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Developmental genetic bases behind the independent origin of the tympanic membrane in mammals and diapsids

Author

Listed:
  • Taro Kitazawa

    (Graduate School of Medicine, The University of Tokyo
    Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Chiyoda-ku)

  • Masaki Takechi

    (Evolutionary Morphology Laboratory, RIKEN
    Iwate Medical University
    Present address: Section of Molecular Craniofacial Embryology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University (TMDU), 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8549, Japan)

  • Tatsuya Hirasawa

    (Evolutionary Morphology Laboratory, RIKEN)

  • Noritaka Adachi

    (Evolutionary Morphology Laboratory, RIKEN)

  • Nicolas Narboux-Nême

    (Évolution des Régulations Endocriniennes, CNRS UMR 7221, Muséum National, d’Histoire Naturelle)

  • Hideaki Kume

    (Graduate School of Medicine, The University of Tokyo)

  • Kazuhiro Maeda

    (Medical Research Institute, Tokyo Women’s Medical University)

  • Tamami Hirai

    (Evolutionary Morphology Laboratory, RIKEN)

  • Sachiko Miyagawa-Tomita

    (Medical Research Institute, Tokyo Women’s Medical University)

  • Yukiko Kurihara

    (Graduate School of Medicine, The University of Tokyo
    Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Chiyoda-ku)

  • Jiro Hitomi

    (Iwate Medical University)

  • Giovanni Levi

    (Évolution des Régulations Endocriniennes, CNRS UMR 7221, Muséum National, d’Histoire Naturelle)

  • Shigeru Kuratani

    (Evolutionary Morphology Laboratory, RIKEN)

  • Hiroki Kurihara

    (Graduate School of Medicine, The University of Tokyo
    Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Chiyoda-ku
    Institute for Biology and Mathematics of Dynamical Cell Processes (iBMath), The University of Tokyo)

Abstract

The amniote middle ear is a classical example of the evolutionary novelty. Although paleontological evidence supports the view that mammals and diapsids (modern reptiles and birds) independently acquired the middle ear after divergence from their common ancestor, the developmental bases of these transformations remain unknown. Here we show that lower-to-upper jaw transformation induced by inactivation of the Endothelin1-Dlx5/6 cascade involving Goosecoid results in loss of the tympanic membrane in mouse, but causes duplication of the tympanic membrane in chicken. Detailed anatomical analysis indicates that the relative positions of the primary jaw joint and first pharyngeal pouch led to the coupling of tympanic membrane formation with the lower jaw in mammals, but with the upper jaw in diapsids. We propose that differences in connection and release by various pharyngeal skeletal elements resulted in structural diversity, leading to the acquisition of the tympanic membrane in two distinct manners during amniote evolution.

Suggested Citation

  • Taro Kitazawa & Masaki Takechi & Tatsuya Hirasawa & Noritaka Adachi & Nicolas Narboux-Nême & Hideaki Kume & Kazuhiro Maeda & Tamami Hirai & Sachiko Miyagawa-Tomita & Yukiko Kurihara & Jiro Hitomi & Gi, 2015. "Developmental genetic bases behind the independent origin of the tympanic membrane in mammals and diapsids," Nature Communications, Nature, vol. 6(1), pages 1-7, November.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms7853
    DOI: 10.1038/ncomms7853
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