Skip to main content
SpringerLink
Log in

The impact of genetic parental distance on developmental stability and fitness in Drosophila buzzatii

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Measures of genetic parental distances (GPD) based on microsatellite loci (D 2 and IR), have been suggested to be better correlated with fitness than individual heterozygosity (H), as they contain information about past events of inbreeding or admixture. We investigated if GPD increased with increasing genetic divergence between parental populations in Drosophila buzzatii and if the measures indicate past events of admixture. Further we evaluated the relationship between GPD, fitness and fluctuating asymmetry (FA) of size and shape. We investigated three populations of Drosophila buzzati, from Argentina, Europe and Australia. From these populations two intraspecific hybridisation lines were made; one between the Argentinean and European populations, which have been separated 200 years and one between the populations from Argentina and Australia, which have been separated 80 years. By doing this we obtained hybrid progeny having different levels of GPD. We found that D 2 and H can be used as indicators of admixture when comparing hybrid individuals with their parentals. IR was not informative. Our results does not exclude the presence of genetic fitness correlations (GFC) over individuals with a broad fitness range from populations in equilibrium, but we doubt the presence of GFC using GPD measures in admixed populations. Shape FA could be a relevant measure for fitness, however, only when comparing populations, not at individual level.

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

  • Amos W, Worthington WJ, Fullard K et al (2001) The influence of parental relatedness on reproductive success. Proc Roy Soc Lond B 268:2021–2027

    Article  CAS  Google Scholar 

  • Andersen DH, Pertoldi C, Scali V et al (2002) Intraspecific hybridization, developmental stability and fitness in Drosophila mercatorum. Evol Ecol Res 4:603–621

    Google Scholar 

  • Bean K, Amos W, Pomeroy PP et al (2004) Patterns of parental relatedness and pup survival in the grey seal (Halichoerus grypus). Mol Ecol 13:2365–2370

    Article  PubMed  CAS  Google Scholar 

  • Borrell YJ, Pineda H, McCarthy I et al (2004) Correlations between fitness and heterozygosity at allozyme and microsatellite loci in the Atlantic salmon, Salmo salar L. Heredity 92:585–593

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • Charlesworth B, Hughes KA (1999) The maintenance of genetic variation in life-history traits. In: Singh RS, Krimbas CB (eds) Evolutionary genetics: from molecules to morphology, vol 1. Cambridge Univ. Press, Cambridge, pp 369–392

    Google Scholar 

  • Coltman DW, Slate J (2003) Microsatellite measures of inbreeding: a meta-analysis. Evolution 57:971–983

    PubMed  CAS  Google Scholar 

  • Coltman DW, Don Bowen W, Wright JM (1998) Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc Roy Soc Lond B 265:803–809

    Article  CAS  Google Scholar 

  • Corander J, Marttinen P (2006) Bayesian identification of admixture events using multi-locus molecular markers. Mol Ecol 15:2833–2843

    Article  PubMed  Google Scholar 

  • Coulson TN, Pemberton JM, Albon SD et al (1998) Microsatellites reveal heterosis in red deer. Proc Roy Soc Lond B 265:489–495

    Article  CAS  Google Scholar 

  • Dryden IL, Mardia KV (1998) Statistical shape analysis. Wiley, Chichester

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Frydenberg J, Pertoldi C, Dahlgaard J, Loeschcke V (2002) Genetic variation in original and colonizing Drosophila buzzatii populations analysed by microsatellites loci isolated with a new PCR screening method. Mol Ecol 11:181–190

    Article  PubMed  CAS  Google Scholar 

  • Goudet J (2002) Fstat. A program to estimate and test gene diversities and fixation indices (version 2.9.3.2). URL: http://www.unil.ch/izea/softwares/fstat.html

  • Haldane JBS (1955) The measurement of variation. Evolution 9:484

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:9

    Google Scholar 

  • Hansen TF, Houle D (2004) Evolvability, stabilizing selection, and the problem of stasis. In: Pigliucci M, Preston K (eds) Phenotypic integration: studying the ecology and evolution of complex phenotypes, Oxford University Press, Oxford, pp 130–150

    Google Scholar 

  • Klingenberg CP, Leamy LJ (2001) Quantitative genetics of geometric shape in the mouse mandible. Evolution 55:2342–2352

    PubMed  CAS  Google Scholar 

  • Klingenberg CP, McIntyre GS (1998) Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution 52:1363–1375

    Article  Google Scholar 

  • Klingenberg CP, Zaklan SD (2000) Morphological integration between developmental compartments in the Drosophila wing. Evolution 54:1273–1285

    PubMed  CAS  Google Scholar 

  • Leamy L, Routman EJ, Cheverud JM (2002) An epistatic genetic basis for fluctuating asymmetry of mandible size in mice. Evolution 56:642–653

    PubMed  Google Scholar 

  • Lens L, Van Dongen S, Galbusera P et al (2000) Developmental instability and inbreeding in natural bird populations exposed to different levels of habitat disturbance. J Evol Biol 13:889–896

    Article  Google Scholar 

  • Lens L, Van Dongen S, Kark S et al (2002) Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biol Rev 77:27–38

    PubMed  Google Scholar 

  • Lerner IM (1954) Genetic homeostasis. Oliver and Boyd, London

    Google Scholar 

  • Lesbarrères D, Craig RP, Laurila A et al (2005) Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria. Mol Ecol 14:311–323

    Article  PubMed  Google Scholar 

  • Miller RG (1981) Simultaneous statistical inference. McGraw Hill, New York

    Google Scholar 

  • Neff BD (2004) Mean d2 and divergence time: transformations and standardizations. J Hered 21:165–171

    Article  Google Scholar 

  • Oosterhout C, Hutchinson B, Wills D et al (2003) MicroChecker version 2.2.3. URL http://www.Microchecker.hull.ac.uk/

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

    Article  Google Scholar 

  • Pertoldi C, Kristensen TN, Andersen DH et al (2006a) Review: developmental instability as an estimator of genetic stress. Heredity 96:122–127

    Article  PubMed  CAS  Google Scholar 

  • Pertoldi C, García-Perea R, Godoy A et al (2006b) Morphological consequences of range fragmentation and population decline on the endangered Iberian lynx (Lynx pardinus). J Zool 268:73–86

    Article  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Rasband W (2001) ImageJ. A program for image processing and analysis in Java. URL http://www.rsb.info.nih.gov/ij/

  • Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rohlf FJ, Marcus LF (1993) A revolution in morphometrics. Trends Ecol Evol 8:129–132

    Article  Google Scholar 

  • Rossiter SJ, Jones G, Ransome RD et al (2001) Outbreeding increases offspring survival in wild greater horseshoe bats (Rhinolophus ferrumequinum). Proc Roy Soc Lond B 268:1055–1061

    Article  CAS  Google Scholar 

  • Rowe G, Beebee TJC (2001) Fitness and microsatellite diversity estimates were not correlated in two outbred anuran populations. Heredity 87:558–565

    Article  PubMed  CAS  Google Scholar 

  • Sgró CM, Partridge L (2000) Evolutionary responses of the life history of wild-caught Drosophila melanogaster to two standard methods of laboratory culture. Am Nat 156:341–353

    Article  Google Scholar 

  • Tsitrone A, Rousset F, David P (2001) Heterosis, marker mutational processes and population inbreeding history. Genetics 159:1845–1859

    PubMed  CAS  Google Scholar 

  • Valdes AM, Slatkin M, Freimer NB (1993) Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics 133:737–749

    PubMed  CAS  Google Scholar 

  • Waser NM (1993) Sex, mating systems, inbreeding and outbreeding. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding. University of Chicago Press, Chicago, pp 1–13

    Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugenic 15:323–354

    Google Scholar 

  • Xu X, Peng M, Fang Z et al (2000) The direction of microsatellite mutations is dependent upon allele length. Nat Genet 24:396–399

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Jørgen Bundgaard for providing the Masca flies and the Editor and two anonymous reviewers for valuable comments. The work was supported by grants from the Villum Kann Rasmussen Foundation (VKR-05-024) and the Oticon Foundation (03-1397) to Ditte Holm Andersen and by grants from the Danish Research Agency (21-01-0526 and 21-03-0125) and the Marie Curie Fellowship of the European Community Host Development program under contract number HPMD-CT-2000-00009 to Cino Pertoldi, and support to Valerio Scali by the Canziani Bequest and M.I.U.R. (Ministero Industria Universitá Ricerca).

Author information

Authors and Affiliations

  1. Dipartimento di Biologia Evoluzionistica Sperimentale, University of Bologna, Via Selmi 3, 40126, Bologna, Italy

    Ditte Holm Andersen, Sandro Cavicchi & Valerio Scali

  2. Department of Ecology and Genetics, Aarhus University, Ny Munkegade, Building 1540, 8000, Aarhus C, Denmark

    Ditte Holm Andersen, Cino Pertoldi & Volker Loeschcke

  3. Department of Applied Biology, Estación Biológica Doñana, CSIC, Pabellón del Perú, Avda. Maria Luisa, s/n, 41013, Seville, Spain

    Cino Pertoldi

  4. Department of Wildlife Ecology & Biodiversity, National Environmental Research Institute, Kalø Grenåvej 14, 8410, Ronde, Denmark

    Cino Pertoldi

Authors
  1. Ditte Holm Andersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cino Pertoldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Volker Loeschcke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sandro Cavicchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Valerio Scali
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ditte Holm Andersen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Andersen, D.H., Pertoldi, C., Loeschcke, V. et al. The impact of genetic parental distance on developmental stability and fitness in Drosophila buzzatii . Genetica 134, 223–233 (2008). https://doi.org/10.1007/s10709-007-9229-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-007-9229-3

Keywords

Search

Navigation