EVIDENCE OF LOCAL ADAPTATION TO COARSE-GRAINED ENVIRONMENTAL VARIATION IN ARABIDOPSIS THALIANA

Abstract Plants can achieve an appropriate phenotype in particular conditions either constitutively or plastically, depending in part on the grain size of the environmental conditions being considered. Coarse-grained environmental variation should result in selection for local adaptation and no selection on plasticity to novel levels of the coarse-grained environmental factors. We tested the hypotheses that natural populations of the well-studied model system Arabidopsis thaliana are locally adapted to spatially coarse-grained environmental variation, and that the photoperiodic regime per se is at least partially responsible for that local adaptation, by exposing natural populations to photoperiodic regimes characteristic of their native and foreign (novel) environments. We also tested the hypothesis that plasticity to novel photoperiodic regimes should appear random. We found that populations showed evidence of local adaptation at a spatially coarse grain, although not to photoperiodic regime per se. We also found that the plasticities to novel photoperiodic regimes appeared random and did not generally show evidence of adaptive divergence. Our study highlights the need for caution in extrapolating from the finding of local adaptation to the causes of local adaptation.

[1]  T. Mitchell-Olds,et al.  Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis , 2006, Nature.

[2]  C. Dean,et al.  Arabidopsis, the Rosetta stone of flowering time? , 2002, Science.

[3]  E. M. Meyerowitz,et al.  Arabidopsis thaliana , 2022, CABI Compendium.

[4]  The Intraspecific Phylogenetics of Arabidopsis thaliana in Worldwide Populations , 2000 .

[5]  S. Sultan,et al.  Shade tolerance plasticity in response to neutral vs green shade cues in Polygonum species of contrasting ecological breadth. , 2005, The New phytologist.

[6]  Steven E. Jacobsen,et al.  Gardening the genome: DNA methylation in Arabidopsis thaliana , 2005, Nature Reviews Genetics.

[7]  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.

[8]  R. O’Hara,et al.  Bias and Precision in QST Estimates: Problems and Some Solutions , 2005, Genetics.

[9]  B. Frankland Perception of light quantity , 1986 .

[10]  S. A. Dudley THE RESPONSE TO DIFFERING SELECTION ON PLANT PHYSIOLOGICAL TRAITS: EVIDENCE FOR LOCAL ADAPTATION , 1996, Evolution; international journal of organic evolution.

[11]  M. Hoffmann,et al.  Analysis of molecular data of Arabidopsis thaliana (L.) Heynh. (Brassicaceae) with Geographical Information Systems (GIS) , 2003, Molecular ecology.

[12]  Rupert G. Miller The jackknife-a review , 1974 .

[13]  V. Corre Variation at two flowering time genes within and among populations of Arabidopsis thaliana: comparison with markers and traits , 2005 .

[14]  P. H. Tienderen GENERALISTS, SPECIALISTS, AND THE EVOLUTION OF PHENOTYPIC PLASTICITY IN SYMPATRIC POPULATIONS OF DISTINCT SPECIES , 1997 .

[15]  Bryan F. J. Manly,et al.  Randomization and regression methods for testing for associations with geographical, environmental and biological distances between populations , 1986, Researches on Population Ecology.

[16]  Ph. Van GENERALISTS, SPECIALISTS, AND THE EVOLUTION OF PHENOTYPIC PLASTICITY IN SYMPATRIC POPULATIONS OF DISTINCT SPECIES. , 1997 .

[17]  R. Macknight,et al.  It's time to flower: the genetic control of flowering time , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[18]  M. Moran Arguments for rejecting the sequential Bonferroni in ecological studies , 2003 .

[19]  J. Clausen,et al.  Effect of varied environments on western North American plants , 1940 .

[20]  G. Coupland,et al.  Time measurement and the control of flowering in plants. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[21]  H. Stenøien,et al.  Quantifying latitudinal clines to light responses in natural populations of Arabidopsis thaliana (Brassicaceae). , 2002, American journal of botany.

[22]  M. Hoffmann,et al.  Evidence for a large-scale population structure of Arabidopsis thaliana from genome-wide single nucleotide polymorphism markers , 2006, Theoretical and Applied Genetics.

[23]  R Gomulkiewicz,et al.  Adaptive phenotypic plasticity: consensus and controversy. , 1995, Trends in ecology & evolution.

[24]  R. Abbott,et al.  Population genetic structure and outcrossing rate of Arabidopsis thaliana (L.) Heynh. , 1989, Heredity.

[25]  C. Ballaré,et al.  Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. , 1999, Trends in plant science.

[26]  T. Sharbel,et al.  Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe , 2000, Molecular ecology.

[27]  R. Maurício,et al.  Neutral genetic variation among wild North American populations of the weedy plant Arabidopsis thaliana is not geographically structured , 2004, Molecular ecology.

[28]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[29]  P. Keddy,et al.  Competitive Effect and Response Rankings in 20 Wetland Plants: Are They Consistent Across Three Environments? , 1994 .

[30]  J. Gillespie Polymorphism in Patchy Environments , 1974, The American Naturalist.

[31]  David Tilman,et al.  Competition Among Grasses Along a Nitrogen Gradient: Initial Conditions and Mechanisms of Competition , 1993 .

[32]  O. Savolainen,et al.  Genetic variation at marker loci and in quantitative traits in natural populations of Arabidopsis Thaliana , 1997, Heredity.

[33]  K. Gross,et al.  Resource competition and suppression of plants colonizing early successional old fields , 1999, Oecologia.

[34]  S. Pickett,et al.  Role of resources and disturbance in the organization of an old-field plant community. , 1990 .

[35]  B. Schmid,et al.  Latitudinal population differentiation in two species of Solidago (Asteraceae) introduced into Europe. , 1998, American journal of botany.

[36]  O. Savolainen,et al.  Environmental and genetic effects on flowering differences between northern and southern populations of Arabidopsis lyrata (Brassicaceae). , 2004, American journal of botany.

[37]  A. Green,et al.  PLANT PERFORMANCE ACROSS LATITUDE: THE ROLE OF PLASTICITY AND LOCAL ADAPTATION IN AN AQUATIC PLANT , 2003 .

[38]  J. M. Westerman Genotype-environment interaction and developmental regulation in Arabidopsis thaliana II. Inbred lines; analysis , 1970, Heredity.

[39]  M. Pigliucci,et al.  Adaptive phenotypic plasticity: the case of heterophylly in aquatic plants , 2000 .

[40]  PLASTICITY TO LIGHT CUES AND RESOURCES IN ARABIDOPSIS THALIANA: TESTING FOR ADAPTIVE VALUE AND COSTS , 2000, Evolution; international journal of organic evolution.

[41]  B. Menge,et al.  Community Regulation: Variation in Disturbance, Competition, and Predation in Relation to Environmental Stress and Recruitment , 1987, The American Naturalist.

[42]  Mattias Jakobsson,et al.  The Pattern of Polymorphism in Arabidopsis thaliana , 2005, PLoS biology.

[43]  D. Tilman,et al.  Non-neutral patterns of species abundance in grassland communities. , 2005, Ecology letters.

[44]  EXPERIMENTAL DEMONSTRATION OF A CAUSAL RELATIONSHIP BETWEEN HETEROGENEITY OF SELECTION AND GENETIC DIFFERENTIATION IN QUANTITATIVE TRAITS , 2004, Evolution; international journal of organic evolution.

[45]  M. Pigliucci,et al.  Effects of gibberellin mutations on tolerance to apical meristem damage in Arabidopsis thaliana , 2005, Heredity.

[46]  M. Cruzan,et al.  Aerenchyma development and elevated alcohol dehydrogenase activity as alternative responses to hypoxic soils in the Piriqueta caroliniana complex. , 2007, American journal of botany.

[47]  H. Kudoh,et al.  Phenotypic plasticity in Cardamine flexuosa: variation among populations in plastic response to chilling treatments and photoperiods , 1995, Oecologia.

[48]  Genetic similarity among ecotypes of Arabidopsis thaliana estimated by analysis of restriction fragment length polymorphisms , 1993, Theoretical and Applied Genetics.

[49]  D. Tilman,et al.  PLANT COMPETITION AND RESOURCE AVAILABILITY IN RESPONSE TO DISTURBANCE AND FERTILIZATION , 1993 .

[50]  Johanna Schmitt,et al.  Testing the Adaptive Plasticity Hypothesis: Density-Dependent Selection on Manipulated Stem Length in Impatiens capensis , 1996, The American Naturalist.

[51]  O. Savolainen,et al.  Genetic variability in natural populations of Arabidopsis thaliana in northern Europe , 2004, Molecular ecology.

[52]  F. Chapin,et al.  Competitive Ability and Adaptation to Fertile and Infertile Soils in Two Eriophorum Species , 1989 .

[53]  C. Hardtke,et al.  Genetic similarity among Arabidopsis thaliana ecotypes estimated by DNA sequence comparison , 1996, Plant Molecular Biology.

[54]  Hudson R. DeYoe,et al.  ECOTYPIC DIVERGENCE IN ALPINE POLEMONIUM VISCOSUM: GENETIC STRUCTURE, QUANTITATIVE VARIATION, AND LOCAL ADAPTATION , 1991, Evolution; international journal of organic evolution.

[55]  M. Pigliucci,et al.  Comparative Studies of Evolutionary Responses to Light Environments in Arabidopsis , 2002, The American Naturalist.

[56]  M. Pigliucci Ecological and evolutionary genetics of Arabidopsis , 1998 .

[57]  J. Schmitt,et al.  ADAPTIVE DIVERGENCE IN PLASTICITY IN NATURAL POPULATIONS OF IMPATIENS CAPENSIS AND ITS CONSEQUENCES FOR PERFORMANCE IN NOVEL HABITATS , 2001, Evolution; international journal of organic evolution.

[58]  F. Bazzaz,et al.  Growth responses of rhizomatous plants to fertilizer application and interference , 1992 .

[59]  H. Kudoh,et al.  Phenotypic Variability in Life History Traits and Phenology of Field Populations of Cardamine flexuosa and C. fallax (Cruciferae) in Honshu, Japan , 1993 .

[60]  Genotype-environment interaction and developmental regulation in Arabidopsis thaliana I. Inbred lines; description , 1970, Heredity.

[61]  D. Tilman,et al.  DYNAMICS OF NITROGEN COMPETITION BETWEEN SUCCESSIONAL GRASSES , 1991 .

[62]  P. V. Tienderen,et al.  EVOLUTION OF GENERALISTS AND SPECIALISTS IN SPATIALLY HETEROGENEOUS ENVIRONMENTS. , 1991 .

[63]  E. H. Pyle,et al.  EVIDENCE OF ADAPTIVE DIVERGENCE IN PLASTICITY: DENSITY‐ AND SITE‐DEPENDENT SELECTION ON SHADE‐AVOIDANCE RESPONSES IN IMPATIENS CAPENSIS , 2000, Evolution; international journal of organic evolution.

[64]  J. Suzuki,et al.  Latitudinal variation in plant size and relative growth rate in Arabidopsis thaliana , 1998, Oecologia.

[65]  R. B. Jackson,et al.  Linking molecular insight and ecological research , 2002 .

[66]  R. Levins Theory of Fitness in a Heterogeneous Environment. II. Developmental Flexibility and Niche Selection , 1963, The American Naturalist.