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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.

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References

  1. 1

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

  2. 2

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

  3. 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)

  4. 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)

  5. 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)

  6. 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)

  7. 7

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

  8. 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)

  9. 9

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

  10. 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)

  11. 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)

  12. 12

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

  13. 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)

  14. 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)

  15. 15

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

  16. 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)

  17. 17

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

  18. 18

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

  19. 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)

  20. 20

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

  21. 21

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

  22. 22

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

  23. 23

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

  24. 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)

  25. 25

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

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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.).

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Correspondence to Sean B. Carroll.

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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.

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