The TMJ Disc Is a Common Ancestral Feature in All Mammals, as Evidenced by the Presence of a Rudimentary Disc During Monotreme Development

Abstract

The novel mammalian jaw joint, known in humans as the temporomandibular joint or TMJ, is cushioned by a fibrocartilage disc. This disc is secondarily absent in therian mammals that have lost their dentition, such as giant anteaters and some baleen whales. The disc is also absent in all monotremes. However, it is not known if the absence in monotremes is secondary to the loss of dentition, or if it is an ancestral absence. We use museum held platypus and echidna histological sections to demonstrate that the developing monotreme jaw joint forms a disc primordium that fails to mature and become separated from the mandibular condyle. We then show that monotreme developmental anatomy is similar to that observed in transgenic mouse mutants with reduced cranial musculature. We therefore suggest that the absence of the disc on monotremes is a consequence of the changes in jaw musculature associated with the loss of adult teeth. Taken together, these data indicate that the ancestors of extant monotremes likely had a jaw joint disc, and that the disc evolved in the last common ancestor of all mammals.

Evolution and development of the mammalian jaw joint: Making a novel structure

“…These changes cannot have occurred in isolation, and the development of each is partially dependent upon one or more of the other processes. For example, the development of the disc requires the development and function of the lateral pterygoid muscle (Anthwal & Tucker, 2020 ; Purcell et al, 2012 ), and the glenoid fossa forms through tissue interaction with the condylar cartilage (Li et al, 2021 ; Wang et al, 2011 ). These interdependent aspects will be discussed in more detail.…”

“…These include Pax9 mutant mice, which lack the coronoid process (Anthwal et al, 2015 ; Peters et al, 1998 ), Tgf‐beta mutants which fail to form the angular process (Anthwal et al, 2008 ), and Tbx1 mutants with hypoplastic jaw musculature (Aggarwal et al, 2010 ; Anthwal et al, 2015 ). Similarly, the TMJ forms in mammals with reduced musculature, resulting in diminished dentary bones, such as anteaters, monotremes, and whales (El Adli & Deméré, 2015 ; Anthwal & Tucker, 2020 ; Cox & Jeffery, 2011 ; Naples, 1999 ). This demonstrates that the TMJ and musculature have a reduced developmental linkage than perhaps was the case in early mammals.…”

“…This demonstrates that the TMJ and musculature have a reduced developmental linkage than perhaps was the case in early mammals. The linkage between the musculature and the TMJ is not wholly severed, however, since the development of the TMJ disc is dependent on muscle tissue interactions (see later and (Anthwal & Tucker, 2020 ; Purcell et al, 2012 ).…”

FACEts of mechanical regulation in the morphogenesis of craniofacial structures

“… 223 , 224 In monotremes, such as platypus, a primordial disc is formed but does not mature, and a similar phenotype is observed in mouse mutants with severely reduced cranial musculature due to Tbx1 deletion in the mesoderm. 225 As a result, species-specific muscle forces may participate in the evolutionary changes of disc formation in TMJs.…”

Transient role of the middle ear as a lower jaw support across mammals

“…Monotremes hatch out of the egg after 10 days post-oviposition ( Griffiths, 1978 ). The formation of the dentary-squamosal joint in monotremes has recently been followed and shown to form from 10 days after hatching in the platypus ( Anthwal and Tucker, 2020 ). Breakdown of Meckel’s cartilage in both marsupials and monotremes occurs relatively late postnatally ( Urban et al, 2017 ), with a robust Meckel’s still evident in nest young platypuses ( Zeller, 1993 ).…”