Inferring Population Size History from Large Samples of Genome-Wide Molecular Data - An Approximate Bayesian Computation Approach

PLoS Genetics

Volumn 12, Issue 3, 2016, Pages

  Boitard, Simon ^a,b   Rodríguez, Willy ^c   Jay, Flora ^d,e   Mona, Stefano ^a   Austerlitz, Frédéric ^d  

^a SORBONNE UNIVERSITÉ   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d Université Paris Diderot   (France)

^e UFR 919 Laboratoire d'Informatique Pour la Mécanique et les Sciences de l'Ingénieur   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ANIMAL EXPERIMENT; CONTROLLED STUDY; DOMESTICATION; EFFECTIVE POPULATION SIZE; ERROR; FLECKVIEH CATTLE; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENOME; NONHUMAN; POPULATION SIZE; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICS; ZYGOTE; ANIMAL; BAYES THEOREM; BOVINE; BREEDING; GENETICS; POPULATION DENSITY; POPULATION GENETICS;

ALLELES; ANIMALS; BAYES THEOREM; BREEDING; CATTLE; GENETICS, POPULATION; LINKAGE DISEQUILIBRIUM; POLYMORPHISM, SINGLE NUCLEOTIDE; POPULATION DENSITY;

EID: 84962431683     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005877     Document Type: Article

References (72)

1. Lorenzen E, Nogues-Bravo D, Orlando L, Weinstock J, Binladen J, Marske K, et al. Species-specific responses of Late Quaternary megafauna to climate and humans. Nature. 2011;479(7373):359–364. doi: 10.1038/nature1057422048313
2. Akey JM, Zhang G, Zhang K, Jin L, Shriver MD, Interrogating a High-Density SNP Map for Signatures of Natural Selection. Genome Research. 2002;12(12):1805–1814. Available from: http://genome.cshlp.org/content/12/12/1805.abstract. doi: 10.1101/gr.63120212466284
3. Goldstein DB, Chikhi L, HUMAN MIGRATIONS AND POPULATION STRUCTURE: What We Know and Why it Matters. Annual Review of Genomics and Human Genetics. 2002;3(1):129–152. Available from: http://dx.doi.org/10.1146/annurev.genom.3.022502.103200. doi: 10.1146/annurev.genom.3.022502.10320012142358
4. Quéméré E, Amelot X, Pierson J, Crouau-Roy B, Chikhi L, Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region. Proceedings of the National Academy of Sciences. 2012;109(32):13028–13033. Available from: http://www.pnas.org/content/109/32/13028.abstract. doi: 10.1073/pnas.1200153109
5. Pybus OG, Rambaut A, Harvey PH, An Integrated Framework for the Inference of Viral Population History From Reconstructed Genealogies. Genetics. 2000;155(3):1429–1437. Available from: http://www.genetics.org/content/155/3/1429.abstract. 10880500
6. Ho SYW, Shapiro B, Skyline-plot methods for estimating demographic history from nucleotide sequences. Molecular Ecology Resources. 2011;11(3):423–434. Available from: http://dx.doi.org/10.1111/j.1755-0998.2011.02988.x. doi: 10.1111/j.1755-0998.2011.02988.x21481200
7. Burgarella C, Navascuès M, Zabal-Aguirre M, Berganzo E, Riba M, Mayol M, et al. Recent population decline and selection shape diversity of taxol-related genes. Molecular Ecology. 2012;21(12):3006–3021. Available from: http://dx.doi.org/10.1111/j.1365-294X.2012.05532.x. doi: 10.1111/j.1365-294X.2012.05532.x22574693
8. Nikolic N, Chevalet C, Detecting past changes of effective population size. Evolutionary Applications. 2014;7(6):663–681. Available from: http://dx.doi.org/10.1111/eva.12170. doi: 10.1111/eva.1217025067949
9. Li H, Durbin R, Inference of human population history from individual whole-genome sequences. Nature. 2011;475:493–496. doi: 10.1038/nature1023121753753
10. Schiffels S, Durbin R, Inferring human population size and separation history from multiple genome sequences. Nature Genetics. 2014;46:919–925. doi: 10.1038/ng.301524952747
11. Sheehan S, Harris K, Song YS, Estimating Variable Effective Population Sizes from Multiple Genomes: A Sequentially Markov Conditional Sampling Distribution Approach. Genetics. 2013;194(3):647–662. Available from: http://www.genetics.org/content/194/3/647.abstract. doi: 10.1534/genetics.112.14909623608192
12. MacLeod IM, Larkin DM, Lewin HA, Hayes BJ, Goddard ME, Inferring Demography from Runs of Homozygosity in Whole-Genome Sequence, with Correction for Sequence Errors. Molecular Biology and Evolution. 2013;30(9):2209–2223. Available from: http://mbe.oxfordjournals.org/content/30/9/2209.abstract. doi: 10.1093/molbev/mst12523842528
13. Bhaskar A, Wang YXR, Song YS, Efficient inference of population size histories and locus-specific mutation rates from large-sample genomic variation data. Genome Research. 2015; Available from: http://genome.cshlp.org/content/early/2015/01/05/gr.178756.114.abstract. doi: 10.1101/gr.178756.11425564017
14. McVean GAT, Cardin NJ, Approximating the coalescent with recombination. Philosophical Transactions of the Royal Society B: Biological Sciences. 2005;360(1459):1387–1393. Available from: http://rstb.royalsocietypublishing.org/content/360/1459/1387.abstract. doi: 10.1098/rstb.2005.1673
15. Marjoram P, Wall J, Fast “coalescent” simulation. BMC Genetics. 2006;7(1):16. Available from: http://www.biomedcentral.com/1471-2156/7/16. doi: 10.1186/1471-2156-7-1616539698
16. Hudson RR, Properties of a neutral allele model with intragenic recombination. Theoret Popul Biol. 1983;23:183–201. doi: 10.1016/0040-5809(83)90013-8
17. Sørensen AC, Sørensen MK, Berg P, Inbreeding in Danish Dairy Cattle Breeds. Journal of Dairy Science. 2005;88 (5):1865–1872. doi: 10.3168/jds.S0022-0302(05)72861-715829680
18. Boichard D, Maignel L, Verrier E, Analyse généalogique des races bovines laitières françaises. INRA Prod Anim. 1996;9 (5):323–335.
19. Leroy G, Mary-Huard T, Verrier E, Danvy S, Charvolin E, Danchin-Burge C, Methods to estimate effective population size using pedigree data: Examples in dog, sheep, cattle and horse. Genetics Selection Evolution. 2013;45(1):1. Available from: http://www.gsejournal.org/content/45/1/1. doi: 10.1186/1297-9686-45-1
20. Beaumont MA, Zhang W, Balding DJ, Approximate Bayesian Computation in Population Genetics. Genetics. 2002;162(4):2025–2035. Available from: http://www.genetics.org/content/162/4/2025.abstract. 12524368
21. Wollstein A, Lao O, Becker C, Brauer S, Trent RJ, Nürnberg P, et al. Demographic History of Oceania Inferred from Genome-wide Data. Current Biology. 2010;20(22):1983–1992. Available from: http://www.sciencedirect.com/science/article/pii/S0960982210013436. doi: 10.1016/j.cub.2010.10.04021074440
22. Li S, Jakobsson M, Estimating demographic parameters from large-scale population genomic data using Approximate Bayesian Computation. BMC Genetics. 2012;13(1):22. Available from: http://www.biomedcentral.com/1471-2156/13/22. doi: 10.1186/1471-2156-13-2222453034
23. Theunert C, Tang K, Lachmann M, Hu S, Stoneking M, Inferring the History of Population Size Change from Genome-Wide SNP Data. Molecular Biology and Evolution. 2012;29(12):3653–3667. Available from: http://mbe.oxfordjournals.org/content/29/12/3653.abstract. doi: 10.1093/molbev/mss17522787284
24. Nadachowska-Brzyska K, Burri R, Olason PI, Kawakami T, Smeds L, Ellegren H, Demographic Divergence History of Pied Flycatcher and Collared Flycatcher Inferred from Whole-Genome Re-sequencing Data. PLoS Genet. 201311;9(11):e1003942. Available from: http://dx.doi.org/10.1371/journal.pgen.1003942. doi: 10.1371/journal.pgen.100394224244198
25. Veeramah KR, Woerner AE, Johnstone L, Gut I, Gut M, Marques-Bonet T, et al. Examining Phylogenetic Relationships Among Gibbon Genera Using Whole Genome Sequence Data Using an Approximate Bayesian Computation Approach. Genetics. 2015;200(1):295–308. Available from: http://www.genetics.org/content/200/1/295.abstract. doi: 10.1534/genetics.115.17442525769979
26. Hayes BJ, Visscher PM, McPartlan HC, Goddard ME, Novel Multilocus Measure of Linkage Disequilibrium to Estimate Past Effective Population Size. Genome Research. 2003;13(4):635–643. Available from: http://genome.cshlp.org/content/13/4/635.abstract. doi: 10.1101/gr.38710312654718
27. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD, Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data. PLoS Genet. 200910;5(10):e1000695. Available from: http://dx.doi.org/10.1371/journal.pgen.1000695. doi: 10.1371/journal.pgen.100069519851460
28. Lukić S, Hey J, Demographic Inference Using Spectral Methods on SNP Data, with an Analysis of the Human Out-of-Africa Expansion. Genetics. 2012;192(2):619–639. Available from: http://www.genetics.org/content/192/2/619.abstract. doi: 10.1534/genetics.112.14184622865734
29. Excoffier L, Dupanloup I, Huerta-Sánchez E, Sousa VC, Foll M, Robust Demographic Inference from Genomic and SNP Data. PLoS Genet. 201310;9(10):e1003905. Available from: http://dx.doi.org/10.1371/journal.pgen.1003905. doi: 10.1371/journal.pgen.100390524204310
30. Patin E, Siddle KJ, Laval G, Quach H, Harmant C, Becker N, et al. The impact of agricultural emergence on the genetic history of African rainforest hunter-gatherers and agriculturalists. Nature Communications. 2014;5: art. 3163. Available from: http://www.documentation.ird.fr/hor/fdi:010061680. doi: 10.1038/ncomms416324495941
31. Liu X, Fu YX, Exploring population size changes using SNP frequency spectra. Nature genetics. 2015;47(5):555–559. doi: 10.1038/ng.325425848749
32. Blum M, Françcois O, Non-linear regression models for Approximate Bayesian Computation. Statistics and Computing. 2010;20(1):63–73. Available from: http://dx.doi.org/10.1007/s11222-009-9116-0. doi: 10.1007/s11222-009-9116-0
33. Blum MGB, Nunes MA, Prangle D, Sisson SA, A comparative review of dimension reduction methods in approximate Bayesian computation. Statistical Science. 2013;28:189–208. doi: 10.1214/12-STS406
34. Felius M, Beerling ML, Buchanan DS, Theunissen B, Koolmees PA, Lenstra JA, On the history of cattle genetic resources. Diversity. 2014;6(4):705–750. doi: 10.3390/d6040705
35. Groenen M, Archibald A, Uenishi H, Tuggle C, Takeuchi Y, Rothschild M, et al. Analyses of pig genomes provide insight into porcine demography and evolution. Nature. 2012;491:393–398. doi: 10.1038/nature1162223151582
36. Zhao S, Zheng P, Dong S, Zhan X, Wu Q, Guo X, et al. Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nature Genetics. 2013;45(1):67–71. doi: 10.1038/ng.249423242367
37. Green RE, Braun EL, Armstrong J, Earl D, Nguyen N, Hickey G, et al. Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science. 2014;346 (6215). Available from: http://www.sciencemag.org/content/346/6215/1254449.abstract. doi: 10.1126/science.1254449
38. Hung CM, Shaner PJL, Zink RM, Liu WC, Chu TC, Huang WS, et al. Drastic population fluctuations explain the rapid extinction of the passenger pigeon. Proceedings of the National Academy of Sciences. 2014;111(29):10636–10641. Available from: http://www.pnas.org/content/111/29/10636.abstract. doi: 10.1073/pnas.1401526111
39. O’Connell J, Gurdasani D, Delaneau O, Pirastu N, Ulivi S, Cocca M, et al. A General Approach for Haplotype Phasing across the Full Spectrum of Relatedness. PLoS Genet. 20144;10(4):e1004234. Available from: http://dx.doi.org/10.1371/journal.pgen.1004234. doi: 10.1371/journal.pgen.100423424743097
40. Daetwyler HD, Capitan A, Pausch H, Stothard P, van Binsbergen R, Brondum RF, et al. Whole-genome sequencing of 234 bulls facilitates mapping of monogenic and complex traits in cattle. Nat Genet. 2014;46:858–865. doi: 10.1038/ng.303425017103
41. Consortium TBH, Genome-Wide Survey of SNP Variation Uncovers the Genetic Structure of Cattle Breeds. Science. 2009;324(5926):528–532. Available from: http://www.sciencemag.org/content/324/5926/528.abstract. doi: 10.1126/science.1167936
42. Zeder MA, Domestication and early agriculture in the Mediterranean Basin: Origins, diffusion, and impact. Proceedings of the National Academy of Sciences. 2008;105(33):11597–11604. Available from: http://www.pnas.org/content/105/33/11597.abstract. doi: 10.1073/pnas.0801317105
43. Edwards CJ, Ginja C, Kantanen J, Pérez-Pardal L, Tresset A, Stock F, et al. Dual Origins of Dairy Cattle Farming—Evidence from a Comprehensive Survey of European Y-Chromosomal Variation. PLoS ONE. 20111;6(1):e15922. Available from: http://dx.doi.org/10.1371/journal.pone.0015922. doi: 10.1371/journal.pone.001592221253012
44. Gautier M, Laloë D, Moazami-Goudarzi K, Insights into the Genetic History of French Cattle from Dense SNP Data on 47 Worldwide Breeds. PLoS ONE. 20109;5(9):e13038. Available from: http://dx.doi.org/10.1371/journal.pone.0013038. doi: 10.1371/journal.pone.001303820927341
45. Felius M, Koolmees PA, Theunissen B, Consortium ECGD, Lenstra JA, On the Breeds of Cattle—Historic and Current Classifications. Diversity. 2011;3(4):660–692. Available from: http://www.mdpi.com/1424-2818/3/4/660. doi: 10.3390/d3040660
46. Csilléry K, Blum MGB, Gaggiotti OE, Françcois O, Approximate Bayesian Computation (ABC) in practice. Trends in Ecology and Evolution. 2010;25(7):410–418. Available from: http://www.sciencedirect.com/science/article/pii/S0169534710000662. doi: 10.1016/j.tree.2010.04.00120488578
47. McEvoy BP, Powell JE, Goddard ME, Visscher PM, Human population dispersal “Out of Africa” estimated from linkage disequilibrium and allele frequencies of SNPs. Genome Research. 2011; Available from: http://genome.cshlp.org/content/early/2011/04/25/gr.119636.110.abstract. doi: 10.1101/gr.119636.11021518737
48. Hill WG, Estimation of effective population size from data on linkage disequilibrium. Genetics Research. 1981;38:209–216. Available from: http://journals.cambridge.org/article_S0016672300020553. doi: 10.1017/S0016672300020553
49. Gattepaille LM, Jakobsson M, Blum M, Inferring population size changes with sequence and SNP data: lessons from human bottlenecks. Heredity. 2013;110:409–419. doi: 10.1038/hdy.2012.12023423148
50. Rogers AR, How Population Growth Affects Linkage Disequilibrium. Genetics. 2014; Available from: http://www.genetics.org/content/early/2014/06/04/genetics.114.166454.abstract. doi: 10.1534/genetics.114.166454
51. Corbin LJ, Liu AYH, Bishop SC, Woolliams JA, Estimation of historical effective population size using linkage disequilibria with marker data. Journal of Animal Breeding and Genetics. 2012;129(4):257–270. Available from: http://dx.doi.org/10.1111/j.1439-0388.2012.01003.x. doi: 10.1111/j.1439-0388.2012.01003.x22775258
52. Bhaskar A, Song YS, Descartes’ rule of signs and the identifiability of population demographic models from genomic variation data. Ann Statist. 201412;42(6):2469–2493. Available from: http://dx.doi.org/10.1214/14-AOS1264. doi: 10.1214/14-AOS1264
53. Bunnefeld L, Frantz LAF, Lohse K, Inferring Bottlenecks from Genome-Wide Samples of Short Sequence Blocks. Genetics. 2015;201(3):1157–1169. Available from: http://www.genetics.org/content/201/3/1157.abstract. doi: 10.1534/genetics.115.17986126341659
54. Harris K, Nielsen R, Inferring Demographic History from a Spectrum of Shared Haplotype Lengths. PLoS Genet. 20136;9(6):e1003521. Available from: http://dx.doi.org/10.1371/journal.pgen.1003521. doi: 10.1371/journal.pgen.100352123754952
55. Nielsen R, Korneliussen T, Albrechtsen A, Li Y, Wang J, SNP Calling, Genotype Calling, and Sample Allele Frequency Estimation from New-Generation Sequencing Data. PLoS ONE. 20127;7(7):e37558. Available from: http://dx.doi.org/10.1371/journal.pone.0037558. doi: 10.1371/journal.pone.003755822911679
56. Maruki T, Lynch M, Genome-Wide Estimation of Linkage Disequilibrium from Population-Level High-Throughput Sequencing Data. Genetics. 2014; Available from: http://www.genetics.org/content/early/2014/05/27/genetics.114.165514.abstract. doi: 10.1534/genetics.114.165514
57. Flury C, Tapio M, Sonstegard T, Drögemüller C, Leeb T, Simianer H, et al. Effective population size of an indigenous Swiss cattle breed estimated from linkage disequilibrium. Journal of Animal Breeding and Genetics. 2010;127(5):339–347. Available from: http://dx.doi.org/10.1111/j.1439-0388.2010.00862.x. doi: 10.1111/j.1439-0388.2010.00862.x20831557
58. Shin DH, Cho KH, Park KD, Lee HJ, Kim H, Accurate Estimation of Effective Population Size in the Korean Dairy Cattle Based on Linkage Disequilibrium Corrected by Genomic Relationship Matrix. Asian Australas J Anim Sci. 2013;26(12):1672–1679. Available from: http://ajas.info/journal/view.php?number=4618. doi: 10.5713/ajas.2013.1332025049757
59. Kijas JW, Lenstra JA, Hayes B, Boitard S, Porto Neto LR, San Cristobal M, et al. Genome-wide analysis of the world’s sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biol. 2012;10(2):e1001258. Available from: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?cmd=prlinks&dbfrom=pubmed&retmode=ref&id=22346734. doi: 10.1371/journal.pbio.100125822346734
60. Chikhi L, Sousa VC, Luisi P, Goossens B, Beaumont MA, The Confounding Effects of Population Structure, Genetic Diversity and the Sampling Scheme on the Detection and Quantification of Population Size Changes. Genetics. 2010;186(3):983–995. Available from: http://www.genetics.org/content/186/3/983.abstract. doi: 10.1534/genetics.110.11866120739713
61. Peter BM, Wegmann D, Excoffier L, Distinguishing between population bottleneck and population subdivision by a Bayesian model choice procedure. Molecular Ecology. 2010;19(21):4648–4660. Available from: http://dx.doi.org/10.1111/j.1365-294X.2010.04783.x. doi: 10.1111/j.1365-294X.2010.04783.x20735743
62. Heller R, Chikhi L, Siegismund HR, The Confounding Effect of Population Structure on Bayesian Skyline Plot Inferences of Demographic History. PLoS ONE. 20135;8(5):e62992. Available from: http://dx.doi.org/10.1371/journal.pone.0062992. doi: 10.1371/journal.pone.006299223667558
63. Mazet O, Rodríguez W, Chikhi L, Demographic inference using genetic data from a single individual: Separating population size variation from population structure. Theoretical Population Biology. 2015;104:46–58. Available from: http://www.sciencedirect.com/science/article/pii/S0040580915000581. doi: 10.1016/j.tpb.2015.06.00326120083
64. Mazet O, Rodriguez W, Grusea S, Boitard S, Chikhi L, On the importance of being structured: instantaneous coalescence rates and human evolution—lessons for ancestral population size inference. Heredity. 2015; 26647653
65. Cornuet JM, Santos F, Beaumont MA, Robert CP, Marin JM, Balding DJ, et al. Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics. 2008;24(23):2713–2719. Available from: http://bioinformatics.oxfordjournals.org/content/24/23/2713.abstract. doi: 10.1093/bioinformatics/btn51418842597
66. Sandor C, Li W, Coppieters W, Druet T, Charlier C, Georges M, Genetic Variants in REC8, RNF212, and PRDM9 Influence Male Recombination in Cattle. PLoS Genet. 20127;8(7):e1002854. Available from: http://dx.doi.org/10.1371/journal.pgen.1002854. doi: 10.1371/journal.pgen.100285422844258
67. Rogers AR, Huff CD, Linkage Disequilibrium Between Loci With Unknown Phase. Genetics. 2009;182:839–844. Available from: http://dx.doi.org/10.1534/genetics.108.093153. doi: 10.1534/genetics.108.09315319433632
68. Hudson RR, Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics. 2002;18:337–338. 11847089
69. Yang J, Lee SH, Goddard ME, Visscher PM, GCTA: A Tool for Genome-wide Complex Trait Analysis. The American Journal of Human Genetics. 2011;88(1):76–82. Available from: http://www.sciencedirect.com/science/article/pii/S0002929710005987. doi: 10.1016/j.ajhg.2010.11.01121167468
70. Csilléry K, Françcois O, Blum MGB, abc: an R package for approximate Bayesian computation (ABC). Methods in Ecology and Evolution. 2012;3(3):475–479. Available from: http://dx.doi.org/10.1111/j.2041-210X.2011.00179.x. doi: 10.1111/j.2041-210X.2011.00179.x
71. Tavaré S, Zeitouni O, Lectures on probability theory and statistics. Springer Berlin Heidelberg; 2004.
72. Hoze C, Fouilloux MN, Venot E, Guillaume F, Dassonneville R, Fritz S, et al. High-density marker imputation accuracy in sixteen French cattle breeds. Genetics Selection Evolution. 2013;45(1):33. Available from: http://www.gsejournal.org/content/45/1/33. doi: 10.1186/1297-9686-45-33