Comparison of single genome and allele frequency data reveals discordant demographic histories

G3: Genes, Genomes, Genetics

Volumn 7, Issue 11, 2017, Pages 3605-3620

  Beichman, Annabel C ^a   Phung, Tanya N ^a   Lohmueller, Kirk E ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Demographic inference; Markovian coalescent; Nonmodel organisms; Pairwise sequentially; Population genetics; Site frequency spectrum

Indexed keywords

BEHAVIOR; CASE REPORT; DEMOGRAPHY; EUROPEAN; GENE FREQUENCY; GENETIC VARIATION; HAN CHINESE; HETEROZYGOSITY; HUMAN; POPULATION GENETICS; SIMULATION; YORUBA (PEOPLE); ASIAN CONTINENTAL ANCESTRY GROUP; BIOLOGICAL MODEL; CAUCASIAN; GENETICS; HETEROZYGOTE; HUMAN GENOME; MOLECULAR EVOLUTION; POPULATION;

ASIAN CONTINENTAL ANCESTRY GROUP; EUROPEAN CONTINENTAL ANCESTRY GROUP; EVOLUTION, MOLECULAR; GENE FREQUENCY; GENETIC VARIATION; GENOME, HUMAN; HETEROZYGOTE; HUMANS; MODELS, GENETIC; POPULATION;

EID: 85032885612     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.117.300259     Document Type: Article

References (102)

1. 1000 Genomes Project Consortium, 2015 A global reference for human genetic variation. Nature 526: 68-74
2. Adams, A. M., and R. R. Hudson, 2004 Maximum-likelihood estimation of demographic parameters using the frequency spectrum of unlinked singlenucleotide polymorphisms. Genetics 168: 1699-1712
3. Albert, V. A., W. B. Barbazuk, J. P. Der, J. Leebens-Mack, H. Ma et al., 2013 The Amborella genome and the evolution of flowering plants. Science 342: 1241089
4. Arbiza, L., E. Zhong, and A. Keinan, 2012 NRE: a tool for exploring neutral loci in the human genome. BMC Bioinformatics 13: 301
5. Ardlie, K., S. N. Liu-Cordero, M. A. Eberle, M. Daly, J. Barrett et al., 2001 Lower-than-expected linkage disequilibrium between tightly linked markers in humans suggests a role for gene conversion. Am. J. Hum. Genet. 69: 582-589
6. Bhaskar, A., Y. R. Wang, and Y. S. Song, 2015 Efficient inference of population size histories and locus-specific mutation rates from large-sample genomic variation data. Genome Res. 25: 268-279
7. Blum, M. G., and M. Jakobsson, 2011 Deep divergences of human gene trees and models of human origins. Mol. Biol. Evol. 28: 889-898
8. Boitard, S., W. Rodriguez, F. Jay, S. Mona, and F. Austerlitz, 2016 Inferring population size history from large samples of genome-wide molecular data-an approximate Bayesian computation approach. PLoS Genet. 12: e1005877
9. Bosse,M.,H.-J. Megens,O.Madsen, L. A. Frantz, Y. Paudel et al., 2014 Untangling the hybrid nature of modern pig genomes: a mosaic derived from biogeographically distinct and highly divergent Sus scrofa populations. Mol. Ecol. 23: 4089-4102
10. Boyko, A. R., S. H. Williamson, A. R. Indap, J. D. Degenhardt, R. D. Hernandez et al., 2008 Assessing the evolutionary impact of amino acid mutations in the human genome. PLoS Genet. 4: e1000083
11. Bunnefeld, L., L. A. F. Frantz, and K. Lohse, 2015 Inferring bottlenecks from genome-wide samples of short sequence blocks. Genetics 201: 1157-1169
12. Cahill, J. A., A. E. Soares, R. E. Green, and B. Shapiro, 2016 Inferring species divergence times using pairwise sequential Markovian coalescent modelling and low-coverage genomic data. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 371: 20150138
13. Chen, G. K., P. Marjoram, and J. D. Wall, 2009 Fast and flexible simulation of DNA sequence data. Genome Res. 19: 136-142
14. Chikhi, L., V. C. Sousa, P. Luisi, B. Goossens, and M. A. Beaumont, 2010 The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics 186: 983-995
15. Danecek, P., A. Auton, G. Abecasis, C. A. Albers, E. Banks et al., 2011 The variant call format and VCFtools. Bioinformatics 27: 2156-2158
16. Drmanac, R., A. B. Sparks, M. J. Callow, A. L. Halpern, N. L. Burns et al., 2010 Human genome sequencing using unchained base reads on selfassembling DNA nanoarrays. Science 327: 78-81
17. Ewing, G., and J. Hermisson, 2010 MSMS: a coalescent simulation program including recombination, demographic structure and selection at a single locus. Bioinformatics 26: 2064-2065
18. Excoffier, L., I. Dupanloup, E. Huerta-Sánchez, V. C. Sousa, and M. Foll, 2013 Robust demographic inference from genomic and SNP data. PLoS Genet. 9: e1003905
19. Fagundes, N. J., N. Ray, M. Beaumont, S. Neuenschwander, F. M. Salzano et al., 2007 Statistical evaluation of alternative models of human evolution. Proc. Natl. Acad. Sci. USA 104: 17614-17619
20. Fitak, R. R., E. Mohandesan, J. Corander, and P. A. Burger, 2016 The de novo genome assembly and annotation of a female domestic dromedary of North African origin. Mol. Ecol. Resour. 16: 314-324
21. Freedman, A. H., I. Gronau, R. M. Schweizer, D. Ortega-Del Vecchyo, E. Han et al., 2014 Genome sequencing highlights the dynamic early history of dogs. PLoS Genet. 10: e1004016
22. Frisse, L., R. R. Hudson, A. Bartoszewicz, J. D. Wall, J. Donfack et al., 2001 Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am. J. Hum. Genet. 69: 831-843
23. Gao, F., and A. Keinan, 2016 Explosive genetic evidence for explosive human population growth. Curr. Opin. Genet. Dev. 41: 130-139
24. Garrigan, D., and M. F. Hammer, 2006 Reconstructing human origins in the genomic era. Nat. Rev. Genet. 7: 669-680
25. Garud, N. R., P. W. Messer, E. O. Buzbas, and D. A. Petrov, 2015 Recent selective sweeps in North American Drosophila melanogaster show signatures of soft sweeps. PLoS Genet. 11: e1005004
26. Gattepaille, L. M., M. Jakobsson, and M. G. Blum, 2013 Inferring population size changes with sequence and SNP data: lessons from human bottlenecks. Heredity 110: 409-419
27. Gazave, E., L. Ma, D. Chang, A. Coventry, F. Gao et al., 2014 Neutral genomic regions refine models of recent rapid human population growth. Proc. Natl. Acad. Sci. USA 111: 757-762
28. Gravel, S., B. M. Henn, R. N. Gutenkunst, A. R. Indap, G. T. Marth et al., 2011 Demographic history and rare allele sharing among human populations. Proc. Natl. Acad. Sci. USA 108: 11983-11988
29. Groenen, M. A. M., A. L. Archibald, H. Uenishi, C. K. Tuggle, Y. Takeuchi et al., 2012 Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491: 393-398
30. Gutenkunst, R. N., R. D. Hernandez, S. H. Williamson, and C. D. Bustamante, 2009 Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5: e1000695
31. Han, E., J. S. Sinsheimer, and J. Novembre, 2014 Characterizing bias in population genetic inferences from low-coverage sequencing data. Mol. Biol. Evol. 31: 723-735
32. Han, E., J. S. Sinsheimer, and J. Novembre, 2015 Fast and accurate site frequency spectrum estimation from low coverage sequence data. Bioinformatics 31: 720-725
33. Harpending, H. C., M. A. Batzer, M. Gurven, L. B. Jorde, A. R. Rogers et al., 1998 Genetic traces of ancient demography. Proc. Natl. Acad. Sci. USA 95: 1961-1967
34. Harris, K., and R. Nielsen, 2013 Inferring demographic history from a spectrum of shared haplotype lengths. PLoS Genet. 9: e1003521
35. Hawks, J., K. Hunley, S.-H. Lee, and M. Wolpoff, 2000 Population bottlenecks and Pleistocene human evolution. Mol. Biol. Evol. 17: 2-22
36. Heller, R., L. Chikhi, and H. R. Siegismund, 2013 The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PLoS One 8: 1-10
37. Henn, B. M., L. L. Cavalli-Sforza, and M. W. Feldman, 2012 The great human expansion. Proc. Natl. Acad. Sci. USA 109: 17758-17764
38. Henn, B. M., L. R. Botigué, S. Peischl, I. Dupanloup, M. Lipatov et al., 2016 Distance from sub-Saharan Africa predicts mutational load in diverse human genomes. Proc. Natl. Acad. Sci. USA 113: E440-E449
39. Holliday, J. A., L. Zhou, R. Bawa, M. Zhang, and R. W. Oubida, 2016 Evidence for extensive parallelism but divergent genomic architecture of adaptation along altitudinal and latitudinal gradients in Populus trichocarpa. New Phytol. 209: 1240-1251
40. Hsieh, P., K. R. Veeramah, J. Lachance, S. A. Tishkoff, J. D. Wall et al., 2016 Whole-genome sequence analyses of Western Central African Pygmy hunter-gatherers reveal a complex demographic history and identify candidate genes under positive natural selection. Genome Res. 26: 279-290
41. Hudson, R. R., 2002 Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18: 337-338
42. Hung, C.-M., P.-J. L. Shaner, R. M. Zink, W.-C. Liu, T.-C. Chu et al., 2014 Drastic population fluctuations explain the rapid extinction of the passenger pigeon. Proc. Natl. Acad. Sci. USA 111: 10636-10641
43. Ibarra-Laclette, E., E. Lyons, G. Hernández-Guzmán, C. A. Pérez-Torres, L. Carretero-Paulet et al., 2013 Architecture and evolution of a minute plant genome. Nature 498: 94-98
44. Jouganous, J., W. Long, A. P. Ragsdale, and S. Gravel, 2017 Inferring the joint demographic history of multiple populations: beyond the diffusion approximation. Genetics 206: 1549-1567
45. Keinan, A., and A. G. Clark, 2012 Recent explosive human population growth has resulted in an excess of rare genetic variants. Science 336: 740-743
46. Keinan, A., J. C. Mullikin, N. Patterson, and D. Reich, 2007 Measurement of the human allele frequency spectrum demonstrates greater genetic drift in East Asians than in Europeans. Nat. Genet. 39: 1251-1255
47. Kidd, J. M., S. Gravel, J. Byrnes, A. Moreno-Estrada, S. Musharoff et al., 2012 Population genetic inference from personal genome data: impact of ancestry and admixture on human genomic variation. Am. J. Hum. Genet. 91: 660-671
48. Kim, S. Y., K. E. Lohmueller, A. Albrechtsen, Y. Li, T. Korneliussen et al., 2011 Estimation of allele frequency and association mapping using next-generation sequencing data. BMC Bioinformatics 12: 231
49. Kong, A., G. Thorleifsson, D. F. Gudbjartsson, G. Masson, A. Sigurdsson et al., 2010 Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467: 1099-1103
50. Li, H., and R. Durbin, 2011 Inference of human population history from individual whole-genome sequences. Nature 475: 493-496
51. Liu, X., and Y.-X. Fu, 2015 Exploring population size changes using SNP frequency spectra. Nat. Genet. 47: 555-559
52. Lohmueller, K. E., C. D. Bustamante, and A. G. Clark, 2009 Methods for human demographic inference using haplotype patterns from genomewide single-nucleotide polymorphism data. Genetics 182: 217-231
53. Malaspinas, A. S., M. C. Westaway, C. Muller, V. C. Sousa, O. Lao et al., 2016 A genomic history of Aboriginal Australia. Nature 538: 207-214
54. Mallick, S., H. Li, M. Lipson, I. Mathieson, M. Gymrek et al., 2016 The Simons Genome Diversity Project: 300 genomes from 142 diverse populations. Nature 538: 201-206
55. Marjoram, P., and J. D. Wall, 2006 Fast 'coalescent' simulation. BMC Genet. 7: 1-9
56. Marth, G. T., E. Czabarka, J. Murvai, and S. T. Sherry, 2004 The allele frequency spectrum in genome-wide human variation data reveals signals of differential demographic history in three large world populations. Genetics 166: 351-372
57. Mazet, O., W. Rodriguez, and L. Chikhi, 2015a Demographic inference using genetic data from a single individual: separating population size variation from population structure. Theor. Popul. Biol. 104: 46-58
58. Mazet, O., W. Rodriguez, S. Grusea, S. Boitard, and L. Chikhi, 2015b On the importance of being structured: instantaneous coalescence rates and human evolution-lessons for ancestral population size inference? Heredity 116: 362-371
59. McCoy, R. C., N. R. Garud, J. L. Kelley, C. L. Boggs, and D. A. Petrov, 2014 Genomic inference accurately predicts the timing and severity of a recent bottleneck in a nonmodel insect population. Mol. Ecol. 23: 136-150
60. McVean, G. A., and N. J. Cardin, 2005 Approximating the coalescent with recombination. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360: 1387-1393
61. Meyer, M., M. Kircher, M.-T. Gansauge, H. Li, F. Racimo et al., 2012 A high-coverage genome sequence from an archaic Denisovan individual. Science 338: 222-226
62. Murray, G. G. R., A. E. R. Soares, B. J. Novak, N. K. Schaefer, J. A. Cahill et al., 2017 Natural selection shaped the rise and fall of passenger pigeon genomic diversity. bioRxiv. Available at:: https://doi.org/10.1101/ 154294
63. Nadachowska-Brzyska, K., R. Burri, P. I. Olason, T. Kawakami, L. A. Smeds et al., 2013 Demographic divergence history of pied flycatcher and collared flycatcher inferred from whole-genome re-sequencing data. PLoS Genet. 9: e1003942
64. Nadachowska-Brzyska, K., C. Li, L. Smeds, G. Zhang, and H. Ellegren, 2015 Temporal dynamics of avian populations during Pleistocene revealed by whole-genome sequences. Curr. Biol. 25: 1375-1380
65. Nadachowska-Brzyska, K., R. Burri, L. Smeds, and H. Ellegren, 2016 PSMC analysis of effective population sizes in molecular ecology and its application to black-and-white Ficedula flycatchers. Mol. Ecol. 25: 1058-1072
66. Nei, M., T. Maruyama, and R. Chakraborty, 1975 The bottleneck effect and genetic variability in populations. Evolution 29: 1-10
67. Nelson, M. R., D. Wegmann, M. G. Ehm, D. Kessner, P. S. Jean et al., 2012 An abundance of rare functional variants in 202 drug target genes sequenced in 14,002 people. Science 337: 100-104
68. Nielsen, R., 2000 Estimation of population parameters and recombination rates from single nucleotide polymorphisms. Genetics 154: 931-942
69. Nielsen, R., M. J. Hubisz, I. Hellmann, D. Torgerson, A. M. Andres et al., 2009 Darwinian and demographic forces affecting human protein coding genes. Genome Res. 19: 838-849
70. Nielsen, R., J. S. Paul, A. Albrechtsen, and Y. S. Song, 2011 Genotype and SNP calling from next-generation sequencing data. Nat. Rev. Genet. 12: 443-451
71. Orlando, L., A. Ginolhac, G. Zhang, D. Froese, A. Albrechtsen et al., 2013 Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499: 74-78
72. Orozco-terWengel, P., 2016 The devil is in the details: the effect of population structure on demographic inference. Heredity 116: 349-350
73. Pagani, L., D. J. Lawson, E. Jagoda, A. Mörseburg, A. Eriksson et al., 2016 Genomic analyses inform on migration events during the peopling of Eurasia. Nature 538: 238-242
74. Palkopoulou, E., S. Mallick, P. Skoglund, J. Enk,N. Rohland et al., 2015 Complete genomes reveal signatures of demographic and genetic declines in the woolly mammoth. Curr. Biol. 25: 1395-1400
75. Peter, B. M., D. Wegmann, and L. Excoffier, 2010 Distinguishing between population bottleneck and population subdivision by a Bayesian model choice procedure. Mol. Ecol. 19: 4648-4660
76. Phung, T. N., C. D. Huber, and K. E. Lohmueller, 2016 Determining the effect of natural selection on linked neutral divergence across species. PLoS Genet. 12: e1006199
77. Plagnol, V., and J. D. Wall, 2006 Possible ancestral structure in human populations. PLoS Genet. 2: e105
78. Polanski, A., and M. Kimmel, 2003 New explicit expressions for relative frequencies of single-nucleotide polymorphisms with application to statistical inference on population growth. Genetics 165: 427-436
79. Prado-Martinez, J., P. H. Sudmant, J. M. Kidd, H. Li, J. L. Kelley et al., 2013 Great ape genetic diversity and population history. Nature 499: 471-475
80. Prufer, K., F. Racimo, N. Patterson, F. Jay, S. Sankararaman et al., 2014 The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505: 43-49
81. Ptak, S. E., and M. Przeworski, 2002 Evidence for population growth in humans is confounded by fine-scale population structure. Trends Genet. 18: 559-563
82. Schiffels, S., and R. Durbin, 2014 Inferring human population size and separation history from multiple genome sequences. Nat. Genet. 46: 919-925
83. Scholz, C. A., T. C. Johnson, A. S. Cohen, J. W. King, J. A. Peck et al., 2007 East African megadroughts between 135 and 75 thousand years ago and bearing on early-modern human origins. Proc. Natl. Acad. Sci. USA 104: 16416-16421
84. Schraiber, J. G., and J. M. Akey, 2015 Methods and models for unravelling human evolutionary history. Nat. Rev. Genet. 16: 727-740
85. Schrider, D. R., A. G. Shanku, and A. D. Kern, 2016 Effects of linked selective sweeps on demographic inference and model selection. Genetics 204: 1207-1223
86. Sjödin, P., A. E. Sjöstrand, M. Jakobsson, andM. G. Blum, 2012 Resequencing data provide no evidence for a human bottleneck in Africa during the penultimate glacial period. Mol. Biol. Evol. 29: 1851-1860
87. Slatkin, M., and R. R. Hudson, 1991 Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129: 555-562
88. Song, S., E. Sliwerska, S. Emery, and J. M. Kidd, 2016 Modeling human population separation history using physically phased genomes. Genetics 205: 385-395
89. Sovic, M. G., B. C. Carstens, and H. L. Gibbs, 2016 Genetic diversity in migratory bats: results from RADseq data for three tree bat species at an Ohio windfarm. PeerJ 4: e1647
90. Tajima, F., 1989 The effect of change in population size on DNA polymorphism. Genetics 123: 597-601
91. Takahata, N., and Y. Satta, 1998 Footprints of intragenic recombination at HLA loci. Immunogenetics 47: 430-441
92. Takahata, N., Y. Satta, and J. Klein, 1995 Divergence time and population size in the lineage leading to modern humans. Theor. Popul. Biol. 48: 198-221
93. Tennessen, J. A., A. W. Bigham, T. D. O'Connor, W. Fu, E. E. Kenny et al., 2012 Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science 337: 64-69
94. Terhorst, J., and Y. S. Song, 2015 Fundamental limits on the accuracy of demographic inference based on the sample frequency spectrum. Proc. Natl. Acad. Sci. USA 112: 7677-7682
95. Terhorst, J., J. A. Kamm, and Y. S. Song, 2017 Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat. Genet. 49: 303-309
96. Thornton, K., and P. Andolfatto, 2006 Approximate Bayesian inference reveals evidence for a recent, severe bottleneck in a Netherlands population of Drosophila melanogaster. Genetics 172: 1607-1619
97. Trucchi, E., P. Gratton, J. D. Whittington, R. Cristofari, Y. Le Maho et al., 2014 King penguin demography since the last glaciation inferred from genome-wide data. Proc. Biol. Sci. 281: 20140528
98. Wakeley, J., 2009 Coalescent Theory: An Introduction. Roberts & Co. Publishers, Greenwood Village, CO
99. Wall, J. D., and J. K. Pritchard, 2003 Haplotype blocks and linkage disequilibrium in the human genome. Nat. Rev. Genet. 4: 587-597
100. Wang, G.-D., W. Zhai, H.-C. Yang, L. Wang, L. Zhong et al., 2016 Out of southern East Asia: the natural history of domestic dogs across the world. Cell Res. 26: 21-33
101. Weissman, D. B., and O. Hallatschek, 2017 Minimal-assumption inference from population-genomic data. Elife 6: e24836
102. Zhao, S., P. Zheng, S. Dong, X. Zhan, Q. Wu et al., 2012 Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nat. Genet. 45: 67-71