Epistasis for Fitness-Related Quantitative Traits in Arabidopsis thaliana Grown in the Field and in the Greenhouse

The extent to which epistasis contributes to adaptation, population differentiation, and speciation is a long-standing and important problem in evolutionary genetics. Using recombinant inbred (RI) lines of Arabidopsis thaliana grown under natural field conditions, we have examined the genetic architecture of fitness-correlated traits with respect to epistasis; we identified both single-locus additive and two-locus epistatic QTL for natural variation in fruit number, germination, and seed length and width. For fruit number, we found seven significant epistatic interactions, but only two additive QTL. For seed germination, length, and width, there were from two to four additive QTL and from five to eight epistatic interactions. The epistatic interactions were both positive and negative. In each case, the magnitude of the epistatic effects was roughly double that of the effects of the additive QTL, varying from −41% to +29% for fruit number and from −5% to +4% for seed germination, length, and width. A number of the QTL that we describe participate in more than one epistatic interaction, and some loci identified as additive also may participate in an epistatic interaction; the genetic architecture for fitness traits may be a network of additive and epistatic effects. We compared the map positions of the additive and epistatic QTL for germination, seed width, and seed length from plants grown in both the field and the greenhouse. While the total number of significant additive and epistatic QTL was similar under the two growth conditions, the map locations were largely different. We found a small number of significant epistatic QTL × environment effects when we tested directly for them. Our results support the idea that epistatic interactions are an important part of natural genetic variation and reinforce the need for caution in comparing results from greenhouse-grown and field-grown plants.

[1]  J. Cheverud,et al.  GENE EFFECTS ON A QUANTITATIVE TRAIT: TWO‐LOCUS EPISTATIC EFFECTS MEASURED AT MICROSATELLITE MARKERS AND AT ESTIMATED QTL , 1997, Evolution; international journal of organic evolution.

[2]  C. Goodnight EPISTASIS AND THE INCREASE IN ADDITIVE GENETIC VARIANCE: IMPLICATIONS FOR PHASE 1 OF WRIGHT'S SHIFTING‐BALANCE PROCESS , 1995, Evolution; international journal of organic evolution.

[3]  Thomas Mitchell-Olds,et al.  Epistasis and balanced polymorphism influencing complex trait variation , 2005, Nature.

[4]  L. Hurst Epistasis and the Evolutionary Process , 2000, Heredity.

[5]  R. Mauricio,et al.  QTL-based evidence for the role of epistasis in evolution. , 2005, Genetical research.

[6]  E. Lander,et al.  Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. , 1989, Genetics.

[7]  K. Chase,et al.  Epistat : a computer program for identifying and testing interactions between pairs of quantitative trait loci , 1997, Theoretical and Applied Genetics.

[8]  R. Mauricio Mapping quantitative trait loci in plants: uses and caveats for evolutionary biology , 2001, Nature Reviews Genetics.

[9]  M. Wade,et al.  PERSPECTIVE: THE THEORIES OF FISHER AND WRIGHT IN THE CONTEXT OF METAPOPULATIONS: WHEN NATURE DOES MANY SMALL EXPERIMENTS , 1998, Evolution; international journal of organic evolution.

[10]  D. Roze,et al.  Epistasis in RNA Viruses , 2004, Science.

[11]  N. Barton,et al.  A general model for the evolution of recombination. , 1995, Genetical research.

[12]  T. Mackay,et al.  Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. , 2002, Genetics.

[13]  N. Syed,et al.  Genetics of quantitative traits in Arabidopsis thaliana , 2003, Heredity.

[14]  T. Mackay,et al.  Quantitative trait loci for floral morphology in Arabidopsis thaliana. , 2000, Genetics.

[15]  Claus O. Wilke,et al.  Co-infection Weakens Selection Against Epistatic Mutations in RNA Viruses , 2004, Genetics.

[16]  Michael J. Wade,et al.  THE ONGOING SYNTHESIS: A REPLY TO COYNE, BARTON, AND TURELLI , 2000, Evolution; international journal of organic evolution.

[17]  Detlef Weigel,et al.  Quantitative trait loci controlling light and hormone response in two accessions of Arabidopsis thaliana. , 2002, Genetics.

[18]  L. Avery,et al.  Ordering gene function: the interpretation of epistasis in regulatory hierarchies. , 1992, Trends in genetics : TIG.

[19]  M. Daly,et al.  MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. , 1987, Genomics.

[20]  T. Mackay,et al.  Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. , 2003, Genetics.

[21]  M. Purugganan,et al.  Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[22]  S. Wright Evolution and the Genetics of Populations, Volume 3: Experimental Results and Evolutionary Deductions , 1977 .

[23]  Kirk A. Stowe,et al.  Epistasis and genotype-environment interaction for quantitative trait loci affecting flowering time in Arabidopsis thaliana , 2005, Genetica.

[24]  S. Otto,et al.  Evolution of sex: Resolving the paradox of sex and recombination , 2002, Nature Reviews Genetics.

[25]  C. Petropoulos,et al.  Evidence for Positive Epistasis in HIV-1 , 2004, Science.

[26]  M. Whitlock,et al.  GENE INTERACTION AFFECTS THE ADDITIVE GENETIC VARIANCE IN SUBDIVIDED POPULATIONS WITH MIGRATION AND EXTINCTION , 1993, Evolution; international journal of organic evolution.

[27]  A. Paterson,et al.  Mapping QTLs with epistatic effects and QTL×environment interactions by mixed linear model approaches , 1999, Theoretical and Applied Genetics.

[28]  R. Jansen,et al.  University of Groningen High Resolution of Quantitative Traits Into Multiple Loci via Interval Mapping , 2022 .

[29]  M. Toro,et al.  EPISTASIS AND THE TEMPORAL CHANGE IN THE ADDITIVE VARIANCE‐COVARIANCE MATRIX INDUCED BY DRIFT , 2004, Evolution; international journal of organic evolution.

[30]  GENETIC ARCHITECTURE OF A SELECTION RESPONSE IN ARABIDOPSIS THALIANA , 2003, Evolution; international journal of organic evolution.

[31]  Weller Ji Maximum likelihood techniques for the mapping and analysis of quantitative trait loci with the aid of genetic markers. , 1986 .

[32]  M. Wade,et al.  THE ONGOING SYNTHESIS: A REPLY TO COYNE, BARTON, AND TURELLI , 2000, Evolution; international journal of organic evolution.

[33]  J. Weller Maximum likelihood techniques for the mapping and analysis of quantitative trait loci with the aid of genetic markers. , 1986, Biometrics.

[34]  P. Phillips The language of gene interaction. , 1998, Genetics.

[35]  R. Amasino,et al.  FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering , 1999, Plant Cell.

[36]  J. D. de Visser,et al.  An experimental test for synergistic epistasis and its application in Chlamydomonas. , 1997, Genetics.

[37]  N. Barton,et al.  The exquisite corpse: a shifting view of the shifting balance , 2000 .

[38]  C. Lister,et al.  Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana , 1993 .

[39]  G. Churchill,et al.  A statistical framework for quantitative trait mapping. , 2001, Genetics.

[40]  M. Toro,et al.  Epistasis and the conversion of non-additive to additive genetic variance at population bottlenecks. , 2000, Theoretical population biology.

[41]  M. Rausher,et al.  EXPERIMENTAL MANIPULATION OF PUTATIVE SELECTIVE AGENTS PROVIDES EVIDENCE FOR THE ROLE OF NATURAL ENEMIES IN THE EVOLUTION OF PLANT DEFENSE , 1997, Evolution; international journal of organic evolution.

[42]  R. Lenski,et al.  Test of synergistic interactions among deleterious mutations in bacteria , 1997, Nature.

[43]  M. Wade A gene's eye view of epistasis, selection and speciation , 2002 .

[44]  A. Kondrashov,et al.  Multidimensional epistasis and the disadvantage of sex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Rafael Sanjuán,et al.  The contribution of epistasis to the architecture of fitness in an RNA virus. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[46]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[47]  J. Cheverud,et al.  EPISTASIS AND THE EVOLUTION OF ADDITIVE GENETIC VARIANCE IN POPULATIONS THAT PASS THROUGH A BOTTLENECK , 1999, Evolution; international journal of organic evolution.

[48]  T. Johnson,et al.  Quantitative trait loci affecting survival and fertility-related traits in Caenorhabditis elegans show genotype-environment interactions, pleiotropy and epistasis. , 1999, Genetics.

[49]  R. Doerge,et al.  Permutation tests for multiple loci affecting a quantitative character. , 1996, Genetics.

[50]  R. Malmberg The evolution of epistasis and the advantage of recombination in populations of bacteriophage T4. , 1977, Genetics.

[51]  Eric S. Lander,et al.  Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction fragment length polymorphisms , 1988, Nature.

[52]  M. Koornneef,et al.  The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type , 1994 .

[53]  R. Mauricio Costs of Resistance to Natural Enemies in Field Populations of the Annual Plant Arabidopsis thaliana , 1998, The American Naturalist.

[54]  M. Schläppi RNA Levels and Activity of FLOWERING LOCUS C Are Modified in Mixed Genetic Backgrounds of Arabidopsis thaliana , 2001, International Journal of Plant Sciences.

[55]  Z. Zeng Precision mapping of quantitative trait loci. , 1994, Genetics.

[56]  J. Cheverud,et al.  EPISTASIS AS A SOURCE OF INCREASED ADDITIVE GENETIC VARIANCE AT POPULATION BOTTLENECKS , 1996, Evolution; international journal of organic evolution.

[57]  EFFECTS OF GENETIC DRIFT ON VARIANCE COMPONENTS UNDER A GENERAL MODEL OF EPISTASIS , 2004, Evolution; international journal of organic evolution.

[58]  J. Cheverud,et al.  Epistasis affecting litter size in mice , 2004, Journal of evolutionary biology.

[59]  M. Wade,et al.  Epistasis and the Evolutionary Process , 2000 .

[60]  Jb Holland Computer note. EPISTACY: A SAS program for detecting two-locus epistatic interactions using genetic marker information , 1998 .

[61]  L. Rieseberg,et al.  Effects of genetic background on response to selection in experimental populations of Arabidopsis thaliana. , 2003, Genetics.

[62]  R. Doerge,et al.  Empirical threshold values for quantitative trait mapping. , 1994, Genetics.

[63]  T. Mackay,et al.  Genotype-environment interaction at quantitative trait loci affecting sensory bristle number in Drosophila melanogaster. , 1998, Genetics.