A new developmental mechanism for the separation of the mammalian middle ear ossicles from the jaw

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.

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

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.2606 ◽

2016 ◽

Vol 283 (1822) ◽

pp. 20152606 ◽

Cited By ~ 16

Author(s):

Héctor E. Ramírez-Chaves ◽

Stephen W. Wroe ◽

Lynne Selwood ◽

Lyn A. Hinds ◽

Chris Leigh ◽

...

Keyword(s):

Middle Ear ◽

Functional Divergence ◽

Mammalian Development ◽

Meckel's Cartilage ◽

Topological Change ◽

Meckel’S Cartilage ◽

Fossil Evidence ◽

Jaw Joint ◽

Land Vertebrates

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.

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Integrated hearing and chewing modules decoupled in a Cretaceous stem therian mammal

Science ◽

10.1126/science.aay9220 ◽

2019 ◽

Vol 367 (6475) ◽

pp. 305-308 ◽

Cited By ~ 11

Author(s):

Fangyuan Mao ◽

Yaoming Hu ◽

Chuankui Li ◽

Yuanqing Wang ◽

Morgan Hill Chase ◽

...

Keyword(s):

Middle Ear ◽

New Genus ◽

New Genus And Species ◽

Bone Contact ◽

Meckel's Cartilage ◽

Therian Mammal ◽

Meckel’S Cartilage ◽

Genetic Mechanisms ◽

Evolution Of Mammals

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.

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