Dominance of Deleterious Alleles Controls the Response to a Population Bottleneck

PLoS Genetics

Volumn 11, Issue 8, 2015, Pages

  Balick, Daniel J ^a,b,c   Do, Ron ^c,d   Cassa, Christopher A ^a,b,c   Reich, David ^b,c   Sunyaev, Shamil R ^a,b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; COMPUTER SIMULATION; CONTROLLED STUDY; DOMINANT GENE; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC DRIFT; GENETIC LINKAGE; HAPLOIDY; HUMAN; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MUTATION RATE; NATURAL SELECTION; POPULATION BOTTLENECK; POPULATION DISTRIBUTION; POPULATION DYNAMICS; POPULATION SIZE; PROCESS MODEL; RECESSIVE INHERITANCE; ANIMAL; BIOLOGICAL MODEL; EVOLUTION; GENETIC SELECTION; GENETICS; POPULATION GENETICS; STATISTICAL MODEL; STATISTICS AND NUMERICAL DATA;

ANIMALS; BIOLOGICAL EVOLUTION; COMPUTER SIMULATION; GENE FREQUENCY; GENES, DOMINANT; GENETICS, POPULATION; HUMANS; MODELS, GENETIC; MODELS, STATISTICAL; POPULATION DYNAMICS; SELECTION, GENETIC;

EID: 84940733223     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005436     Document Type: Article

References (54)

1. Eyre-Walker A, Keightley PD, (2007) The distribution of fitness effects of new mutations. Nat. Rev. Genet. 8:610–618. doi: 10.1038/nrg2146 17637733
2. Sella G, et. al. (2009) Pervasive Natural Selection in the Drosophila Genome? PLoS Genet 5: e1000495. doi: 10.1371/journal.pgen.1000495 19503600
3. Cutter AD, Payseur BA, (2013) Genomic signatures of selection at linked sites: unifying the disparity among species. Nat. Rev. Genet. 14:262–74. doi: 10.1038/nrg3425 23478346
4. Mukai T, (1972) Mutation rate and dominance of genes affecting viability in Drosophila Melanogaster. Genetics 72:335–355. 4630587
5. Garcia-Dorado A, Caballero A, (2000) On the average coefficient of dominance of deleterious spontaneous mutations. Genetics 155:1991–2001. 10924491
6. Simmons MJ, Crow JF, (1977) Mutations affecting fitness in Drosophila populations. Ann. Rev. Genet. 11:49–78. doi: 10.1146/annurev.ge.11.120177.000405 413473
7. Deng HW, Lynch M, (1996) Estimation of deleterious-mutation parameters in natural populations. Genetics 144:349–360. 8878698
8. Garcia-Dorado A, Lopez-Fanzul C, Caballero A, (1999) Properties of spontaneous mutations affecting quantitative traits. Genet. Res. 74:341–350. doi: 10.1017/S0016672399004206 10689810
9. Manna F, Martin G, Lenormand T, (2011) Fitness landscapes: An alternative theory for the dominance of mutation. Genetics 189:923–937. doi: 10.1534/genetics.111.132944 21890744
10. Phadnis N, Fry JD, (2005) Widespread correlations between dominance and homozygous effects of mutations: Implications for theories of dominance. Genetics 171:385–392. doi: 10.1534/genetics.104.039016 15972465
11. Agrawal AF, Whitlock MC, (2011) Inferences about the distribution of dominance drawn from yeast gene knockout data. Genetics 187:553–566. doi: 10.1534/genetics.110.124560 21098719
12. Lynch M, Walsh B, (1998) Genetics and analysis of quantitative traits. Sinauer Assocs., Inc., Sunderland, MA.
13. Newman DL, et al. (2001) The importance of genealogy in determining genetic associations with complex traits. Am. J. Hum. Genet. 69:1146–1148. doi: 10.1086/323659 11590549
14. Herron BJ, et al. (2002) Efficient generation and mapping of recessive developmental mutations using ENU mutagenesis. Nat. Genet. 30:185–189. doi: 10.1038/ng812 11818962
15. Wang J, et al. (1999) Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet. Res. 74:165–178. doi: 10.1017/S0016672399003900 10584559
16. Whitlock MC, (2002) Selection, load and inbreeding depression in a large metapopulation. Genetics 160:1191–1202. 11901133
17. Garcia-Dorado A, (2008) A simple method to account for natural selection when predicting inbreeding depression. Genetics 180:1559–1566. doi: 10.1534/genetics.108.090597 18791247
18. Peischl S, Excoffier L, (2015) Expansion load: recessive mutations and the role of standing genetic variation. Molecular Ecology 24:2084–2094. doi: 10.1111/mec.13154 25786336
19. Robertson A, (1952) The effect of inbreeding on the variation due to recessive genes. Genetics 37:189–207. 17247385
20. Bryant EH, McCommas SA, Combs LM, (1986) The effect of an experimental bottleneck upon quantitative genetic-variation in the housefly. Genetics 114:1191–1211. 17246359
21. Wang JL, et. al. (1998) Bottleneck effect on genetic variance: A theoretical investigation of the role of dominance. Genetics 150:435–447, 1998. 9725859
22. Zhang XS, Wang J, Hill WG, (2004) Redistribution of gene frequency and changes of genetic variation following a bottleneck in population size. Genetics 167:1475–1492. doi: 10.1534/genetics.103.025874 15280256
23. Goodnight CJ, (1987) On the effect of founder events on the epistatic genetic variance. Evolution 41: 80–91. doi: 10.2307/2408974
24. Goodnight CJ, (1988) Epistasis and the effect of founder events on the additive genetic variance. Evolution 42: 441–454. doi: 10.2307/2409030
25. Cheverud JM, Routman EJ, (1996) Epistasis as a source of increased additive genetic variance at population bottlenecks. Evolution 50:1042–1051. doi: 10.2307/2410645
26. Hill WG, Caballero A, Wang J, (1998) The effect of linkage disequilibrium and deviation from Hardy-Weinberg proportions on the changes in genetic variance with bottlenecking. Heredity 81:174–186. doi: 10.1046/j.1365-2540.1998.00390.x
27. Naciri-Graven Y, Goudet J, (2003) The additive genetic variance after bottlenecks is affected by the number of loci involved in epistatic interactions. Evolution 57:706–716. doi: 10.1554/0014-3820(2003)057%5B0706:TAGVAB%5D2.0.CO;2 12778542
28. Barton NH, Turelli M, (2004) Effects of genetic drift on variance components under a general model of epistasis. Evolution 58:2111–2132. doi: 10.1554/03-684 15562679
29. Hill WG, Barton NH, Turelli M, (2006) Prediction of effects of genetic drift on variance components under a general model of epistasis. Theor. Popul. Biol. 70:56–62. doi: 10.1016/j.tpb.2005.10.001 16360188
30. Turelli M, Barton NH, (2006) Will population bottlenecks and multilocus epistasis increase additive genetic variance? Evolution 60:1763–1776. doi: 10.1111/j.0014-3820.2006.tb00521.x 17089962
31. Kirkpatrick M, Jarne P, (2000) The effects of a bottleneck on inbreeding depression and the genetic load. Am. Nat. 155(2):154–167. doi: 10.1086/303312 10686158
32. Lachaise D, Singh RS, Uyenoyama MK, et al. (2004) Nine relatives from one African ancestor: population biology and evolution of the Drosophila melanogaster subgroup species. In: (eds.) The Evolution of Population Biology. pp. 315–344. [Online]. Cambridge: Cambridge University Press.
33. Kimura M, (1964) Diffusion models in population genetics. J. Ap. Prob. 1:177–232. doi: 10.2307/3211856
34. Nei M, (1968) The frequency distribution of lethal chromosomes in finite populations. Proc. Natl. Acad. Sci. USA 60: 517–524. doi: 10.1073/pnas.60.2.517 5248809
35. Simons YB, Turchin MC, Pritchard JK, Sella G, (2014) The deleterious mutation load is insensitive to recent population history. Nat. Gen. 46, 220–224. doi: 10.1038/ng.2896
36. Do R, et al. (2015) No evidence that selection has been less effective at removing deleterious mutations in Europeans than in Africans. Nat. Gen. 47:126–131. doi: 10.1038/ng.3186
37. Fu W, et al. (2013) Analysis of 6,515 exomes reveals the recent origin of most human protein-coding variants. Nature 493:216–20. doi: 10.1038/nature11690 23201682
38. Stenson PD, et al. (2009) The Human Gene Mutation Database: providing a comprehensive central mutation database for molecular diagnostics and personalized genomics. Hum Genomics 4(2):69–72. doi: 10.1186/1479-7364-4-2-69 20038494
39. Partners Center for Personalized Genetic Medicine, Brigham and Women’s Hospital (2014) Laboratory for Molecular Medicine Tests. Available: http://personalizedmedicine.partners.org/laboratory-for-molecular-medicine/tests/default.aspx. Accessed 1 July 2014.
40. Solomon BD, Nguyen A, Bear KA, Wolfsberg TG, (2013) Clinical Genomic Database. Proc. Natl. Acad. Sci. USA 110(24):9851–9855. doi: 10.1073/pnas.1302575110 23696674
41. The 1000 Genomes Project Consortium (2012) An integrated map of genetic variation from 1,092 human genomes. Nature 491(7422):56–65. doi: 10.1038/nature11632 23128226
42. Slatkin M, (2004) A population-genetic test of founder effects and implications for Ashkenazi Jewish diseases. Am. J. Hum. Genet. 75:282–293. doi: 10.1086/423146 15208782
43. Gazave E, Chang D, Clark AG, Keinan A, (2013) Population growth inflates the per-individual number of deleterious mutations and reduces their mean effect. Genetics 195(3):969–78. doi: 10.1534/genetics.113.153973 23979573
44. Peischl S, Dupanloup I, Kirkpatrick M, Excoffier L, (2013) On the accumulation of deleterious mutations during range expansions. Mol. Ecol. 22: 5972–5982. doi: 10.1111/mec.12524 24102784
45. Keinan A, Mullikin JC, Patterson N, Reich D, (2007) Measurement of the human allele frequency spectrum demonstrates greater genetic drift in East Asians than in Europeans. Nat. Genet. 39:1251–1255. doi: 10.1038/ng2116 17828266
46. Lohmueller KE, et al. (2008) Proportionally more deleterious genetic variation in European than in African populations. Nature 451(7181):994–997. doi: 10.1038/nature06611 18288194
47. Gravel S, et al. (2011) Demographic history and rare allele sharing among human populations. Proc. Natl. Acad. Sci. USA 108:11983–11988. doi: 10.1073/pnas.1019276108 21730125
48. Tennessen JA, et al. (2012) Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science 337(6090):64–69. doi: 10.1126/science.1219240 22604720
49. Gronau I, et al. (2011) Bayesian inference of ancient human demography from individual genome sequences. Nat. Genet. 43:1031–1034. doi: 10.1038/ng.937 21926973
50. Li H, Durbin R, (2012) Inference of human population history from whole genome sequence of a single individual. Nature 475:493–496. doi: 10.1038/nature10231
51. Sheehan S, Harris K, Song YS, (2013) Estimating variable effective population sizes from multiple genomes: a sequentially markov conditional sampling distribution approach. Genetics 194:647–62. doi: 10.1534/genetics.112.149096 23608192
52. Harris K, Nielsen R, (2013) Inferring demographic history from a spectrum of shared haplotype lengths. PLoS Genet. 9:e1003521. doi: 10.1371/journal.pgen.1003521 23754952
53. Macleod IM, et al. (2013) Inferring demography from runs of homozygosity in whole-genome sequence, with correction for sequence errors. Mol. Biol. Evol. 30:2209–2223. doi: 10.1093/molbev/mst125 23842528
54. Lohmueller KE, (2014) The Impact of Population Demography and Selection on the Genetic Architecture of Complex Traits. PLoS Genet. 10(5):e10004379. doi: 10.1371/journal.pgen.1004379