Epistasis and natural selection shape the mutational architecture of complex traits

Nature Communications

Volumn 5, Issue , 2014, Pages

  Jones, Adam G ^a   Bürger, Reinhard ^b   Arnold, Stevan J ^c  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF VIENNA   (Austria)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPISTASIS; GENETIC VARIATION; MUTATION; NATURAL SELECTION;

ARTICLE; EPISTASIS; GENE INTERACTION; GENE MUTATION; GENETIC MODEL; GENETIC TRAIT; GENETIC VARIABILITY; HUMAN; MOLECULAR EVOLUTION; NATURAL SELECTION; NONHUMAN; POPULATION GENETICS; SIMULATION; BIOLOGICAL MODEL; COMPUTER SIMULATION; GENETIC SELECTION; GENOTYPE; MULTIFACTORIAL INHERITANCE; MUTATION; PHENOTYPE;

COMPUTER SIMULATION; EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOTYPE; HUMANS; MODELS, GENETIC; MULTIFACTORIAL INHERITANCE; MUTATION; PHENOTYPE; SELECTION, GENETIC;

EID: 84900862007     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4709     Document Type: Article

References (51)

1. Wagner, G. P. &Altenberg, L. Perspective: complex adaptations and the evolution of evolvability. Evolution 50, 967-976 (1996).
2. Wagner, G. P., Pavlic?ev, M. &Cheverud, J. M. The road to modularity. Nat. Rev. Genet. 8, 921-931 (2007). (Pubitemid 350129175)
3. Mackay, T. F. C., Stone, E. A. &Ayroles, J. F. The genetics of quantitative traits: challenges and prospects. Nat. Rev. Genet. 10, 565-577 (2009).
4. Plomin, R., Haworth, C. M. A. &Davis, O. S. P. Common disorders are quantitative traits. Nat. Rev. Genet. 10, 872-878 (2009).
5. Altshuler, D., Daly, M. J. &Lander, E. S. Genetic mapping in human disease. Science 322, 881-888 (2008).
6. Mackay, T. F. C. The genetic architecture of quantitative traits. Annu. Rev. Genet. 35, 303-339 (2001). (Pubitemid 34032979)
7. Manolio, T. A. et al. Finding the missing heritability of complex diseases. Nature 461, 747-753 (2009).
8. Zuk, O., Hechter, E., Sunyaev, S. R. &Lander, E. S. The mystery of missing heritability: genetic interactions create phantom heritability. Proc. Natl Acad. Sci. USA 109, 1193-1198 (2012).
9. Huang, W. et al. Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proc. Natl Acad. Sci. USA 109, 15553-15559 (2012).
10. Hill, W. G., Goddard, M. E. &Visscher, P. M. Data and theory point mainly to additive genetic variance for complex traits. PLoS Genet. 4, e1000008 (2008).
11. Yan, J. et al. Common SNPs explain a large proportion of the heritability for human height. Nat. Genet. 42, 565-569 (2010).
12. Hansen, T. F. Why epistasis is important for selection and adaptation. Evolution 67, 3501-3511 (2013).
13. Carmelli, D., Cardon, L. R. &Fabsitz, R. Clustering of hypertension, diabetes, and obesity in adult male twins-same genes or same environments? Am. J. Hum. Genet. 55, 566-573 (1994). (Pubitemid 24272411)
14. Lande, R. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33, 402-416 (1979).
15. Lande, R. The genetic covariance between characters maintained by pleiotropic mutations. Genetics 94, 203-215 (1980). (Pubitemid 10037870)
16. Houle, D. Genetic covariances of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45, 630-648 (1991).
17. Brodie, III E. D. Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46, 1284-1298 (1992). (Pubitemid 23398781)
18. Jones, A. G., Arnold, S. J. &Bu?rger, R. Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift. Evolution 57, 1747-1760 (2003). (Pubitemid 37096392)
19. Jones, A. G., Arnold, S. J. &Bu?rger, R. Evolution and stability of the G-matrix on a landscape with a moving optimum. Evolution 58, 1639-1654 (2004). (Pubitemid 39147697)
20. Jones, A. G., Arnold, S. J. &Bu?rger, R. The mutation matrix and the evolution of evolvability. Evolution 61, 727-745 (2007). (Pubitemid 46537647)
21. Kroymann, J. &Mitchell-Olds, T. Epistasis and balanced polymorphism influencing complex trait variation. Nature 435, 95-98 (2005). (Pubitemid 40655914)
22. Phillips, P. C. Epistasis-the essential role of gene interactions in the structure and evolution of genetic systems. Nat. Rev. Genet. 9, 855-867 (2008).
23. Barton, N. H. &Keightley, P. D. Understanding quantitative genetic variation. Nat. Rev. Genet. 3, 11-21 (2002). (Pubitemid 34506600)
24. Pavlic?ev, M. et al. Genetic variation in pleiotropy: differential epistasis as a source of variation in the allometric relationships between bone lengths and body weight. Evolution 62, 199-213 (2008).
25. Leamy, L. J., Pomp, D. &Lightfoot, J. T. Genetic variation in the pleiotropic association between physical activity and body weight in mice. Genet. Sel. Evol. 41, 41 (2009).
26. Zhivotovsky, L. A. &Gavrilets, S. Quantitative variability and multilocus polymorphism under epistatic selection. Theor. Pop. Biol. 42, 254-283 (1992). (Pubitemid 24408320)
27. Gavrilets, S. &de Jong, G. Pleiotropic models of polygenic variation, stabilizing selection, and epistasis. Genetics 134, 609-625 (1993). (Pubitemid 23156955)
28. Hansen, T. F. &Wagner, G. P. Modeling genetic architecture: a multilinear theory of gene interaction. Theor. Popul. Biol. 59, 61-68 (2001).
29. Carter, A. J. R., Hermisson, J. &Hansen, T. F. The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theor. Popul. Biol. 68, 179-196 (2005). (Pubitemid 41415590)
30. Le Rouzic, A., A? lvarez-Castro, J. M. &Hansen, T. F. The evolution of canalization and evolvability in stable and fluctuating environments. Evol. Biol. 40, 317-340 (2013).
31. Hermisson, J., Hansen, T. F. &Wagner, G. P. Epistasis in polygenic traits and the evolution of genetic architecture under stabilizing selection. Am. Nat. 161, 708-734 (2003). (Pubitemid 36619184)
32. Wagner, A. Does evolutionary plasticity evolve? Evolution 50, 1008-1023 (1996).
33. Wagner, A. Robustness and evolvability: a paradox resolved. Proc. R. Soc. B 275, 91-100 (2008). (Pubitemid 350146738)
34. Wagner, G. P., Booth, G. &Homayoun-Chaichian, H. A population genetic theory of canalization. Evolution 51, 329-347 (1997).
35. Rajon, E. &Masel, J. Compensatory evolution and the origin of innovations. Genetics 193, 1209-1220 (2013).
36. Bu?rger, R. The Mathematical Theory of Selection, Recombination, and Mutation (Wiley, 2000).
37. Hermisson, J. &Wagner, G. P. The population genetic theory of hidden variation and genetic robustness. Genetics 168, 2271-2284 (2004). (Pubitemid 40066360)
38. Bu?rger, R. Predictions of the dynamics of a polygenic character under directional selection. J. Theor. Biol. 162, 487-513 (1993).
39. Barton, N. H. &Turelli, M. Effects of genetic drift on variance components under a general model of epistasis. Evolution 58, 2111-2132 (2004). (Pubitemid 39448266)
40. Schluter, D. Adaptive radiation along genetic lines of least resistance. Evolution 50, 1766-1774 (1996). (Pubitemid 26394290)
41. Arnold, S. J., Jones, A. G. &Pfrender, M. E. The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica 112, 9-32 (2001). (Pubitemid 34119650)
42. Draghi, J. A., Parsons, T. L., Wagner, G. P. &Plotkin, J. B. Mutational robustness can facilitate adaptation. Nature 463, 353-355 (2010).
43. Masel, J. &Trotter, M. V. Robustness and evolvability. Trends Genet. 26, 406-414 (2010).
44. Hansen, T. F., A? lvarez-Castro, J. M., Carter, A. J. R., Hermisson, J. &Wagner, G. P. Evolution of genetic architecture under directional selection. Evolution 60, 1523-1536 (2006). (Pubitemid 44808247)
45. Fierst, J. L. &Hansen, T. F. Genetic architecture and postzygotic reproductive isolation: evolution of Bateson-Dobzhansky-Muller incompatibilities in a polygenic model. Evolution 64, 675-693 (2010).
46. Cheverud, J. M. et al. Pleiotropic effects on mandibular morphology II: differential epistasis and genetic variation in morphological integration. J. Exp. Zool. 302, 424-435 (2004). (Pubitemid 39428814)
47. Pavlic?ev, M., Cheverud, J. M. &Wagner, G. P. Evolution of adaptive phenotypic variation patterns by direct selection for evolvability. Proc. R. Soc. Lond. B 278, 1903-1912 (2011).
48. Turelli, M. &Barton, N. H. Will population bottlenecks and multilocus epistasis increase additive genetic variance? Evolution 60, 1763-1776 (2006). (Pubitemid 44808228)
49. Draghi, J. A. &Whitlock, M. C. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 66, 2891-2902 (2012).
50. Schwenk, K. &Wagner, G. P. Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes. (eds Pigliucci, M. &Preston, K.) 390-408 (Oxford Univ. Press, 2004).
51. Falconer, D. S. &Mackay, T. F. C. Introduction to Quantitative Genetics, 4th edn (Longman, 1996).