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Skin Color Variation in Orang Asli Tribes of Peninsular Malaysia

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Skin Color Variation in Orang Asli Tribes of Peninsular Malaysia Skin Color Variation in Orang Asli Tribes of Peninsular Malaysia Khai C. Ang1*, Mee S. Ngu2, Katherine P. Reid1, Mei S. Teh2, Zamzuraida S. Aida2, Danny X.R. Koh2, Arthur Berg3, Stephen Oppenheimer4, Hood Salleh5, Mahani M. Clyde2, Badrul M. Md-Zain2, Victor A. Canfield6, Keith C. Cheng1* 1 Department of Experimental Pathology & Jake Gittlen Cancer Research Foundation, Penn State College of Medicine, Hershey, Pennsylvania, United States of America, 2 School of Environmental and Natural Resource Sciences, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, Bangi, Selangor, Malaysia, 3 Department of Biostatistics & Bioinformatics, Penn State College of Medicine, Hershey, Pennsylvania, United States of America, 4 Institute of Cognitive and Evolutionary Anthropology, School of Anthropology and Museum Ethnography: University of Oxford, Oxford, United Kingdom, 5 Academic Heritage Museum, Chancellery Building, Universiti Kebangsaan Malaysia, Bangi, Selangor, Malaysia, 6 Department of Pharmacology, Penn State College of Medicine, Hershey, Pennsylvania, United States of America Abstract Pigmentation is a readily scorable and quantitative human phenotype, making it an excellent model for studying multifactorial traits and diseases. Convergent human evolution from the ancestral state, darker skin, towards lighter skin colors involved divergent genetic mechanisms in people of European vs. East Asian ancestry. It is striking that the European mechanisms result in a 10–20-fold increase in skin cancer susceptibility while the East Asian mechanisms do not. Towards the mapping of genes that contribute to East Asian pigmentation there is need for one or more populations that are admixed for ancestral and East Asian ancestry, but with minimal European contribution. This requirement is fulfilled by the Senoi, one of three indigenous tribes of Peninsular Malaysia collectively known as the Orang Asli. The Senoi are thought to be an admixture of the Negrito, an ancestral dark-skinned population representing the second of three Orang Asli tribes, and regional Mongoloid populations of Indo-China such as the Proto-Malay, the third Orang Asli tribe. We have calculated skin reflectance-based melanin indices in 492 Orang Asli, which ranged from 28 (lightest) to 75 (darkest); both extremes were represented in the Senoi. Population averages were 56 for Negrito, 42 for Proto-Malay, and 46 for Senoi. The derived allele frequencies for SLC24A5 and SLC45A2 in the Senoi were 0.04 and 0.02, respectively, consistent with greater South Asian than European admixture. Females and individuals with the A111T mutation had significantly lighter skin (p = 0.001 and 0.0039, respectively). Individuals with these derived alleles were found across the spectrum of skin color, indicating an overriding effect of strong skin lightening alleles of East Asian origin. These results suggest that the Senoi are suitable for mapping East Asian skin color genes. Citation: Ang KC, Ngu MS, Reid KP, Teh MS, Aida ZS, et al. (2012) Skin Color Variation in Orang Asli Tribes of Peninsular Malaysia. PLoS ONE 7(8): e42752. doi:10.1371/journal.pone.0042752 Editor: Toomas Kivisild, University of Cambridge, United Kingdom Received April 28, 2012; Accepted July 10, 2012; Published August 13, 2012 Copyright: ß 2012 Ang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by National Institutes of Health grants 5R01 AR052535 and 3R01 AR052535-03S1 from the National Institute of Arthritis and Musculoskeletal and Skin Diseases to KCC, the Jake Gittlen Cancer Research Foundation of the Penn State Cancer Institute, and UKM-GUP-ASP-07-04-146and UKM-ST-08-FRGS0012-2010 from Universiti Kebangsaan Malaysia (UKM) to BMMZ, MMC, KCA and HS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] (KCA); [email protected] (KCC) Introduction The differing mechanisms for light skin in Europeans vs. East Asians are associated with disparate skin cancer susceptibility: The genetic basis of variation in human skin color across global incidences of the most lethal skin cancer, melanoma [4], are 10–20 populations is still largely a mystery. Although partially delineated fold greater in Europeans than in Africans [4,5]. In stark contrast, for Europeans, skin color remains poorly understood for East the lighter skin colors of East Asian populations are associated with Asians [1]. For mixed individuals, we are far from specifying skin almost no increase in melanoma; their incidences are comparable color purely from genotype. Modern humans are thought to have with those of Africans [5]. A molecular understanding of this retained dark skin in equatorial regions such as central Africa in disparity can only be gained after the alleles involved in skin order to prevent destruction of the essential nutrient, folate, by UV lightening for both groups are identified. light [2]. Conversely, it is thought that lighter skin color was The genetic basis of East Asian skin color is not explained by selected for in northerly latitudes to increase the penetration of skin color alleles identified to date. The most pervasive contributor solar UV light, which is in turn required for a necessary to European skin color is the A111T allele of SLC24A5 photoactivation step in the formation of vitamin D, another (SLC24A5A111T), which is associated with a single nucleotide essential vitamin [2,3]. Selective pressure resulted in convergent polymorphism (SNP) at rs1426654. This mutation from the evolution towards lighter skin, once each in the European and East ancestral state is 100% fixed in the CEU (European) population of Asian branches of human ancestry, through divergent genetic HapMap [6] and is associated with the strongest genomic signal mechanisms. for selection – as measured by the size of the region of diminished PLOS ONE | www.plosone.org 1 August 2012 | Volume 7 | Issue 8 | e42752 Skin Color Variation in the Orang Asli variation – in European genomes [7]. This discovery was made Table 1. Orang Asli classification by tribe and subtribe. possible by studies of a zebrafish mutant with a nonsense mutation in the orthologous gene: goldenb1 [7]. A missense mutation at rs16891982 in a second gene, SLC45A2, changes the ancestral Orang Asli leucine to phenylalanine at amino acid 374 (L374F), and is 96%– 98% fixed in northern Europeans [6,7,8]. From functional Tribe Negrito Senoi Proto Malay A111T admixture studies, SLC24A5 and the L374F mutation in Subtribe Batek Che Wong* Jakun* L374F SLC45A2 (SLC45A2 ) have each been estimated to contribute Jahai Jah Hut* Orang Kanak about 1/3 of the difference between West African and European Kensiu* Mah Meri* Orang Kuala/Laut skin color [7]. East Asians largely lack these mutations [6,7,8,9]. Kintak* Semai* Seletar Contributors to European skin, hair or eye color (ASIP [10], TYR [11], SLC24A4 [12], KITLG, OCA2, or MC1R, [12,13,14]) are not Lanoh Semak Beri* Semelai common enough among East Asians to be a primary contributor Mendrik Temiar* Temuan* to East Asian skin color. It is reasonable to hypothesize that there A111T *Denotes subtribes sampled. exists an East Asian equivalent of SLC24A5 . doi:10.1371/journal.pone.0042752.t001 We have noted that South Asians (e.g. Indians, Pakistanis, Sri Lankans) have high allele frequencies for SLC24A5A111T. Detection expected to segregate with lighter skin color. Since the Senoi are SLC24A5A111T of the strong contributions of to skin color among expected to lack the additional mutations that are responsible for South Asians [15] has been facilitated by the scarcity of L374F the even lighter skin of Northeastern Asians (e.g. Chinese and SLC45A2 [10] and other European skin color alleles in those Japanese), using the Senoi for mapping will allow us to focus on populations [14]. The Senoi are believed to be an admixture finding the primary East Asian skin color alleles without being between the Negrito (formerly known as Semang) and regional distracted by those additional mutations. We have characterized Mongoloid populations from Indo-China such as the Proto-Malay skin color distribution in the Orang Asli populations. We have also [16,17]. The Senoi tribe of the Orang Asli of Peninsular Malaysia estimated the extent of admixture of Orang Asli populations with thus represents the East Asian equivalent to South Asians. In this Europeans and South Asians by genotyping for SLC24A5A111T and population, putative East Asian skin color alleles would be SLC45A2L374F. Figure 1. Map of Peninsular Malaysia indicating sampling sites. For Orang Asli tribes and their corresponding village locations, see Table S1. doi:10.1371/journal.pone.0042752.g001 PLOS ONE | www.plosone.org 2 August 2012 | Volume 7 | Issue 8 | e42752 Skin Color Variation in the Orang Asli Results and Discussion are consistent with those reported by Shriver et al. and Parra et al. [11,27] and with our visual impressions. Distribution of Melanin Indices in Orang Asli To confirm and quantitate our visual impression that females The aboriginal populations of Peninsular Malaysia, the Orang are of lighter skin color than males, we plotted M-indices of the Asli (Malay for ‘‘original people’’, Figure 1)
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