WHY EPISTASIS IS IMPORTANT FOR SELECTION AND ADAPTATION
Version of Record online: 12 AUG 2013
© 2013 The Author(s). Evolution © 2013 The Society for the Study of Evolution.
Volume 67, Issue 12, pages 3501–3511, December 2013
How to Cite
Hansen, T. F. (2013), WHY EPISTASIS IS IMPORTANT FOR SELECTION AND ADAPTATION. Evolution, 67: 3501–3511. doi: 10.1111/evo.12214
- Issue online: 2 DEC 2013
- Version of Record online: 12 AUG 2013
- Accepted manuscript online: 26 JUL 2013 09:01AM EST
- Manuscript Accepted: 4 JUL 2013
- Manuscript Received: 25 MAR 2013
- 2007. A unified model for functional and statistical epistasis and its application in quantitative trait loci analysis. Genetics 176:1151–1167. , and .
- 2011. Multiallelic models of genetic effects and variance decomposition in non-equilibrium populations. Genetica 139:119–1134. , and .
- 2012a. Estimation and interpretation of genetic effects with epistasis using the NOIA model. Methods Mol. Biol. 871:191–204. , , and .
- 2012b. Modeling of genetic interactions improves prediction of hybrid patterns—a case study in domestic fowl. Genet. Res. Camb. 94:255–266. , , , , and .
- 2006. Unresolved boundaries of evolutionary theory and the question of how inheritance systems evolve: 75 years of debate on the evolution of dominance. J. Exp. Zool. 306B:329–359.
- 2012. The limits to parapatric speciation: Dobzhansky–Muller incompatibilities in a continent-island model. Genetics 191:845–863. , , and .
- 1995. A general model for the evolution of recombination. Genet. Res. 65:123–144.
- 2001. The role of hybridization in evolution. Mol. Ecol. 10:551–568. .
- 1989. Evolutionary quantitative genetics: how little do we know? Ann. Rev. Genet. 23:337–370. , and .
- 2004. Effects of genetic drift on variance components under a general model of epistasis. Evolution 58:2111–2132. , and .
- 2000. The evolution of genetic architectures and the divergence of natural populations. Pp. 245–263 in J. B. Wolf, E. D. Broodie, and M. J. Wade eds. Epistasis and the evolutionary process. Oxford Univ. Press, Oxford, U.K. , and .
- 2005. Epistasis underlying a fitness trait within a natural population of the pitcher-plant mosquito, Wyeomyia smithii. Genetics 169:485–488. , , and .
- 1980. The mathematical theory of quantitative genetics. Claredon, Oxford, U.K.
- 2000. The mathematical theory of selection, recombination, and mutation. Wiley, Chichester, U.K.
- 2000. Perspective: sex, recombination, and the efficacy of selection—was Weismann right? Evolution 54:337–351.
- 1995. Muller's ratchet, epistasis and mutation effects. Genetics 141:431–437.
- 2006. Epistasis and the release of genetic variation during long-term selection. Nat. Genet. 38:418–420. , , , , and .
- 2007. Brave new world: the epistatic foundations of natives adapting to invaders. Genetica 129:193–204.
- 2005. The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theor. Popul. Biol. 68:179–196. , , and .
- 1990. Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet. Res. 55:199–221.
- 1998. The effect of synergistic epistasis on the inbreeding load. Genet. Res. 71:85–89. .
- 1995. Epistasis and its contribution to genetic variance components. Genetics 139:1455–1461. , and .
- 1996. Epistasis as a source of increased additive genetic variance at population bottlenecks. Evolution 50:1042–1051. , and .
- 1954. An extension of the concept of partitioning hereditary variance for analysis of covariances among relatives when epistasis is present. Genetics 39:859–882.
- 2008. Maintaining evolvability. J. Genet. 87:349–353.
- 2010. On epistasis: why it is unimportant in polygenic directional selection. Philos. Trans. R. Soc. B 365:1241–1244. .
- 1970. An introduction to population genetics theory. Harper & Row, New York, NY. , and .
- 2005. On the theoretical and empirical framework for studying genetic interactions within and among species. Am. Nat. 165:524–536. , and .
- 1996. Introduction to quantitative genetics. 4th ed. Longman, Harlow, U.K. , and .
- 1965. The effect of linkage on directional selection. Genetics 52:349–363.
- 2000. The contribution of epistasis to the evolution of natural populations: a case study of an annual plant. Pp. 232–244 in J. B. Wolf, E. D. Broodie, and M. J. Wade eds. Epistasis and the evolutionary process. Oxford Univ. Press, Oxford, U.K. ., and
- 2010. Genetic architecture and post-zygotic reproductive isolation: evolution of Bateson-Dobzhansky-Muller incompatibilities in a polygenic model. Evolution 64:675–693. , and .
- 1918. The correlation between relatives on the supposition of Mendelian inheritance. Trans. R. Soc. Edinburgh 3:399–433.
- 2005. The evolutionary genetics of canalization. Quart. Rev. Biol. 80:287–316.
- 2009. Genetic architecture of quantitative traits in mice, flies, and humans. Genome Res. 19:723–733. , and .
- 1997. Impact of dominance and epistasis on the genetic make-up of simulated populations under selection: a model development. J. Anim. Breed. Genet. 114:165–175. , , , and .
- 1993. Equilibria in an epistatic viability model under arbitrary strength of selection. J. Math. Biol. 31:397–410.
- 2004. Fitness landscapes and the origin of species. Princeton Univ. Press, Princeton, NJ.
- 1989. Genotypic variation for a quantitative character maintained under stabilizing selection without mutations: epistasis. Genetics 123:217–227.
- 2011. Order-preserving principles underlying genotype-phenotype maps ensure high additive proportions of genetic variance. J. Evol. Biol. 24:2269–2279. , , , and .
- 1960. Theoretical consequences of truncation selection based on the individual phenotype. Aust. J. Biol. Sci. 13:307–343.
- 1961. Accommodation of gene-chromosome configuration effects in quantitative inheritance and selection theory. Aust. J. Biol. Sci. 14:402–414. .
- 1987. On the effect of founder events on the epistatic genetic variance. Evolution 41:80–91.
- 1988. Epistasis and the effect of founder events on the additive genetic variance. Evolution 42:441–454. .
- 2007. Compensatory vs. pseudocompensatory evolution in molecular and developmental interactions. Genetica 129:45–55.
- 2007. The effect of non-additive genetic interactions on selection in multi-locus genetic models. Heredity 98:349–359. , and .
- 2006. The evolution of genetic architecture. Annu. Rev. Ecol. Evol. Syst. 37:123–157.
- 2011. Epigenetics: adaptation or contingency? Pp. 357–376 in B. Hallgrimsson, and B. K. Hall eds. Epigenetics: linking genotype and phenotype in development and evolution. University of California Press, Berkeley, CA. .
- 2001a. Modeling genetic architecture: a multilinear theory of gene interaction. Theor. Popul. Biol. 59:61–86. , and .
- 2001b. Epistasis and the mutation load: a measurement-theoretical approach. Genetics 158:477–485. , and .
- 2011. Heritability is not evolvability. Evol. Biol. 38:258–277. , , and .
- 2006. Evolution of genetic architecture under directional selection. Evolution 60:1523–1536. , , , , and .
- 2003 Epistasis in polygenic traits and the evolution of genetic architecture under stabilizing selection. Am. Nat. 161:708–734. , , and .
- 2008. Data and theory point to mainly additive genetic variance for complex traits. PLoS Genet. 4:e100008:1–10. , , and .
- 2011. Measurement and meaning in biology. Quart. Rev. Biol. 86:3–34. , , , and .
- 2013. Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proc. Natl. Amer. Sci: In press. , , , , , , , , , , et al.
- 2003. Selection dynamics and limits under additive x additive epistastic gene action. Crop Sci. 43:489–497.
- 2009. Overview of QTL detection in plants and tests for synergistic epistatic interactions. Genetica 136:225–236. , , , and .
- 2000. Gene interaction and the origins of species. Pp. 197–212 in J. B. Wolf, E. D. Broodie, and M. J. Wade eds. Epistasis and the evolutionary process. Oxford Univ. Press, Oxford, U.K.
- 1975. General two-locus selection models: some objectives, results, and interpretations. Theor. Pop. Biol. 7:364–398.
- 1993. The origins of order. Self-organization and selection in evolution. Oxford Univ. Press, Oxford, U.K.
- 2000. The evolution of genetic canalization under fluctuating selection. Evolution 54:1–12.
- 1996. Metabolic models in selection response. J. Theor. Biol. 182:311–316.
- 2005. Epistasis in monkey flowers. Genetics 171:1917–1931.
- 1954. The correlation between relatives in a random mating population. Proc. R. Soc. Lond. B 143:103–113.
- 1956. A model of a genetic system which leads to closer linkage by natural selection. Evolution 10:278–287.
- 1965. Attainment of quasi linkage equilibrium when gene frequencies are changing by natural selection. Genetics 52:875–890. .
- 1966. The mutational load with epistatic gene interactions in fitness. Genetics 54:1337–1351. , and .
- 1988. Deleterious mutations and the evolution of sexual reproduction. Nature 336:435–440.
- 2008. Dissection of the genetic architecture of body weight in chicken reveals the impact of epistasis on domestication traits. Genetics 179:1591–1599. , , and .
- 2011. A modeling framework for the analysis of artificial-selection time series. Genet. Res. 93:155–173. , , and .
- 2013. The evolution of canalization and evolvability in stable and fluctuating environments. Evol. Biol. 40:317–340. , , and .
- 1974. The genetic basis of evolutionary change. Columbia, NY.
- 1960. The evolutionary dynamics of complex polymorphisms. Evolution 14:458–472. , and .
- 1998. Genetics and analysis of quantitative characters. Sinauer, Sunderland, MA. , and .
- 1995. Mutational meltdowns in sexual populations. Evolution 49:1067–1080. , , and .
- 2005. QTL-based evidence for the role of epistasis in evolution. Genet. Res. 86:89–95. , and .
- 1978. The evolution of sex. Cambridge Univ. Press, Cambridge, U.K.
- 2005. Biological vs. statistical epistasis. BioEssays 12:637–646. , and .
- 1994. Genetic architecture, genetic behavior, and character evolution. Ann. Rev. Ecol. Syst. 25:31–45.
- 1983. Effect of linkage disequilibrium of selection for a quantitative character with epistasis. Theor. Appl. Genet. 65:25–30. , and .
- 1992. Introduction to theoretical population genetics. Springer, Berlin, Germany.
- 1993. The evolution of multilocus systems under weak selection. Genetics 134:627–47. .
- 1995. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139:1805–1813.
- 2001. The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55:1085–1094. , and .
- 2001. Selection for recombination in small populations. Evolution 55:1921–1931. , and .
- 2010. Directionality of epistasis in a murine intercross population. Genetics 185:1489–1505. , , , , and .
- 2011. Evolution of pleiotropy: epistatic interaction pattern supports a mechanistic model underlying variation in genotype-phenotype map. J. Exp. Zool. (Mol. Dev. Evol.) 316B:371–385. , , , and .
- 2008. Epistasis—the essential role of gene interactions in the structure and evolution of genetic systems. Nat. Rev. Genet. 9:855–867.
- 1998. The evolution of canalization and the breaking of von Baer's laws: modeling the evolution of development with epistasis. Evolution 52:647–656.
- 2002 A general population genetic theory for the evolution of developmental interactions. Proc. Natl. Amer. Sci. 99:15518–15523. .
- 2004. Developmental associations between traits: covariance and beyond. Genetics 166:513–526. .
- 1999. Transgressive segregation, adaptation and speciation. Heredity 83:363–372. , , and .
- 2012. The QTN program and the alleles that matter for evolution: all that's gold does not glitter. Evolution 66:1–17.
- 1997. Evolutionary quantitative genetics. Chapman & Hall, New York, NY.
- 2008. Genetic architecture of complex traits: large phenotypic effects and pervasive epistasis. PNAS 105:19910–19914. , , , , , , , , , et al.
- 2012. Using known QTLs to detect directional epistatic interactions. Genet. Res. 94:39–48. , and .
- 1981. Mechanisms of speciation—a population genetics approach. Ann. Rev. Ecol. Syst. 12:23–48.
- 2000. Epistasis and complex traits. Pp. 41–57 in J. B. Wolf, E. D. Broodie, and M. J. Wade eds. Epistasis and the evolutionary process. Oxford Univ. Press, Oxford, U.K. .
- 1984. Heritable genetic variation via mutation-selection balance: Lerch's Zeta meets the abdominal bristle. Theor. Popul. Biol. 25:138–193.
- 1994. Genetic and statistical analyses of strong selection on polygenic traits: what, me normal? Genetics 138:913–941. , and .
- 2006. Will population bottlenecks and multilocus epistasis increase additive genetic variance? Evolution 60:1763–1776. .
- 2003. Effects of genetic background on response to selection in experimental populations of Arabidopsis thaliana. Genetics 163:277–286. , , and .
- 2005. Robustness and evolvability in living systems. Princeton Univ. Press, Princeton, NJ.
- 2010. The measurement theory of fitness. Evolution 64:1358–1376.
- 1997. A population genetic theory of canalization. Evolution 51:329–347. , , and .
- 1998. Genetic measurement theory of epistatic effects. Genetica 102/103:569–580. , , and .
- 2005. The rank ordering of genotypic fitness values predicts genetic constraint on natural selection on landscapes lacking sign epistasis. Genetics 171:1397–1405.
- 2005. Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:1165–1174. , , and .
- 1995. Multiple fitness peaks and epistasis. Ann. Rev. Ecol. Syst. 26:601–629. , , , and .
- Wolf, J. B., E. D. III Broodie, and M. J. Wade eds. 2000. Epistasis and the evolutionary process. Oxford Univ. Press, Oxford, U.K.
- 1969. Evolution and the genetics of populations. Vol. 2: The theory of gene frequencies. Chicago Univ. Press, Chicago, IL.
- 1977. Evolution and the genetics of populations. Vol. 3: Experimental results and evolutionary deductions. Chicago Univ. Press, Chicago, IL. .
- 1967. Computer simulation of directional selection in large populations II. The additive x additive and mixed model. Genetics 56:73–87.
- 2008. Long-term adaptation of epistatic genetic networks. Evolution 62:2215–2235. , , , and .
- 1992. Quantitative variability and multilocus polymorphism under epistatic selection. Theor. Popul. Biol. 42:254–283. , and .
- 2012. The mystery of missing heritability: Genetic interactions create phantom heritability. Proc. Natl. Amer. Sci. 109:1193–1198. , , , and .
- 2011. Complex genetic architecture of Drosophila aggressive behavior. Proc. Natl. Amer. Sci. 108:17070–17075. , , , , , , , and .
Associate Editor: I. Gordo