title: A synthetic framework for modeling the genetic basis of phenotypic plasticity and its costs.
abstract: The phenotype of an individual is controlled not only by its genes, but also by the environment in which it grows. A growing body of evidence shows that the extent to which phenotypic changes are driven by the environment, known as phenotypic plasticity, is also under genetic control, but an overall picture of genetic variation for phenotypic plasticity remains elusive. Here, we develop a model for mapping quantitative trait loci (QTLs) that regulate environment-induced plastic response. This model enables geneticists to test whether there exist actual QTLs that determine phenotypic plasticity and, if there are, further test how plasticity QTLs control the costs of plastic response by dissecting the genetic correlation of phenotypic plasticity and trait value. The model was used to analyze real data for grain yield of winter wheat (Triticum aestivum), leading to the detection of pleiotropic QTLs and epistatic QTLs that affect phenotypic plasticity and its cost in this crop.
authors.affiliation: Center for Computational Biology, Beijing Forestry University, Beijing, 100083, China.
authors.forename: Yi
authors.initials: Y
authors.lastname: Zhai
authors.affiliation: Center for Computational Biology, Beijing Forestry University, Beijing, 100083, China.
authors.forename: Yafei
authors.initials: Y
authors.lastname: Lv
authors.affiliation: Center for Computational Biology, Beijing Forestry University, Beijing, 100083, China.
authors.forename: Xin
authors.initials: X
authors.lastname: Li
authors.affiliation: Center for Computational Biology, Beijing Forestry University, Beijing, 100083, China.
authors.forename: Weimiao
authors.initials: W
authors.lastname: Wu
authors.affiliation: Center for Computational Biology, Beijing Forestry University, Beijing, 100083, China.
authors.forename: Wenhao
authors.initials: W
authors.lastname: Bo
authors.affiliation: Center for Computational Biology, Beijing Forestry University, Beijing, 100083, China.
authors.forename: Dengfeng
authors.initials: D
authors.lastname: Shen
authors.affiliation: Center for Computational Biology, Beijing Forestry University, Beijing, 100083, China.
authors.forename: Fang
authors.initials: F
authors.lastname: Xu
authors.affiliation: Center for Computational Biology, Beijing Forestry University, Beijing, 100083, China.
authors.forename: Xiaoming
authors.initials: X
authors.lastname: Pang
authors.affiliation: The Nurturing Station for the State Key Laboratory of Subtropical Silviculture, Zhejiang Agricultural and Forestry University, Lin'an, Zhejiang, 311300, China.
authors.forename: Bingsong
authors.initials: B
authors.lastname: Zheng
authors.affiliation: Center for Computational Biology, Beijing Forestry University, Beijing, 100083, China.|Center for Statistical Genetics, The Pennsylvania State University, Hershey, PA, 17033, USA.
authors.forename: Rongling
authors.initials: R
authors.lastname: Wu
mesh_terms: D002874:Chromosome Mapping / Q000379:methods; D004777:Environment; D004843:Epistasis, Genetic; D058685:Genetic Pleiotropy; D014644:Genetic Variation; D008957:Models, Genetic; D040641:Quantitative Trait Loci; D012639:Seeds; D014908:Triticum / Q000235:genetics*
keywords: epistasis; genetic mapping; phenotypic plasticity; plasticity cost; pleiotropy; quantitative trait locus (QTL); winter wheat
references.citation: Agraval AA. 2001. Phenotypic plasticity in the interactions and evolution of species. Science 294: 321-326.
references.citation: Auld JR, Agrawal AA, Relyea RA. 2009. Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proceedings of the Royal Society of London. Series B 277: 503-511.
references.citation: Baldwin JM. 1896. A new factor in evolution. American Naturalist 30: 441-451.
references.citation: Beldade P, Mateus RA, Keller RA. 2011. Evolution and molecular mechanisms of adaptive developmental plasticity. Molecular Ecology 20: 1347-1363.
references.citation: Callahan HS, Dhanoolal N, Ungerer MC. 2005. Plasticity genes and plasticity costs: a new approach using an Arabidopsis recombinant inbred population. New Phytologist 166: 129-140.
references.citation: Cheverud JM. 2000. Detecting epistasis among quantitative trait loci. Epistasis and the evolutionary process. New York, NY, USA: Oxford University Press.
references.citation: Cheverud JM, Routman EJ, Duarte F, van-Swinderen B, Cothran K, Perel C. 1996. Quantitative trait loci for murine growth. Genetics 142: 1305-1319.
references.citation: Churchill GA, Doerge RW. 1994. Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971.
references.citation: DeWitt TJ, Sih A, Wilson DS. 1998. Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution 13: 77-81.
references.citation: Fusco G, Minelli A. 2010. Phenotypic plasticity in development and evolution, facts and concepts. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365: 547-556.
references.citation: Lacaze X, Hayes PM, Korol A. 2009. Genetics of phenotypic plasticity: QTL analysis in barley, Hordeum vulgare. Heredity 102: 163-173.
references.citation: Lander ES, Botstein D. 1989. Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121: 185-199.
references.citation: Laperche A, Devienne-Barret F, Maury O, Le Gouis J, Ney B. 2006. A simplified conceptual model of carbon/nitrogen functioning for QTL analysis of winter wheat adaptation to nitrogen deficiency. TAG. Theoretical and Applied Genetics 113: 1131-1146.
references.citation: Le Gouis J, Beghin D, Heumez E, Pluchard P. 2000. Genetic differences for nitrogen uptake and nitrogen utilisation efficiencies in winter wheat. European Journal of Agronomy 12: 163-173.
references.citation: Li Q, Huang Z, Xu M, Wang C, Gai J, Huang Y, Pang X, Wu RL. 2010. Functional mapping of genotype-environment interactions for soybean growth by a semiparametric approach. Plant Methods 6: 13.
references.citation: Li Y, Álvarez OA, Gutteling EW, Tijsterman M, Fu J, Riksen JAG, Hazendonk E, Prins P, Plasterk RHA, Jansen RC et al. 2006. Mapping determinants of gene expression plasticity by genetical genomics in C. elegans. PLoS Genetics 2: e222.
references.citation: Ma C-X, Yu QB, Berg A, Fu GF, Yap JS, Tan AX, Kirst M, Cui YH, Wu RL. 2008. A statistical model for testing the pleiotropic control of phenotypic plasticity of a count trait. Genetics 179: 627-636.
references.citation: Nicoglou A. 2011. Defining the boundaries of development with plasticity. Biological Theory 6: 36-47.
references.citation: Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F. 2010. Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15: 684-692.
references.citation: Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP. 2010. Phenotypic plasticity's impacts on diversification and speciation. Trends in Ecology & Evolution 25: 459-467.
references.citation: Pigliucci M. 2005. Evolution of phenotypic plasticity: where are we going now? Trends in Ecology and Evolution 20: 481-486.
references.citation: Relyea RA. 2002. Costs of phenotypic plasticity. American Naturalist 159: 272-282.
references.citation: Routman EJ, Cheverud JM. 1997. Gene effects on a quantitative trait: two-locus epistatic effects measured at microsatellite markers and at estimated QTL. Evolution 51: 1654-1662.
references.citation: Scheiner SM. 1993. Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24: 35-68.
references.citation: Schlichting CD. 1986. The evolution of phenotypic plasticity in plants. Annual Review of Ecology and Systematics 17: 667-693.
references.citation: Schlichting CD, Smith H. 2002. Phenotypic plasticity: linking molecular mechanisms with evolutionary outcomes. Evolutionary Ecology 16: 189-211.
references.citation: Sommer RJ, Ogawa A. 2011. Hormone signaling and phenotypic plasticity in nematode development and evolution. Current Biology 21: R758-R766.
references.citation: Sultan SE. 2000. Phenotypic plasticity for plant development, function and life history. Trends in Plant Science 5: 537-542.
references.citation: Sultan SE. 2010. Plant developmental responses to the environment: eco-devo insights. Current Opinion in Plant Biology 13: 96-101.
references.citation: Ungerer MC, Halldorsdottir SS, Purugganan MD, Mackay TF. 2003. Genotype-environment interactions at quantitative trait loci affecting inflorescence development in Arabidopsis thaliana. Genetics 165: 353-365.
references.citation: Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH. 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology & Evolution 10: 212-217.
references.citation: Waddington CH. 1942. Canalization of development and the inheritance of acquired characters. Nature 150: 563-565.
references.citation: Wang Z, Pang X, Lv Y, Xu F, Zhou T, Li X, Feng S, Li J, Li Z, Wu RL. 2013. A dynamic framework for quantifying the genetic architecture of phenotypic plasticity. Briefings in Bioinformatics 14: 82-95.
references.citation: Ward JK, Samanta Roy D, Chatterjee I, Bone CR, Springer CJ, Kelly JK. 2012. Identification of a major QTL that alters flowering time at elevated [CO2] in Arabidopsis thaliana. PLoS ONE 7: e49028.
references.citation: West-Eberhard MJ. 2005. Developmental plasticity and the origin of species differences. Proceedings of the National Academy of Sciences, USA 102: 6543-6549.
references.citation: Wu RL. 1998. The detection of plasticity genes in heterogeneous environments. Evolution 52: 967-977.
references.citation: Wu RL, Lin M. 2006. Functional mapping - how to map and study the genetic architecture of dynamic complex traits. Nature Reviews Genetics 7: 229-237.
references.citation: Wu RL, Ma C-X, Casella G. 2007. Statistical genetics of quantitative traits: linkage, maps, and QTL. New York, NY, USA: Springer-Verlag.
references.citation: Yap JS, Li Y, Das K, Li JH, Wu RL. 2011. Functional mapping of reaction norms to multiple environmental signals through nonparametric covariance estimation. BMC Plant Biology 11: 23.
references.citation: Zheng BS, Le Gouis J, Leflon M, Rong WY, Laperche A, Brancourt-Hulmel M. 2010. Using probe genotypes to dissect QTL × environment interactions for grain yield components in winter wheat. TAG. Theoretical and Applied Genetics 121: 1501-1517.
references.citation: Zhou S, Campbell TG, Stone EA, Mackay TFC, Anholt RRH. 2012. Phenotypic plasticity of the Drosophila transcriptome. PLoS Genetics 8: e1002593.