The temporomandibular joint is the one of the most used joints in the body, articulating the upper and lower jaw in Mammals. A fibrous articular disc sits between the skeletal elements of the joint and acts as a cushion. Temporomandibular joint development occurs by the coming together of two membranous bones: the condylar process of the dentary bone in the mandible and the squamosal bone in the skull. The interaction of the condylar with the squamosal induces the formation of a glenoid (or mandibular) fossa on the latter. The articular disc sits between the two within a synovial capsule. The temporomandibular joint disc attaches to the superior head of the lateral pterygoid muscle anteriorly, and to ligaments posteriorly including the disco-mallear ligament that runs thought the capsule of the middle ear, joining the malleus to the temporomandibular joint disc. The temporomandibular joint articulates the jaw in all Mammals and is referred to as the squamosal dentary joint in those Mammals without a fused temporal bone. In non-Mammals the upper and lower jaw articulate via the endochondral quadrate and articular, known as the primary jaw joint. Temporomandibular joint developmental anatomy reflects its evolutionary history as this novel jaw joint forms after the development of the primary joint, which, in Mammals, is integrated into the middle ear. In recent years, a number of studies have advanced the understanding of middle ear evolution in the context of anatomical development, but little work has sought to understand the temporomandibular joint in an evolutionary and comparative developmental biology context. This is despite the crucial role that the formation of the temporomandibular joint has in mammalian evolution.
An important part of the temporomandibular joint is the disc that cushions its action. The origin of the disc is uncertain. The insertion of the lateral pterygoid muscle into the disc on the medial aspect, and the presence of the disco-malleolar ligament, has led to speculation that the disc represents a fibrocartilage sesamoid within a tendon. According to this hypothesis, this tendon, originally associated with the musculature of the articular (homologous to the malleus) of the primary jaw joint, would have become trapped as the dentary and squamosal moved together to create the Mammalian jaw joint. However, studies in mice indicate that the disc develops from a region of flattered mesenchyme cells adjacent to, or possibly part of, the perichondrium of the developing condylar cartilage. Formation of the disc condensation is dependent on Ihh gene signaling from the cartilage. and Fgf signaling via Spry 1 and 2 genes from the adjacent muscles. Therefore, the disc may have its origins in either a tendon, the novel secondary cartilage of the condylar process, or a combination of the two.
Interestingly the disc is absent in extant Monotremes. Monotremes and Therian Mammals (Marsupials and Eutherians) are evolutionary distant, with the common ancestor of the two subclasses being a Mammal-like Reptile from around 160 million years ago. Monotremes have a number of 'Reptile; like anatomical features such as a cloaca, external embryonic development in an egg, a straight cochlea in the inner ear and a sprawling posture. The absence of a disc in both Echidna and Platypus suggests that the disc evolved after the split between Monotremes and Therian Mammals, and is therefore a Therian novelty. Alternatively, absence of the temporomandibular joint disc in extant Monotremes might be due to a secondary loss linked to the loss of teeth, and associated changes in the muscles of mastication. Extant adult Monotremes are edentulous, possibly due to the expansion of the trigeminal during the evolution of electroreceptivity limiting the available space for tooth roots within the maxilla.
The juvenile Platypus has rudimentary teeth that regress, while the Echidna shows only thickening of the dental epithelium during development. In contrast, fossil Monotremes have a Mammalian tribosphenic dentition, a structure unique to the Mammal lineage that allows occlusion of upper and lower molar teeth for grinding of food in addition to crushing and shearing during mastication. his indicates that extant Monotremes evolved from Animals with the ability to chew in the Mammalian manner, involving lateral and rotational movements. The presence or absence of a disc in such fossils is difficult to ascertain due to lack of preservation of soft tissue. In support of mastication playing a role in disc formation, edentulous Therian Mammals, or those lacking enamel, often lack a disc. These species include some (but not all) Baleen Whales, Giant Ant Eaters and Sloths.
In a paper published in the journal Frontiers in Cell and Developmental Biology on 19 May 2020, Neal Anthwal and Abigail Tucker of the Centre for Craniofacial and Regenerative Biology at King’s College London, present the results of a study which examined the development of the temporomandibular joint in Monotremes and made comparison with Mouse developmental models where muscle development is perturbed, in order to discriminate between these two scenarios.
Platypus, Ornithorhynchus anatinus, and Short-beaked Echidna, Tachyglossus aculeatus, slides were imaged from the collections at the Cambridge University Museum of Zoology. All museum samples have been studied in previously published works. CT scans of adult Platypus were a gift of Anjali Goswami of the Natural History Museum, London.
If the temporomandibular joint disc is a therian novelty, then no evidence of a disc would be expected in extant Monotremes during development of the temporomandibular joint. The development of the jaw joint was therefore examined in museum held histological sections of developing post-hatching Platypus and compared with the Mouse.
As other authors have previously described, in embryonic day 16.5 Mice the disc anlage is observed as thickened layer of mesenchyme connected to the superior aspect of the condylar cartilage. At postnatal day 0, the disc has separated from the condylar process and sits within the synovial cavity of the jaw joint. In a Platypus sample estimated to be 6.5 days post-hatching, the temporomandibular joint had been initiated, but the joint cavity had not yet formed. Close examination of the superior surface of the condylar cartilage revealed a double layer of thickened mesenchyme in the future fibrocartilage layer of the condylar. The outer layer is similar to that known to develop into the articular disc in Therian Mammals. This thickened mesenchyme persisted in older samples, estimated to be 10 days post-hatching, where the synovial cavity of the temporomandibular joint was beginning to form above. In the most mature Platypus sample examined (around 80 days post-hatching) the fibrocartilage layer of the condylar process was thick and had a double-layered structure. The outer layer was connected via a tendon to the lateral pterygoid muscle. At this late stage of postnatal development, the Platypus puggle would have been expected to start leaving the burrow and to be eating a mixed diet, although full weaning does not occur until around 205 days post-hatching. In the mature Platypus, the condylar process sits within a glenoid fossa, which was not fully formed at earlier stages. A disc-like structure lying over the condylar and connected to the adjacent muscles was therefore evident in the Platypus postnatally but did not lift off the condylar at any stage.
Next Anthwar and Tucker examined the development of the temporomandibular joint in a museum derived young Short-beaked Echidna puggle specimen with a crown-rump length of 83mm, which they estimate to be around 18 days post-hatching. The temporomandibular joint is not fully developed. The condylar process possessed a thick, doubled fibrocartilage outer layer, much as was observed in the Platypus. The outer fibrocartilage layer was connected by connective tissue to the lateral pterygoid muscle. Clear disc-like structures were therefore present during development in both extant Monotremes.
Taken together, the developmental evidence suggests that extant Monotremes initiate a layer of fibrocartilage connected to the lateral pterygoid muscle, similar to the initiation of the TMJ disc in therian mammals. However, unlike in Therian Mammals, the monotreme fibrocartilage failed to separate from the condylar to form an articular disc in the temporomandibular joint. Interactions with musculature, both mechanical and molecular, have been suggested to be responsible for the proper formation of the temporomandibular joint disc. Lack of mechanical force or changes in signaling from the muscle in Monotremes might therefore result in the disc remaining attached to the condylar. In order to examine how changes in muscle might influence disc development, Anthwar and Tucker next examined disc development in the Mesp1Cre;Tbx1flox conditional mutant Mouse (Tbx1CKO). This mouse has a mesoderm specific deletion of the T-box transcription factor Tbx1, resulting in severely perturbed development of the pharyngeal arch mesodermderived muscles of the head, resulting in their significant reduction or absence.
Anthwar and Tucker used alcian blue/alizarin red stained histological sections to investigate the development of the temporomandibular joint disc in TbxCKO Mice at embryonic day 15.5. This is the stage when future disc mesenchyme is first observed. In wildtype embryos, the future disc mesenchyme was observed as a condensation attached to the superior surface of the condylar fibrocartilage. A distinct disc-like mesenchyme was also observed superior to the condylar of the Tbx1CKO. This mesenchyme and the fibrocartilage layer of the condylar cartilage both appeared thicker in the Tbx1CKO compared to its wildtype littermate. At embryonic day 18.5, the wildtype temporomandibular joint disc had separated from the condylar process and sat within a synovial joint cavity. In the Tbx1CKO an upper synovial cavity had formed, similar to the wildtype, but there was little evidence of the earlier disc with no separation from the condylar. Instead, a thickened band of fibrocartilage was observed on the superior surface of the condylar process. The lateral pterygoid muscle was either massively reduced or absent in the Tbx1CKO, while other muscles, such as the temporalis, were present but much reduced in volume.
The absence of an articular disc in Monotremes has been thought to be either a secondary loss related to the absence of a mature dentition, or the disc being a later acquisition in the Therian clade. The data presented here show that a mesenchyme similar to the a range of mandibular movements during chewing, including rolling, yaw and front to back movements. It is not clear if these species had evolved an articular disc, since fibrocartilage is rarely fossilised. However, the synovial secondary jaw joint was likely present in stem Mammals such as Morganuconodon, and the lateral pterygoid has been proposed to have inserted into the condylar of the dentary forming the secondary articulation in basal Mammaliforms. When this is considered alongside the presence of the first stages of disc formation during Monotreme development, it is likely that the common stem Jurassic Mammal-like Reptilian ancestor of both Monotremes and Therian Mammals had a disc. The data presented here confirms an essential biomechanical component in disc development. Therefore, Anthwar and Tucker were able to consider when during Mammalian evolution these forces were able to act to enable disc formation. For example, it is probable that many late Triassic and early Jurassic Mammaliaforms such Hadrocodium possessed an articular disc, since they possessed a well-formed squamosal dentary joint and occluding teeth capable of grinding food between the cusps of tribosphenic teeth during mastication.
One hypothesis for the origin of the articular disc is that it formed from the tendon of a muscle of jaw closure of the primary jaw joint interrupted by the formation of the novel Mammalian jaw joint. The tendons and skeleton of the front of the head are derived from the cranial neural crest, whereas the musculature is mesoderm derived. Interactions between the mesoderm and neural crest co-ordinate the muscular skeletal development of the head. A striking piece of evidence for the tendon origin of the disc is the expression in the developing articular disc of Scleraxis, a specific regulator of tendon and ligament development. If the disc is derived from a tendon, then it may be thought of as a fibrocartilage sesamoid. Such sesamoids are found in joints and in tendons that are subject to compression, like the tendons that pass around bony pulleys such as the flexor digitorum profundus tendon in quadrupeds, the patella tendon and ligament and the cartilago transiliens in Crocodilians. Fibrocartilages also form at the enthesis of long bones. Interestingly, it has been demonstrated that much like the temporomandibular joint disc, enthesis fibrocartilage cells are derived from Hh responsive cells and that these cells are responsive to mechanical loading. To support the tendon origin of the temporomandibular joint disc, Anthwar and Tucker's data show that the formation of the disc is dependent on interactions between the skeletal and muscle components of the temporomandibular joint. Such tissue interaction is also a key process in the formation of tendons and ligaments.
The mechanism by which the disc fails to separate from the condylar in Monotremes is not yet clear. Hh signaling is known to be involved in both the initiation of the disc, and the later separation from the condylar. It is still possible that the role in Hh in separation of the disc is a Therian innovation, and as such the reason that Monotremes fail to do so is a lack of the later Hh dependent developmental program for disc separation. However, the absence of the disc in Therian edentates, such as some Whales and Giant Anteaters, strongly suggests that the loss is secondary. The absence of teeth and associated changes in jaw function in Monotremes lends itself to the hypothesis that related changes in the lateral pterygoid muscle are responsible for the failure of disc maturation. Secondary loss, through changes in interactions between the developing disc and muscles, is supported by the failure of the disc to elevate off the condylar in Tbx1CKO Mice that fail to form the lateral pterygoid muscle. These interactions may be either, or a combination of, biomechanical stimulation acting in addition to the compressive force of the TMJ joint, or molecular signaling from the muscles, such as Fgf and Tgf-beta signaling pathways that are known to act in the muscle-tendon-bone/cartilage axis. The source of this signal is likely the lateral pterygoid muscle, which acts to abduct, protrude and laterally move the jaw. These movements are of decreased importance in extant tooth-less monotremes due to feeding modalities that do not rely on chewing with an occluded dentition. As such the formation and maturation of the disc is unlikely to be directly dependent on the presence of teeth, and its absence in edentates is instead a function of the associated changes in musculature. This is supported by the fact that the temporomandibular joint disc forms during embryonic development in Mice, quite some time before the eruption of the teeth at the end of the second postnatal week. Baleen Whales vary in the presence or absence of temporomandibular joint discs, and indeed temporomandibular joint synovial cavities. Significantly, the toothless Gray Whale has no disc and the lateral and medial pterygoid muscles are fused and function as the medial pterygoid, a situation also reported in the adult Platypus. In addition, although they have a full carnivore dentition, the Marsupial Tasmanian Devil has a poorly developed lateral pterygoid muscle and completely lacks the temporomandibular joint disc. Evidence that disc maturation is, at least in part, dependent on biomechanical, rather than molecular signaling, cues is found in the disrupted development of the disc in mice after ex utero surgical manipulation, where the jaw is sutured closed at embryonic day 15.5 but the muscle is unaffected.
Monotremes appear to have two distinct layers in the disc remnant attached to the upper surface of the condylar cartilage, whereas the Tbx1CKO Mouse has only one continuous fibrocartilage by embryonic day 18.5. This may reflect the near total absence of the lateral pterygoid muscle in the Mouse mutant, compared to its presence in a reduced form in Monotremes. Unfortunately, due to the rarity of fresh material, it is not possible to further examine the mechanistic aspects of temporomandibular joint development in edentulous monotreme species at the present time.
In conclusion, Anthwar and Tucker demonstrate that during development, Monotremes show evidence of initiation of a fibrocartilage articular disc, despite all adult Monotremes not having an articular temporomandibular joint disc. Maturation and separation of the disc is dependent on interaction with the developing musculature, either through biomechanical stimulation or molecular signals, as demonstrated by the failure of disc maturation and separation in Mouse mutants with hypomorphic cranial muscles. Therefore, toothed ancestors of Monotremes likely had a temporomandibular joint disc. Anthwar and Tucker's research suggests that changes in the cranial musculature that occurred as a consequence of a move toward edentulous dietary niches resulted in absence of the temporomandibular joint disc in Monotremes, a parallel loss occurring in edentulous Therian Mammals. Finally, the presence of the disc anlage in Monotremes indicates that the Mammal-like Reptile ancestor of all modern Mammals likely possessed a disc to cushion the novel jaw articulation.
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