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Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism

Abstract

Cases of convergent evolution that involve changes in the same developmental pathway, called parallelism, provide evidence that a limited number of developmental changes are available to evolve a particular phenotype1. To our knowledge, in no case are the genetic changes underlying morphological convergence understood. However, morphological convergence is not generally assumed to imply developmental parallelism2. Here we investigate a case of convergence of larval morphology in insects and show that the loss of particular trichomes, observed in one species of the Drosophila melanogaster species group, has independently evolved multiple times in the distantly related D. virilis species group3. We present genetic and gene expression data showing that regulatory changes of the shavenbaby/ovo (svb/ovo) gene underlie all independent cases of this morphological convergence. Our results indicate that some developmental regulators might preferentially accumulate evolutionary changes and that morphological parallelism might therefore be more common than previously appreciated.

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Figure 1: The pattern of dorsal trichomes has evolved repeatedly in the D. virilis species group.
Figure 2: Dorsal first-abdominal segments of parental and species-hybrid larvae.
Figure 3: The expression pattern of svb is strictly correlated with the pattern of fine trichomes across the D. virilis group of species.
Figure 4: In Drosophila borealis western, which has an intermediate dorsal pattern of fine trichomes and naked cuticle, the expression of svb (lower panel) is strictly correlated with the pattern of trichomes (upper panel) along the anterior–posterior axis.

References

  1. Hodin, J. Plasticity and constraints in development and evolution. Mol. Dev. Evol. 288, 1–20 (2000)

    CAS  Article  Google Scholar 

  2. 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 

  3. Dickinson, W. J., Tang, Y., Schuske, K. & Akam, M. Conservation of molecular prepatterns during the evolution of cuticle morphology in Drosophila larvae. Evolution 47, 1396–1406 (1993)

    CAS  Article  Google Scholar 

  4. Bokor, P. & DiNardo, S. The roles of hedgehog, wingless and lines in patterning the dorsal epidermis in Drosophila. Development 122, 1083–1092 (1996)

    CAS  PubMed  Google Scholar 

  5. 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)

    ADS  CAS  Article  Google Scholar 

  6. Spicer, G. S. & Bell, C. D. Molecular phylogeny of the Drosophila virilis species group (Diptera: Drosophilidae) inferred from mitochondrial 12S and 16S ribosomal RNA genes. Ann. Ent. Soc. Am. 95, 156–161 (2002)

    CAS  Article  Google Scholar 

  7. Darwin, C. The Origin of Species by means of Natural Selection or The Preservation of Favored Races in the Struggle for Life (Modern Library, New York, 1859)

    Google Scholar 

  8. Endler, J. A. Natural Selection in the Wild (Monographs in Population Biology, ed. May, R. M.) (Princeton Univ. Press, 1986)

    Google Scholar 

  9. Kuhn, D. T., Sawyer, M., Ventimiglia, J. & Sprey, T. E. Cuticle morphology changes with each larval molt in D. melanogaster. Drosophila Inform. Serv. 71, 218–222 (1992)

    Google Scholar 

  10. Hatini, V., Bokor, P., Goto-Mandeville, R. & DiNardo, S. Tissue- and stage-specific modulation of Wingless signaling by the segment polarity gene lines. Genes Dev. 14, 1364–1376 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Payre, F., Vincent, A. & Carreno, S. ovo/svb integrates Wingless and DER pathways to control epidermis differentiation. Nature 400, 271–275 (1999)

    ADS  CAS  Article  Google Scholar 

  12. Throckmorton, L. H. in The Genetics and Biology of Drosophila (eds Ashburner, M., Carson, H. L. & Thompson, J. N.) 227–296 (Academic, London, 1982)

    Google Scholar 

  13. Hsu, T.-C. Chromosomal Variation and Evolution in the virilis group of Drosophila. Thesis, Univ. Texas (1951).

  14. Wray, G. A. & Abouheif, E. When is homology not homology? Curr. Opin. Genet. Dev. 8, 675–680 (1998)

    CAS  Article  Google Scholar 

  15. Stewart, C.-B. & Wilson, A. C. Sequence convergence and functional adaptation of stomach lysozymes from foregut fermenters. Cold Spring Harb. Symp. Quant. Biol. 52, 891–899 (1987)

    CAS  Article  Google Scholar 

  16. ffrench-Constant, R. H. The molecular and population genetics of cyclodiene insecticide resistance. Insect Biochem. Mol. Biol. 24, 335–345 (1994)

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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Acknowledgements

We thank C. Braendle, M. Grbic, A. McGregor, H. Teotonio, L. Waltzer and members of the F.P. lab for comments on the manuscript. This work was supported by a grant from Association pour la Recherche sur le Cancer (ARC) to F.P., fellowships from Ministère de la Jeunesse, de l'Éducation Nationale et de la Recherche and ARC to I.D., and a BBSRC David Phillips Research Fellowship and NIH Grant to D.L.S.

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Correspondence to David L. Stern.

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Supplementary information

41586_2003_BFnature01768_MOESM1_ESM.pdf

Supplementary Figure: Examples of the dorsal third abdominal segment from four individuals of each species, illustrating the relative absence of variation in trichome patterns within strains. Although we have not performed an extensive population sampling of these species, we have examined several geographic isolates of most species and have not yet found any evidence for intraspecific polymorphisms. (PDF 381 kb)

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Sucena, E., Delon, I., Jones, I. et al. Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism. Nature 424, 935–938 (2003). https://doi.org/10.1038/nature01768

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