Pattern and polarity in the development and evolution of the gnathostome jaw: Both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula

Claudia Compagnucci, Melanie Debiais-Thibaud, Marion Coolen, Jennifer Fish, John N. Griffin, Federica Bertocchini, Maryline Minoux, Filippo M. Rijli, Véronique Borday-Birraux, Didier Casane, Sylvie Mazan, Michael J. Depew

Research output: Contribution to journalArticle

Abstract

The acquisition of jaws constitutes a landmark event in vertebrate evolution, one that in large part potentiated their success and diversification. Jaw development and patterning involves an intricate spatiotemporal series of reciprocal inductive and responsive interactions between the cephalic epithelia and the cranial neural crest (CNC) and cephalic mesodermal mesenchyme. The coordinated regulation of these interactions is critical for both the ontogenetic registration of the jaws and the evolutionary elaboration of variable jaw morphologies and designs. Current models of jaw development and evolution have been built on molecular and cellular evidence gathered mostly in amniotes such as mice, chicks and humans, and augmented by a much smaller body of work on the zebrafish. These have been partnered by essential work attempting to understand the origins of jaws that has focused on the jawless lamprey. Chondrichthyans (cartilaginous fish) are the most distant group to amniotes within extant gnathostomes, and comprise the crucial clade uniting amniotes and agnathans; yet despite their critical phylogenetic position, evidence of the molecular and cellular underpinnings of jaw development in chondrichthyans is still lacking. Recent advances in genome and molecular developmental biology of the lesser spotted dogfish shark, Scyliorhinus canicula, make it ideal for the molecular study of chondrichthyan jaw development. Here, following the 'Hinge and Caps' model of jaw development, we have investigated evidence of heterotopic (relative changes in position) and heterochronic (relative changes in timing) shifts in gene expression, relative to amniotes, in the jaw primordia of S. canicula embryos. We demonstrate the presence of clear proximo-distal polarity in gene expression patterns in the shark embryo, thus establishing a baseline molecular baüplan for branchial arch-derived jaw development and further validating the utility of the 'Hinge and Caps' model in comparative studies of jaw development and evolution. Moreover, we correlate gene expression patterns with the absence of a lambdoidal junction (formed where the maxillary first arch meets the frontonasal processes) in chondrichthyans, further highlighting the importance of this region for the development and evolution of jaw structure in advanced gnathostomes.

Original languageEnglish
Pages (from-to)428-448
Number of pages21
JournalDevelopmental Biology
Volume377
Issue number2
DOIs
Publication statusPublished - May 15 2013

Keywords

  • Branchial arch
  • Evolution
  • Heterotopy
  • Jaws
  • Shark

ASJC Scopus subject areas

  • Developmental Biology
  • Cell Biology
  • Molecular Biology

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    Compagnucci, C., Debiais-Thibaud, M., Coolen, M., Fish, J., Griffin, J. N., Bertocchini, F., Minoux, M., Rijli, F. M., Borday-Birraux, V., Casane, D., Mazan, S., & Depew, M. J. (2013). Pattern and polarity in the development and evolution of the gnathostome jaw: Both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula. Developmental Biology, 377(2), 428-448. https://doi.org/10.1016/j.ydbio.2013.02.022