A test of the influence of continental axes of orientation on patterns of human gene flow.

The geographic distribution of genetic variation reflects trends in past population migrations and can be used to make inferences about these migrations. It has been proposed that the east-west orientation of the Eurasian landmass facilitated the rapid spread of ancient technological innovations across Eurasia, while the north-south orientation of the Americas led to a slower diffusion of technology there. If the diffusion of technology was accompanied by gene flow, then this hypothesis predicts that genetic differentiation in the Americas along lines of longitude will be greater than that in Eurasia along lines of latitude. We use 678 microsatellite loci from 68 indigenous populations in Eurasia and the Americas to investigate the spatial axes that underlie population-genetic variation. We find that genetic differentiation increases more rapidly along lines of longitude in the Americas than along lines of latitude in Eurasia. Distance along lines of latitude explains a sizeable portion of genetic distance in Eurasia, whereas distance along lines of longitude does not explain a large proportion of Eurasian genetic variation. Genetic differentiation in the Americas occurs along both latitudinal and longitudinal axes and has a greater magnitude than corresponding differentiation in Eurasia, even when adjusting for the lower level of genetic variation in the American populations. These results support the view that continental orientation has influenced migration patterns and has played an important role in determining both the structure of human genetic variation and the distribution and spread of cultural traits.

[1]  M. Feldman,et al.  Features of evolution and expansion of modern humans, inferred from genomewide microsatellite markers. , 2003, American journal of human genetics.

[2]  Alfred W. Crosby,et al.  Ecological Imperialism: The Biological Expansion of Europe, 900-1900 , 1988 .

[3]  M. Seielstad,et al.  Genetic structure of the Han Chinese population revealed by genome-wide SNP variation. , 2009, American journal of human genetics.

[4]  M. Feldman,et al.  Clines, Clusters, and the Effect of Study Design on the Inference of Human Population Structure , 2005, PLoS genetics.

[5]  J. Long,et al.  Human Genetic Diversity and the Nonexistence of Biological Races , 2003, Human biology.

[6]  Nicolas Ray,et al.  Inferring Past Demography Using Spatially Explicit Population Genetic Models , 2009, Human biology.

[7]  Cecil M. Lewis,et al.  Mitochondrial DNA and the Peopling of South America , 2007, Human biology.

[8]  Michael F. Seldin,et al.  Analysis of East Asia Genetic Substructure Using Genome-Wide SNP Arrays , 2008, PloS one.

[9]  Michael W. Mahoney,et al.  PCA-Correlated SNPs for Structure Identification in Worldwide Human Populations , 2007, PLoS genetics.

[10]  R R Sokal,et al.  Genetic structure of human populations in the British Isles. , 1993, Annals of human biology.

[11]  Andrea Manica,et al.  A geographically explicit genetic model of worldwide human-settlement history. , 2006, American journal of human genetics.

[12]  M. Nei,et al.  Estimation of average heterozygosity and genetic distance from a small number of individuals. , 1978, Genetics.

[13]  G. Barbujani,et al.  Genomic Boundaries between Human Populations , 2006, Human Heredity.

[14]  Sophie Ancelet,et al.  Bayesian Clustering Using Hidden Markov Random Fields in Spatial Population Genetics , 2006, Genetics.

[15]  Oscar Gaggiotti,et al.  Identifying the Environmental Factors That Determine the Genetic Structure of Populations , 2006, Genetics.

[16]  L. Chikhi,et al.  DNAs from the European Neolithic , 2006, Heredity.

[17]  Nicholas I. Fisher,et al.  Statistical Analysis of Spherical Data. , 1987 .

[18]  Yusuke Nakamura,et al.  Japanese population structure, based on SNP genotypes from 7003 individuals compared to other ethnic groups: effects on population-based association studies. , 2008, American journal of human genetics.

[19]  P. Menozzi,et al.  Synthetic maps of human gene frequencies in Europeans. , 1978, Science.

[20]  M. Stephens,et al.  Interpreting principal component analyses of spatial population genetic variation , 2008, Nature Genetics.

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

[22]  C. Tyler-Smith,et al.  Genetic differentiation in South Amerindians is related to environmental and cultural diversity: evidence from the Y chromosome. , 2001, American journal of human genetics.

[23]  Luigi Luca Cavalli-Sforza,et al.  Measuring the Rate of Spread of Early Farming in Europe , 1971 .

[24]  L. E. Leidy,et al.  Guns, germs and steel: The fates of human societies , 1999 .

[25]  P. Hedrick A STANDARDIZED GENETIC DIFFERENTIATION MEASURE , 2005, Evolution; international journal of organic evolution.

[26]  Zachary A. Szpiech,et al.  Statistical Applications in Genetics and Molecular Biology Comparing Spatial Maps of Human Population-Genetic Variation Using Procrustes Analysis , 2011 .

[27]  William Cronon Ecological Imperialism: The Biological Expansion of Europe, 900–1900. By Alfred W. Crosby. (Cambridge: Cambridge University Press, 1986. xiv + 368 pp. $22.95.) , 1987 .

[28]  A. Fix GENE FREQUENCY CLINES IN EUROPE: DEMIC DIFFUSION OR NATURAL SELECTION? , 1996 .

[29]  Jérôme Goudet,et al.  Going the distance: human population genetics in a clinal world. , 2007, Trends in genetics : TIG.

[30]  A. Di Rienzo,et al.  Tracing European founder lineages in the Near Eastern mtDNA pool. , 2000, American journal of human genetics.

[31]  Richard A. Nichols,et al.  A method for quantifying differentiation between populations at multi-allelic loci and its implications for investigating identity and paternity , 2008, Genetica.

[32]  Scott M. Williams,et al.  The Genetic Structure and History of Africans and African Americans , 2009, Science.

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

[34]  D. F. Roberts,et al.  The History and Geography of Human Genes , 1996 .

[35]  B S Weir,et al.  Estimation of the coancestry coefficient: basis for a short-term genetic distance. , 1983, Genetics.

[36]  D. Reich,et al.  Principal components analysis corrects for stratification in genome-wide association studies , 2006, Nature Genetics.

[37]  Oskar Hallatschek,et al.  LIFE AT THE FRONT OF AN EXPANDING POPULATION , 2008, Evolution; international journal of organic evolution.

[38]  G. Bertorelle,et al.  Genetics and the population history of Europe. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Christopher A. Edmonds,et al.  Mutations arising in the wave front of an expanding population. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[40]  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.

[41]  Ron Pinhasi,et al.  Tracing the Origin and Spread of Agriculture in Europe , 2005, PLoS biology.

[42]  John Novembre,et al.  Global distribution of genomic diversity underscores rich complex history of continental human populations. , 2009, Genome research.

[43]  Nicholas I. Fisher,et al.  Statistical Analysis of Spherical Data. , 1987 .

[44]  J. G. D. Clark,et al.  Radiocarbon dating and the expansion of farming culture from the Near East over Europe , 1965, Proceedings of the Prehistoric Society.

[45]  N. Rosenberg,et al.  Standardized Subsets of the HGDP‐CEPH Human Genome Diversity Cell Line Panel, Accounting for Atypical and Duplicated Samples and Pairs of Close Relatives , 2006, Annals of human genetics.

[46]  A. Ammerman,et al.  A population model for the diffusion of early farming in Europe , 1973 .

[47]  David R. Anderson,et al.  Model Selection and Inference: A Practical Information-Theoretic Approach , 2001 .

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

[49]  Lounès Chikhi,et al.  Estimating the impact of prehistoric admixture on the genome of Europeans. , 2004, Molecular biology and evolution.

[50]  A. Agresti Categorical data analysis , 1993 .

[51]  Oskar Hallatschek,et al.  Gene surfing in expanding populations. , 2007, Theoretical population biology.

[52]  Sewall Wright,et al.  Variability within and among natural populations , 1978 .

[53]  Ole A. Andreassen,et al.  The Impact of Divergence Time on the Nature of Population Structure: An Example from Iceland , 2009, PLoS genetics.

[54]  John Novembre,et al.  Spatial patterns of variation due to natural selection in humans , 2009, Nature Reviews Genetics.

[55]  S. Heath,et al.  Investigation of the fine structure of European populations with applications to disease association studies , 2008, European Journal of Human Genetics.

[56]  F. Morón,et al.  Genetic Structure of the Spanish Population , 2010, BMC Genomics.

[57]  John Novembre,et al.  The Geographic Spread of the CCR5 Δ32 HIV-Resistance Allele , 2005, PLoS biology.

[58]  M. Waters,et al.  Redefining the Age of Clovis: Implications for the Peopling of the Americas , 2007, Science.

[59]  Pablo Villoslada,et al.  Analysis and Application of European Genetic Substructure Using 300 K SNP Information , 2008, PLoS genetics.

[60]  Jinchuan Xing,et al.  Fine-scaled human genetic structure revealed by SNP microarrays. , 2009, Genome research.

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

[62]  Luigi Luca Cavalli-Sforza,et al.  The Neolithic Transition and the Genetics of Populations in Europe. , 2009 .

[63]  Shuhua Xu,et al.  Genomic dissection of population substructure of Han Chinese and its implication in association studies. , 2009, American journal of human genetics.

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

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

[66]  J. Ott Genetic data analysis II , 1997 .

[67]  Michael H. Kutner Applied Linear Statistical Models , 1974 .

[68]  Colonization Models and Initial Genetic Diversity in the Americas , 2002, Human biology.

[69]  Mattias Jakobsson,et al.  Genetic Variation and Population Structure in Native Americans , 2007, PLoS genetics.

[70]  M. Feldman,et al.  The application of molecular genetic approaches to the study of human evolution , 2003, Nature Genetics.

[71]  Nicolas Ray,et al.  Principal component analysis under population genetic models of range expansion and admixture. , 2010, Molecular biology and evolution.

[72]  V. Barnett,et al.  Applied Linear Statistical Models , 1975 .

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

[74]  C. F. C. Hawkes,et al.  The Dawn of European civilization , 1949, Nature.

[75]  Shameek Biswas,et al.  Genome-wide insights into the patterns and determinants of fine-scale population structure in humans. , 2009, American journal of human genetics.

[76]  Olivier François,et al.  Spatially explicit Bayesian clustering models in population genetics , 2010, Molecular ecology resources.

[77]  M. Salemme,et al.  When Patagonia was colonized: people mobility at high latitudes during Pleistocene/Holocene transition , 2003 .

[78]  D. Reich,et al.  Population Structure and Eigenanalysis , 2006, PLoS genetics.

[79]  G. Barbujani,et al.  Autocorrelation of gene frequencies under isolation by distance. , 1987, Genetics.

[80]  N. Mantel The detection of disease clustering and a generalized regression approach. , 1967, Cancer research.

[81]  G. McVean A Genealogical Interpretation of Principal Components Analysis , 2009, PLoS genetics.

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

[83]  Sohini Ramachandran,et al.  Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[85]  Andrew Collins,et al.  The genome-wide patterns of variation expose significant substructure in a founder population. , 2008, American journal of human genetics.

[86]  Briggs Buchanan,et al.  Spatial gradients in Clovis-age radiocarbon dates across North America suggest rapid colonization from the north , 2007, Proceedings of the National Academy of Sciences.

[87]  R. Cann The history and geography of human genes , 1995, The Journal of Asian Studies.

[88]  R. Sokal,et al.  Multiple regression and correlation extensions of the mantel test of matrix correspondence , 1986 .