Meckel’s cartilage breakdown offers clues to mammalian middle ear evolution

Abstract

A key transformation in mammalian ear evolution was incorporation of the primary jaw joint of premammalian synapsids into the definitive mammalian middle ear of living mammals. This evolutionary transition occurred in two-steps, starting with a partial or "transitional" mammalian middle ear in which the ectotympanic and malleus were still connected to the mandible by an ossified Meckel's Cartilage (MC), as observed in many Mesozoic mammals. This was followed by MC breakdown, freeing the ectotympanic and the malleus from the mandible and creating the definitive mammalian middle ear. Here we report novel findings on the role of chondroclasts in MC breakdown, shedding light on how therian mammals lost MC connecting the ear to the jaw. Genetic or pharmacological loss of clast cells in mice and opossums leads to persistence of embryonic MC beyond juvenile stages, with MC ossification in mutant mice. The persistent MC causes a distinctive postnatal groove on the mouse dentary. This morphology phenocopies the ossified MC and Meckelian groove observed in Mesozoic mammals. Clast cell recruitment to MC is not observed in reptiles, where MC persists as a cartilaginous structure. We hypothesize that ossification of MC is an ancestral feature of mammaliaforms, and that a shift in the timing of clast cell recruitment to MC prior to its ossification is a key developmental mechanism for the evolution of the definitive mammalian middle ear in extant therians.A key transformation in mammalian ear evolution was incorporation of the primary jaw joint of premammalian synapsids into the definitive mammalian middle ear (DMME) of living mammals 1-5. The quadrate and articular in the jaw joint of reptiles and the incus and malleus of the middle ear of mammals are homologs 6-12. These structures are formed by a

Disconnecting bones within the jaw‐otic network modules underlies mammalian middle ear evolution

“…Our analysis of the jaw‐otic complex using anatomical networks delimits three alternative modular configurations for the bones involved in the mammalian middle ear evolution: (i) mandibular; (ii) transitional otic‐mandibular; and (iii) otic modules. The mandibular module is analogous to the mandibular middle ear complex described in non‐mammalian synapsids and mammaliaforms; the transitional otic‐mandibular module occurs in the intermediate stage of the mammalian middle ear evolution and is analogous to the transitional mammalian middle ear described in some Mesozoic mammals, in which the ear bones connect only partially to the lower jaw; and the otic module is analogous to the definitive mammalian middle ear described for extant mammals (Wang et al., ; Luo et al., , ; Ji et al., ; Luo, ; Meng et al., ; Anthwal et al., ; Han et al., ; Urban et al., ). The different organizational steps of these network modules allowed us to divide the evolution of the mammalian ear into five evolutionary stages (Fig.…”

“…393–395; Luo & Crompton, ; Rybczynski, ; Wang et al., ; Martinelli & Rougier, ; Luo, ; Huttenlocker & Abdala, ; Lautenschlager et al., , ). The embryonic Meckel's cartilage was probably persistent in the adult lower jaw of some synapsid taxa (Kermack et al., ; Sues, ; Rougier et al., ; Wang et al., ; Rich et al., ; Kemp, ; Luo, ; Luo et al., ; Ramírez‐Chaves et al., ; Han et al., ), as could be inferred by the Meckelian groove or sulcus in the lingual side of some lower jaws (Kermack et al., ; Sues, ; Bonaparte et al., , ; Rich et al., ; Kemp, ; Meng et al., ; Ramírez‐Chaves et al., ; Anthwal et al., ; Luo et al., ; Urban et al., ). However, connectivity only can be reliably inferred in fossils when the element is present as hard fossilized tissue; thus, to register the connectivity of Meckel's cartilage, we have only coded it when newly ossified in early mammals.…”

“…In contrast, modern mammals have a single jawbone, the dentary, which articulates to the squamosal, and four closely connected auditory bones: ectotympanic, malleus, incus and stapes. Many aspects of the origin and evolution of the mammalian middle ear are now better understood thanks to the richness of the synapsids fossil record (Watson, ; Hopson, ; Carroll, , chapters 17–18; Rubidge & Sidor, ; Sidor, , ; Luo, ; Han et al., ; Luo et al., ) and recent advances in developmental biology (Luo, ; Anthwal et al., , ; Ramírez‐Chaves et al., ; Urban et al., ).…”

“…E); and (iii) the definitive mammalian middle ear type, with the middle ear bones fully disconnected from the dentary and isolated from participating in any chewing action (Fig. F; Luo, ; Meng et al., ; Ramírez‐Chaves et al., ; Anthwal et al., ; Han et al., ; Luo et al., ). These configurations can also be seen as changes in the topological arrangement of the ear bones throughout their evolution.…”

The role of miniaturization in the evolution of the mammalian jaw and middle ear

“…More derived groups and crown mammals eventually lost the ancestral quadrate-articular joint. In addition to fossil evidence, this sequence of events was identified historically in embryonic stages of living mammals 14,15 and recent morphogenetic studies, gene patterning and regulatory networks have elucidated the development of these structures further 16,17 .…”