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Genome-Wide Patterns of Population Structure and Admixture Among Hispanic/Latino Populations

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Genome-Wide Patterns of Population Structure and Admixture Among Hispanic/Latino Populations Genome-wide patterns of population structure and admixture among Hispanic/Latino populations Katarzyna Bryca,1, Christopher Velezb,1, Tatiana Karafetc, Andres Moreno-Estradaa,d, Andy Reynoldsa, Adam Autona,2, Michael Hammerc, Carlos D. Bustamantea,d,3,4, and Harry Ostrerb,3,4 aDepartment of Biological Statistics and Computational Biology, Cornell University, Ithaca, NY 14850; bHuman Genetics Program, Department of Pediatrics, New York University School of Medicine, New York, NY 10016; cArizona Research Laboratories Division of Biotechnology and Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721; and dDepartment of Genetics, Stanford University School of Medicine, Stanford, CA 94305 Hispanic/Latino populations possess a complex genetic structure among social classes in colonial (and postcolonial) populations that reflects recent admixture among and potentially ancient with European ancestry often correlating with higher social substructure within Native American, European, and West African standing. As a consequence, present-day Hispanic/Latino pop- source populations. Here, we quantify genome-wide patterns of ulations exhibit very large variation in ancestry proportions (as SNP and haplotype variation among 100 individuals with ancestry estimated from genetic data) not only across geographic regions from Ecuador, Colombia, Puerto Rico, and the Dominican Republic (1, 2), but also within countries themselves (3, 4). In addition, the genotyped on the Illumina 610-Quad arrays and 112 Mexicans process of admixture was apparently sex-biased and preferen- genotyped on Affymetrix 500K platform. Intersecting these data tially occurred between European males and Amerindian and/or with previously collected high-density SNP data from 4,305 individ- African females; this process has been shown to be remarkably uals, we use principal component analysis and clustering methods consistent among countries and populations including Argentina FRAPPE and STRUCTURE to investigate genome-wide patterns of (5), Ecuador (6), Mexico (7), Cuba (8), Brazil (9), Uruguay (10), African, European, and Native American population structure Colombia (11), and Costa Rica (11). within and among Hispanic/Latino populations. Comparing autoso- The rich diversity of variation in ancestry among Hispanic/ mal, X and Y chromosome, and mtDNA variation, we find evidence Latino populations, coupled with consistent differences among of a significant sex bias in admixture proportions consistent with populations in the incidence of chronic heritable diseases, suggests disproportionate contribution of European male and Native Amer- that Hispanic/Latino populations may be very well suited for fi ican female ancestry to present-day populations. We also nd that admixture mapping (12, 13). For example, differences in relative patterns of linkage-disequilibria in admixed Hispanic/Latino popu- European ancestry proportions correlate with higher susceptibility lations are largely affected by the admixture dynamics of the pop- in Puerto Ricans to asthma as compared with Mexicans (14). Data ulations, with faster decay of LD in populations of higher African have also shown an increased risk of breast cancer in Latinas with ancestry. Finally, using the locus-specific ancestry inference method LAMP fi greater European ancestry (15) and an interplay between African , we reconstruct ne-scale chromosomal patterns of admix- ancestry and cardiovascular disease and hypertension in Puerto ture. We document moderate power to differentiate among poten- Ricans from Boston (16). Hispanic/Latinos are also likely to play tial subcontinental source populations within the Native American, an increasingly important role in multi- and transethnic genetic European, and African segments of the admixed Hispanic/Latino studies of complex disease. Genome-wide scans have identified genomes. Our results suggest future genome-wide association candidate markers for onset of type 2 diabetes in Mexican- scans in Hispanic/Latino populations may require correction for local Americans from Texas (17) as well as a region on chromosome 5 genomic ancestry at a subcontinental scale when associating differ- associated with asthma in Puerto Ricans (18). ences in the genome with disease risk, progression, and drug effi- Quantifying the relative contributions of ancestry, environ- cacy, as well as for admixture mapping. ment (including socio-economic status), and ancestry by envi- ronment interaction to disease outcome in diverse Hispanic/ human genomics | population genetics | Hispanic/Latino Latino populations will also be critical to applying a genomic perspective to the practice of medicine in the United States and “ ” he term Hispanic/Latinos refers to the ethnically diverse in Latin America. For example, whereas European ancestry was Tinhabitants of Latin America and to people of Latin Amer- associated with increased asthma susceptibility in Puerto Ricans ican descent throughout the world. Present-day Hispanic/Latino populations exhibit complex population structure, with sig- fi ni cant genetic contributions from Native American and Euro- This paper results from the Arthur M. Sackler Colloquium of the National Academy of pean populations (primarily involving local indigenous Sciences, "In the Light of Evolution IV: The Human Condition," held December 10–12, populations and migrants from the Iberian peninsula and 2009, at the Arnold and Mabel Beckman Center of the National Academies of Sciences Southern Europe) as well as West Africans brought to the and Engineering in Irvine, CA. The complete program and audio files of most presentations Americas through the trans-Atlantic slave trade (1, 2). These are available on the NAS Web site at www.nasonline.org/SACKLER_Human_Condition. complex historical events have affected patterns of genetic and Author contributions: C.D.B. and H.O. designed research; K.B., C.V., T.K., and M.H. per- formed research; K.B., A.A., M.H., C.D.B., and H.O. contributed new reagents/analytic genomic variation within and among present-day Hispanic/Lat- tools; K.B., T.K., A.M.-E., A.R., A.A., and C.D.B. analyzed data; and K.B., C.V., A.M.-E., ino populations in a heterogeneous fashion, resulting in rich and C.D.B., and H.O. wrote the paper. varied ancestry within and among populations as well as marked The authors declare no conflict of interest. differences in the contribution of European, Native American, This article is a PNAS Direct Submission. and African ancestry to autosomal, X chromosome, and uni- Data deposition: Genotype data from 100 Hispanic/Latinos have been deposited in the parentally inherited genomes. Gene Expression Omnibus (GEO) series record GSE21248. Many key demographic variables differed among colonial 1K.B. and C.V. contributed equally to this work. Latin American populations, including the population size of the 2Present address: Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK. local pre-Columbian Native American population, the extent 3C.D.B. and H.O. contributed equally to this work. and rate at which European settlers displaced native pop- 4To whom correspondence may be addressed. E-mail: [email protected] or harry. ulations, whether or not slavery was introduced in a given region, [email protected]. and, if so, the size and timing of introduction of the African slave This article contains supporting information online at www.pnas.org/cgi/content/full/ populations. There were also strong differences in ancestry 0914618107/DCSupplemental. 8954–8961 | PNAS | May 11, 2010 | vol. 107 | suppl. 2 www.pnas.org/cgi/doi/10.1073/pnas.0914618107 Downloaded by guest on October 1, 2021 (14), it was also shown that the effect was moderated by socio- Latino populations. We also note that several of the individuals economic status (19). This suggests that quantifying fine-scale from the Maya and Quechua Native American samples (and to a patterns of genomic diversity among diverse U.S. and non-U.S. lesser extent Nahua and Pima) from the Human Genome Diver- Hispanic/Latino may be critical to the efficient and effective sity Panel (CEPH-HGDP) show moderate levels of European design of medical and population genomic studies. A fine-scale admixture, consistent with previous studies of these populations population genomics perspective may also provide a powerful (25). Interestingly, this is not the case for the Aymara and Quechua means for understanding the roles of ancestry, genetics, and samples genotyped by Mao et al. (26). environmental covariates on disease onset and severity (13). We also undertook principal component analysis (PCA) of the Here, we introduce a larger, high-density SNP and haplotype autosomal genotype data from Hispanic/Latino and putative dataset to investigate historical population genetics questions— ancestral populations using the smartpca program from the such as variation in sex-biased ancestry and genome-wide admix- software package eigenstrat (Fig. 2A) (27). The first two principal ture proportions within and among Latino populations—as well as components of the PCA strongly support the notion that the provide a genomic resource for the study of population sub- three ancestral populations contributing to the Hispanic/Latino structure within putative European, African, and Native American genomic diversity correspond exactly to Native American, source populations. Our dataset includes three Latino populations European, and African ancestry. The Hispanic/Latino pop- that are underrepresented in whole-genome analyses, namely,
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