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The role of the pupal determinant broad during embryonic development of a direct-developing insect

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Abstract

Metamorphosis is one of the most common, yet dramatic of life history strategies. In insects, complete metamorphosis with morphologically distinct larval stages arose from hemimetabolous ancestors that were more direct developing. Over the past century, several ideas have emerged that suggest the holometabolous pupa is developmentally homologous to the embryonic stages of the hemimetabolous ancestor. Other theories consider the pupal stage to be a modification of a hemimetabolous nymph. To address this question, we have isolated an ortholog of the pupal determinant, broad (br), from the hemimetabolous milkweed bug and examined its role during embryonic development. We show that Oncopeltus fasciatus br (Of’br) is expressed in two phases. The first occurs during germ band invagination and segmentation when Of’br is expressed ubiquitously in the embryonic tissues. The second phase of Of’br expression appears during the pronymphal phase of embryogenesis and persists through nymphal differentiation to decline just before hatching. Knock-down of Of’br transcripts results in defects that range from posterior truncations in the least-affected phenotypes to completely fragmented embryonic tissues in the most severe cases. Analysis of the patterning genes engrailed and hunchback reveal loss of segments and a failure in neural differentiation after Of’br depletion. Finally, we show that br is constitutively expressed during embyrogenesis of the ametabolous firebrat, Thermobia domestica. This suggests that br expression is prominent during embryonic development of ametabolous and hemimetabolous insects but was lost with the emergence of the completely metamorphosing insects.

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Acknowledgments

We thank Dr. Paul Liu and Thom Kaufman (Indiana University, Bloomington) for a gift of the digoxigenin-labeled Of’en probe as well as cDNAs for Of’Kr, Of’hb, and Of’eve. We also thank Bilal Ahmad and Shaunna Harris for the initial isolation of the Thermobia broad gene, and Dr. Takashi Koyama for consultation on molecular techniques. This study was supported by NSF grant IBN-9904959 to JWT and NIH grant GM60122 to LMR.

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Author notes

  1. Deniz F. Erezyilmaz

    Present address: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, 08544, USA

  2. Melody R. Rynerson

    Present address: Department of Genome Sciences, University of Washington, Seattle, WA, 98195, USA

  3. James W. Truman & Lynn M. Riddiford

    Present address: Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, VA, 20147, USA

Authors and Affiliations

  1. Department of Biology, University of Washington, Seattle, WA, 98195-1800, USA

    Deniz F. Erezyilmaz, Melody R. Rynerson, James W. Truman & Lynn M. Riddiford

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  1. Deniz F. Erezyilmaz
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  2. Melody R. Rynerson
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  3. James W. Truman
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Correspondence to Deniz F. Erezyilmaz.

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Communicated by P. Simpson

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Erezyilmaz, D.F., Rynerson, M.R., Truman, J.W. et al. The role of the pupal determinant broad during embryonic development of a direct-developing insect. Dev Genes Evol 219, 535–544 (2009). https://doi.org/10.1007/s00427-009-0315-7

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