Learning about human population history from ancient and modern genomes

Genome-wide data, both from SNP arrays and from complete genome sequencing, are becoming increasingly abundant and are now even available from extinct hominins. These data are providing new insights into population history; in particular, when combined with model-based analytical approaches, genome-wide data allow direct testing of hypotheses about population history. For example, genome-wide data from both contemporary populations and extinct hominins strongly support a single dispersal of modern humans from Africa, followed by two archaic admixture events: one with Neanderthals somewhere outside Africa and a second with Denisovans that (so far) has only been detected in New Guinea. These new developments promise to reveal new stories about human population history, without having to resort to storytelling.

[1]  S. Pääbo,et al.  Multiplexed DNA Sequence Capture of Mitochondrial Genomes Using PCR Products , 2010, PloS one.

[2]  H. Poinar,et al.  Ancient DNA: Do It Right or Not at All , 2000, Science.

[3]  Jonathan Scott Friedlaender,et al.  The Genetic Structure of Pacific Islanders , 2008, PLoS genetics.

[4]  Philip L. F. Johnson,et al.  Patterns of damage in genomic DNA sequences from a Neandertal , 2007, Proceedings of the National Academy of Sciences.

[5]  F. Balloux,et al.  Geography predicts neutral genetic diversity of human populations , 2005, Current Biology.

[6]  David Reich,et al.  Principal component analysis of genetic data , 2008, Nature Genetics.

[7]  M. Stoneking,et al.  Demographic History of Oceania Inferred from Genome-wide Data , 2010, Current Biology.

[8]  S. Oppenheimer,et al.  Ancient voyaging and Polynesian origins. , 2011, American journal of human genetics.

[9]  Markus Scholz,et al.  Genetic Variation and Recent Positive Selection in Worldwide Human Populations: Evidence from Nearly 1 Million SNPs , 2009, PloS one.

[10]  R. Villems,et al.  Ancient DNA from European Early Neolithic Farmers Reveals Their Near Eastern Affinities , 2010, PLoS biology.

[11]  P. Kirch Peopling of the Pacific: A Holistic Anthropological Perspective , 2010 .

[12]  M. Miyamoto,et al.  Updated Three-Stage Model for the Peopling of the Americas , 2008, PloS one.

[13]  Carlos D Bustamante,et al.  Ascertainment bias in studies of human genome-wide polymorphism. , 2005, Genome research.

[14]  Adrian W. Briggs,et al.  Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA , 2009, Nucleic acids research.

[15]  Adrian W. Briggs,et al.  Targeted Retrieval and Analysis of Five Neandertal mtDNA Genomes , 2009, Science.

[16]  A. Krogh,et al.  Ancient human genome sequence of an extinct Palaeo-Eskimo , 2010, Nature.

[17]  Amit R. Indap,et al.  Genes mirror geography within Europe , 2008, Nature.

[18]  H. Bandelt,et al.  Single, Rapid Coastal Settlement of Asia Revealed by Analysis of Complete Mitochondrial Genomes , 2005, Science.

[19]  S. Pääbo Molecular cloning of Ancient Egyptian mummy DNA , 1985, Nature.

[20]  W. Haak,et al.  Survival and recovery of DNA from ancient teeth and bones , 2011 .

[21]  M. Stoneking,et al.  Neandertal DNA Sequences and the Origin of Modern Humans , 1997, Cell.

[22]  Daniel Falush,et al.  Inferring Human Colonization History Using a Copying Model , 2008, PLoS genetics.

[23]  M. Stoneking,et al.  Dating the age of admixture via wavelet transform analysis of genome-wide data , 2011, Genome Biology.

[24]  Alexander F. Auch,et al.  Metagenomics to Paleogenomics: Large-Scale Sequencing of Mammoth DNA , 2006, Science.

[25]  L. Excoffier,et al.  Inferring admixture proportions from molecular data. , 1998, Molecular biology and evolution.

[26]  B. Rannala,et al.  The Bayesian revolution in genetics , 2004, Nature Reviews Genetics.

[27]  Alkes L. Price,et al.  Reconstructing Indian Population History , 2009, Nature.

[28]  Philip L. F. Johnson,et al.  A Draft Sequence of the Neandertal Genome , 2010, Science.

[29]  Jinchuan Xing,et al.  Toward a more uniform sampling of human genetic diversity: a survey of worldwide populations by high-density genotyping. , 2010, Genomics.

[30]  Adrian W. Briggs,et al.  The Neandertal genome and ancient DNA authenticity , 2009, The EMBO journal.

[31]  E. Lander Initial impact of the sequencing of the human genome , 2011, Nature.

[32]  Z. Xuan,et al.  Genome-wide in situ exon capture for selective resequencing , 2007, Nature Genetics.

[33]  Martin Kircher,et al.  A Complete mtDNA Genome of an Early Modern Human from Kostenki, Russia , 2010, Current Biology.

[34]  S. Gabriel,et al.  Calibrating a coalescent simulation of human genome sequence variation. , 2005, Genome research.

[35]  C. Lalueza-Fox,et al.  Palaeogenetic evidence supports a dual model of Neolithic spreading into Europe , 2007, Proceedings of the Royal Society B: Biological Sciences.

[36]  N. Risch,et al.  Estimation of individual admixture: Analytical and study design considerations , 2005, Genetic epidemiology.

[37]  Paul Mellars,et al.  Going East: New Genetic and Archaeological Perspectives on the Modern Human Colonization of Eurasia , 2006, Science.

[38]  G. Summerhayes,et al.  Lapita: Ancestors and Descendants , 2009 .

[39]  Chris Tyler-Smith,et al.  The human Y chromosome: an evolutionary marker comes of age , 2003, Nature Reviews Genetics.

[40]  S. Pääbo,et al.  Mitochondrial genome variation and the origin of modern humans , 2000, Nature.

[41]  Christian Gieger,et al.  Correlation between Genetic and Geographic Structure in Europe , 2008, Current Biology.

[42]  Mapping Human Genetic Diversity in Asia , 2013 .

[43]  N. J. Fagundes,et al.  A Reevaluation of the Native American MtDNA Genome Diversity and Its Bearing on the Models of Early Colonization of Beringia , 2008, PloS one.

[44]  A. von Haeseler,et al.  DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA. , 2001, Nucleic acids research.

[45]  M. Stoneking,et al.  Genome-wide analysis indicates more Asian than Melanesian ancestry of Polynesians. , 2008, American journal of human genetics.

[46]  Jonathan Scott Friedlaender,et al.  A Human Genome Diversity Cell Line Panel , 2002, Science.

[47]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[48]  C. E. Pearson,et al.  Table S2: Trans-factors and trinucleotide repeat instability Trans-factor , 2010 .

[49]  Huanming Yang,et al.  Resequencing of 200 human exomes identifies an excess of low-frequency non-synonymous coding variants , 2010, Nature Genetics.

[50]  M. Stoneking,et al.  South Asia, the Andamanese, and the genetic evidence for an "early" human dispersal out of Africa. , 2003, American journal of human genetics.

[51]  M. Kayser The Human Genetic History of Oceania: Near and Remote Views of Dispersal , 2010, Current Biology.

[52]  Mark Stoneking,et al.  Mitochondrial DNA and human evolution. , 2005, Annual review of genomics and human genetics.

[53]  Qiaomei Fu,et al.  The complete mitochondrial DNA genome of an unknown hominin from southern Siberia , 2010, Nature.

[54]  E. Birney,et al.  Enredo and Pecan: genome-wide mammalian consistency-based multiple alignment with paralogs. , 2008, Genome research.

[55]  Shuichi Matsumura,et al.  Ancient DNA from the First European Farmers in 7500-Year-Old Neolithic Sites , 1975, Science.

[56]  Eric S. Lander,et al.  Sequencing the nuclear genome of the extinct woolly mammoth , 2008, Nature.

[57]  M. Stoneking,et al.  Mitochondrial DNA and human evolution , 1987, Nature.

[58]  Philip L. F. Johnson,et al.  A Complete Neandertal Mitochondrial Genome Sequence Determined by High-Throughput Sequencing , 2008, Cell.

[59]  C. Lalueza-Fox,et al.  The genetic origins of the Andaman Islanders. , 2003, American journal of human genetics.

[60]  Maido Remm,et al.  Population genetic structure in Indian Austroasiatic speakers: the role of landscape barriers and sex-specific admixture. , 2011, Molecular biology and evolution.

[61]  M. Beaumont,et al.  Novel high-resolution characterization of ancient DNA reveals C > U-type base modification events as the sole cause of post mortem miscoding lesions , 2007, Nucleic acids research.

[62]  Kirk E Lohmueller,et al.  Methods for Human Demographic Inference Using Haplotype Patterns From Genomewide Single-Nucleotide Polymorphism Data , 2009, Genetics.

[63]  T. Denham,et al.  Farming and Language in Island Southeast Asia , 2010, Current Anthropology.

[64]  L. Excoffier,et al.  A statistical evaluation of models for the initial settlement of the american continent emphasizes the importance of gene flow with Asia. , 2010, Molecular biology and evolution.

[65]  G. Chaubey,et al.  Reconstructing the Origin of Andaman Islanders , 2005, Science.

[66]  J. Wall,et al.  Inconsistencies in Neanderthal Genomic DNA Sequences , 2007, PLoS genetics.

[67]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[68]  S. Pääbo Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Philip L. F. Johnson,et al.  Genetic history of an archaic hominin group from Denisova Cave in Siberia , 2010, Nature.

[70]  Kirk E Lohmueller,et al.  Detecting ancient admixture and estimating demographic parameters in multiple human populations. , 2009, Molecular biology and evolution.

[71]  Ian Barnes,et al.  Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae , 2006, Nature.

[72]  M. Metspalu,et al.  Paleo-Eskimo mtDNA Genome Reveals Matrilineal Discontinuity in Greenland , 2008, Science.

[73]  Jody Hey,et al.  The study of structured populations — new hope for a difficult and divided science , 2003, Nature Reviews Genetics.

[74]  John Wakeley,et al.  Estimating Divergence Times from Molecular Data on Phylogenetic and Population Genetic Timescales , 2002 .

[75]  Zachary A. Szpiech,et al.  Genotype, haplotype and copy-number variation in worldwide human populations , 2008, Nature.

[76]  K. Hawkes,et al.  African populations and the evolution of human mitochondrial DNA. , 1991, Science.

[77]  Simon J. Greenhill,et al.  Language Phylogenies Reveal Expansion Pulses and Pauses in Pacific Settlement , 2009, Science.

[78]  D. Altshuler,et al.  A map of human genome variation from population-scale sequencing , 2010, Nature.

[79]  R. Foley,et al.  Multiple dispersals and modern human origins , 2005 .

[80]  Shuichi Matsumura,et al.  Genetic Discontinuity Between Local Hunter-Gatherers and Central Europe’s First Farmers , 2009, Science.

[81]  H. Ostrer,et al.  The History of African Gene Flow into Southern Europeans, Levantines, and Jews , 2011, PLoS genetics.

[82]  M. Stoneking Human origins. , 2008, EMBO reports.

[83]  R. Nielsen,et al.  Ascertainment biases in SNP chips affect measures of population divergence. , 2010, Molecular biology and evolution.

[84]  S. Pääbo,et al.  Genetic analyses from ancient DNA. , 2004, Annual review of genetics.

[85]  Mary K Kuhner,et al.  Coalescent genealogy samplers: windows into population history. , 2009, Trends in ecology & evolution.

[86]  D. Reich,et al.  Sensitive Detection of Chromosomal Segments of Distinct Ancestry in Admixed Populations , 2009, PLoS genetics.

[87]  Stephen L. Hauser,et al.  Genome-wide patterns of population structure and admixture in West Africans and African Americans , 2009, Proceedings of the National Academy of Sciences.

[88]  Jody Hey,et al.  Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics , 2007, Proceedings of the National Academy of Sciences.

[89]  J. Krause From genes to genomes: what is new in ancient DNA? , 2010 .

[90]  P. Underhill,et al.  Melanesian and Asian origins of Polynesians: mtDNA and Y chromosome gradients across the Pacific. , 2006, Molecular biology and evolution.

[91]  M. Feldman,et al.  Worldwide Human Relationships Inferred from Genome-Wide Patterns of Variation , 2008 .

[92]  Philip L. F. Johnson,et al.  Targeted Investigation of the Neandertal Genome by Array-Based Sequence Capture , 2010, Science.

[93]  Li Jin,et al.  Y chromosome sequence variation and the history of human populations , 2000, Nature Genetics.

[94]  M. Hubbe,et al.  Testing Evolutionary and Dispersion Scenarios for the Settlement of the New World , 2010, PloS one.

[95]  M. Miyamoto,et al.  A Three-Stage Colonization Model for the Peopling of the Americas , 2008, PloS one.

[96]  J. Hey Isolation with migration models for more than two populations. , 2010, Molecular biology and evolution.

[97]  D. Turnbull,et al.  Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA , 1999, Nature Genetics.

[98]  R. Nielsen Population genetic analysis of ascertained SNP data , 2004, Human Genomics.

[99]  Mark Stoneking,et al.  High-throughput sequencing of complete human mtDNA genomes from the Philippines. , 2011, Genome research.

[100]  P. Forster Ice Ages and the mitochondrial DNA chronology of human dispersals: a review. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[101]  Kenneth K. Kidd,et al.  Hunter-gatherer genomic diversity suggests a southern African origin for modern humans , 2011, Proceedings of the National Academy of Sciences.

[102]  C. Stringer,et al.  U-series and ESR analyses of bones and teeth relating to the human burials from Skhul. , 2005, Journal of human evolution.

[103]  Tom H. Pringle,et al.  Complete Khoisan and Bantu genomes from southern Africa , 2010, Nature.

[104]  A. Wilson,et al.  DNA sequences from the quagga, an extinct member of the horse family , 1984, Nature.