title: Beyond the single gene: How epistasis and gene-by-environment effects influence crop domestication.
abstract: Domestication is a multifaceted evolutionary process, involving changes in individual genes, genetic interactions, and emergent phenotypes. There has been extensive discussion of the phenotypic characteristics of plant domestication, and recent research has started to identify the specific genes and mutational mechanisms that control domestication traits. However, there is an apparent disconnect between the simple genetic architecture described for many crop domestication traits, which should facilitate rapid phenotypic change under selection, and the slow rate of change reported from the archeobotanical record. A possible explanation involves the middle ground between individual genetic changes and their expression during development, where gene-by-gene (epistatic) and gene-by-environment interactions can modify the expression of phenotypes and opportunities for selection. These aspects of genetic architecture have the potential to significantly slow the speed of phenotypic evolution during crop domestication and improvement. Here we examine whether epistatic and gene-by-environment interactions have shaped how domestication traits have evolved. We review available evidence from the literature, and we analyze two domestication-related traits, shattering and flowering time, in a mapping population derived from a cross between domesticated foxtail millet and its wild progenitor. We find that compared with wild progenitor alleles, those favored during domestication often have large phenotypic effects and are relatively insensitive to genetic background and environmental effects. Consistent selection should thus be able to rapidly change traits during domestication. We conclude that if phenotypic evolution was slow during crop domestication, this is more likely due to cultural or historical factors than epistatic or environmental constraints.
authors.affiliation: Botany Department, Oklahoma State University, Stillwater, OK 74078.
authors.forename: Andrew N
authors.initials: AN
authors.lastname: Doust
authors.forename: Lewis
authors.initials: L
authors.lastname: Lukens
authors.forename: Kenneth M
authors.initials: KM
authors.lastname: Olsen
authors.forename: Margarita
authors.initials: M
authors.lastname: Mauro-Herrera
authors.forename: Ann
authors.initials: A
authors.lastname: Meyer
authors.forename: Kimberly
authors.initials: K
authors.lastname: Rogers
mesh_terms: D018556:Crops, Agricultural / Q000235:genetics*; D004843:Epistasis, Genetic; D035264:Flowers / Q000235:genetics / Q000502:physiology; D059647:Gene-Environment Interaction; D017343:Genes, Plant / Q000235:genetics*; D056426:Genetic Loci / Q000235:genetics; D010641:Phenotype; D019655:Quantitative Trait, Heritable
keywords: G × E; QTL; Setaria; domestication syndrome; genotype-by-environment interactions
references.citation: Mol Ecol. 2010 Aug;19(16):3271-84
references.pmid: 20584132
references.citation: Nat Genet. 2008 Jun;40(6):761-7
references.pmid: 18454147
references.citation: PLoS Genet. 2013 May;9(5):e1003477
references.pmid: 23671421
references.citation: Evolution. 1973 Jun;27(2):311-325
references.pmid: 28564784
references.citation: Breed Sci. 2012 Jun;62(2):178-85
references.pmid: 23136529
references.citation: Proc Natl Acad Sci U S A. 2009 Aug 25;106(34):14444-9
references.pmid: 19706531
references.citation: Theor Appl Genet. 2010 Nov;121(8):1455-64
references.pmid: 20617300
references.citation: Theor Appl Genet. 2005 Apr;110(6):1108-18
references.pmid: 15782297
references.citation: Science. 2006 Mar 31;311(5769):1886
references.pmid: 16574859
references.citation: Science. 2009 Aug 7;325(5941):714-8
references.pmid: 19661422
references.citation: Ann Bot. 2007 Nov;100(5):903-24
references.pmid: 17495986
references.citation: Nat Biotechnol. 2012 May 13;30(6):555-61
references.pmid: 22580951
references.citation: Nat Genet. 2011 Sep 25;43(11):1160-3
references.pmid: 21946354
references.citation: Trends Plant Sci. 2010 Sep;15(9):529-37
references.pmid: 20541451
references.citation: Nat Genet. 2012 May 13;44(6):720-4
references.pmid: 22581231
references.citation: Theor Popul Biol. 2005 Nov;68(3):179-96
references.pmid: 16122771
references.citation: Genome. 2007 Aug;50(8):757-66
references.pmid: 17893735
references.citation: Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3289-94
references.pmid: 17360640
references.citation: Plant Cell Physiol. 2011 May;52(5):738-49
references.pmid: 21389058
references.citation: Science. 2006 Mar 31;311(5769):1936-9
references.pmid: 16527928
references.citation: Annu Rev Plant Biol. 2013;64:47-70
references.pmid: 23451788
references.citation: J Exp Bot. 2010 Feb;61(4):935-44
references.pmid: 20067978
references.citation: Genetics. 1995 Mar;139(3):1455-61
references.pmid: 7768453
references.citation: Proc Natl Acad Sci U S A. 2012 Jul 10;109(28):E1913-21
references.pmid: 22711828
references.citation: Plant Cell. 2000 May;12(5):637-46
references.pmid: 10810140
references.citation: Nature. 1997 Apr 3;386(6624):485-8
references.pmid: 9087405
references.citation: Nat Genet. 2011 Feb;43(2):159-62
references.pmid: 21217756
references.citation: Mol Ecol. 2006 Apr;15(5):1335-49
references.pmid: 16626457
references.citation: Genetics. 1996 Aug;143(4):1807-17
references.pmid: 8844166
references.citation: Nat Genet. 2011 Feb;43(2):163-8
references.pmid: 21217757
references.citation: PLoS Genet. 2013 Feb;9(2):e1003295
references.pmid: 23509438
references.citation: Mol Ecol. 2012 Sep;21(18):4593-604
references.pmid: 22646149
references.citation: Genetics. 2010 Mar;184(3):799-812
references.pmid: 20008571
references.citation: J Exp Bot. 2012 Jul;63(12):4333-41
references.pmid: 22717409
references.citation: Front Plant Sci. 2013 Aug 01;4:290
references.pmid: 23914199
references.citation: Am J Bot. 2008 Feb;95(2):113-22
references.pmid: 21632337
references.citation: G3 (Bethesda). 2013 Feb;3(2):283-95
references.pmid: 23390604
references.citation: New Phytol. 2009 Nov;184(3):708-720
references.pmid: 19674325
references.citation: Genetics. 2002 Dec;162(4):1927-35
references.pmid: 12524360
references.citation: Genetics. 1995 Sep;141(1):333-46
references.pmid: 8536981
references.citation: Genes Genet Syst. 2010;85(4):265-71
references.pmid: 21178306
references.citation: Cell. 2006 Dec 29;127(7):1309-21
references.pmid: 17190597
references.citation: Evolution. 2011 Jan;65(1):171-83
references.pmid: 20666839
references.citation: Ann Bot. 2007 Nov;100(5):1009-15
references.pmid: 17638711
references.citation: Proc Natl Acad Sci U S A. 2008 Sep 16;105(37):13982-6
references.pmid: 18768818
references.citation: Nat Rev Genet. 2008 Nov;9(11):855-67
references.pmid: 18852697