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

Taro Kitazawa; Masaki Takechi; Tatsuya Hirasawa; Noritaka Adachi; Nicolas Narboux-Nême; Hideaki Kume; Kazuhiro Maeda; Tamami Hirai; Sachiko Miyagawa-Tomita; Yukiko Kurihara; Jiro Hitomi; Giovanni Levi; Shigeru Kuratani; Hiroki Kurihara

doi:10.1038/ncomms7853

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

Nat Commun. 2015 Apr 22:6:6853. doi: 10.1038/ncomms7853.

Authors

Affiliations

¹ 1] Department of Physiological Chemistry and Metabolism, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan [2] Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Chiyoda-ku, Tokyo 102-0076, Japan.
² 1] Evolutionary Morphology Laboratory, RIKEN, 2-2-3 Minatojimaminami-machi, Chuo-ku, Kobe 650-0047, Japan [2] Division of Human Embryology, Department of Anatomy, Iwate Medical University, 2-1-1 Nishitokuta, Yahaba-cho, Shiwa-gun, Iwate 028-3694, Japan.
³ Evolutionary Morphology Laboratory, RIKEN, 2-2-3 Minatojimaminami-machi, Chuo-ku, Kobe 650-0047, Japan.
⁴ volution des Régulations Endocriniennes, CNRS UMR 7221, Muséum National, d'Histoire Naturelle, Paris, Cedex 05 75231, France.
⁵ Department of Physiological Chemistry and Metabolism, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
⁶ Division of Cardiovascular Development and Differentiation, Department of Pediatric Cardiology, Medical Research Institute, Tokyo Women's Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo 162-8666, Japan.
⁷ Division of Human Embryology, Department of Anatomy, Iwate Medical University, 2-1-1 Nishitokuta, Yahaba-cho, Shiwa-gun, Iwate 028-3694, Japan.
⁸ 1] Department of Physiological Chemistry and Metabolism, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan [2] Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Chiyoda-ku, Tokyo 102-0076, Japan [3] Institute for Biology and Mathematics of Dynamical Cell Processes (iBMath), The University of Tokyo, 3-8-1 Komaba, Tokyo 153-8914, Japan.

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.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Ambystoma mexicanum / embryology*
Ambystoma mexicanum / genetics
Animals
Base Sequence
Embryo, Mammalian
Embryo, Nonmammalian
Endothelin-1 / genetics*
Endothelin-1 / metabolism
Evolution, Molecular
Gene Expression Regulation, Developmental
Goosecoid Protein / genetics
Goosecoid Protein / metabolism
Homeodomain Proteins / genetics
Homeodomain Proteins / metabolism
Lizards / embryology*
Lizards / genetics
Mandible / embryology
Maxilla / embryology
Mice / embryology*
Mice / genetics
Molecular Sequence Data
Paired Box Transcription Factors / genetics
Paired Box Transcription Factors / metabolism
Receptor, Endothelin A / genetics*
Receptor, Endothelin A / metabolism
Sharks / embryology*
Sharks / genetics
Transcription Factors / genetics
Transcription Factors / metabolism
Tympanic Membrane / embryology*

Substances

Dlx5 protein, mouse
Dlx6 protein, mouse
Endothelin-1
Goosecoid Protein
Homeodomain Proteins
Nkx3-2 protein, mouse
Paired Box Transcription Factors
Receptor, Endothelin A
Transcription Factors
PAX1 transcription factor

Associated data

GENBANK/AB985798