The effect of an extreme and prolonged population bottleneck on patterns of deleterious variation: Insights from the Greenlandic Inuit

Genetics

Volumn 205, Issue 2, 2017, Pages 787-801

  Pedersen, Casper Emil T ^a   Lohmueller, Kirk E ^b,c   Grarup, Niels ^d   Bjerregaard, Peter ^e   Hansen, Torben ^d   Siegismund, Hans R ^a   Moltke, Ida ^a   Albrechtsen, Anders ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Capital Region   (Denmark)

^e UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Disease mapping; Founder population; Genetic load; Isolated human populations; Neutral theory

Indexed keywords

ALLELE; ARTICLE; BOTTLENECK POPULATION; CAMBODIAN; GENE FREQUENCY; GENETIC LOAD; GENETIC VARIATION; GREENLAND; HAN CHINESE; HUMAN; INUIT; MBUTI PYGMY; NIGERIAN; NORTHERN EUROPEAN; POPULATION DISTRIBUTION; PRIORITY JOURNAL; SIMULATION; WHOLE EXOME SEQUENCING; EXOME; GENETICS; MIGRATION; MOLECULAR EVOLUTION; SINGLE NUCLEOTIDE POLYMORPHISM;

EVOLUTION, MOLECULAR; EXOME; GENE FREQUENCY; GENETIC LOAD; GREENLAND; HUMAN MIGRATION; HUMANS; INUITS; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 85021849263     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.116.193821     Document Type: Article

References (55)

1. Adams, A. M., and R. R. Hudson, 2004 Maximum-likelihood estimation of demographic parameters using the frequency spectrum of unlinked single-nucleotide polymorphisms. Genetics 168: 1699–1712.
2. 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.
3. Brandvain, Y., and S. I. Wright, 2016 The limits of natural selection in a nonequilibrium world. Trends Genet. 32: 201–210.
4. Busing, F. M. T. A., E. Meijer, and R. V. D. Leeden, 1999 Delete-m Jackknife for unequal m. Stat. Comput. 9: 3–8.
5. Campbell, C. D., and E. E. Eichler, 2013 Properties and rates of germline mutations in humans. Trends Genet. 29: 575–584.
6. Casals, F., A. Hodgkinson, J. Hussin, Y. Idaghdour, V. Bruat et al., 2013 Whole-exome sequencing reveals a rapid change in the frequency of rare functional variants in a founding population of humans. PLoS Genet. 10: e1004260.
7. Charlesworth, B., 2009 Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10: 195–205.
8. Cooper, G. M., E. A. Stone, G. Asimenos, E. D. Green, S. Batzoglou et al., 2005 Distribution and intensity of constraint in mammalian genomic sequence. Genome Res. 15: 901–913.
9. Danecek, P., A. Auton, G. Abecasis, C. A. Albers, E. Banks et al., 2011 The variant call format and VCFtools. Bioinformatics 27: 2156–2158.
10. Do, R., D. Balick, H. Li, I. Adzhubei, S. Sunyaev et al., 2015 No evidence that selection has been less effective at removing deleterious mutations in Europeans than in Africans. Nat. Genet. 47: 126–131.
11. Dong, C., P. Wei, X. Jian, R. Gibbs, E. Boerwinkle et al., 2015 Comparison and integration of deleteriousness prediction methods for nonsynonymous SNVs in whole exome sequencing studies. Hum. Mol. Genet. 24: 2125–2137.
12. Fenner, J. N., 2005 Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies. Am. J. Phys. Anthropol. 128: 415–423.
13. Fu, W., R. M. Gittelman, M. J. Bamshad, and J. M. Akey, 2014 Characteristics of neutral and deleterious protein-coding variation among individuals and populations. Am. J. Hum. Genet. 95: 421–436.
14. Fumagalli, M., I. Moltke, N. Grarup, F. Racimo, P. Bjerregaard et al., 2015 Greenlandic Inuit show genetic signatures of diet and climate adaptation. Science 349: 1343–1347.
15. Goode, D. L., G. M. Cooper, J. Schmutz, M. Dickson, E. Gonzales et al., 2010 Evolutionary constraint facilitates interpretation of genetic variation in resequenced human genomes. Genome Res. 20: 301–310.
16. Gravel, S., 2016 When is selection effective? Genetics 203: 451–462.
17. Gudmand-Høyer, E., H. J. Fenger, P. Kern-Hansen, and P. R. Madsen, 1987 Sucrase deficiency in Greenland. Incidence and genetic aspects. Scand. J. Gastroenterol. 22: 24–28.
18. Gulløv, H. C., 2004 Grønlands Forhistorie. Gyldendal, Copenhagen.
19. 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.
20. Harris, K., and R. Nielsen, 2016 The genetic cost of Neanderthal introgression. Genetics 203: 881–891.
21. Henn, B. M., L. R. Botigué, C. D. Bustamante, A. G. Clark, and S. Gravel, 2015 Estimating the mutation load in human genomes. Nat. Rev. Genet. 16: 333–343.
22. 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–E444.
23. Hong, E. P., and J. W. Park, 2012 Sample size and statistical power calculation in genetic association studies. Genomics Inform. 10: 117.
24. Jorgensen, M. E., P. Bjeregaard, K. Borch-Johnsen, V. Backer, U. Becker et al., 2002 Diabetes and impaired glucose tolerance among the Inuit population of Greenland. Diabetes Care 25: 1766–1771.
25. Kapur, S., S. Mehra, D. Gajjar, A. Vasavada, M. Kapoor et al., 2009 Analysis of single nucleotide polymorphisms of CRYGA and CRYGB genes in control population of western Indian origin. Indian J. Ophthalmol. 57: 197–201.
26. Kimura, M., T. Maruyama, and J. F. Crow, 1963 Mutation load in small populations. Genetics 48: 1303–1312.
27. Korneliussen, T., A. Albrechtsen, and R. Nielsen, 2014 ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15: 356.
28. Kristiansson, K., J. Naukkarinen, and L. Peltonen, 2008 Isolated populations and complex disease gene identification. Genome Biol. 9: 109.
29. Kurki, M. I., E. I. Gaál, J. Kettunen, T. Lappalainen, A. Menelaou et al., 2014 High risk population isolate reveals low frequency variants predisposing to intracranial aneurysms. PLoS Genet. 10: e1004134.
30. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan et al., 2009 The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078–2079.
31. Lim, E. T., P. Würtz, A. S. Havulinna, P. Palta, T. Tukiainen et al., 2014 Distribution and medical impact of loss-of-function variants in the Finnish founder population. PLoS Genet. 10: e1004494.
32. Liu, X., and Y.-X. Fu, 2015 Exploring population size changes using SNP frequency spectra. Nat. Genet. 47: 555–559.
33. Lohmueller, K. E., 2014a The distribution of deleterious genetic variation in human populations. Curr. Opin. Genet. Dev. 29: 139–146.
34. Lohmueller, K. E., 2014b The impact of population demography and selection on the genetic architecture of complex traits. PLoS Genet. 10: e1004379.
35. Lohmueller, K. E., A. R. Indap, S. Schmidt, A. R. Boyko, R. D. Hernandez et al., 2008 Proportionally more deleterious genetic variation in European than in African populations. Nature 451: 994–997.
36. Maier, V., C. Jolicoeur, H. Rayburn, N. Takegahara, A. Kumanogoh et al., 2011 Semaphorin 4C and 4G are ligands of Plexin-B2 required in cerebellar development. Mol. Cell. Neurosci. 46: 419–431.
37. Marcadier, J. L., M. Boland, C. R. Scott, K. Issa, Z. Wu et al., 2014 Congenital sucrose-isomaltase deficiency: identification of a common Inuit founder mutation. Can. Med. Assoc. J. 187: 102–107.
38. Marsden, C. D., D. Ortega-Del Vecchyo, D. P. O’Brien, J. F. Taylor, O. Ramirez et al., 2016 Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs. Proc. Natl. Acad. Sci. USA 133: 152–157.
39. 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.
40. McNair, A., E. Gudmand-Hoyer, S. Jarnum, and L. Orrild, 1972 Sucrose malabsorption in Greenland. BMJ 2: 19–21.
41. McVean, G. A., D. M. Altshuler, R. M. Durbin, G. R. Abecasis, D. R. Bentley et al., 2012 An integrated map of genetic variation from 1,092 human genomes. Nature 491: 56–65.
42. Messer, P. W., 2013 SLiM: Simulating evolution with selection and linkage. Genetics 194: 1037–1039.
43. Moltke, I., N. Grarup, M. E. Jørgensen, P. Bjerregaard, J. T. Treebak et al., 2014 A common Greenlandic TBC1D4 variant confers muscle insulin resistance and type 2 diabetes. Nature 512: 190–193.
44. Moltke, I., M. Fumagalli, T. S. Korneliussen, J. E. Crawford, P. Bjerregaard et al., 2015 Uncovering the genetic history of the present-day Greenlandic population. Am. J. Hum. Genet. 96: 54–69.
45. Morton, N. E., J. F. Crow, and H. J. Muller, 1956 An estimate of the mutational damage in man from data on consanguineous marriages. Proc. Natl. Acad. Sci. USA 42: 855–863.
46. Nielsen, R., C. Bustamante, A. G. Clark, S. Glanowski, T. B. Sackton et al., 2005 A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol. 3: e170.
47. Ohta, T., 1973 Slightly deleterious mutant substitutions in evolution. Nature 246: 96–98.
48. Peltonen, L., A. Palotie, and K. Lange, 2000 Use of population isolates for mapping complex traits. Nat. Rev. Genet. 1: 182–190.
49. Perez-Oliva, A. B., C. Lachaud, P. Szyniarowski, I. Muñoz, T. Macartney et al., 2015 USP 45 deubiquitylase controls ERCC 1-XPF endonuclease- mediated DNA damage responses. EMBO J. 34: 326–343.
50. Raghavan, M., M. DeGiorgio, A. Albrechtsen, I. Moltke, P. Skoglund et al., 2014 The genetic prehistory of the new world arctic. Science 345: 1255832.
51. Simons, Y. B., and G. Sella, 2016 The impact of recent population history on the deleterious mutation load in humans and close evolutionary relatives. Curr. Opin. Genet. Dev. 41: 150–158.
52. Simons, Y. B., M. C. Turchin, J. K. Pritchard, and G. Sella, 2014 The deleterious mutation load is insensitive to recent population history. Nat. Genet. 46: 220–224.
53. Tachmazidou, I., G. Dedoussis, L. Southam, A. E. Farmaki, G. R. Ritchie et al., 2013 A rare functional cardioprotective APOC3 variant has risen in frequency in distinct population isolates. Nat. Commun. 4: 2872.
54. Tajima, F., 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 595: 585–595.
55. Zuk, O., S. F. Schaffner, K. Samocha, R. Do, E. Hechter et al., 2014 Searching for missing heritability: designing rare variant association studies. Proc. Natl. Acad. Sci. USA 111: E455–E464.