Skip to main content
SpringerLink
Log in

Fluctuating asymmetry of meristic traits: an isofemale line analysis in an invasive drosophilid, Zaprionus indianus

  • Original Paper
  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Metric (e.g., body size) and meristic (e.g., bristle number) traits are of general use in quantitative genetic studies, and the phenotypic variance is subdivided into a genetic and a non-genetic environmental component. The non-genetic variance may have two origins: a common garden effect between individuals and a developmental instability within the same individual. Developmental instability may be studied by considering the fluctuating asymmetry (FA) between the two sides of the body. The isofemale line technique is a convenient method for investigating the architecture of natural populations but has been rarely implemented for investigating FA. In this paper, we use this experimental design for analyzing four meristic traits in eight populations of the cosmopolitan Zaprionus indianus. A study of the correlation between left and right side of each line revealed that almost 90% of the variability was due to a developmental noise, while a much higher correlation among the means of the lines from the same population was observed. A slight trend toward a directional asymmetry was observed: more thoracic bristles on the left side. Four kinds of indices, scaled or non-scaled to the mean were used for comparing the different traits. Unscaled values (mean absolute values or standard deviation of each line) revealed a linear increase with the means. Interestingly the results of ovariole number were included in the same regression. With the scaled indices (mean absolute divided by each individual value or stadard deviation devided by the mean), the differences among traits were considerably decreased, but still remained significant. The mean FA of the various traits were not correlated, suggesting that each trait harbors its own developmental stability. The CVs of FA were high with a magnitude similar to those of the trait themselves, slightly less than 10%. Finally, even with the isofemale line design, which is a powerful means for unravelling slight genetic variations, we did not to find any clear indication of a genetic component of FA under the optimal environmental conditions used in this study.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allemand R, David JR, Fouillet P (1997) La symétrie bilatérale du nombre de soies ternopleurales: différence entre deux espèces jumelles de Zaprionus (Diptera, Drosophilidae). Arch Zool Expérimentale et Générale 118:123–132

    Google Scholar 

  • Araripe LO, Klaczko LB, Moreteau B, David JR (2004) Male sterility thresholds in a tropical cosmopolitan drosophilid, Zaprionus indianus. J Therm Biol 29:73–80

    Article  Google Scholar 

  • Bourguet D (2000) Fluctuating asymmetry and fitness in Drosophila melanogaster. J Evol Biol 13:515–521

    Article  Google Scholar 

  • Brown NA, Wolpert L (1990) The development of handedness in left/right asymmetry. Development 109:1–9

    CAS  PubMed  Google Scholar 

  • Carter AJR, Weier TM, Houle D (2009) The effect of inbreeding on fluctuating asymmetry of wing veins in two laboratory strains of Drosophila melanogaster. Heredity 102:563–572

    Article  CAS  PubMed  Google Scholar 

  • Chakir M, Moreteau B, Capy P, David JR (2007) Phenotypic variability of wild living and laboratory grown Drosophila: consequences of nutritional and thermal heterogeneity in growth conditions. J Therm Biol 32:1–11

    Article  CAS  Google Scholar 

  • Coyne JA, Beecham E (1987) Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics 117:727–737

    CAS  PubMed  PubMed Central  Google Scholar 

  • David JR, Gilbert P, Legout H, Capy P, Moreteau B (2005) Isofemale lines in Drosophila: an empirical approach to quantitative traits analysis in natural populations. Heredity 94:3–12

    Article  CAS  PubMed  Google Scholar 

  • David JR, Legout H, Moreteau B (2006a) Phenotypic plasticity of body size in a temperate population of Drosophila melanogaster: when the temperature-size rule does not apply. J Genet 85:9–23

    Article  PubMed  Google Scholar 

  • David JR, Araripe LO, Bitner-Mathe BC, Capy P, Goni B, Klaczko LB, Legout H, Martins MB, Vouidibio J, Yassin A, Moreteau B (2006b) Quantitative trait analysis and geographic variability of natural populations of Zaprionus indianus, a recent invader in Brazil. Heredity 96:53–62

    CAS  PubMed  Google Scholar 

  • David JR, Araripe L, Bitner-Mathe BC, Goni B, Klaczko LB, Legout H, Martins MB, Vouidibio J, Yassin A, Moreteau B (2006c) Sexual dimorphism of body size and sternopleural bristle number: a comparison of geographic populations in an invasive cosmopolitan drosophilid. Genetica 128:109–122

    Article  PubMed  Google Scholar 

  • Debat V, Milton CC, Rutherford S, Klingenberg CP, Hoffmann AA (2006) Hsp90 and the quantitative variation of wing shape in Drosophila melanogaster. Evolut Int J org Evolut 60:2529–2538

    Article  CAS  Google Scholar 

  • Debat V, Cornette R, Korol AB, Nevo E, Soulet D, David JR (2008) Multidimensional analysis of Drosophila wing variation in evolution canyon. J Genet 87:407–419

    Article  PubMed  Google Scholar 

  • Debat V, Debelle A, Dworkin I (2009) Plasticity, canalization, and developmental stability of the Drosophila wing: joint effects of mutations and developmental temperature. Evolut Int J org Evolut 63–11:2864–2876

    Article  Google Scholar 

  • Debat V, Bloyer S, Faradji F, Gidaszewski N, Navarro N, Orozco-Terwengel P, et al (2011) Developmental stability: a major role for Cyclin G in Drosophila melanogaster. PLoS Genet 7:e1002314 (PMID: 21998598)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delpuech JM, Moreteau B, Chiche J, Pla E, Vouidibio J, David JR (1995) Phenotypic plasticity and reaction norms in temperate and tropical populations of Drosophila melanogaster: ovarian size and developmental temperature. Evolut Int J Org Evolut 49(4):670–676

    Article  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, edn 4. Longmans Green, Harlow

    Google Scholar 

  • Fowler K, Whitlock MC (1994) Fluctuating asymmetry does not increase with moderate inbreeding in Drosophila melanogaster. Heredity 73:373–376

    Article  PubMed  Google Scholar 

  • Gibert P, Moreteau B, Moreteau JC et al (1998) Genetic variability in quantitative traits in Drosophila Melanogaster (fruit fly) natural populations: analysis of wild-living flies and of several laboratory generations. Heredity 80:326–335

    Article  Google Scholar 

  • Giddings LV, Kaneshiro KY, Anderson W (1989) Genetics, speciation and the founder principle. Oxford Univ. Press, Oxford

    Google Scholar 

  • Gómez FH, Norry FM (2012) Is the number of possible QTL for asymmetry phenotypes dependent on thermal stress? J Therm Biol 37(1):1–5

    Article  Google Scholar 

  • Graham JH, Freeman DC, Emlen JM (1993) Antisymmetry, directional asymmetry, and dynamic morphogenesis. Genetica 89:121–137

    Article  Google Scholar 

  • Imasheva AG, Loeschcke V, Zhivotovsky DA, Lazebny OE (1997) Effects of extreme temperatures on phenotypic variation and developmental stability in Drosophila melanogaster and Drosophila buzzatii. Biol J Linn Soc 61:117–126

    Google Scholar 

  • Imasheva AG, Bosenko DV, Bubli OA (1999) Variation in morphological traits of Drosophila melanogaster (fruit fly) under nutritional stress. Heredity 82:187–192

    Article  PubMed  Google Scholar 

  • Indrasamy H, Woods RE, McKenzie JA, Batterham P (2000) Fluctuating asymmetry for specific bristle characters in Notch mutants of Drosophila melanogaster. Genetica 109:151–159

    Article  CAS  PubMed  Google Scholar 

  • Karan D, Morin JP, Gravot E, Moreteau B, David JR (1999) Body size reaction norms in Drosophila melanogaster: temporal stability and genetic architecture in a natural population. Genet Sel Evol 31:491–508

    Article  PubMed Central  Google Scholar 

  • Klingenberg CP, Zaklan SD (2000) Morphological integration between developmental compartments in the Drosophila wing. Evolut Int J Org Evolut 54:1273–1275

    Article  CAS  Google Scholar 

  • Kurbalija Z, Stamenkovic-Radak M, Pertoldi C, Andjelkovic M (2010) Outbreeding causes developmental instability in Drosophila subobscura. Evolut Ecol 24(4):839–864

    Article  Google Scholar 

  • Levin M, Palmer AR (2007) Left–right patterning from the inside out: widespread evidence for intracellular control. Bioessays 29:271–287

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland

    Google Scholar 

  • Markow TA, Ricker IP (1992) Male size developmental stability, and mating success in natural populations of three Drosophila species. Heredity 69:122–127

    Article  PubMed  Google Scholar 

  • Maynard Smith J, Szathmary E (1995) The major transitions in evolution. Oxford University Press, Oxford

    Google Scholar 

  • McManus IC (2002) Right hand, left hand: the origins of asymmetry in brains, bodies, atoms and cultures. Weidenfeld and Nicolson/Harvard University Press, London

    Google Scholar 

  • Møller AP, Swadle JP (1997) Asymmetry, developmental stability and evolution. Oxford Univ Press, Oxford

    Google Scholar 

  • Moreteau B, Brochen A, Pla E, David JR (2000) Ovarian fluctuating asymmetry: a stable property among Drosophila species. Drosoph Inf Ser 83:51–54

    Google Scholar 

  • Nakamura, T, Hamada, H (2012) Left–right patterning: conserved and divergent mechanisms. Development 139:3257–3262

    Article  CAS  PubMed  Google Scholar 

  • Palmer AR (1994) Fluctuating asymmetry analyses: a primer. In: Markow TA (ed) Developmental instability: its origin and evolutionary implications. Kluwer, Dordrecht, pp 335–364

    Chapter  Google Scholar 

  • Palmer AR (1996) Waltzing with asymmetry. Bioscience 46:518–536

    Article  Google Scholar 

  • Palmer AR (1999) Detecting publication bias in Meta-analyses: a case study of fluctuating asymmetry and sexual selection. Am Nat 154:220–233

    Google Scholar 

  • Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Ann Rev Ecol Syst 17:391–421

    Article  Google Scholar 

  • Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power of statistical tests. Acta Zool Fenn 191:55–70

    Google Scholar 

  • Palmer AR, Strobeck C (2003) Fluctuating asymmetry analysis revisited. In: Polak M (ed). Oxford University Press, Oxford, pp 279–319

  • Pétavy G, Morin JP, Moreteau B, David JR (1997) Growth temperature and phenotypic plasticity in two Drosophila sibling species: probable adaptive changes in flight capacities. J Evol Biol 10:875–887

    Google Scholar 

  • Pétavy G, David JR, Debat V, Pertoldi C, Moreteau B (2006) Phenotypic and genetic variability of sternopleural bristle number in Drosophila melanogaster under daily thermal stress: developmental instability and anti-asymmetry. Evol Ecol Res 8:149–167

    Google Scholar 

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

    Google Scholar 

  • Roff DA, Mousseau TA (1987) Quantitative genetics and fitness: lessons from Drosophila. Heredity 58:103–118

    Article  PubMed  Google Scholar 

  • Santos M (2001) Fluctuating asymmetry is non-genetically related to mating success in Drosophila buzzatii. Evolut Int J Org Evolut 55:2248–2256

    Article  CAS  Google Scholar 

  • Simpson P, Woehl R, Usui K (1999) The development and evolution of bristle patterns in Diptera. Development 126(7):1349–1364

    CAS  PubMed  Google Scholar 

  • Soto IM, Carreira VP, Soto EM, Hasson E (2008) Wing morphology and fluctuating asymmetry depend on the host plant in catophilic Drosophila. J Evol Biol 21:598–609

    Article  CAS  PubMed  Google Scholar 

  • Swain DF (1987) A problem with the use of meristic characters to estimate developmental stability. Am Nat 129:761–768

    Article  Google Scholar 

  • Trotta V, Calboli, FCF, Garoia F, Grifoni D, Cavicchi S (2005) Fluctuating asymmetry as measure of ecological stress in Drosophila melanogaster (Diptera: Drosophilidae). Eur J Entomol 102:195–200

    Article  Google Scholar 

  • Vandenberg LN, Levin M (2013) A unified model for left–right asymmetry? Comparison and synthesis of molecular models of embryonic laterality. Dev Biol 379:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vilela CR (1999) Is Zaprionus indianus Gupta, 1970 (Diptera, Drosophilidae) currently colonizing the neotropical region? Drosoph Inf Ser 82:37–39

    Google Scholar 

  • Vishalakshi C, Singh BN (2008) Effects of developmental temperature stress on fluctuating asymmetry in certain morphological traits in Drosophila ananassae. J Therm Biol 33:201–208

    Article  Google Scholar 

  • Waddington CH (1957) The strategy of the genes. George Allen Unwin London, UK

    Google Scholar 

  • Whitlock, M (1996) The heritability of fluctuating asymmetry and the genetic control of developmental stability. Proc R Soc Lond B Biol 263(1372):849–853

    Article  CAS  Google Scholar 

  • Woods RE, Hercus MJ, Hoffmann AA (1998) Estimating the heritability of fluctuating asymmetry in field Drosophila. Evolut Int J org Evolut 52:816–824

    Article  Google Scholar 

  • Woods RE, Sgro CM, Hercus MJ, Hoffmann AA (1999) The association between fluctuating asymmetry, trait variability, trait heritability, and stress: a multiply replicated experiment on combined stresses in Drosophila melanogaster. Evolution 53:493–505

    Article  Google Scholar 

  • Woods RE, Sgro CM, Hercus MJ, Hoffmann AA (2002) Fluctuating asymmetry, fecundity and development time in Drosophila: is there an association under optimal and stress conditions? J Evol Biol 15:146–157

    Article  Google Scholar 

  • Yassin A, David JR, Bitner-Mathé BC (2009) Phenotypic variability of natural populations of an invasive drosophilid, Zaprionus indianus, on different continents: comparison of wild-living and laboratory-grown flies. C R Biol 332:898–908

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Blanche Bittner Mathé for comments and suggestions on data in this paper. This work was supported by Coordenação de Aperfeiçoamento de Nível Superior (CAPES) and Comite Français d’Evaluation de la Coopéation Universitaire avec le Brésil (COFECUBE). This paper results from a French-Brazilian cooperation programme on Zaprionus.

Author information

Authors and Affiliations

  1. Departamento de Biologia, Instituto de Biociências, Letras e Ciências Exatas, de São José do Rio Preto, Rua Cristovão Colombo, 2265, São José do Rio Preto, São Paulo, CEP 15054-000, Brazil

    Lilian Madi-Ravazzi

  2. Departamento das Ciências da Computação e Estatística, Instituto de Biociências, Letras e Ciências Exatas, de São José do Rio Preto, Rua Cristovão Colombo, 2265, São José do Rio Preto, São Paulo, CEP 15054-000, Brazil

    Luis Fernando Segala

  3. Institut de Systématique, Evolution, Biodiversité, UMR7205, CNRS, MNHN, UPMC, EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités, 75005, Paris, France

    Vincent Debat & Jean R. David

  4. Laboratoire Évolution, Génomes, Comportement, Écologie (EGCE) CNRS, IRD, Univ. Paris-sud, Université Paris-Saclay, 91198, Gif sur Yvette, France

    Vincent Debat & Jean R. David

Authors
  1. Lilian Madi-Ravazzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luis Fernando Segala
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vincent Debat
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jean R. David
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lilian Madi-Ravazzi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Madi-Ravazzi, L., Segala, L.F., Debat, V. et al. Fluctuating asymmetry of meristic traits: an isofemale line analysis in an invasive drosophilid, Zaprionus indianus . Genetica 145, 307–317 (2017). https://doi.org/10.1007/s10709-017-9966-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-017-9966-x

Keywords

Search

Navigation