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

• Published in: Nature communications Vol. 6; no. 1; p. 6853
• Main Authors: Kitazawa, Taro, Takechi, Masaki, Hirasawa, Tatsuya, Adachi, Noritaka, Narboux-Nême, Nicolas, Kume, Hideaki, Maeda, Kazuhiro, Hirai, Tamami, Miyagawa-Tomita, Sachiko, Kurihara, Yukiko, Hitomi, Jiro, Levi, Giovanni, Kuratani, Shigeru, Kurihara, Hiroki
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 22.04.2015; Nature Publishing Group; Nature Pub. Group
• Subjects: 14; 38; 38/1; 631/136/1660; 631/181/2474; 631/181/2806; 64; 64/110; 64/60; 82; Ambystoma mexicanum - embryology; Ambystoma mexicanum - genetics; Animals; Base Sequence; Development Biology; 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; Humanities and Social Sciences; Life Sciences; Lizards - embryology; Lizards - genetics; Mandible - embryology; Maxilla - embryology; Mice - embryology; Mice - genetics; Molecular Sequence Data; Morphogenesis; multidisciplinary; Paired Box Transcription Factors - genetics; Paired Box Transcription Factors - metabolism; Receptor, Endothelin A - genetics; Receptor, Endothelin A - metabolism; Science; Science (multidisciplinary); Sharks - embryology; Sharks - genetics; Transcription Factors - genetics; Transcription Factors - metabolism; Tympanic Membrane - embryology; Morphogenesis; Evolutionary genetics; Evolutionary developmental biology
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/ncomms7853

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. The evolution of the amniote middle ear remains unclear. Here, the authors show that inactivation of the Edn1-Dlx5/6 cascade during development results in loss of the tympanic membrane in mouse and duplication in chicken, which suggests independent evolution of the tympanic membrane in different amniotes.