Distance from sub-Saharan Africa predicts mutational load in diverse human genomes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 4, 2016, Pages E440-E449

  Henn, Brenna M ^a   Botigué, Laura R ^a   Peischl, Stephan ^b,c   Dupanloup, Isabelle ^b   Lipatov, Mikhail ^a   Maples, Brian K ^d   Martin, Alicia R ^d   Musharoff, Shaila ^d   Cann, Howard ^e   Snyder, Michael P ^d   Excoffier, Laurent ^b,c   Kidd, Jeffrey M ^f   Bustamante, Carlos D ^d  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF BERN   (Switzerland)

^c SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e FONDATION JEAN DAUSSET CEPH   (France)

^f UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Expansion load; Founder effect; Mutation; Purifying selection; Range expansion

Indexed keywords

AFRICA SOUTH OF THE SAHARA; ALGERIA; ALLELE; ARTICLE; CAMBODIA; CONGO; DOMINANT INHERITANCE; EXOME; FOUNDER EFFECT; GENE DELETION; GENE FREQUENCY; GENETIC VARIABILITY; HETEROZYGOSITY; HUMAN; HUMAN CELL; HUMAN GENOME; HYPOTHESIS; MEXICO; MUTATIONAL LOAD; NAMIBIA; PAKISTAN; POPULATION DISPERSAL; PRIORITY JOURNAL; PURIFYING SELECTION; RECESSIVE INHERITANCE; RUSSIAN FEDERATION; SIMULATION; SOCIAL DISTANCE; AMERICAN INDIAN; ANIMAL; ANIMAL BEHAVIOR; ASIAN CONTINENTAL ANCESTRY GROUP; BIOLOGICAL MODEL; BLACK PERSON; COMPARATIVE STUDY; COMPUTER SIMULATION; CONSERVED SEQUENCE; ETHNIC GROUP; GENE FLOW; GENETIC DISORDER; GENETIC DRIFT; GENETIC SELECTION; GENETICS; GENOTYPE; MIGRATION; MOLECULAR EVOLUTION; MUTATION;

AFRICA SOUTH OF THE SAHARA; AFRICAN CONTINENTAL ANCESTRY GROUP; ALLELES; ANIMALS; ASIAN CONTINENTAL ANCESTRY GROUP; COMPUTER SIMULATION; CONSERVED SEQUENCE; ETHNIC GROUPS; EVOLUTION, MOLECULAR; FOUNDER EFFECT; GENE FLOW; GENETIC DISEASES, INBORN; GENETIC DRIFT; GENOME, HUMAN; GENOTYPE; HOMING BEHAVIOR; HUMAN MIGRATION; HUMANS; INDIANS, CENTRAL AMERICAN; MODELS, GENETIC; MUTATION; SELECTION, GENETIC;

EID: 84955508579     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1510805112     Document Type: Article

References (67)

1. Morton NE, Crow JF, Muller HJ (1956) An estimate of the mutational damage in man from data on consanguienous marriages. Proc Natl Acad Sci USA 42(11):855-863.
2. Tabor HK, et al.; NHLBI Exome Sequencing Project (2014) Pathogenic variants for Mendelian and complex traits in exomes of 6, 517 European and African Americans: Implications for the return of incidental results. Am J Hum Genet 95(2):183-193.
3. Ohta T (1973) Slightly deleterious mutant substitutions in evolution. Nature 246(5428): 96-98.
4. Gravel S (2014) When is selection effective? bioRXiv, dx.doi.org/10.1101/010934.
5. Henn BM, Botigué LR, Bustamante CD, Clark AG, Gravel S (2015) Estimating the mutation load in human genomes. Nat Rev Genet 16(6):333-343.
6. Lohmueller KE (2014) The distribution of deleterious genetic variation in human populations. Curr Opin Genet Dev 29:139-146.
7. Peischl S, Excoffier L (2015) Expansion load: Recessive mutations and the role of standing genetic variation. Mol Ecol 24(9):2084-2094.
8. Casals F, 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 9(9):e1003815.
9. Kehdy FSG, et al.; Brazilian EPIGEN Project Consortium (2015) Origin and dynamics of admixture in Brazilians and its effect on the pattern of deleterious mutations. Proc Natl Acad Sci USA 112(28):8696-8701.
10. Lohmueller KE, et al. (2008) Proportionally more deleterious genetic variation in European than in African populations. Nature 451(7181):994-997.
11. Fu W, Gittelman RM, Bamshad MJ, Akey JM (2014) Characteristics of neutral and deleterious protein-coding variation among individuals and populations. Am J Hum Genet 95(4):421-436.
12. Simons YB, Turchin MC, Pritchard JK, Sella G (2014) The deleterious mutation load is insensitive to recent population history. Nat Genet 46(3):220-224.
13. Do R, et al. (2015) No evidence that selection has been less effective at removing deleterious mutations in Europeans than in Africans. Nat Genet 47(2):126-131.
14. Fu W, et al.; NHLBI Exome Sequencing Project (2013) Analysis of 6, 515 exomes reveals the recent origin of most human protein-coding variants. Nature 493(7431):216-220.
15. Tennessen JA, et al.; Broad GO; Seattle GO; NHLBI Exome Sequencing Project (2012) Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science 337(6090):64-69.
16. Boyko AR, et al. (2008) Assessing the evolutionary impact of amino acid mutations in the human genome. PLoS Genet 4(5):e1000083.
17. Bittles AH, Black ML (2010) Evolution in health and medicine Sackler colloquium: Consanguinity, human evolution, and complex diseases. Proc Natl Acad Sci USA 107 (Suppl 1):1779-1786.
18. Slatkin M (2004) A population-genetic test of founder effects and implications for Ashkenazi Jewish diseases. Am J Hum Genet 75(2):282-293.
19. Agrawal AF, Whitlock MC (2011) Inferences about the distribution of dominance drawn from yeast gene knockout data. Genetics 187(2):553-566.
20. Cann HM, et al. (2002) A human genome diversity cell line panel. Science 296(5566): 261-262.
21. Henn BM, et al. (2011) Hunter-gatherer genomic diversity suggests a southern African origin for modern humans. Proc Natl Acad Sci USA 108(13):5154-5162.
22. Henn BM, et al. (2012) Genomic ancestry of North Africans supports back-to-Africa migrations. PLoS Genet 8(1):e1002397.
23. Wang S, et al. (2007) Genetic variation and population structure in native Americans. PLoS Genet 3(11):e185.
24. Maples BK, Gravel S, Kenny EE, Bustamante CD (2013) RFMix: A discriminative modeling approach for rapid and robust local-ancestry inference. Am J Hum Genet 93(2): 278-288.
25. Ramachandran S, et al. (2005) Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc Natl Acad Sci USA 102(44):15942-15947.
26. Prugnolle F, Manica A, Balloux F (2005) Geography predicts neutral genetic diversity of human populations. Curr Biol 15(5):R159-R160.
27. Li H, Durbin R (2011) Inference of human population history from individual wholegenome sequences. Nature 475(7357):493-496.
28. Meyer M, et al. (2012) A high-coverage genome sequence from an archaic Denisovan individual. Science 338(6104):222-226.
29. Kidd JM, et al. (2012) Population genetic inference from personal genome data: Impact of ancestry and admixture on human genomic variation. Am J Hum Genet 91(4):660-671.
30. Cooper GM, et al.; NISC Comparative Sequencing Program (2005) Distribution and intensity of constraint in mammalian genomic sequence. Genome Res 15(7):901-913.
31. Cooper GM, et al. (2010) Single-nucleotide evolutionary constraint scores highlight disease-causing mutations. Nat Methods 7(4):250-251.
32. Peischl S, Dupanloup I, Kirkpatrick M, Excoffier L (2013) On the accumulation of deleterious mutations during range expansions. Mol Ecol 22(24):5972-5982.
33. Goode DL, et al. (2010) Evolutionary constraint facilitates interpretation of genetic variation in resequenced human genomes. Genome Res 20(3):301-310.
34. 1000 Genomes Project Consortium (2012) An integrated map of genetic variation from 1, 092 human genomes. Nature 491:56-65.
35. Lohmueller KE, et al. (2011) Natural selection affects multiple aspects of genetic variation at putatively neutral sites across the human genome. PLoS Genet 7(10): e1002326.
36. Kimura M, Maruyama T, Crow JF (1963) The mutation load in small populations. Genetics 48:1303-1312.
37. Reich DE, Lander ES (2001) On the allelic spectrum of human disease. Trends Genet 17(9):502-510.
38. Gao Z, Waggoner D, Stephens M, Ober C, Przeworski M (2015) An estimate of the average number of recessive lethal mutations carried by humans. Genetics 199(4): 1243-1254.
39. Lachance J, Tishkoff SA (2014) Biased gene conversion skews allele frequencies in human populations, increasing the disease burden of recessive alleles. Am J Hum Genet 95(4):408-420.
40. McQuillan R, et al.; ROHgen Consortium (2012) Evidence of inbreeding depression on human height. PLoS Genet 8(7):e1002655.
41. Hamosh A, Scott AF, Amberger JS, Bocchini CA, McKusick VA (2005) Online Mendelian Inheritance in Man (OMIM), a knowledgebase of human genes and genetic disorders. Nucleic Acids Res 33(Database issue):D514-D517.
42. Henn BM, et al. (2012) Cryptic distant relatives are common in both isolated and cosmopolitan genetic samples. PLoS One 7(4):e34267.
43. Mukai T, Chigusa SI, Mettler LE, Crow JF (1972) Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics 72(2):335-355.
44. Houle D, Hughes KA, Assimacopoulos S, Charlesworth B (1997) The effects of spontaneous mutation on quantitative traits. II. Dominance of mutations with effects on life-history traits. Genet Res 70(1):27-34.
45. Racimo F, Schraiber JG (2014) Approximation to the distribution of fitness effects across functional categories in human segregating polymorphisms. PLoS Genet 10(11):e1004697.
46. Henn BM, Cavalli-Sforza LL, Feldman MW (2012) The great human expansion. Proc Natl Acad Sci USA 109(44):17758-17764.
47. Laval G, Patin E, Barreiro LB, Quintana-Murci L (2010) Formulating a historical and demographic model of recent human evolution based on resequencing data from noncoding regions. PLoS One 5(4):e10284.
48. Marth GT, Czabarka E, Murvai J, Sherry ST (2004) The allele frequency spectrum in genome-wide human variation data reveals signals of differential demographic history in three large world populations. Genetics 166(1):351-372.
49. Tanabe K, et al. (2010) Plasmodium falciparum accompanied the human expansion out of Africa. Curr Biol 20(14):1283-1289.
50. Linz B, et al. (2007) An African origin for the intimate association between humans and Helicobacter pylori. Nature 445(7130):915-918.
51. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A (2010) Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 20(1):110-121.
52. Keinan A, Clark AG (2012) Recent explosive human population growth has resulted in an excess of rare genetic variants. Science 336(6082):740-743.
53. Lohmueller KE (2014) The impact of population demography and selection on the genetic architecture of complex traits. PLoS Genet 10(5):e1004379.
54. Pennings PS, Kryazhimskiy S, Wakeley J (2014) Loss and recovery of genetic diversity in adapting populations of HIV. PLoS Genet 10(1):e1004000.
55. Erickson RP, Mitchison NA (2014) The low frequency of recessive disease: Insights from ENU mutagenesis, severity of disease phenotype, GWAS associations, and demography: An analytical review. J Appl Genet 55(3):319-327.
56. Manna F, Martin G, Lenormand T (2011) Fitness landscapes: An alternative theory for the dominance of mutation. Genetics 189(3):923-937.
57. Sabeti PC, et al.; International HapMap Consortium (2007) Genome-wide detection and characterization of positive selection in human populations. Nature 449(7164): 913-918.
58. Hernandez RD, et al.; 1000 Genomes Project (2011) Classic selective sweeps were rare in recent human evolution. Science 331(6019):920-924.
59. Granka JM, et al. (2012) Limited evidence for classic selective sweeps in African populations. Genetics 192(3):1049-1064.
60. Enard D, Messer PW, Petrov DA (2014) Genome-wide signals of positive selection in human evolution. Genome Res 24(6):885-895.
61. Grossman SR, et al.; 1000 Genomes Project (2013) Identifying recent adaptations in large-scale genomic data. Cell 152(4):703-713.
62. Yi X, et al. (2010) Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329(5987):75-78.
63. Pickrell JK, et al. (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Res 19(5):826-837.
64. Scheinfeldt LB, Tishkoff SA (2013) Recent human adaptation: Genomic approaches, interpretation and insights. Nat Rev Genet 14(10):692-702.
65. Coop G, et al. (2009) The role of geography in human adaptation. PLoS Genet 5(6): e1000500.
66. Sousa V, Peischl S, Excoffier L (2014) Impact of range expansions on current human genomic diversity. Curr Opin Genet Dev 29:22-30.
67. Flicek P, et al. (2013) Ensembl 2013. Nucleic Acids Res 41(Database issue):D48-D55.