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Pleiotropic fitness effects of the Tre1-Gr5a region in Drosophila melanogaster

Nature Genetics volume 38, pages 824–829 (2006)Cite this article

Abstract

The abundance of transposable elements and DNA repeat sequences in mammalian genomes raises the question of whether such insertions represent passive evolutionary baggage or may influence the expression of complex traits. We addressed this question in Drosophila melanogaster, in which the effects of single transposable elements on complex traits can be assessed in genetically identical individuals reared in controlled environments1. Here we demonstrate that single P-element insertions in the intergenic region between the gustatory receptor 5a (Gr5a, also known as Tre)2,3,4 and trapped in endoderm 1 (Tre1)5, which encodes an orphan receptor, exert complex pleiotropic effects on fitness traits, including selective nutrient intake, life span, and resistance to starvation and heat stress. Mutations in this region interact epistatically with downstream components of the insulin signaling pathway. Transposon-induced sex-specific and sex-antagonistic effects further accentuate the complex influences that intergenic transposable elements can contribute to quantitative trait phenotypes.

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Figure 1: P-element insertion sites and pleiotropic effects of insertions in the Tre1-Gr5a region.
Figure 2: Characterization of imprecise excision lines.
Figure 3: Epistatic interactions with the insulin signaling pathway.

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Acknowledgements

This work was supported by grants from the US National Institutes of Health (T.F.C.M., R.R.H.A.) and by the Technical and Scientific Council of Turkey TUBITAK (E.D.O.).

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Authors and Affiliations

  1. Department of Zoology, North Carolina State University, Raleigh, 27695-7617, North Carolina, USA

    Stephanie M Rollmann & Robert R H Anholt

  2. W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, 27695-7617, North Carolina, USA

    Stephanie M Rollmann, Michael M Magwire, Theodore J Morgan, Ergi D Özsoy, Akihiko Yamamoto, Trudy F C Mackay & Robert R H Anholt

  3. Department of Genetics, North Carolina State University, Raleigh, 27695-7617, North Carolina, USA

    Michael M Magwire, Theodore J Morgan, Ergi D Özsoy, Akihiko Yamamoto, Trudy F C Mackay & Robert R H Anholt

  4. Department of Biology, Hacettepe University, Beytepe Ankara, 06800, Turkey

    Ergi D Özsoy

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  1. Stephanie M Rollmann
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  7. Robert R H Anholt
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Contributions

All authors contributed to the experimental design and statistical analysis of data. S.M.R., R.R.H.A. and T.F.C.M. wrote the manuscript. S.M.R. measured starvation resistance and trehalose preference and performed molecular genetic analyses, M.M.M. measured life span, E.D.O. and T.J.M. measured heat stress, and A.Y. maintained D. melanogaster lines and constructed revertant lines.

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Correspondence to Stephanie M Rollmann or Robert R H Anholt.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Table 1

Loci with altered transcriptional regulation in P-element insertion lines. (PDF 93 kb)

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Rollmann, S., Magwire, M., Morgan, T. et al. Pleiotropic fitness effects of the Tre1-Gr5a region in Drosophila melanogaster. Nat Genet 38, 824–829 (2006). https://doi.org/10.1038/ng1823

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