Accounting for genetic architecture improves sequence based genomic prediction for a Drosophila fitness trait

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Ober, Ulrike ^a,d   Huang, Wen ^b,d   Magwire, Michael ^b   Schlather, Martin ^c   Simianer, Henner ^a   Mackay, Trudy F C ^b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MANNHEIM   (Germany)

^d SYNGENTA BIOTECHNOLOGY INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; DROSOPHILA; EPISTASIS; FEMALE; GENETIC ARCHITECTURE; GENETIC ASSOCIATION; GENETIC CORRELATION; GENETIC TRAIT; GENETIC VARIABILITY; GENOMIC BEST LINEAR UNBIASED PREDICTION MODEL; MALE; NONHUMAN; PREDICTION; QUANTITATIVE GENETICS; QUANTITATIVE TRAIT LOCUS MAPPING; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; GENE; GENETICS; PHYSIOLOGY;

ANIMALIA;

ANIMALS; DROSOPHILA; GENES, INSECT;

EID: 84929119577     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126880     Document Type: Article

References (56)

1. Mackay TFC, Stone EA, Ayroles JF. The genetics of quantitative traits: Challenges and prospects. Nat Rev Genet. 2009; 10: 565-577. doi: 10.1038/nrg2612 PMID: 19584810
2. Visscher PM, Brown MA, McCarthy MI, Yang J. Five years of GWAS discovery. Am J Hum Genet. 2012; 90: 7-24. doi: 10.1016/j.ajhg.2011.11.029 PMID: 22243964
3. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, et al. Finding the missing heritability of complex diseases. Nature 2009; 461: 747-753. doi: 10.1038/nature08494 PMID: 19812666
4. Meuwissen THE, Hayes BJ, Goddard ME. Prediction of total genetic value using genomewide dense marker maps. Genetics 2001; 157: 1819-1829. PMID: 11290733
5. VanRaden PM. Efficient methods to compute genomic predictions. J Dairy Sci. 2008; 91: 4414-4423. doi: 10.3168/jds.2007-0980 PMID: 18946147
6. Yang J, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR, et al. Common SNPs explain a large proportion of the heritability for human height. Nat Genet. 2010; 42: 565-569. doi: 10.1038/ng.608 PMID: 20562875
7. Yang J, Manolio TA, Pasquale LR, Boerwinkle E, Caporaso N, Cunningham JM, et al. Genome partitioning of genetic variation for complex traits using common SNPs. Nat Genet. 2011; 43: 519-525. doi: 10.1038/ng.823 PMID: 21552263
8. Schaeffer LR. Strategy for applying genome-wide selection in dairy cattle. J Anim Breed Genet. 2006; 123: 218-223. PMID: 16882088
9. Goddard M. Genomic selection: prediction of accuracy and maximisation of long-term response. Genetica 2009; 185: 1021-1031.
10. Hayes BJ, Bowman PJ, Chamberlain AJ, Goddard ME. Genomic selection in dairy cattle: Progress and challenges. J Dairy Sci. 2009; 92: 433-443. doi: 10.3168/jds.2008-1646 PMID: 19164653
11. Lorenz AJ, Chao S, Asoro FG, Heffner EL, Hayashi T, Iwata H, et al. Genomic selection in plant breeding: Knowledge and prospects. Adv Agron. 2011; 110: 77-123.
12. Hayes BJ, Lewin HA, Goddard ME. The future of livestock breeding: genomic selection for efficiency, reduced emissions intensity, and adaptation. Trends Genet. 2013; 29: 206-214. doi: 10.1016/j.tig. 2012.11.009 PMID: 23261029
13. Ober U, Ayroles JF, Stone EA, Richards S, Zhu D, Stricker C, et al. Using whole-genome sequence data to predict quantitative trait phenotypes in Drosophila melanogaster. PLoS Genet. 2012; 8: e1002685. doi: 10.1371/journal.pgen.1002685 PMID: 22570636
14. de Los Campos G, Vazquez AI, Fernando R, Klimentidis YC, Sorensen D. Prediction of complex human traits using the genomic best linear unbiased predictor. PLoS Genet. 2013; 9: e1003608. doi: 10.1371/journal.pgen.1003608 PMID: 23874214
15. Hu Z, Li Y, Song X, Han Y, Cai X, Xu S, et al. Genomic value prediction for quantitative traits under the epistatic model. BMC Genetics 2011; 12: 15. doi: 10.1186/1471-2156-12-15 PMID: 21269439
16. Long N, Gianola D, Rosa G, Weigel KA. Marker-assisted prediction of non-additive genetic values. Genetica 2011; 139: 843-845. doi: 10.1007/s10709-011-9588-7 PMID: 21674154
17. Mackay TFC, Richards S, Stone EA, Barbadilla A, Ayroles JF, Casillas S, et al. The Drosophila melanogaster Genetics Reference Panel. Nature 2012; 482: 173-178. doi: 10.1038/nature10811 PMID: 22318601
18. Huang W, Massouras A, Inoue Y, Peiffer J, Ràmia M, Tarone AM, et al. Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines. Genome Res. 2014; 24: 1193-1208. doi: 10.1101/gr.171546.113 PMID: 24714809
19. Anderson AR, Hoffmann AA, McKechnie SW. Response to selection for rapid chill-coma recovery in Drosophila melanogaster: physiology and life-history traits. Genet Res. 2005; 85: 15-22. PMID: 16089033
20. Macmillan HA, Sinclair BJ. Mechanisms underlying insect chill-coma. J Insect Physiol. 2011; 57: 12-20. doi: 10.1016/j.jinsphys.2010.10.004 PMID: 20969872
21. Huang W, Richards S, Carbone MA, Zhu D, Anholt RRH, Ayroles JF, et al. Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proc Natl Acad Sci USA 2012; 109: 15553-15559. PMID: 22949659
22. de los Campos, G, Sorensen, D, Gianola, D. Genomic heritability: What is it? Proceeding of the 10th World Congress of Genetics Applied to Livestock Production. 2014. Available: https://asas.org/wcgalpproceedings
23. Astle W, Balding DJ. Population structure and cryptic relatedness in genetic association studies. Statist Sci. 2009; 24: 451-471.
24. Flint J, Mackay TFC. Genetic architecture of quantitative traits in mice, flies, and humans. Genome Res. 2009; 19: 723-733. doi: 10.1101/gr.086660.108 PMID: 19411597
25. Falconer DS, Mackay TFC. Introduction to Quantitative Genetics. 4th ed. Harlow: Longman Group Limited; 1996.
26. Daetwyler HD, Pong-Wong R, Villanueva B, Woolliams JA. The impact of genetic architecture on genome-wide evaluation methods. Genetics 2010; 185: 1021-1031. doi: 10.1534/genetics.110.116855 PMID: 20407128
27. Daetwyler HD, Calus MP, Pong-Wong R, de Los Campos G, Hickey JM. Genomic prediction in animals and plants: simulation of data, validation, reporting, and benchmarking. Genetics 2013; 193: 347-365. doi: 10.1534/genetics.112.147983 PMID: 23222650
28. de los Campos G, Hickey JM, Pong-Wong R, Daetwyler HD, Calus MP. Whole-genome regression and prediction methods applied to plant and animal breeding. Genetics 2013; 193: 327-345. doi: 10.1534/genetics.112.143313 PMID: 22745228
29. Gianola D. Priors in whole-genome regression: the bayesian alphabet returns. Genetics 2013; 194: 573-596. doi: 10.1534/genetics.113.151753 PMID: 23636739
30. Shen X, Alam M, Fikse F, Ronnegard L. A novel generalized ridge regression method for quantitative genetics. Genetics 2013; 193: 1255-1268. doi: 10.1534/genetics.112.146720 PMID: 23335338
31. Makowsky R, Pajewski NM, Klimentidis YC, Vazquez AI, Duarte CW, Allison DB, et al. Beyond missing heritability: Prediction of complex traits. PLoS Genet. 2011, 7: e1002051. doi: 10.1371/journal.pgen.1002051 PMID: 21552331
32. Zhang Z, Liu J, Ding X, Bijma P, de Koning DJ, Zhang Q. Best linear unbiased prediction of genomic breeding values using a trait-specific marker-derived relationship matrix. PLoS One 2010; 5: e12648. doi: 10.1371/journal.pone.0012648 PMID: 20844593
33. Hill WG, Goddard ME, Visscher PM. Data and theory point to mainly additive genetic variance for complex traits. PLoS Genet. 2008; 4: e1000008. doi: 10.1371/journal.pgen.1000008 PMID: 18454194
34. Mackay TFC. Epistasis and quantitative traits: using model organisms to study gene-gene interactions. Nat Rev Genet. 2014; 15: 22-33. doi: 10.1038/nrg3627 PMID: 24296533
35. Carlborg O, Jacobsson L, Ahgren P, Siegel P, Andersson L. Epistasis and the release of genetic variation during long-term selection. Nat Genet. 2006; 38: 418-420. PMID: 16532011
36. Kroymann J, Mitchell-Olds T. Epistasis and balanced polymorphism influencing complex trait variation. Nature 2005; 435: 95-98. PMID: 15875023
37. Steinmetz LM, Sinha H, Richards DR, Spiegelman JI, Oefner PJ, McCusker JH, et al. Dissecting the architecture of a quantitative trait locus in yeast. Nature 2002; 416: 326-330. PMID: 11907579
38. Sinha H, David L, Pascon RC, Clauder-Münster S, Krishnakumar S, Nguyen M, et al. Sequential elimination of major-effect contributors identifies additional quantitative trait loci conditioning high-temperature growth in yeast. Genetics 2008; 180: 1661-1670. doi: 10.1534/genetics.108.092932 PMID: 18780730
39. Stam LF, Laurie CC. Molecular dissection of a major gene effect on a quantitative trait: The level of alcohol dehydrogenase expression in Drosophila melanogaster. Genetics 1996; 144: 1559-1564. PMID: 8978044
40. Waddington CH. Canalization of development and genetic assimilation of acquired characters. Nature 1959; 183: 1654-1655. PMID: 13666847
41. Greene CS, Penrod NM, Williams SM, Moore JH. Failure to replicate a genetic association may provide important clues about genetic architecture. PLoS One 2009; 4: e5639. doi: 10.1371/journal.pone.0005639 PMID: 19503614
42. Zuk O, Hechter E, Sunyaev SR, Lander ES. The mystery of missing heritability: Genetic interactions create phantom heritability. Proc Natl Acad Sci USA 2012; 109: 1193-1198. doi: 10.1073/pnas.1119675109 PMID: 22223662
43. Kauffman SA. The Origins of Order. Oxford: Oxford University Press; 1993.
44. Phillips PC. Epistasis-the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet. 2008; 9: 855-867. doi: 10.1038/nrg2452 PMID: 18852697
45. Morgan TJ, Mackay TFC. Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster. Heredity 2006; 96: 232-242. PMID: 16404413
46. SAS Institute Inc. SAS 9.2 Help and Documentation. Cary: Statistical Analysis Software; 2013.
47. Lippert C, Listgarten J, Liu Y, Kadie CM, Davidson RI, Heckerman D. FaST linear mixed models for genome-wide association studies. Nat Methods 2011; 8: 833-835. doi: 10.1038/nmeth.1681 PMID: 21892150
48. Stone EA. Joint genotyping on the fly: identifying variation among a sequenced panel of inbred lines. Genome Res. 2012; 22: 966-974. doi: 10.1101/gr.129122.111 PMID: 22367192
49. Cingolani P, Platts A, Coon M, Nguyen T, Wang L, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 2012; 6: 80-92. doi: 10.4161/fly.19695 PMID: 22728672
50. McQuilton P, St. Pierre SE, Thurmond J, The FlyBase Consortium. FlyBase 101-the basics of navigating FlyBase. Nucleic Acids Res. 2012; 40: D706-714. doi: 10.1093/nar/gkr1030 PMID: 22127867
51. R Core Team. R: A language and environment for statistical computing. 2013; R Foundation for Statistical Computing. Available: http://www.R-project.org/.
52. Stone M. Cross-validation choice and assessment of statistical predictions. J Roy Statist Soc B. 1974; 36: 111-147.
53. Stone M. An asymptotic equivalence of choice of model by cross-validation and Akaike's criterion. J Roy Statist Soc B. 1977; 39: 44-47.
54. Allen D. The relationship between variable selection and data augmentation and a method of prediction. Technometrics 1977; 16: 125-127.
55. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007; 81: 559-575. PMID: 17701901
56. Schüpbach T, Xenarios I, Bergmann S, Kapur K. FastEpistasis: a high performance computing solution for quantitative trait epistasis. Bioinformatics 2010; 26: 1468-1469. doi: 10.1093/bioinformatics/btq147 PMID: 20375113