Abstract
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.
Highlights
The evolutionary origin of the definitive mammalian middle ear (DMME) is often cited as a textbook example of evolutionary transformation [1,2,3]
Unlike the situation in opossum, we did not observe any apoptotic cells in the mouse Meckel’s cartilage (MC) during its breakdown
Our results suggest that MC breakdown begins at P20 in opossums, consistent with prior studies which found that: MC and malleus are separated by the end of the third week of postnatal development [19], and that by P20 the middle ear ossicles are no longer connected to the dentary [46]
Summary
The evolutionary origin of the definitive mammalian middle ear (DMME) is often cited as a textbook example of evolutionary transformation [1,2,3]. We investigate the cellular and molecular processes driving a crucial first step in the evolution of the mammalian middle ear ossicles (i.e. malleus, incus)—their disconnection from the jaw. This occurred ancestrally in at least three lineages of Mesozoic mammals (monotremes, multituberculates and therians (marsupials þ placentals)) [13,14], and occurs early in the development of extant mammals, through the breakdown of the part of MC connecting the malleus and ectotympanic to the dentary [15,16,17,18].
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