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Genetic variability of sexual size dimorphism in a natural population ofDrosophila melanogaster: An isofemale-line approach

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Abstract

Most animal species exhibit sexual size dimorphism (SSD). SSD is a trait difficult to quantify for genetical purposes since it must be simultaneously measured on two kinds of individuals, and it is generally expressed either as a difference or as a ratio between sexes. Here we ask two related questions: What is the best way to describe SSD, and is it possible to conveniently demonstrate its genetic variability in a natural population? We show that a simple experimental design, the isofemale-line technique (full-sib families), may provide an estimate of genetic variability, using the coefficient of intraclass correlation. We consider two SSD indices, the female-male difference and the female/male ratio. For two size-related traits, wing and thorax length, we found that both SSD indices were normally distributed. Within each family, the variability of SSD was estimated by considering individual values in one sex (the female) with respect to the mean value in the other sex (the male). In a homogeneous sample of 30 lines ofDrosophila melanogaster, both indices provided similar intraclass correlations, on average 0.21, significantly greater than zero but lower than those for the traits themselves: 0.50 and 0.36 for wing and thorax length respectively. Wing and thorax length were strongly positively correlated within each sex. SSD indices of wing and thorax length were also positively correlated, but to a lesser degree than for the traits themselves. For comparative evolutionary studies, the ratio between sexes seems a better index of SSD since it avoids scaling effects among populations or species, permits comparisons between different traits, and has an unambiguous biological significance. In the case ofD. melanogaster grown at 25‡C, the average female/male ratios are very similar for the wing (1.16) and the thorax (1.15), and indicate that, on average, these size traits are 15–16% longer in females.

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References

  • Andersson M. 1994Sexual selection. Princeton University Press, Princeton.

    Google Scholar 

  • Arak A. 1988 Sexual dimorphism in body size: a model and a test.Evolution 42, 820–825.

    Article  Google Scholar 

  • Arnold S. J. 1985 Quantitative genetic models of sexual selection.Evolution 41, 1296–1310.

    CAS  Google Scholar 

  • Badyaev A. V. and Hill G. E. 2000 The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure.Evolution 54, 1784–1794.

    PubMed  CAS  Google Scholar 

  • Badyaev A. V., Hill G. E. and. Whittingham L. A. 2001 The evolution of sexual size dimorphism in the house finch. IV. Population divergence in ontogeny.Evolution 55, 2534–2549.

    PubMed  CAS  Google Scholar 

  • Bird M. A. and Schaffer H. E. 1972 A study of the genetic basis of the sexual dimorphism for wing length inDrosophila melanogaster.Genetics 72, 475–487.

    PubMed  CAS  Google Scholar 

  • Blanckenhorn W. U., Preziosi R. F. and Fairbairn D. J. 1995 Time and energy constraints and the evolution of sexual size dimorphism — to eat or to mate?Evol. Ecol. 9, 369–381.

    Article  Google Scholar 

  • Boulétreau-Merle J., Allemand R., Cohet Y. and David J. R. 1982 Reproductive strategy inDrosophila melanogaster: significance of a genetic divergence between temperate and tropical populations.Oecologia 53, 323–329.

    Article  Google Scholar 

  • Bradbury J. W. and Anderson M. B. 1987Sexual selection: testing the alternatives. Wiley, Chichester.

    Google Scholar 

  • Buvanendran V. 1969 The heritability and genetic correlations of sexual dimorphism for 10-week weight in poultry.Br. Poult. Sci. 10, 321–325.

    PubMed  CAS  Google Scholar 

  • Capy P., Pla E. and David J. R. 1994 Phenotypic and genetic variability of morphometrical traits in natural populations ofDrosophila melanogaster andD. simulans. II. Withinpopulation variability.Genet. Sel. Evol. 26, 15–28.

    Article  Google Scholar 

  • Charnov E. L. 1982The theory of sex allocation. Princeton University Press, Princeton.

    Google Scholar 

  • Cowley D. E. and Atchley W. R. 1988 Quantitative genetics ofDrosophila melanogaster II. Heritabilities and genetic correlations between sexes for head and thorax traits.Genetics 119, 421–433.

    PubMed  CAS  Google Scholar 

  • Cowley D. E., Atchley W. R. and Rutledge J. J. 1986 Quantitative genetics ofDrosophila melanogaster I. sexual dimorphism in genetics parameters for wing traits.Genetics 114, 549–566.

    PubMed  CAS  Google Scholar 

  • Curtsinger J. W. 1986 Quantitative wing variation in inbred and outbred lines ofDrosophila melanogaster.J. Hered. 77, 267–271.

    PubMed  CAS  Google Scholar 

  • Darwin C. 1871The descent of man and selection in relation to sex. John Murray, London.

    Google Scholar 

  • David J. 1962 A new medium for rearingDrosophila in axenic conditions.Drosoph. Inf. Serv. 36, 128.

    Google Scholar 

  • David J. R., Moreteau B., Gautier J. P., 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., Legout H., Pétavy G., Capy P. and Moreteau B. 2004 Isofemale lines in Drosophila: an empirical approach to quantitative trait analysis in natural populations.Heredity (in press).

  • Eisen E. and Hanrahan J. P. 1972 Selection for sexual dimorphism in body weight in mice.Aust. J. Biol. Sci. 25, 1015–1024.

    PubMed  CAS  Google Scholar 

  • Fairbairn D. J. 1997 Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females.Annu. Rev. Ecol. Syst. 28, 659–687.

    Article  Google Scholar 

  • Falconer D. S. 1989Introduction to quantitative genetics. Longman, New York.

    Google Scholar 

  • Frankham R. 1968 Sex and selection for a quantitative trait inDrosophila. II. The sex dimorphism.Aust. J. Biol. Sci. 21, 1215–1223.

    PubMed  CAS  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., Scheiner S. M. and David J. R. 1998b Phenotypic plasticity of body pigmentation in Drosophila: correlated variations between segments.Genet. Sel. Evol. 30, 181–194.

    Article  Google Scholar 

  • Gibert P., Moreteau B., Munjal A. K. and David J. R. 1999 Phenotypic plasticity of abdominal pigmentation inDrosophila kikkawai: multiple interactions between a major gene, sex, abdomen segment and growth temperature.Genetica 105, 165–176.

    Article  PubMed  CAS  Google Scholar 

  • Hedrick A. V. and Temeles E. J. 1989 The evolution of sexual dimorphism in animals: hypotheses and tests.Trends Ecol. Evol. 4, 136–138.

    Article  Google Scholar 

  • Hoffmann A. A. and Parsons P. A. 1988 The analysis of quantitative variation in natural populations with isofemale strains.Genet. Sel. Evol. 20, 87–98.

    Article  Google Scholar 

  • Hollocher H., Hatcher J. L. and Dyreson E. G. 2000 Evolution of abdominal pigmentation differences across species in theDrosophila dunni subgroup.Evolution 54, 2046–2056.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kacmarczyk T. and Craddock E. M. 2000 Cell size is a factor in body size variation among Hawaiian and non-Hawaiian species.Drosoph. Inf. Serv. 83, 144–148.

    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 

  • Kirkpatrick M. and Ryan M. J. 1991 The evolution of mating preferences and the paradox of the lek.Nature 350, 33–38.

    Article  Google Scholar 

  • Kopp A., Duncan I. and Carroll S. B. 2000 Genetic control and evolution of sexually dimorphic characters inDrosophila.Nature 408, 553–559.

    Article  PubMed  CAS  Google Scholar 

  • Korkman N. 1957 Selection with regard to the sex difference of body weight in mice.Hereditas 43, 665–678.

    Article  Google Scholar 

  • LaBarbera M. 1989 Analyzing body size as a factor in ecology and evolution.Annu. Rev. Ecol. Syst. 20, 97–117.

    Article  Google Scholar 

  • Lande R. 1980 Sexual dimorphism, sexual selection and adaptation in phylogenic characters.Evolution 34, 293–305.

    Article  Google Scholar 

  • Leips J. and Mackay T. F. 2000 Quantitative trait loci for life span inDrosophila melanogaster: interactions with genetic background and larval density.Genetics 155, 1773–1788.

    PubMed  CAS  Google Scholar 

  • Mackay T. F. C. 2001 The genetic architecture of quantitative traits.Annu. Rev. Genet. 35, 303–339.

    Article  PubMed  CAS  Google Scholar 

  • Mackay T. F. C., Hackett J. B., Lyman R. F., Wayne M. L. and Anholt R. R. H. 1996 Quantitative genetic variation of odorguided behaviour in a natural population ofDrosophila melanogaster.Genetics 144, 727–735.

    PubMed  CAS  Google Scholar 

  • Maynard Smith J. 1978The evolution of sex. Cambridge University Press, Cambridge.

    Google Scholar 

  • MerilÄ J., Sheldon B. C. and Ellegren H. 1998 Quantitative genetics of sexual size dimorphism in the collared flycatcher,Ficedula albicollis.Evolution 52, 870–880.

    Article  Google Scholar 

  • Michod R. E. and Levin B. R. 1988The evolution of sex. Sinauer, Sunderland.

    Google Scholar 

  • Mignon-Grasteau S., Beaumont C., Poivey J. P. and DeRochambeau H. 1998 Estimation of the genetic parameters of sexual dimorphism of body weight in "label" chicken and muscovy ducks.Genet. Sel. Evol. 30, 481–491.

    Article  Google Scholar 

  • Mignon-Grasteau S., Beaumont C., Le Bihan-Duval E., Poivey J. P., DeRochambeau H. and Ricard F. H. 1999 Genetic parameters of growth curve parameters in male and female chickens.Br. Poult. Sci. 40, 44–51.

    Article  PubMed  CAS  Google Scholar 

  • Nuzhdin S. V., Pasyukova E. G., Dilda C. L., Zeng Z. B. and Mackay T. F. 1997 Sex-specific quantitative trait loci affecting longevity inDrosophila melanogaster.Proc. Natl. Acad. Sci. USA 94, 9734–9739.

    Article  PubMed  CAS  Google Scholar 

  • Palezona D. L. and Alicchio R. 1973 Genetic analysis of sexual dimorphism inDrosophila melanogaster.Monitore Zool. Ital. 4, 63–70.

    Google Scholar 

  • Partridge L., Ewing A. and Chandler A. 1987 Male size and mating success inDrosophila melanogaster: the roles of male and female behavior.Anim. Behav. 35, 555–562.

    Article  Google Scholar 

  • Pilla A. M. 1974 Possibilita di miglioramento genetico dell’anatra muschiata.Ann. Inst. Sper. Zootec. 7, 165–174.

    Google Scholar 

  • Ranta E., Laurila A. and Elmberg J. 1994 Reinventing the wheel: analysis of sexual dimorphism in body size.Oikos 70, 313–321.

    Article  Google Scholar 

  • Ranz J. M., Castillo-Davis C. I., Meiklejohn C. D. and Hartl D. L. 2003 Sex-dependent gene expression and evolution of theDrosophila transcriptome.Science 300, 1742–1745.

    Article  PubMed  CAS  Google Scholar 

  • Reeve J. P. and Fairbairn D. J. 1996 Sexual size dimorphism as a correlated response to selection on body size: an empirical test of the quantitative genetic model.Evolution 50, 1927–1938.

    Article  Google Scholar 

  • Reeve J. P. and Fairbairn D. J. 1999 Change in sexual size dimorphism as a correlated response to selection on fecundity.Heredity 83, 697–706.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Ritchie M. G. and Kyriacou C. P. 1994 Genetic variability of courtship song in a population ofDrosophila melanogaster.Anim. Behav. 48, 425–434.

    Article  Google Scholar 

  • Roff D. A. 1997Evolutionary quantitative genetics. Chapman and Hall, London.

    Google Scholar 

  • Roff D. A. and Mousseau T. A. 1987 Quantitative genetics and fitness: lessons fromDrosophila.Heredity 58, 103–118.

    PubMed  Google Scholar 

  • Santos M., Ruiz A., Barbadilla A., Quezada-Diaz J. E., Hasson E. and Fontdevila A. 1988 The evolutionary history ofDrosophila buzzatii.Heredity 61, 255–262.

    Google Scholar 

  • Schmidt T. A. 1993 Divergent selection for sexual dimorphism in mice — 6 generations of selection. Proceedings of the 44th Annual Meeting EAAP, Aarhus.

  • Simmons L. W. 2001Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton.

    Google Scholar 

  • Singh S. S., Verma S. K., Khan A. G. and Shrivastava A. K. 1989 Studies on genetic variability in juvenile body weights and sexual dimorphism in layer type chicken.Indian J. Poult. Sci. 24, 308–310.

    Google Scholar 

  • Slatkin M. 1984 Ecological causes of sexual dimorphism.Evolution 38, 622–630.

    Article  Google Scholar 

  • Sokal R. R. and Rohlf F. J. 1995Biometry, 3rd edition. Freeman, New York.

    Google Scholar 

  • Stearns S. C. (ed.) 1987The evolution of sex and its consequences. BirkhÄuser, Basel.

    Google Scholar 

  • Thornhill R. and Alcock J. 1983The evolution of insect mating systems. Harvard University Press, Cambridge.

    Google Scholar 

  • Via S. 1984 The quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and among host plants.Evolution 38, 896–905.

    Article  Google Scholar 

  • Vieira C., Pasyukova E. G., Zeng Z. B., Hackett J. B., Lyman R. F. and Mackay T. F. 2000 Genotype-environment interaction for quantitative trait loci affecting life span inDrosophila melanogaster.Genetics 154, 213–227.

    PubMed  CAS  Google Scholar 

  • Wolf J. B., Brodie E. D. and Wade M. J. 2000Epistasis and the evolutionary process. Oxford University Press, New York.

    Google Scholar 

  • Zamudio K. R., Huey R. B. and Crill W. D. 1995 Bigger isn’t always better: body size, developmental and parental temperature and male territorial success inDrosophila melanogaster.Anim. Behav.49, 671–677.

    Google Scholar 

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Authors and Affiliations

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

    Jean R. David, HÉlÈne Legout, Georges PÉtavy & Brigitte Moreteau

  2. CNRS, Laboratoire Biométrie, Biologie Evolutive, Université de Lyon, I69622, Villeurbanne Cedex, France

    Patricia Gibert

  3. Station de Recherches Avicoles, NRA, 37380, Nouzilly, France

    Sandrine Mignon-Grasteau & Catherine Beaumont

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  1. Jean R. David
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  2. Patricia Gibert
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  3. Sandrine Mignon-Grasteau
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  4. HÉlÈne Legout
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  5. Georges PÉtavy
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  6. Catherine Beaumont
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  7. Brigitte Moreteau
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Correspondence to Jean R. David.

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David, J.R., Gibert, P., Mignon-Grasteau, S. et al. Genetic variability of sexual size dimorphism in a natural population ofDrosophila melanogaster: An isofemale-line approach. J Genet 82, 79–88 (2003). https://doi.org/10.1007/BF02715810

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