Skip to main content
SpringerLink
Log in

Phenotypic plasticity of body size in a temperate population ofDrosophila melanogaster: When the temperature—size rule does not apply

  • Research Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

A natural population ofDrosophila melanogaster in southern France was sampled in three different years and 10 isofemale lines were investigated from each sample. Two size-related traits, wing and thorax length, were measured and the wing/thorax ratio was also calculated. Phenotypic plasticity was analysed after development at seven different constant temperatures, ranging from 12‡C to 31‡C. The three year samples exhibited similar reaction norms, suggesting a stable genetic architecture in the natural population. The whole sample (30 lines) was used to determine precisely the shape of each reaction norm, using a derivative analysis. The practical conclusion was that polynomial adjustments could be used in all cases, but with different degrees: linear for the wing/thorax ratio, quadratic for thorax length, and cubic for wing length. Both wing and thorax length exhibited concave reaction norms, with a maximum within the viable thermal range. The temperatures of the maxima were, however, quite different, around 15‡C for the wing and 19.5‡C for the thorax. Assuming that thorax length is a better estimate of body size, it is not possible to state that increasing the temperature results in monotonically decreasing size (the temperature-size rule), although this is often seen to be the case for genetic variations in latitudinal clines. The variability of the traits was investigated at two levels—within and between lines—and expressed as a coefficient of variation. The within-line (environmental) variability revealed a regular, quadratic convex reaction norm for the three traits, with a minimum around 21‡C. This temperature of minimum variability may be considered as a physiological optimum, while extreme temperatures are stressful. The between-line (genetic) variability could also be adjusted to quadratic polynomials, but the curvature parameters were not significant. Our results show that the mean values of the traits and their variance are both plastic, but react in different ways along a temperature gradient. Extreme low or high temperatures decrease the size but increase the variability. These effects may be considered as a functional response to environmental stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Angilletta M. J. and Dunham A. E. 2003 The temperature-size rule in ectotherms: simple evolutionary explanations may not be general.Am. Nat. 162, 332–342.

    Article  PubMed  Google Scholar 

  • Angilletta M. J., Steury T. S. and Sears M. W. 2004 Temperature growth rate and body size in ectotherms: fitting pieces of a life history puzzle.Integr. Comp. Biol. 44, 498–509.

    Article  Google Scholar 

  • Atkinson D. 1994 Temperature and organism size—a biological law for ectotherms?Adv. Ecol. Res. 25, 1–58.

    Article  Google Scholar 

  • Atkinson D. and Sibly R. M. 1997 Why are organisms usually bigger in colder environments? Making sense of a life history puzzle.Trends Ecol. Evol. 12, 235–239.

    Article  Google Scholar 

  • Azevedo R. B. R., James A. C., McCabe J. and Partridge L. 1998 Latitudinal variation of wing: thorax size ratio and wing-aspect ratio inDrosophila melanogaster.Evolution 52, 1353–1362.

    Article  Google Scholar 

  • Barker J. S. F. and Krebs R. A. 1995 Genetic variation and plasticity of thorax length and wing length inDrosophila aldrichi andD. buzzatii.J. Evol. Biol. 8, 689–709.

    Article  Google Scholar 

  • Bergmann C. 1847 Uber die VerhÄltnisse der WÄrmeökonomie der Thiere zu ihrer Grösse.Gött. Stud. 3, 595–708.

    Google Scholar 

  • Bijlsma R. and Loeschcke V. 1997Environmental stress, adaptation and evolution. BirkhÄuser, Basel.

    Google Scholar 

  • Blanckenhorn W. U. 2000 The evolution of body size: what keeps organisms small?Q. Rev. Biol. 75, 385–407.

    Article  PubMed  CAS  Google Scholar 

  • Blanckenhorn W. U. and Demont M. 2004 Bergmann and Converse Bergmann latitudinal clines in arthropods: two ends of a continuum?Integr. Comp. Biol. 44, 413–414.

    Article  Google Scholar 

  • Bochdanovits Z. and de Jong G. 2003a Temperature dependence of fitness components in geographical populations ofDrosophila melanogaster: changing the association between size and fitness.Biol. J. Linn. Soc. 80, 717–725.

    Article  Google Scholar 

  • Bochdanovits Z. and de Jong G. 2003b Temperature dependent larval resource allocation shaping adult body size inDrosophila melanogaster.J. Evol. Biol. 16, 1159–1167.

    Article  PubMed  CAS  Google Scholar 

  • Capy P., Pla E. and David J. R. 1993 Phenotypic and genetic variability of morphometrical traits in natural populations ofDrosophila melanogaster andD. simulans. I. Geographic variations.Genet. Sel. Evol. 25, 517–536.

    Article  Google Scholar 

  • Cavicchi S., Guerra D., Giorgi G. and Pezzoli C. 1985 Temperature related divergence in experimental populations ofDrosophila melanogaster. I. Genetic and developmental basis of wing size and shape variation.Genetics 109, 665–689.

    PubMed  Google Scholar 

  • Coyne J. A. and Beecham E. 1987 Heritability of two morphological characters within and among natural populations ofDrosophila melanogaster.Genetics 117, 727–737.

    PubMed  CAS  Google Scholar 

  • David J. R. and Capy P. 1988 Genetic variation ofDrosophila melanogaster natural populations.Trends Genet. 4, 106–111.

    Article  PubMed  CAS  Google Scholar 

  • David J. R. and Clavel M. F. 1965 Interaction entre le génotype et le milieu d’élevage. Conséquences sur les caractéristiques du développement de la Drosophile.Bull. Biol. Fr. Belg. 99, 369–378.

    Google Scholar 

  • David J. R. and Kitagawa O. 1982 Possible similarities in ethanol tolerance and latitudinal variations betweenDrosophila virilis andD. melanogaster.Jpn. J. Genet. 57, 89–95.

    Google Scholar 

  • David J. R., Moreteau B., Gauthier J. R., Pétavy G., Stockel J. and Imasheva A. 1994 Reaction norms of size characters in relation to growth temperature inDrosophila melanogaster. an isofemale lines analysis.Genet. Sel. Evol. 26, 229–251.

    Article  Google Scholar 

  • David J. R., Gibert P., Gravot E., Pétavy G., Morin J. P., Karan D. and Moreteau B. 1997 Phenotypic plasticity and developmental temperature inDrosophila: analysis and significance of reaction norms of morphometrical traits.J. Therm. Biol. 22, 441–451.

    Article  Google Scholar 

  • David J. R., Gibert P. and Moreteau B. 2004 Evolution of reaction norms. InPhenotypic plasticity: functional and conceptual approaches (ed. T. J. De Witt and S. M. Scheiner), pp. 50–63. Oxford University Press, New York.

    Google Scholar 

  • David J. R., Gibert P., Legout H., Capy P. and Moreteau B. 2005 Isofemale lines inDrosophila: an empirical approach to quantitative traits analysis in natural populations.Heredity 94, 3–12.

    Article  PubMed  CAS  Google Scholar 

  • Debat V. and David P. 2001 Mapping phenotypes: canalization, plasticity and developmental stability.Trends Ecol. Evol. 16, 555–561.

    Article  Google Scholar 

  • Delpuech J. M., Moreteau B., Chiche J., Pla E., Vouidibio J. and David J. R. 1995 Phenotypic plasticity and reaction norms in temperate and tropical populations ofDrosophila melanogaster. Ovarian size and developmental temperatures.Evolution 49, 670–675.

    Article  Google Scholar 

  • Falconer D. S. and Mackay T. F. C. 1996Introduction to quantitalive genetics. Longman, London.

    Google Scholar 

  • Gibert P. and de Jong G. 2001 Temperature dependence of development rate and adult size inDrosophila species: biophysical parameters.J. Therm. Biol. 14, 267–276.

    Google Scholar 

  • Gibert P., Moreteau B., Moreteau J. C. and David J. R. 1998a Genetic variability of quantitative traits inDrosophila melanogaster (fruit fly) natural populations: analysis of wild living flies and of several laboratory generations.Heredity 80, 326–335.

    Article  Google Scholar 

  • Gibert P., Moreteau B., David J. R. and Scheiner S. 1998b Describing the evolution of reaction norm shape: body pigmentation inDrosophila.Evolution 52, 1501–1506.

    Article  Google Scholar 

  • Gibert P., Capy P., Imasheva A., Moreteau B., Morin J. P., Pétavy G. and David J. R. 2004a Comparative analysis of morphometrical traits amongDrosophila melanogaster andD. simulons: genetic variability, clines and phenotypic plasticity.Genetica 120, 165–179.

    Article  PubMed  CAS  Google Scholar 

  • Gibert P., Moreteau B. and David J. R. 2004b Phenotypic plasticity of body pigmentation inDrosophila melanogaster. genetic repeatability of quantitative parameters in two successive generations.Heredity 92, 499–507.

    Article  PubMed  CAS  Google Scholar 

  • Gibson G. and Dworkin I. 2004 Uncovering cryptic genetic variation.Nat. Rev. Genet. 5, 681–690.

    Article  PubMed  CAS  Google Scholar 

  • Gilchrist A. S. and Partridge L. 1999 A comparison of the genetic basis of wing size divergence in three parallel body size clines ofDrosophila melanogaster.Genetics 153, 1775–1787.

    PubMed  CAS  Google Scholar 

  • Gilchrist A. S., Azevedo R. B., Partridge L. and O’Higgins P. 2000 Adaptation and constraint in the evolution ofDrosophila melanogaster wing shape.Evol. Dev. 2, 114–124.

    Article  PubMed  CAS  Google Scholar 

  • Harvey P. H. and Pagel M. D. 1991The comparative method in evolutionary biology. Oxford University Press, Oxford.

    Google Scholar 

  • Hoffmann A. A. and Hercus M. J. 2000 Environmental stress as an evolutionary force.Bioscience 50, 217–226.

    Article  Google Scholar 

  • Hoffmann A. A. and MerilÄ J. 1999 Heritable variation and evolution under favourable and unfavourable conditions.Trends Ecol. Evol. 14, 96–101.

    Article  PubMed  Google Scholar 

  • Hoffmann A. A. and Parsons P. A. 1997Extreme emnronmental change and evolution. Cambridge University Press, Cambridge.

    Google Scholar 

  • Houle D. 1992 Comparing evolvability and variability of quantitative traits.Genetics 130, 195–204.

    PubMed  CAS  Google Scholar 

  • Huey R. B., Gilchrist G. W., Carlson M. L., Berrigan D. and Serra L. 2000 Rapid evolution of a geographic cline in size in an introduced fly.Science 287, 308–309.

    Article  PubMed  CAS  Google Scholar 

  • Imasheva A. G., Bubli O. A. and Lazebny O. E. 1994 Variation in wing length in Eurasian natural populations ofDrosophila melanogaster.Heredity 72, 508–514.

    PubMed  Google Scholar 

  • Imasheva A. G., Loeschcke V., Zhivotovsky L. A. and Lazebny O. E. 1997 Effects of extreme temperatures on phenotypic variation and developmental stability inDrosophila melanogaster andD. buzzatii.Biol. J. Linn. Soc. 61, 117–126.

    Article  Google Scholar 

  • Imasheva A. G., Moreteau B. and David J. R. 2000 Growth temperature and genetic variability of wing dimensions inDrosophila: opposite trends in two sibling species.Genet. Res. 76, 237–247.

    Article  PubMed  CAS  Google Scholar 

  • James A. C., Azevedo R. B. and Partridge L. 1997 Genetic and environmental responses to temperature ofDrosophila melanogaster from a latitudinal cline.Genetics 146, 881–890.

    PubMed  CAS  Google Scholar 

  • Karan D., Munjal A. K., Gibert P., Moreteau B., Parkash R. and David J. R. 1998 Latitudinal clines for morphometrical traits inDrosophila kikkawai: a study of natural populations from the Indian subcontinent.Genet. Res.. 71, 31–38.

    Article  PubMed  CAS  Google Scholar 

  • Karan D., Morin J. P., Gravot E., Moreteau B. and David J. R. 1999 Body size reaction norms inDrosophila melanogaster: temporal stability and genetic architecture in a natural population.Genet. Sel. Evol. 31, 491–508.

    Article  Google Scholar 

  • Karan D., Dubey S., Moreteau B., Parkash R. and David J. R. 2000 Geographical clines for quantitative traits in natural populations of a tropical drosophilid:Zaprionus indianus.Genetica 108, 91–100.

    Article  PubMed  CAS  Google Scholar 

  • Misra R. K. and Reeve E. C. R. 1964 Clines in body dimensions in populations ofDrosophila subobscura.Genet. Res. 5, 240–256.

    Article  Google Scholar 

  • Moreteau B., Gibert P., Moreteau J. C., Huey R. B. and David J. R. 2003 Morphometrical evolution in aDrosophila clade: theDrosophila obscura group.J. Zool. Syst. Evol. Res. 41, 64–71.

    Article  Google Scholar 

  • Morin J. P., Moreteau B., Pétavy G. and David J. R. 1999 Divergence of reaction norms of size characters between tropical and temperate populations ofDrosophila melanogaster andD. simulans.J. Evol. Biol. 12, 329–339.

    Article  Google Scholar 

  • Noach E. J. K., de Jong G. and Scharloo W. 1996 Phenotypic plasticity in morphological traits in two populations ofDrosophila melanogaster.J. Evol. Biol. 9, 831–844.

    Article  Google Scholar 

  • Partridge L. and Coyne J. A. 1997 Bergmann’s rule in ectotherms: is it adaptative?Evolution 51, 632–635.

    Article  Google Scholar 

  • Prevosti A. 1955 Geographical variability in quantitative traits in populations ofDrosophila subobscura.Cold Spring Harbor Symp. Quant. Biol. 20, 294–299.

    PubMed  CAS  Google Scholar 

  • Pétavy G., Morin J. P., Moreteau B. and David J. R. 1997 Growth temperature and phenotypic plasticity in twoDrosophila sibling species: probable adaptive changes in flight capacities.J. Evol. Biol. 10, 875–887.

    Article  Google Scholar 

  • Pétavy G., David J. R., Gibert P. and Moreteau B. 2001 Viability and rate of development at different temperatures inDrosophila: a comparison of constant and alternating thermal regimes.J. Therm. Biol. 26, 29–39.

    Article  PubMed  Google Scholar 

  • Pétavy G., David J. R., Debat V, Gibert P. and Moreteau B. 2004 Specific effects of cycling stressful temperatures upon phenotypic and genetic variability of size traits inD. melanogaster.Evol. Ecol. Res. 6, 873–890.

    Google Scholar 

  • Peters R. H. 1983The ecological implications of body size. Cambridge University Press, Cambridge.

    Google Scholar 

  • Polak M. 2003Developmental instability: causes and consequences. Oxford University Press, Oxford.

    Google Scholar 

  • Reiss M. J. 1989The allometry of growth and reproduction. Cambridge University Press, Cambridge.

    Google Scholar 

  • Rutherford S. L. and Lindquist S. 1998 Hsp90 as a capacitor for morphological evolution.Nature 396, 336–342.

    Article  PubMed  CAS  Google Scholar 

  • Sokal R. R. and Rohlf F. J. 1995Biometry: the principles and practice of statistics in biological research, 3rd edition. Freeman, New York.

    Google Scholar 

  • Stalker H. D. 1980 Chromosome studies in wild populations ofDrosophila melanogaster. II. Relationship of inversion frequencies to latitude, season, wing-loading and flight activity.Genetics 95, 211–223.

    PubMed  Google Scholar 

  • Stalker H. D. and Carson H. L. 1947 Morphological variation in natural populations ofDrosophila robusta Sturtevant.Evolution 1, 237–248.

    Article  Google Scholar 

  • StatSoft (1999)Statistica Version 5.5. StatSoft, Inc., Tulsa, USA.

    Google Scholar 

  • van der Have T. M. and de Jong G. 1996 Adult size in ectotherms: temperature effects on growth and differentiation.J. Therm. Biol. 183, 329–340.

    Article  Google Scholar 

  • Van Voorhies W. A. 1996 Bergmann size clines: a simple explanation for their occurrence in ectotherms.Evolution 50, 1259–1264.

    Article  Google Scholar 

  • Zhang X. S. and Hill W. G. 2005 Evolution of the environment component of the phenotypic variance: stabilizing selection in changing environments and the cost of homogeneity.Evolution 59, 1237–1244.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire Populations, Génétique et Evolution, CNRS, 91198, Gif-sur-Yvette cedex, France

    Jean R. David, Héléne Legout & Brigitte Moreteau

Authors
  1. Jean R. David
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Héléne Legout
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brigitte Moreteau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean R. David.

Rights and permissions

Reprints and permissions

About this article

Cite this article

David, J.R., Legout, H. & Moreteau, B. Phenotypic plasticity of body size in a temperate population ofDrosophila melanogaster: When the temperature—size rule does not apply. J Genet 85, 9–23 (2006). https://doi.org/10.1007/BF02728965

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02728965

Keywords

Search

Navigation