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Mutational effects on constraints on character evolution and phenotypic plasticity inArabidopsis thaliana

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Abstract

Although the concept of genetic constraints plays an important role in our understanding of the evolution of natural populations, there are still few empirical investigations probing the nature and limits of constraints in plant and animal species, aside from some studies inDrosophila. In the work reported here, we use an induced mutation - artificial selection protocol to analyse constraints on character means and phenotypic plasticity to nutrients inArabidopsis thaliana, an annual crucifer. We induced point mutations in a highly inbred line characterized by an extreme phenotype (very fast life cycle, early flowering, reduced leaf production) and little plasticity. We then selected individuals with increased leaf numbers. The goals were to determine if: (i) it is possible to increase leaf production; (ii) this has an effect on reproductive fitness; (iii) a mutation-selection process simultaneously alters the environmental insensitivity of the plant, thereby allowing phenotypic plasticity; and (iv) changes in the target trait affect other characters or their plasticities. The results demonstrate that: (a) mutations do increase leaf number; (b) this yields a much higher reproductive fitness, owing to the extension of the very short life cycle of the base inbred line; (c) there are no changes in plasticity of leaf number or of any other trait, possibly because few loci are involved in the control of plasticity; (d) changes in leaf number are related to alterations in three other traits comprising a strong set of covarying characters inA. thaliana. Two uncorrelated traits are capable of independent evolution from the constrained set. We therefore suggest that environmentally insensitive ecotypes of A.thaliana can quickly evolve to form ecologically specialized, relatively environmentally invariant genotypes.

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References

  • Aarssen L. W. and Clauss M. J. 1992 Genotypic variation in fecundity allocation inArabidopsis thaliana.J. Ecol. 80, 109–114.

    Article  Google Scholar 

  • Abbott R. J. and Gomes M. F. 1989 Population genetic structure and outcrossing rate ofArabidopsis thaliana (L.) Heynh.Heredity 62, 411–418.

    Article  Google Scholar 

  • Arnold S. J. 1992 Constraints on phenotypic evolution.Am. Nat. 140, S85-S107.

    Article  PubMed  Google Scholar 

  • Bradshaw A. D. 1965 Evolutionary significance of phenotypic plasticity in plants.Adv. Genet. 13, 115–155.

    Article  Google Scholar 

  • Cheverud J. M. 1988 The evolution of genetic correlation and developmental constraints. InPopulation genetics and evolution (ed. G. de Jong), pp. 94–101. Springer, Berlin.

    Google Scholar 

  • Clauss M. J. and Aarssen L. W. 1994a Patterns of reproductive effort inArabidopsis thaliana: confounding effects of size and developmental stage.Ecoscience 1, 153–159.

    Google Scholar 

  • Clauss M. J. and Aarssen L. W. 1994b Phenotypic plasticity of size-fecundity relationships inArabidopsis thaliana.J. Ecol. 82, 447–455.

    Article  Google Scholar 

  • Falconer D. S. 1952 The problem of environment and selection.Am. Nat. 86, 293–298.

    Article  Google Scholar 

  • Falconer D. S. 1990 Selection in different environments: effects on environmental sensitivity (reaction norm) and on mean performance.Genet. Res. 56, 57–70.

    Google Scholar 

  • Fry J. D., deRonde K. A. and Mackay T. F. C. 1995 Polygenic mutation inDrosophila melanogaster: genetic analysis of selection lines.Genetics 139, 1293–1307.

    PubMed  CAS  Google Scholar 

  • Fry J. D., Heinsohn S. L. and Mackay T. F. C. 1996 The contribution of new mutations to genotype-environment interaction for fitness inDrosophila melanogaster.Evolution 50, 2316–2327.

    Article  Google Scholar 

  • Gould S. J. 1980 The evolutionary biology of constraint.Daedalus 109, 39–52.

    Google Scholar 

  • Hempel F. D. and Feldman L. J. 1994 Bi-directional inflorescence development inArabidopsis thaliana: acropetal initiation of flowers and basipetal initiation of paraclades.Planta 192, 276–286.

    Article  Google Scholar 

  • Jones M. E. 1971 The population genetics ofArabidopsis thaliana. II. Population structure.Heredity 27, 51–58.

    Article  Google Scholar 

  • Keightley P. D. and Ohnishi O. 1998 EMS-induced polygenic mutation rates for nine quantitative characters inDrosophila melanogaster.Genetics 148, 753–766.

    PubMed  CAS  Google Scholar 

  • Koornneef M., Dellaert L. W. M. and Veen J. H. v. der 1982 EMS- and radiation-induced mutation frequencies at individual loci inArabidopsis thaliana (L.) Heynh.Mut. Res. 93, 109–123.

    CAS  Google Scholar 

  • Koufopanou V. and Bell G. 1991 Developmental mutants ofVolvox: does mutation recreate the patterns of phylogenetic diversity?Evolution 45, 1806–1822.

    Article  Google Scholar 

  • Mackay T. F. C., Fry J. D., Lyman R. F. and Nuzhdin S. V. 1994 Polygenic mutation inDrosophila melanogaster. estimates from response to selection of inbred strains.Genetics 136, 937–951.

    PubMed  CAS  Google Scholar 

  • Markwell J. and Osterman J. C. 1992 Occurrence of temperature-sensitive phenotypic plasticity in chlorophyll-deficient mutants ofArabidopsis thaliana.Plant Physiol. 98, 392–394.

    Article  PubMed  CAS  Google Scholar 

  • Maynard Smith J., Burian R., Kauffman S., Alberch P., Campbell J., Goodwin B., Lande R., Raup D. and Wolpert L. 1985 Developmental constraints and evolution.Q. Rev. Biol. 60, 265–287.

    Article  Google Scholar 

  • Napp-Zinn K. 1985Arabidopsis thaliana. InCRC handbook of flowering (ed. A. H. Halevy), pp. 492–503. CRC Press, Boca Raton.

    Google Scholar 

  • Oyama S. 1993 Constraints and development.Neth. J. Zool. 43, 6–16.

    Article  Google Scholar 

  • Pigliucci M. 1996 How organisms respond to environmental changes: from phenotypes to molecules (and vice versa).Trends Ecol. Evol. 11, 168–173.

    Article  Google Scholar 

  • Pigliucci M. and Byrd N. 1998 Genetics and evolution of phenotypic plasticity to nutrient stress inArabidopsis: drift, constraints or selection?Biol. J. Linn. Soc. 64, 17–40.

    Google Scholar 

  • Pigliucci M. and Schlichting C. D. 1995 Reaction norms ofArabidopsis (Brassicaceae). III. Response to nutrients in 26 populations from a worldwide collection.Am. J. Bot. 82, 1117–1125.

    Article  Google Scholar 

  • Pigliucci M. and Schlichting C. D. 1996 Reaction norms ofArabidopsis. IV. Relationships between plasticity and fitness.Heredity 76, 427–436.

    Article  PubMed  Google Scholar 

  • Pigliucci M. and Schlichting C. D. 1998 Reaction norms ofArabidopsis. V. Flowering time controls phenotypic architecture in response to nutrient stress.J. Evol. Biol. 11, 285–301.

    Article  Google Scholar 

  • Pigliucci M., Schlichting C. D. and Whitton J. 1995a Reaction norms ofArabidopsis. II. Response to stress and unordered environmental variation.Funct. Ecol. 9, 537–547.

    Article  Google Scholar 

  • Pigliucci M., Whitton J. and Schlichting C. D. 1995b Reaction normsof Arabidopsis. I. Plasticity of characters and correlations across water, nutrient and light gradients.J. Evol. Biol. 8, 421–438.

    Article  Google Scholar 

  • Redei G. P. 1992 A heuristic glance at the past ofArabidopsis genetics. InMethods in Arabidopsis research (ed. N. -H. C. C. Koncz and J. Schell), pp. 1–15. World Scientific, Singapore.

    Google Scholar 

  • Redei G. P. and Koncz C. 1992 Classical mutagenesis. InMethods in Arabidopsis research (ed. N.-H. C. C. Koncz and J. Schell), pp. 16–82. World Scientific, Singapore.

    Google Scholar 

  • Rice W. R. 1989 Analyzing tables of statistical tests.Evolution 43, 223–225.

    Article  Google Scholar 

  • SAS 1990SAS/STAT user’s guide. SAS Institute, Cary, NC, USA.

    Google Scholar 

  • Scheiner S. M. 1993 Genetics and evolution of phenotypic plasticity.Annu. Rev. Ecol. Syst. 24, 35–68.

    Article  Google Scholar 

  • Schlichting C. D. 1986 The evolution of phenotypic plasticity in plants.Annu. Rev. Ecol. Syst. 17, 667–693.

    Article  Google Scholar 

  • Schlichting C. D. and Levin D. A. 1986 Phenotypic plasticity: an evolving plant character.Biol. J. Linn. Soc. 29, 37–47.

    Article  Google Scholar 

  • Schlichting C. D. and Pigliucci M. 1993 Evolution of phenotypic plasticity via regulatory genes.Am. Nat. 142, 366–370.

    Article  CAS  PubMed  Google Scholar 

  • Schlichting C. D. and Pigliucci M. 1995 Gene regulation, quantitative genetics and the evolution of reaction norms.Evol. Ecol. 9, 154–168.

    Article  Google Scholar 

  • Schlichting C. D. and Pigliucci M 1998Phenotypic evolution: A reaction norm perspective. Sinauer, Sunderland, MA, USA.

    Google Scholar 

  • Sokal R. R. and Rohlf F. J. 1981Biometry. Freeman, New York.

    Google Scholar 

  • Sultan S. E. 1987 Evolutionary implications of phenotypic plasticity in plants.Evol. Biol. 21, 127–178.

    Google Scholar 

  • Sultan S. E. 1995 Phenotypic plasticity and plant adaptation.Acta Bot. Neerl. 44, 363–383.

    Google Scholar 

  • Thompson J. D. 1991 Phenotypic plasticity as a component of evolutionary change.Trends Ecol. Evol. 6, 246–249.

    Article  Google Scholar 

  • Thompson L. 1994 The spatiotemporal effects of nitrogen and litter on the population dynamics ofArabidopsis thaliana.J. Ecol. 82, 63–68.

    Article  Google Scholar 

  • van Tienderen P. H. 1991 Evolution of generalists and specialists in spatially heterogeneous environments.Evolution 45, 1317–1331.

    Article  Google Scholar 

  • van Tienderen P. H. and Koelewijn H. P. 1994 Selection on reaction norms, genetic correlations and constraints.Genet. Res. 64, 115–125.

    PubMed  Google Scholar 

  • van Tienderen P. H., Hammad I. and Zwaal F. C. 1996 Pleiotropic effects of flowering time genes in the annual cruciferArabidopsis thaliana (Brassicaceae).Am. J. Bot. 83, 169–174.

    Article  Google Scholar 

  • Via S. 1987 Genetic constraints on the evolution of phenotypic plasticity. InGenetic constraints on adaptive evolution (ed. V. Loeschcke), pp. 47–71. Springer, Berlin.

    Google Scholar 

  • Wagner G. P. 1995 Adaptation and the modular design of organisms. InAdvances in artificial life (ed. F. Moran, A. Moreno, J. J. Merelo and P. Chacon), pp. 317–328. Springer, Berlin.

    Google Scholar 

  • Wagner G. P. and Altenberg L. 1996 Complex adaptations and the evolution of evolvability.Evolution 50, 967–976.

    Article  Google Scholar 

  • Zhang J. and Lechowicz M. J. 1994 Correlation between time of flowering and phenotypic plasticity inArabidopsis thaliana (Brassicaceae).Am.J. Bot. 81, 1336–1342.

    Article  Google Scholar 

  • Zhang J. and Lechowicz M. J. 1995 Responses to CO2 enrichment by two genotypes ofArabidopsis thaliana differing in their sensitivity to nutrient availability.Ann. Bot. 75, 491–499.

    Article  Google Scholar 

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Authors and Affiliations

  1. Departments of Botany and of Ecology & Evolutionary Biology, University of Tennessee, 37996-1100, Knoxville, TN, USA

    Massimo Pigliucci

  2. Department of Ecology & Evolutionary Biology U-43, University of Connecticut, 06269, Storrs, CT, USA

    Gaines A. Tyler & Carl D. Schlichting

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  1. Massimo Pigliucci
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  2. Gaines A. Tyler
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  3. Carl D. Schlichting
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Correspondence to Massimo Pigliucci.

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Pigliucci, M., Tyler, G.A. & Schlichting, C.D. Mutational effects on constraints on character evolution and phenotypic plasticity inArabidopsis thaliana . J. Genet. 77, 95–103 (1998). https://doi.org/10.1007/BF02966595

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  • DOI: https://doi.org/10.1007/BF02966595

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