Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies

Abstract

Some morphological traits differ greatly between related species, but it is not clear whether diversity evolves through changes in the same genes and whether similar, independent (that is, convergent) changes occur by the same mechanism1,2. Pigmentation in fruitflies presents an attractive opportunity to explore these issues because pigmentation patterns are diverse, similar patterns have arisen in independent clades, and numerous genes governing their formation have been identified3,4,5 in Drosophila melanogaster. Here we show that both evolutionary diversification and convergence can be due to evolution at the same locus, by comparing abdominal pigmentation and trichome patterns and the expression of Bric-à-brac2 (Bab2), which regulates both traits in D. melanogaster3,6, in 13 species representing the major clades7,8 of the subfamily Drosophilinae. Modifications of Bab2 expression are frequently correlated with diverse pigmentation and trichome patterns that evolved independently in multiple lineages. In a few species, Bab2 expression is not correlated with changes in pigmentation but is correlated with a conserved pattern of trichomes, indicating that this locus can be circumvented to evolve new patterns when a correlated trait is under different constraints.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Modulation of Bab2 expression is correlated with diverse abdominal pigmentation patterns.
Figure 2: Modulation of Bab2 expression underlies the diversification and evolutionary convergence of cuticular traits throughout the Drosophilinae.
Figure 3: Bab2 expression is correlated with the distribution of cuticular trichomes.

References

  1. Wray, G. A. Do convergent developmental mechanisms underlie convergent phenotypes? Brain Behav. Evol. 59, 327–336 (2002)

    Article  Google Scholar 

  2. Maynard Smith, J. et al. Developmental constraints and evolution. Q. Rev. Biol. 60, 265–287 (1985)

    Article  Google Scholar 

  3. Kopp, A., Duncan, I., Godt, D. & Carroll, S. B. Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408, 553–559 (2000)

    ADS  CAS  Article  Google Scholar 

  4. Kopp, A. & Duncan, I. Control of cell fate and polarity in the adult abdominal segments of Drosophila by optomotor-blind. Development 124, 3715–3726 (1997)

    CAS  PubMed  Google Scholar 

  5. 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 

  6. Couderc, J. L. et al. The bric-à-brac locus consists of two paralogous genes encoding BTB/POZ domain proteins and acts as a homeotic and morphogenetic regulator of imaginal development in Drosophila. Development 129, 2419–2433 (2002)

    CAS  PubMed  Google Scholar 

  7. Grimaldi, D. A. A phylogenetic, revised classification of genera in the Drosophilidae (Diptera). Bull. Am. Mus. Nat. Hist. 197, 1–139 (1990)

    Google Scholar 

  8. 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 

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

    Google Scholar 

  10. Lachaise, D. et al. Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from Sao Tome. Proc. R. Soc. Lond. B 267, 1487–1495 (2000)

    CAS  Article  Google Scholar 

  11. 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)

    CAS  Article  Google Scholar 

  12. Ayala, F. J. Sibling species of the Drosophila serrata group. Evolution 19, 538–545 (1965)

    Article  Google Scholar 

  13. 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)

    ADS  CAS  Article  Google Scholar 

  14. Kopp, A., Graze, R. M., Xu, S., Carroll, S. B. & Nuzhdin, S. V. Quantitative trait loci responsible for variation in sexually dimorphic traits in Drosophila melanogaster. Genetics 163, 771–787 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Calleja, M. et al. Generation of medial and lateral dorsal body domains by the pannier gene of Drosophila. Development 127, 3971–3980 (2000)

    CAS  PubMed  Google Scholar 

  16. Kopp, A., Blackman, R. K. & Duncan, I. Wingless, decapentaplegic and EGF receptor signaling pathways interact to specify dorso-ventral pattern in the adult abdomen of Drosophila. Development 126, 3495–3507 (1999)

    CAS  PubMed  Google Scholar 

  17. Abzhanov, A. & Kaufman, T. C. Crustacean (malacostracan) Hox genes and the evolution of the arthropod trunk. Development 127, 2239–2249 (2000)

    CAS  PubMed  Google Scholar 

  18. Schutt, C. & Nothiger, R. Structure, function and evolution of sex-determining systems in dipteran insects. Development 127, 667–677 (2000)

    CAS  PubMed  Google Scholar 

  19. Wulbeck, C. & Simpson, P. The expression of pannier and achaete-scute homologues in a mosquito suggests an ancient role of pannier as a selector gene in the regulation of the dorsal body pattern. Development 129, 3861–3871 (2002)

    CAS  PubMed  Google Scholar 

  20. Majerus, M. E. N. Ladybirds (HarperCollins, London, 1994)

    Google Scholar 

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

    Google Scholar 

  22. Madhavan, M. M. & Madhavan, K. Morphogenesis of the epidermis of adult abdomen of Drosophila. J. Embryol. Exp. Morphol. 60, 1–31 (1980)

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  24. Kwiatowski, J. & Ayala, F. J. Phylogeny of Drosophila and related genera: Conflict between molecular and anatomical analyses. Mol. Phylogenet. Evol. 13, 319–328 (1999)

    CAS  Article  Google Scholar 

  25. Maddison, D. & Maddison, W. MacClade 4: Analysis of Phylogeny and Character Evolution (Sinauer, Sunderland, Massachusetts, 2000)

    MATH  Google Scholar 

Download references

Acknowledgements

We thank C. Nelson for help with fly collection; D. Lachaise and P. O'Grady for species identification; T. Markow, L. Andrew (Tucson Stock Center), J. Coyne and D. Lachaise for providing fly stocks; F. Laski and D. Godt for the Bab2 antibody; V. Kassner for invaluable technical assistance; A. Rokas for help with character reconstruction; and B. Williams, A. Kopp, A. Rokas and C. Nelson for discussions on the project. N.G. has been funded by the Howard Hughes Medical Institute and the Philippe foundation and is supported by an EMBO long-term post-doctoral fellowship. The project was supported by the Howard Hughes Medical Institute (S.B.C.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sean B. Carroll.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gompel, N., Carroll, S. Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies. Nature 424, 931–935 (2003). https://doi.org/10.1038/nature01787

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01787

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing