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Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila

Nature volume 433, pages 481–487 (2005)Cite this article

Abstract

The gain, loss or modification of morphological traits is generally associated with changes in gene regulation during development. However, the molecular bases underlying these evolutionary changes have remained elusive. Here we identify one of the molecular mechanisms that contributes to the evolutionary gain of a male-specific wing pigmentation spot in Drosophila biarmipes, a species closely related to Drosophila melanogaster. We show that the evolution of this spot involved modifications of an ancestral cis-regulatory element of the yellow pigmentation gene. This element has gained multiple binding sites for transcription factors that are deeply conserved components of the regulatory landscape controlling wing development, including the selector protein Engrailed. The evolutionary stability of components of regulatory landscapes, which can be co-opted by chance mutations in cis-regulatory elements, might explain the repeated evolution of similar morphological patterns, such as wing pigmentation patterns in flies.

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Figure 1: Expression of the Yellow protein prefigures adult wing pigmentation.
Figure 2: Cis-regulatory changes at the yellow locus are responsible for species-specific differences in Yellow distribution.
Figure 3: The cis-regulatory sequences governing spot formation evolved in the context of an ancestral wing enhancer.
Figure 4: The spot element evolved through the acquisition of sites for both activators and repressors.
Figure 5: Concerted changes in the expression of Yellow and Ebony underlie the evolution of novel wing patterns.
Figure 6: Cryptic prepatterns and the evolution of novel gene expression patterns through the evolution of cis-regulatory sequences.

References

  1. Carroll, S. B., Grenier, J. K. & Weatherbee, S. D. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design 2nd edn (Blackwell Science, Malden, Massachusetts, 2004)

    Google Scholar 

  2. Davidson, E. H. Genomic Regulatory Systems: Development and Evolution (Academic, San Diego, 2001)

    Google Scholar 

  3. Stern, D. L. Evolutionary developmental biology and the problem of variation. Evolution 54, 1079–1091 (2000)

    Article  CAS  Google Scholar 

  4. Averof, M. & Patel, N. H. Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388, 682–686 (1997)

    Article  ADS  CAS  Google Scholar 

  5. Gompel, N. & Carroll, S. B. Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies. Nature 424, 931–935 (2003)

    Article  ADS  CAS  Google Scholar 

  6. Yoon, H. S. & Baum, D. A. Transgenic study of parallelism in plant morphological evolution. Proc. Natl Acad. Sci. USA 101, 6524–6529 (2004)

    Article  ADS  CAS  Google Scholar 

  7. Sucena, E. & Stern, D. L. Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. Proc. Natl Acad. Sci. USA 97, 4530–4534 (2000)

    Article  ADS  CAS  Google Scholar 

  8. Shapiro, M. D. et al. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717–723 (2004)

    Article  ADS  CAS  Google Scholar 

  9. Stern, D. L. A role of Ultrabithorax in morphological differences between Drosophila species. Nature 396, 463–466 (1998)

    Article  ADS  CAS  Google Scholar 

  10. Wang, R. L., Stec, A., Hey, J., Lukens, L. & Doebley, J. The limits of selection during maize domestication. Nature 398, 236–239 (1999)

    Article  ADS  CAS  Google Scholar 

  11. Wittkopp, P. J., Vaccaro, K. & Carroll, S. B. Evolution of yellow gene regulation and pigmentation in Drosophila . Curr. Biol. 12, 1547–1556 (2002)

    Article  CAS  Google Scholar 

  12. Wang, X. & Chamberlin, H. M. Multiple regulatory changes contribute to the evolution of the Caenorhabditis lin-48 ovo gene. Genes Dev. 16, 2345–2349 (2002)

    Article  CAS  Google Scholar 

  13. Belting, H. G., Shashikant, C. S. & Ruddle, F. H. Modification of expression and cis-regulation of Hoxc8 in the evolution of diverged axial morphology. Proc. Natl Acad. Sci. USA 95, 2355–2360 (1998)

    Article  ADS  CAS  Google Scholar 

  14. Bock, I. R. & Wheeler, M. R. in Studies in Genetics (ed. Wheeler, M. R.) 1–102 (Univ. of Texas, Austin, 1972)

    Google Scholar 

  15. Majerus, M. E. N. Melanism: Evolution in Action (Oxford Univ. Press, Oxford, 1998)

    Google Scholar 

  16. Singh, B. N. & Chatterjee, S. Greater mating success of Drosophila biarmipes males possessing an apical dark black wing patch. Ethology 75, 81–83 (1987)

    Article  Google Scholar 

  17. Kopp, A. & True, J. R. Evolution of male sexual characters in the oriental Drosophila melanogaster species group. Evol. Dev. 4, 278–291 (2002)

    Article  Google Scholar 

  18. True, J. R., Edwards, K. A., Yamamoto, D. & Carroll, S. B. Drosophila wing melanin patterns form by vein-dependent elaboration of enzymatic prepatterns. Curr. Biol. 9, 1382–1391 (1999)

    Article  CAS  Google Scholar 

  19. Wittkopp, P. J., True, J. R. & Carroll, S. B. Reciprocal functions of the Drosophila Yellow and Ebony proteins in the development and evolution of pigment patterns. Development 129, 1849–1858 (2002)

    CAS  PubMed  Google Scholar 

  20. Chia, W. et al. Molecular analysis of the yellow locus of Drosophila . EMBO J. 5, 3597–3605 (1986)

    Article  CAS  Google Scholar 

  21. Geyer, P. K. & Corces, V. G. Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the yellow locus in Drosophila melanogaster . Genes Dev. 1, 996–1004 (1987)

    Article  CAS  Google Scholar 

  22. Kopp, A. & True, J. R. Phylogeny of the oriental Drosophila melanogaster species group: a multilocus reconstruction. Syst. Biol. 51, 786–805 (2002)

    Article  Google Scholar 

  23. Schawaroch, V. Phylogeny of a paradigm lineage: the Drosophila melanogaster species group (Diptera: Drosophilidae). Biol. J. Linn. Soc. 76, 21–37 (2002)

    Article  Google Scholar 

  24. Garcia-Bellido, A., Ripoll, P. & Morata, G. Developmental compartmentalization of the wing disk of Drosophila . Nat. New Biol. 245, 251–253 (1973)

    Article  CAS  Google Scholar 

  25. Blair, S. S. Engrailed expression in the anterior lineage compartment of the developing wing blade of Drosophila . Development 115, 21–33 (1992)

    CAS  PubMed  Google Scholar 

  26. Solano, P. J. et al. Genome-wide identification of in vivo Drosophila Engrailed-binding DNA fragments and related target genes. Development 130, 1243–1254 (2003)

    Article  CAS  Google Scholar 

  27. Wittkopp, P. J., Williams, B. L., Selegue, J. E. & Carroll, S. B. Drosophila pigmentation evolution: Divergent genotypes underlying convergent phenotypes. Proc. Natl Acad. Sci. USA 100, 1808–1813 (2003)

    Article  ADS  CAS  Google Scholar 

  28. Llopart, A., Elwyn, S., Lachaise, D. & Coyne, J. A. Genetics of a difference in pigmentation between Drosophila yakuba and Drosophila santomea . Evolution 56, 2262–2277 (2002)

    Article  CAS  Google Scholar 

  29. Russo, C. A., Takezaki, N. & Nei, M. Molecular phylogeny and divergence times of drosophilid species. Mol. Biol. Evol. 12, 391–404 (1995)

    CAS  PubMed  Google Scholar 

  30. Powell, J. R. Progress and Prospects in Evolutionary Biology: the Drosophila Model (Oxford Univ. Press, New York, 1997)

    Google Scholar 

  31. Hardy, D. E. Diptera: Cyclorrhapha II, Series Schizophora, Section Acalypterae I, Family Drosophilidae (Univ. of Hawaii Press, Honolulu, 1965)

    Google Scholar 

  32. De Celis, J. F. Pattern formation in the Drosophila wing: The development of the veins. BioEssays 25, 443–451 (2003)

    Article  CAS  Google Scholar 

  33. Blair, S. S. Compartments and appendage development in Drosophila . BioEssays 17, 299–309 (1995)

    Article  CAS  Google Scholar 

  34. Gonzalez, P., Rao, P. V., Nunez, S. B. & Zigler, J. S. Jr Evidence for independent recruitment of zeta-crystallin/quinone reductase (CRYZ) as a crystallin in camelids and hystricomorph rodents. Mol. Biol. Evol. 12, 773–781 (1995)

    CAS  PubMed  Google Scholar 

  35. Monod, J. Le Hasard et la Nécessité. Essai sur la Philosophie Naturelle de la Biologie Moderne (Éditions du Seuil, Paris, 1970)

    Google Scholar 

  36. Kauffman, S. A. At Home in the Universe: the Search for the Laws of Self-organization and Complexity (Oxford Univ. Press, New York, 1995)

    Google Scholar 

  37. Wheeler, M. R. & Clayton, F. E. A new Drosophila culture technique. Drosophila Inf. Serv. 40, 98 (1965)

    Google Scholar 

  38. Ashburner, M. Drosophila. A Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 1989)

    Google Scholar 

  39. Spradling, A. C. & Rubin, G. M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218, 341–347 (1982)

    Article  ADS  CAS  Google Scholar 

  40. Miller, D. F., Holtzman, S. L. & Kaufman, T. C. Customized microinjection glass capillary needles for P-element transformations in Drosophila melanogaster . Biotechniques 33, 366–375 (2002)

    Article  CAS  Google Scholar 

  41. Flybase. http://flybase.bio.indiana.edu.

  42. Barolo, S., Carver, L. A. & Posakony, J. W. GFP and β-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila . Biotechniques 29, 726–732 (2000)

    Article  CAS  Google Scholar 

  43. Celniker, S. E. et al. Finishing a whole-genome shotgun: release 3 of the Drosophila melanogaster euchromatic genome sequence. Genome Biol. 3, RESEARCH0079 (2002)

  44. Human Genome Sequencing Center. Drosophila genome project. http://www.hgsc.bcm.tmc.edu/projects/drosophila/ (2002).

  45. Schendel, P. F. in Current Protocols in Molecular Biology (eds Ausubel, F. M. et al.) 16.7.1–16.7.7 (Wiley, New York, 1993)

    Google Scholar 

  46. Bock, I. R. Current status of the Drosophila melanogaster species-group (Diptera). Syst. Entomol. 5, 341–356 (1980)

    Article  Google Scholar 

  47. Mayor, C. et al. VISTA: Visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16, 1046–1047 (2000)

    Article  CAS  Google Scholar 

  48. Remsen, J. & O'Grady, P. Phylogeny of Drosophilinae (Diptera: Drosophilidae), with comments on combined analysis and character support. Mol. Phylogenet. Evol. 24, 249–264 (2002)

    Article  Google Scholar 

Download references

Acknowledgements

We thank J. True, C. E. Nelson, C. M. Walsh and C. T. Hittinger for technical advice; J. True, S. Blair and members of the Carroll laboratory for discussions; B. L. Williams and J. Yoder for critical comments on the manuscript; S. Castrezana and T. Markow (Tucson Drosophila Stock Center) for providing Drosophila stocks; J. P. Gruber for the Euxesta sample; and S. Barolo for the pH Stinger vector. N.G. was funded by an EMBO long-term postdoctoral fellowship; B.P. and N.G. are recipients of a Philippe Foundation fellowship. The project was supported by the Howard Hughes Medical Institute (S.B.C.).

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Author notes

  1. Nicolas Gompel & Benjamin Prud'homme

    Present address: Department of Zoology, Cambridge University, Downing Street, Cambridge, CB2 3EJ, UK

  2. Patricia J. Wittkopp

    Present address: Department of Molecular Biology and Genetics, 227 Biotechnology Building, Cornell University, Ithaca, New York, 14853, USA

  3. Nicolas Gompel: These authors contributed equally to this work

Authors and Affiliations

  1. Howard Hughes Medical Institute and Laboratory of Molecular Biology, University of Wisconsin, 1525 Linden Drive, Wisconsin, 53706, Madison, USA

    Nicolas Gompel, Benjamin Prud'homme, Patricia J. Wittkopp, Victoria A. Kassner & Sean B. Carroll

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Correspondence to Sean B. Carroll.

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Supplementary information

Supplementary Figure 1

Sequence alignment of the wing enhancers of D. melanogaster, D. biarmipes and D. pseudoobscura. (DOC 44 kb)

Supplementary Table 1

Sequences of oligonucleotides used for reporter constructs. (DOC 30 kb)

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Gompel, N., Prud'homme, B., Wittkopp, P. et al. Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433, 481–487 (2005). https://doi.org/10.1038/nature03235

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