scholarly journals Mammalian development does not recapitulate suspected key transformations in the evolutionary detachment of the mammalian middle ear

2016 ◽  
Vol 283 (1822) ◽  
pp. 20152606 ◽  
Author(s):  
Héctor E. Ramírez-Chaves ◽  
Stephen W. Wroe ◽  
Lynne Selwood ◽  
Lyn A. Hinds ◽  
Chris Leigh ◽  
...  

The ectotympanic, malleus and incus of the developing mammalian middle ear (ME) are initially attached to the dentary via Meckel's cartilage, betraying their origins from the primary jaw joint of land vertebrates. This recapitulation has prompted mostly unquantified suggestions that several suspected—but similarly unquantified—key evolutionary transformations leading to the mammalian ME are recapitulated in development, through negative allometry and posterior/medial displacement of ME bones relative to the jaw joint. Here we show, using µCT reconstructions, that neither allometric nor topological change is quantifiable in the pre-detachment ME development of six marsupials and two monotremes. Also, differential ME positioning in the two monotreme species is not recapitulated. This challenges the developmental prerequisites of widely cited evolutionary scenarios of definitive mammalian middle ear (DMME) evolution, highlighting the requirement for further fossil evidence to test these hypotheses. Possible association between rear molar eruption, full ME ossification and ME detachment in marsupials suggests functional divergence between dentary and ME as a trigger for developmental, and possibly also evolutionary, ME detachment. The stable positioning of the dentary and ME supports suggestions that a ‘partial mammalian middle ear’ as found in many mammaliaforms—probably with a cartilaginous Meckel's cartilage—represents the only developmentally plausible evolutionary DMME precursor.

2015 ◽  
Author(s):  
Héctor Ramirez-Chaves ◽  
Stephen Wroe ◽  
Lynne Selwood ◽  
Lyn Hinds ◽  
Chris Leigh ◽  
...  

The tympanic ring, malleus and incus of the mammalian middle ear (MME) derive from the ancestral primary jaw joint of land vertebrates. In Mesozoic mammals, evolutionary detachment of the MME from the lower jaw occurred when Meckel’s cartilage - the last connection between MME and dentary – disappeared. This disappearance is famously recapitulated in early mammalian development. Further developmental recapitulation of Mesozoic MME detachment is thought to occur in the form of negative allometry and posterior/medial replacement of MME bones relative to the jaw joint. However, despite being widely accepted, such detailed recapitulation scenarios have never been quantified. Here we show, based on µCT scans of developmental series of several marsupials and monotremes, that negative allometry of MME bones relative to the skull occurs only after MME detachment, ruling it out as a developmental detachment trigger; additionally, there is no positional change of ectotympanic or malleus relative to the dentary. Differential positioning of MME bones in the two monotreme species is also not developmentally recapitulated. Our results challenge the developmental prerequisites of widely accepted evolutionary scenarios regarding MME detachment. Rather, we observe an association of MME detachment and dental eruption, suggesting a detachment trigger relating to the onset of dentary function.


Science ◽  
2019 ◽  
Vol 367 (6475) ◽  
pp. 305-308 ◽  
Author(s):  
Fangyuan Mao ◽  
Yaoming Hu ◽  
Chuankui Li ◽  
Yuanqing Wang ◽  
Morgan Hill Chase ◽  
...  

On the basis of multiple skeletal specimens from Liaoning, China, we report a new genus and species of Cretaceous stem therian mammal that displays decoupling of hearing and chewing apparatuses and functions. The auditory bones, including the surangular, have no bone contact with the ossified Meckel’s cartilage; the latter is loosely lodged on the medial rear of the dentary. This configuration probably represents the initial morphological stage of the definitive mammalian middle ear. Evidence shows that hearing and chewing apparatuses have evolved in a modular fashion. Starting as an integrated complex in non-mammaliaform cynodonts, the two modules, regulated by similar developmental and genetic mechanisms, eventually decoupled during the evolution of mammals, allowing further improvement for more efficient hearing and mastication.


2017 ◽  
Vol 284 (1848) ◽  
pp. 20162416 ◽  
Author(s):  
Daniel J. Urban ◽  
Neal Anthwal ◽  
Zhe-Xi Luo ◽  
Jennifer A. Maier ◽  
Alexa Sadier ◽  
...  

Multiple mammalian lineages independently evolved a definitive mammalian middle ear (DMME) through breakdown of Meckel's cartilage (MC). However, the cellular and molecular drivers of this evolutionary transition remain unknown for most mammal groups. Here, we identify such drivers in the living marsupial opossum Monodelphis domestica , whose MC transformation during development anatomically mirrors the evolutionary transformation observed in fossils. Specifically, we link increases in cellular apoptosis and TGF-BR2 signalling to MC breakdown in opossums. We demonstrate that a simple change in TGF-β signalling is sufficient to inhibit MC breakdown during opossum development, indicating that changes in TGF-β signalling might be key during mammalian evolution. Furthermore, the apoptosis that we observe during opossum MC breakdown does not seemingly occur in mouse, consistent with homoplastic DMME evolution in the marsupial and placental lineages.


2017 ◽  
Vol 1 (4) ◽  
Author(s):  
Neal Anthwal ◽  
Daniel J. Urban ◽  
Zhe-Xi Luo ◽  
Karen E. Sears ◽  
Abigail S. Tucker

1995 ◽  
Vol 170 (2) ◽  
pp. 387-396 ◽  
Author(s):  
Kun Sung Chung ◽  
Howard H. Park ◽  
Kang Ting ◽  
Hiroko Takita ◽  
Suneel S. Apte ◽  
...  

2011 ◽  
Vol 218 (5) ◽  
pp. 517-533 ◽  
Author(s):  
Tamaki Yokohama-Tamaki ◽  
Takashi Maeda ◽  
Tetsuya S. Tanaka ◽  
Shunichi Shibata

2020 ◽  
pp. 002203452096011
Author(s):  
M. Farahat ◽  
G.A.S. Kazi ◽  
E.S. Hara ◽  
T. Matsumoto

During orofacial tissue development, the anterior and posterior regions of the Meckel’s cartilage undergo mineralization, while the middle region undergoes degeneration. Despite the interesting and particular phenomena, the mechanisms that regulate the different fates of Meckel’s cartilage, including the effects of biomechanical cues, are still unclear. Therefore, the purpose of this study was to systematically investigate the course of Meckel’s cartilage during embryonic development from a biomechanical perspective. Histomorphological and biomechanical (stiffness) changes in the Meckel’s cartilage were analyzed from embryonic day 12 to postnatal day 0. The results revealed remarkable changes in the morphology and size of chondrocytes, as well as the occurrence of chondrocyte burst in the vicinity of the mineralization site, an often-seen phenomenon preceding endochondral ossification. To understand the effect of biomechanical cues on Meckel’s cartilage fate, a mechanically tuned 3-dimensional hydrogel culture system was used. At the anterior region, a moderately soft environment (10-kPa hydrogel) promoted chondrocyte burst and ossification. On the contrary, at the middle region, a more rigid environment (40-kPa hydrogel) enhanced cartilage degradation by inducing a higher expression of MMP-1 and MMP-13. These results indicate that differences in the biomechanical properties of the surrounding environment are essential factors that distinctly guide the mineralization and degradation of Meckel’s cartilage and would be valuable tools for modulating in vitro cartilage and bone tissue engineering.


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