Abstract
The origin of the mammalian middle ear ossicles from the craniomandibular articulation of their synapsid ancestors is a key event in the evolution of vertebrates. The richness of the fossil record and the multitude of developmental studies have provided a stepwise reconstruction of this evolutionary innovation, highlighting the homology between the quadrate, articular, pre-articular and angular bones of early synapsids with the incus, malleus, gonial and ectotympanic bones of derived mammals, respectively. There are several aspects involved in this functional exaptation: (i) an increase of the masticatory musculature; (ii) the separation of the quadrate bone from the cranium; and (iii) the disconnection of the post-dentary bones from the dentary. Here, we compared the jaw-otic complex for 43 synapsid taxa using anatomical network analysis, showing that the disconnection of mandibular bones was a key step in the mammalian middle ear evolution, changing the skull anatomical modularity concomitant to the acquisition of new functions. Furthermore, our analysis allows the identification of three types of anatomical modules evolving through five evolutionary stages during the anatomical transformation of the jawbones into middle ear bones, with the ossification and degradation of Meckel's cartilage in mammals as the key ontogenetic event leading the change of anatomical modularity.
Highlights
Several structures of the middle ear of mammals evolved from the lower jaw of basal synapsids through a series of anatomical changes that started about 315 million years ago
We focused on changes in the organization of morphological modules linked to the key events underlying the evolution of the jaw-otic complex in synapsids, such as the cranial disconnection of the quadrate bone (Kemp, 1979, 2007; Kermack et al, 1981; Luo & Crompton, 1994; Laurin, 1998; Luo, 2011), the ossification of the Meckel’s cartilage (Wang et al, 2001; Meng et al, 2011), and the separation of the post-dentary bones from the lower jaw (Rich et al, 2005; Luo et al, 2007; Luo, 2011; Meng et al, 2011; Anthwal et al, 2013; Han et al, 2017; Urban et al, 2017)
Our anatomical network analysis of the mammalian middle ear aligns with current views on the processes leading to its evolution, while providing new sources of information to characterize and trace its evolutionary patterns
Summary
Several structures of the middle ear of mammals evolved from the lower jaw of basal synapsids through a series of anatomical changes that started about 315 million years ago. The evolutionary history of the synapsid lower jaw suggests a trade-off between an increase in the area of muscle attachment and a reduction of some mandibular bones to improve sound transmission During the Permian, synapsids evolved a new powerful adductor musculature attached to jawbones (Kemp, 1969, 1979; Reisz, 1972; Fourie, 1974; Crompton & Parker, 1978).
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