Himalayan mountain range represents a geographic barrier for gene flow between the Tibetan plateau and the South Asian subcontinent. The results suggest that the Tibetans and Nepalese are in part descendants of Tibeto-Burman–speaking groups originating from Northeast Asia. All four populations are represented predominantly by haplogroup O3a5-M134–derived chromosomes, whose Y-STR–based age (±SE) was estimated at 8.1±2.9 thousand years ago (KYA), more recent than its Southeast Asian counterpart. The most pronounced difference between the two regions is reflected in the opposing high-frequency distributions of haplogroups D in Tibet and R in Nepal. With the exception of Tamang, both Newar and Kathmandu exhibit considerable similarities to the Indian Y-haplogroup distribution, particularly in their haplogroup R and H composition. These results indicate gene flow from the Indian subcontinent and, in the case of haplogroup R, from Eurasia as well, a conclusion that is also supported by the admixture analysis. In contrast, whereas haplogroup D is completely absent in Nepal, it accounts for 50.6% of the Tibetan Y-chromosome gene pool. Coalescent analyses suggest that the expansion of haplogroup D derivatives—namely, D1-M15 and D3-P47 in Tibet—involved two different demographic events (5.1±1.8 and 11.3±3.7 KYA, respectively) that are more recent than those of D2-M55 representatives common in Japan. Low frequencies, relative to Nepal, of haplogroup J and R lineages in Tibet are also consistent with restricted gene flow from the subcontinent. Yet the presence of haplogroup O3a5-M134 representatives in Nepal indicates that the Himalayas have been permeable to dispersals from the east. These genetic patterns suggest that this cordillera has been a biased bidirectional barrier. The Himalayan mountain range extends from Pakistan in the west to Burma in the east, along the frontiers of northern India, Nepal, Tibet, and Bhutan. It is home to most of the highest mountains of the world and forms a natural barrier between the Tibetan plateau and the Indian subcontinent. Whereas the Himalayas border Tibet to the south, the Tibetan plateau is bounded on the north by the Kunlun Mountains and on the west by the Karakoram ranges. These unique geographic characteristics of the Tibetan landscape may have provided some degree of genetic encapsulation. 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India and Nepal share a long historical, cultural, and religious legacy resulting from geographic proximity and several pivotal historical events involving political control by Indian royalty. The genetic diversity of populations inhabiting an area is often influenced by the geographic and physical features encompassing the region. Whereas the Hindu Kush Mountains and the arid deserts in Iran have served as obstacles to gene flow,26Wells RS Yuldasheva N Ruzibakiev R Underhill PA Evseeva I Smith JB Jin L Su B Pitchappan R Shanmugalakshmi S et al.The Eurasian heartland: a continental perspective on Y-chromosome diversity.Proc Natl Acad Sci USA. 2001; 98: 10244-10249Crossref PubMed Scopus (351) Google Scholar, 27Regueiro M Cadenas AM Gayden T Underhill PA Herrera RJ Iran: tricontinental nexus for Y-chromosome driven migration.Hum Hered. 2006; 61: 132-143Crossref PubMed Scopus (83) Google Scholar the Nile River Valley,28Krings MA Salem A-eH Bauer K Geisert H Malek AK Chaix L Simon C Welsby D Di Rienzo A Utermaan G et al.mtDNA analysis of Nile River Valley populations: a genetic corridor or barrier for migration?.Am J Hum Genet. 1999; 64: 1166-1176Abstract Full Text Full Text PDF PubMed Scopus (148) Google Scholar the strait of Bab-el Mandeb,29Stringer CB Andrew P Genetic and fossil evidence for the origin of modern humans.Science. 1988; 239: 1263-1268Crossref PubMed Scopus (628) Google Scholar, 30Luis JR Rowold DJ Regueiro M Caeiro B Cinnioğlu C Roseman C Underhill PA Cavalli-Sforza LL Herrera RJ The Levant versus the Horn of Africa: evidence for bidirectional corridors of human migrations.Am J Hum Genet. 2004; 74 (erratum 74:788): 532-544Abstract Full Text Full Text PDF PubMed Scopus (172) Google Scholar and Beringia31Zegura SL Karafet TM Zhivotovsky LA Hammer MF High-resolution SNPs and microsatellite haplotypes point to a single, recent entry of native American Y chromosomes into the Americas.Mol Biol Evol. 2004; 21: 164-175Crossref PubMed Scopus (206) Google Scholar are examples of natural passageways for the migrations of modern humans. The Himalayan range, in addition to being a formidable barrier, provides for dramatically diverse climatic conditions on either side of it: arid and cold on the Tibetan side, as compared with monsoons and extreme dry spells, depending on the season of the year, in the Nepalese territory. We decided to investigate the influence of the Himalayas in populating the region by use of high-resolution Y-chromosome SNP analyses of four geographically targeted populations from the area—namely, Newar, Tamang, and the general population of Kathmandu from Nepal (referred to as “Kathmandu” subsequently), as well as a collection from Tibet. In addition, 15 Y-STR loci were typed to provide information on the temporal origins of these four Himalayan groups. This study is the first of its kind reporting biallelic markers of the Y-chromosome haplogroup diversity in Nepalese populations. This work improves on earlier reports by analyzing a large number of Y-chromosome binary and associated STR markers to define compound Y-chromosome lineages for a sizable number of individuals from informative Tibetan and Nepalese populations. In the process, we uncovered evidence that the Himalayas have acted as an obstacle modulating the skewed dispersal of human groups southward. Blood samples were collected after receipt of informed consent from 344 males who comprise the general population of Tibet (n=156) and three populations from Nepal (n=188), which include Tamang (n=45), Newar (n=66), and Kathmandu (n=77). Figure 1 illustrates the geographical location of the above four populations. With the exception of the Kathmandu group who speak predominantly Nepali, an Indo-European language, the individuals in the remaining three collections are Tibeto-Burman speakers. Genealogical information of sampled individuals was recorded for at least 2 previous generations. 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