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.
Highlights
The amniote middle ear is a classical example of the evolutionary novelty
In contrast to the classical hypothesis that the ventral swelling of the first pharyngeal pouch (PP1) enables acquisition of the lower-jaw-associated tympanic membrane (TM) in mammals[23], our comparative anatomical analysis indicates that the dorsal shift of the primary jaw joint (PJJ) towards PP1 leads to differential coupling of the TM to jaw skeletons in avians and mammals
Gsc-dependent angular the recent paleontological hypothesis that mammals and diapsids independently acquired the middle ear[5,6,7,8], we analysed the dorsoventral patterning of TMs through a developmental biological approach in mouse and chicken embryos
Summary
The amniote middle ear is a classical example of the evolutionary novelty. 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. In diapsids the TM attaches to the quadrate, an upper jaw element, while in mammals it spans the tympanic ring, an angular homologue associated with the lower jaw This raises the possibility that despite the fact that they are derived from histologically comparable elements (endodermal and ectodermal invaginations and intervening tissues), the TMs were independently acquired in synapsids and diapsids, which exhibit distinct developmental topographies[2,3]. We show that lower-to-upper jaw transformation induced by inactivation of the Edn1-Dlx5/6 cascade involving Gsc results in loss of the TM in mouse, but causes duplication of the TM in chicken, indicating that the TMs of mammals and diapsids are coupled with the development of the lower and upper jaws, respectively. This report endows developmental and molecular evidence to support independent origin of the middle ear in different amniote taxa and the novel insight into the developmental process that led to these distinct middle ear patterns
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