Molluscan engrailed expression, serial organization, and shell evolution

Authors

  • David K. Jacobs,

    Corresponding author
    1. Department of Organismal Biology, Ecology, and Evolution, University of California, Los Angeles, 621 Charles East Young Drive, South Los Angeles, CA 90095-1606, USA;
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  • Charles G. Wray,

    1. Department of Organismal Biology, Ecology, and Evolution, University of California, Los Angeles, 621 Charles East Young Drive, South Los Angeles, CA 90095-1606, USA;
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    • 1

      Current address: Jackson Laboratory, 600 Main Street, Bar Harbor, ME 04609-1523, USA

  • Cathy J. Wedeen,

    1. Department of Cell Biology and Anatomy, New York Medical College, Valhalla, NY 10595, USA;
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  • Richard Kostriken,

    1. Department of Cell Biology and Anatomy, New York Medical College, Valhalla, NY 10595, USA;
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  • Rob DeSalle,

    1. Department of Entomology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA; and
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  • Joseph L. Staton,

    1. Department of Organismal Biology, Ecology, and Evolution, University of California, Los Angeles, 621 Charles East Young Drive, South Los Angeles, CA 90095-1606, USA;
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    • 2

      Current address: Belle W. Baruch Institute for Marine Biology and Coastal Research, University of South Carolina, Columbia, SC 29208, USA

  • Ruth D. Gates,

    1. Department of Organismal Biology, Ecology, and Evolution, University of California, Los Angeles, 621 Charles East Young Drive, South Los Angeles, CA 90095-1606, USA;
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  • David R. Lindberg

    1. Museum of Paleontology and Department of Integrative Biology, University of California, Berkeley, CA 94720, USA
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*Author for correspondence (email: djacobs@ucla.edu)

Abstract

SUMMARY Whether the serial features found in some molluscs are ancestral or derived is considered controversial. Here, in situ hybridization and antibody studies show iterated engrailed-gene expression in transverse rows of ectodermal cells bounding plate field development and spicule formation in the chiton, Lepidochitona caverna, as well as in cells surrounding the valves and in the early development of the shell hinge in the clam, Transennella tantilla. Ectodermal expression of engrailed is associated with skeletogenesis across a range of bilaterian phyla, suggesting a single evolutionary origin of invertebrate skeletons. The shared ancestry of bilaterian-invertebrate skeletons may help explain the sudden appearance of shelly fossils in the Cambrian. Our interpretation departs from the consideration of canonical metameres or segments as units of evolutionary analysis. In this interpretation, the shared ancestry of engrailed-gene function in the terminal/posterior addition of serially repeated elements during development explains the iterative expression of engrailed genes in a range of metazoan body plans.

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