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Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data

Author

Listed:
  • Ryan N Gutenkunst
  • Ryan D Hernandez
  • Scott H Williamson
  • Carlos D Bustamante

Abstract

Demographic models built from genetic data play important roles in illuminating prehistorical events and serving as null models in genome scans for selection. We introduce an inference method based on the joint frequency spectrum of genetic variants within and between populations. For candidate models we numerically compute the expected spectrum using a diffusion approximation to the one-locus, two-allele Wright-Fisher process, involving up to three simultaneous populations. Our approach is a composite likelihood scheme, since linkage between neutral loci alters the variance but not the expectation of the frequency spectrum. We thus use bootstraps incorporating linkage to estimate uncertainties for parameters and significance values for hypothesis tests. Our method can also incorporate selection on single sites, predicting the joint distribution of selected alleles among populations experiencing a bevy of evolutionary forces, including expansions, contractions, migrations, and admixture. We model human expansion out of Africa and the settlement of the New World, using 5 Mb of noncoding DNA resequenced in 68 individuals from 4 populations (YRI, CHB, CEU, and MXL) by the Environmental Genome Project. We infer divergence between West African and Eurasian populations 140 thousand years ago (95% confidence interval: 40–270 kya). This is earlier than other genetic studies, in part because we incorporate migration. We estimate the European (CEU) and East Asian (CHB) divergence time to be 23 kya (95% c.i.: 17–43 kya), long after archeological evidence places modern humans in Europe. Finally, we estimate divergence between East Asians (CHB) and Mexican-Americans (MXL) of 22 kya (95% c.i.: 16.3–26.9 kya), and our analysis yields no evidence for subsequent migration. Furthermore, combining our demographic model with a previously estimated distribution of selective effects among newly arising amino acid mutations accurately predicts the frequency spectrum of nonsynonymous variants across three continental populations (YRI, CHB, CEU).Author Summary: The demographic history of our species is reflected in patterns of genetic variation within and among populations. We developed an efficient method for calculating the expected distribution of genetic variation, given a demographic model including such events as population size changes, population splits and joins, and migration. We applied our approach to publicly available human sequencing data, searching for models that best reproduce the observed patterns. Our joint analysis of data from African, European, and Asian populations yielded new dates for when these populations diverged. In particular, we found that African and Eurasian populations diverged around 100,000 years ago. This is earlier than other genetic studies suggest, because our model includes the effects of migration, which we found to be important for reproducing observed patterns of variation in the data. We also analyzed data from European, Asian, and Mexican populations to model the peopling of the Americas. Here, we find no evidence for recurrent migration after East Asian and Native American populations diverged. Our methods are not limited to studying humans, and we hope that future sequencing projects will offer more insights into the history of both our own species and others.

Suggested Citation

  • Ryan N Gutenkunst & Ryan D Hernandez & Scott H Williamson & Carlos D Bustamante, 2009. "Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data," PLOS Genetics, Public Library of Science, vol. 5(10), pages 1-11, October.
  • Handle: RePEc:plo:pgen00:1000695
    DOI: 10.1371/journal.pgen.1000695
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    References listed on IDEAS

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    1. Joshua M Akey & Michael A Eberle & Mark J Rieder & Christopher S Carlson & Mark D Shriver & Deborah A Nickerson & Leonid Kruglyak, 2004. "Population History and Natural Selection Shape Patterns of Genetic Variation in 132 Genes," PLOS Biology, Public Library of Science, vol. 2(10), pages 1-1, September.
    2. Myers, Simon & Fefferman, Charles & Patterson, Nick, 2008. "Can one learn history from the allelic spectrum?," Theoretical Population Biology, Elsevier, vol. 73(3), pages 342-348.
    3. Jody Hey, 2005. "On the Number of New World Founders: A Population Genetic Portrait of the Peopling of the Americas," PLOS Biology, Public Library of Science, vol. 3(6), pages 1-1, May.
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    Cited by:

    1. Krystyna Nadachowska-Brzyska & Reto Burri & Pall I Olason & Takeshi Kawakami & Linnéa Smeds & Hans Ellegren, 2013. "Demographic Divergence History of Pied Flycatcher and Collared Flycatcher Inferred from Whole-Genome Re-sequencing Data," PLOS Genetics, Public Library of Science, vol. 9(11), pages 1-14, November.
    2. Kirk E Lohmueller & Anders Albrechtsen & Yingrui Li & Su Yeon Kim & Thorfinn Korneliussen & Nicolas Vinckenbosch & Geng Tian & Emilia Huerta-Sanchez & Alison F Feder & Niels Grarup & Torben Jørgensen , 2011. "Natural Selection Affects Multiple Aspects of Genetic Variation at Putatively Neutral Sites across the Human Genome," PLOS Genetics, Public Library of Science, vol. 7(10), pages 1-15, October.
    3. Raul Torres & Zachary A Szpiech & Ryan D Hernandez, 2018. "Human demographic history has amplified the effects of background selection across the genome," PLOS Genetics, Public Library of Science, vol. 14(6), pages 1-27, June.
    4. Melissa J Hubisz & Amy L Williams & Adam Siepel, 2020. "Mapping gene flow between ancient hominins through demography-aware inference of the ancestral recombination graph," PLOS Genetics, Public Library of Science, vol. 16(8), pages 1-24, August.
    5. Dominic Nelson & Jerome Kelleher & Aaron P Ragsdale & Claudia Moreau & Gil McVean & Simon Gravel, 2020. "Accounting for long-range correlations in genome-wide simulations of large cohorts," PLOS Genetics, Public Library of Science, vol. 16(5), pages 1-12, May.
    6. Felix M Key & Benjamin Peter & Megan Y Dennis & Emilia Huerta-Sánchez & Wei Tang & Ludmila Prokunina-Olsson & Rasmus Nielsen & Aida M Andrés, 2014. "Selection on a Variant Associated with Improved Viral Clearance Drives Local, Adaptive Pseudogenization of Interferon Lambda 4 (IFNL4)," PLOS Genetics, Public Library of Science, vol. 10(10), pages 1-12, October.
    7. Kelley Harris & Rasmus Nielsen, 2013. "Inferring Demographic History from a Spectrum of Shared Haplotype Lengths," PLOS Genetics, Public Library of Science, vol. 9(6), pages 1-20, June.
    8. Laurent Excoffier & Isabelle Dupanloup & Emilia Huerta-Sánchez & Vitor C Sousa & Matthieu Foll, 2013. "Robust Demographic Inference from Genomic and SNP Data," PLOS Genetics, Public Library of Science, vol. 9(10), pages 1-17, October.
    9. Aurélien Tellier & Peter Pfaffelhuber & Bernhard Haubold & Lisha Naduvilezhath & Laura E Rose & Thomas Städler & Wolfgang Stephan & Dirk Metzler, 2011. "Estimating Parameters of Speciation Models Based on Refined Summaries of the Joint Site-Frequency Spectrum," PLOS ONE, Public Library of Science, vol. 6(5), pages 1-13, May.

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