Skip to main content
SpringerLink
Log in

Changes Across Development Influence Visible and Cryptic Natural Variation of Drosophila melanogaster Olfactory Response

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Relative to an equivalent source of variation that do not present a hidden state, cryptic genetic variation is likely to be an effective source for possible adaptations at times of atypical environmental conditions. In addition to environmental perturbations, it has also been proposed that genetic disturbances can generate release of cryptic genetic variation. The genetic basis and physiology of olfactory response in Drosophila melanogaster is being studied profusely, but almost no analysis has addressed the question if populations harbor cryptic genetic variation for this trait that only manifests when populations experiences a typical or novel conditions. We quantified olfactory responses to benzaldehyde in both larval and adult lifecycle stages among samples of chromosome two substitution lines extracted from different natural populations of Argentina and substituted into a common inbred background. We also evaluated whether an effect of genetic background change, occurred during chromosome substitution, affect larval and adult olfactory response in terms of release of cryptic genetic variation. Results indicate the presence of genetic variation among chromosome substitution lines in both lifecycle stages analyzed. The comparative analyses between chromosome 2 substitution lines and isofemale lines used to generate the chromosome 2 substitution lines shown that only adults exhibited decanalizing process for olfactory response to benzaldehyde in natural populations of D. melanogaster, i.e., release of hidden genetic variation. We propose that this release of hidden genetic variation in adult flies is a consequence of the shift in genetic background context that happens in chromosome 2 substitution lines, that implies the disruption of natural epistatic interactions and generation of novel ones. All in all, we have found that changes across D. melanogaster development influence visible and cryptic natural variation of olfactory behavior. In this sense, changes in the genetic background can affect gene-by-gene interactions (epistasis) generating different or even novel phenotypes as consequence of phenotypic outcome of cryptic genetic variation.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aceves-Piña, E. O., & Quinn, W. G. (1979). Learning in normal and mutant Drosophila larvae. Science, 206, 93–96.

    Article  PubMed  Google Scholar 

  • Anholt, R. R. H., Dilda, C. L., Chang, S., Fanara, J. J., Kulkarni, N. H., Ganguly, I., et al. (2003). The genetic architecture of odor-guided behavior in Drosophila melanogaster: Epistasis and the transcriptome. Nature Genetics, 35, 180–184.

    Article  PubMed  CAS  Google Scholar 

  • Anholt, R. R. H., Lyman, R. F., & Mackay, T. F. C. (1996). Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. Genetics, 143, 293–301.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Anholt, R. R. H., & Mackay, T. F. C. (2004). Quantitative genetic analyses of complex behaviours in Drosophila. Nature Reviews Genetics, 5, 838–849.

    Article  PubMed  CAS  Google Scholar 

  • Anholt, R. R. H., & Mackay, T. F. C. (2015). Dissecting the genetic architecture of behavior in Drosophila melanogaster. Current Opinion in Behavioral Sciences, 2, 1–7.

    Article  PubMed Central  PubMed  Google Scholar 

  • Arya, G. H., Magwire, M. M., Huang, W., Serrano-Negron, Y. L., Mackay, T. F. C., & Anholt, R. R. H. (2015). The genetic basis for variation in olfactory behavior in Drosophila melanogaster. Chemical Senses, 40, 233–243.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ayyub, C., Paranjape, J., Rodrigues, V., & Siddiqi, O. (1990). Genetics of olfactory behavior in Drosophila melanogaster. Journal of Neurogenetics, 6, 243–262.

    Article  PubMed  CAS  Google Scholar 

  • Brown, E. B., Layne, J. E., Zhu, C., Jegga, A. G., & Rollmann, S. M. (2013). Genome-wide association mapping of natural variation in odour-guided behavior in Drosophila. Genes Brain Behavior, 12, 503–515.

    Article  CAS  Google Scholar 

  • Carlborg, O., Jacobsson, L., Ahgren, P., Siegel, P., & Andersson, L. (2006). Epistasis and the release of genetic variation during long-term selection. Nature Genetics, 38, 418–420.

    Article  PubMed  CAS  Google Scholar 

  • Carreira, V. P., Imberti, M., Mensch, J., & Fanara, J. J. (2013). Gene-by-temperature interactions and candidate plasticity genes for morphological traits in Drosophila melanogaster. Plos one, 8(7), 1–10. doi:10.1371/journal.pone.0070851.

    Article  CAS  Google Scholar 

  • Chandler, C. H., Chari, S., & Dworkin, I. (2013). Does your gene need a background check? How genetic background impacts the analysis of mutations, genes, and evolution. Trends in Genetics, 29, 358–366.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cobb, M., Bruneau, S., & Jallon, J. M. (1992). Genetic and developmental factors in the olfactory response of Drosophila melanogaster larvae to alcohols. Proceedings of the Royal Society of London: Biological Sciences, 248, 103–109.

    Article  CAS  Google Scholar 

  • Dworkin, I. (2005a). Canalization, cryptic variation, and developmental buffering: A critical examination and analytical perspective. In B. Hallgrimsson & B. K. Hall (Eds.), Variation (pp. 131–158). Burlington, MA: Elsevier Academic Press.

    Chapter  Google Scholar 

  • Dworkin, I. (2005b). A study of canalization and developmental stability in the sternopleural bristle system of Drosophila melanogaster. Evolution, 59, 1500–1509.

    Article  PubMed  Google Scholar 

  • Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics. Essex, UK: Addison, Wesley, Longman.

    Google Scholar 

  • Fanara, J. J., Robinson, K. O., Rollmann, M., Anholt, R. R. H., & Mackay, T. F. C. (2002). Vanaso is a candidate quantitative trait gene for olfactory behavior in Drosophila melanogaster. Genetics, 162, 1321–1328.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Flatt, T. (2005). The evolutionary genetics of canalization. The Quarterly Review of Biology, 80, 287–316.

    Article  PubMed  Google Scholar 

  • Ganguly, I., Mackay, T. F. C., & Anholt, R. R. H. (2003). Scribble is essential for olfactory behavior in Drosophila melanogaster. Genetics, 164, 1447–1457.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Gerber, B., & Stocker, R. F. (2007). The Drosophila larva as a model for studying chemosensation and chemosensory learning: A review. Chemical Senses, 32, 65–89.

    Article  PubMed  CAS  Google Scholar 

  • Gibson, G., & Dworkin, I. (2004). Uncovering cryptic genetic variation. Nature Reviews Genetics, 5, 681–690.

    Article  PubMed  CAS  Google Scholar 

  • Gibson, G., & Wagner, G. (2000). Canalization in evolutionary genetic: A stabilizing theory? BioEssays, 22, 372–380.

    Article  PubMed  CAS  Google Scholar 

  • Hermisson, J., & Wagner, G. (2004). The population genetic theory of hidden variation and genetic robustness. Genetics, 168, 2271–2284.

    Article  PubMed Central  PubMed  Google Scholar 

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

    PubMed Central  PubMed  CAS  Google Scholar 

  • InfoStat. (2008). InfoStat version 2008. Argentina: Universidad Nacional de Cordoba, Grupo InfoStat.

    Google Scholar 

  • Kaiser, M., & Cobb, M. (2008). The behaviour of Drosophila melanogaster maggots is affected by social, physiological and temporal factors. Animal Behavior, 75, 1619–1628.

    Article  Google Scholar 

  • Lavagnino, N., Anholt, R. R. H., & Fanara, J. J. (2008). Variation in genetic architecture of olfactory behaviour among wild-derived populations of Drosophila melanogaster. Journal of Evolutionary Biology, 21, 988–996.

    Article  PubMed  CAS  Google Scholar 

  • Lavagnino, N., Arya, G. H., Korovaichuk, A., & Fanara, J. J. (2013). Genetic architecture of olfactory behavior in Drosophila melanogaster: Differences and similarities across development. Behavior Genetics, 43, 348–359.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Le Cunff, Y., & Pakdaman, K. (2012). Phenotype-genotype relation in Wagner’s canalization model. Journal of Theoretical Biology, 134, 69–83.

    Article  Google Scholar 

  • Le Rouzic, A., & Carlborg, O. (2008). Evolutionary potential of hidden genetic variation. Trends Ecology and Evolution, 23, 33–37.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Mackay, T. F. C. (2014). Epistasis and quantitative traits: Using model organisms to study gene–gene interactions. Nature Reviews Genetics, 15, 22–33.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mackay, T. F. C., Hackett, J. B., Lyman, R. F., Wayne, M. L., & Anholt, R. R. H. (1996). Quantitative genetic variation of odor-guided behavior in a natural population of Drosophila melanogaster. Genetics, 144, 727–735.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Masel, J., & Trotter, M. V. (2010). Robustness and evolvability. Trends in Genetics, 26, 406–414.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mensch, J., Lavagnino, N., Carreira, V. P., Massaldi, A., Hasson, E., & Fanara, J. J. (2008). Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction. BMC Developmental Biology, 8(78), 1–12. doi:10.1186/1471-213X-8-78.

    Google Scholar 

  • Monte, P., Woodad, C., Ayer, R., Lilly, M., Sun, H., & Carlson, J. (1989). Characterization of the larval olfactory response in Drosophila and its genetic basis. Behavior Genetics, 19, 267–283.

    Article  PubMed  CAS  Google Scholar 

  • Oppliger, F. Y., Guerin, P. M., & Vlimant, M. (2000). Neurophysiological and behavioral evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae. Journal of Insect Physiology, 46, 135–144.

    Article  PubMed  CAS  Google Scholar 

  • Paaby, A. B., & Rockman, M. V. (2014). Cryptic genetic variation: Evolution’s hidden substrate. Nature Reviews Genetics, 15, 247–258.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pigliucci, M. (2010). Genotype–phenotype mapping and the end of the ‘genes as blueprint’ metaphor. Philosophical Transactions Royal Society B, 365, 557–566.

    Article  CAS  Google Scholar 

  • Polaczyk, P. J., Gasperini, R., & Gibson, G. (1998). Naturally occurring genetic variation affects Drosophila photoreceptor determination. Development Genes and Evolution, 207, 462–470.

    Article  PubMed  CAS  Google Scholar 

  • Ramaekers, A., Magnenat, E., Marin, E. C., Gendre, N., Jefferis, G. S. X. E., Luo, L., & Stocker, R. F. (2005). Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Current Biology, 15, 982–992.

    Article  PubMed  CAS  Google Scholar 

  • Robertson, A. (1959). The sampling variance of the genetic correlation coefficient. Biometrics, 15, 469–485.

    Article  Google Scholar 

  • Rodrigues, V. (1980). Olfactory behavior of Drosophila melanogaster. In O. Siddiqi, P. Bvabu, L. M. Hall, & J. C. Hall (Eds.), Development and Neurobiology of Drosophila (pp. 361–372). London: Plenum Press.

    Chapter  Google Scholar 

  • Sambandan, D., Yamamoto, A., Fanara, J. J., Mackay, T. F. C., & Anholt, R. R. H. (2006). Dinamic genetic interactions determine odor-guided behavior in Drosophila melanogaster. Genetics, 174, 1349–1363.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Satorre, I., Fanara, J. J., & Lavagnino, N. (2014). Micro-geographical scale variation in Drosophila melanogaster larval olfactory behaviour is associated with host fruits heterogeneity. Entomologia Experimentalis et Applicata, 152, 23–30.

    Article  Google Scholar 

  • Spencer, C. C., Howell, C. E., Wright, A. R., & Promislow, D. E. (2003). Testing an ‘aging gene’ in long-lived Drosophila strains: Increased longevity depends on sex and genetic background. Aging Cell, 2, 123–130.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stapley, J., Reger, J., Feulner, P. G. D., Smadja, C., Galindo, J., Ekblom, R., et al. (2010). Adaptation genomics: The next generation. Trends in Ecology and Evolution, 25, 705–712.

    Article  PubMed  Google Scholar 

  • Swarup, S., Harbison, S. T., Hahn, L. E., Morozova, T. V., Yamamoto, A., Mackay, T. F. C., & Anholt, R. R. H. (2012). Extensive epistasis for olfactory behavior, sleep and waking activity in Drosophila melanogaster. Genetics Research, 94, 9–20.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Swarup, S., Huang, W., Mackay, T. F. C., & Anholt, R. R. H. (2013). Analysis of natural variation reveals neurogenetic networks for Drosophila olfactory behavior. Proceedings of the National Academy of Sciences of the United States of America, 110, 1017–1022.

    Article  PubMed Central  PubMed  Google Scholar 

  • Travisano, M., & Shaw, R. G. (2012). Lost in the Map. Evolution, 67, 305–314.

    Article  PubMed  CAS  Google Scholar 

  • Vosshall, L. B., & Stocker, R. F. (2007). Molecular architecture of smell and taste in Drosophila. Annual Review of Neuroscience, 30, 505–533.

    Article  PubMed  CAS  Google Scholar 

  • Wang, Y., Arenas, C. D., Stoebel, D. M., & Cooper, T. F. (2012). Genetic background affects epistatic interactions between two beneficial mutations. Biology Letters, 9, 1–4. doi:10.1098/rsbl.2012.0328.

    Google Scholar 

  • Wright, D., Butlin, R. K., & Carlborg, O. (2006). Epistatic regulation of behavioural and morphological traits in the zebrafish (Danio rerio). Behavior Genetics, 36, 914–922.

    Article  PubMed  Google Scholar 

  • Yamamoto, A., Anholt, R. R. H., & Mackay, T. F. C. (2009). Epistatic interactions attenuate mutations affecting startle behaviour in Drosophila melanogaster. Genetics Research, 91, 373–382.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, S., Campbell, T. G., Stone, E. A., Mackay, T. F. C., & Anholt, R. R. H. (2012). Phenotypic plasticity of the Drosophila transcriptome. PLoS Genetics, 8(3), e1002593. doi:10.1371/journal.pgen.1002593.

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhou, S., Stone, E. A., Mackay, T. F. C., & Anholt, R. R. H. (2009). Plasticity of the chemoreceptor repertoire in Drosophila melanogaster. PLoS Genetics, 5(10), e1000681. doi:10.1371/journal.pgen.1000681.

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to thank T. F. C. Mackay (North Carolina State University, Raleigh, N.C., USA) for providing balancer lines. This work was supported by grants from Agencia Nacional de Promoción Científica y Tecnológica (PICT 2012-0640) and Consejo Nacional de Ciencia y Técnica (CONICET, PIP 112-200801-02042). NJL and JJF are members of Carrera del Investigador Científico of CONICET (Argentina).

Author information

Authors and Affiliations

  1. Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428, Buenos Aires, Argentina

    Nicolas J. Lavagnino & Juan José Fanara

  2. Instituto de Ecología, Genética y Evolución (IEGEBA), CONICET, Buenos Aires, Argentina

    Nicolas J. Lavagnino & Juan José Fanara

Authors
  1. Nicolas J. Lavagnino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan José Fanara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan José Fanara.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lavagnino, N.J., Fanara, J.J. Changes Across Development Influence Visible and Cryptic Natural Variation of Drosophila melanogaster Olfactory Response. Evol Biol 43, 96–108 (2016). https://doi.org/10.1007/s11692-015-9352-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-015-9352-5

Keywords

Search

Navigation