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

Nature volume 424, pages 935–938 (2003)Cite this article

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.

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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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  1. Elio Sucena

    Present address: Instituto Gulbenkian de Ciência, Rua da quinta grande 6, 2780-156, Oeiras, Portugal

  2. Elio Sucena and Isabelle Delon: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, 08544, USA

    Elio Sucena & David L. Stern

  2. Centre de Biologie du Développement, Bâtiment 4R3, 118 Route de Narbonne, 31062, cedex4, Toulouse, France

    Isabelle Delon & François Payre

  3. Vanguard High School, 317 East 67th Street, New York, New York, 10021, USA

    Isaac Jones

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  1. Elio Sucena
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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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