Rolling of the jaw is essential for mammalian chewing and tribosphenic molar function

Bhullar, Bhart‐Anjan S.; Manafzadeh, Armita R.; Miyamae, Juri A.; Hoffman, Eva A.; Brainerd, Elizabeth L.; Musinsky, Catherine; Crompton, A. W.

doi:10.1038/s41586-019-0940-x

Cited by 59 publications

(69 citation statements)

References 27 publications

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“…The secondary jaw joint of some of the earliest mammals-like reptiles with a mandibular middle ear, such as Morganuconodon, were able to withstand the biomechanical stresses sufficient for feeding on the hard keratinised bodies of insects, while others such as Kuehneotherium could not [40]. Later animals developed a range of mandibular movements during chewing, including rolling, yaw and front to back movements [18,41–45]. It Is not clear if these species had evolved an articular disc, since fibrocartilage is rarely fossilised.…”

Section: Discussionmentioning

confidence: 99%

The TMJ disc is a common ancestral feature in all mammals, as evidenced by the presence of a rudimentary disc during monotreme development

Anthwal

Tucker

2020

Preprint

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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 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 or all mammals.

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Section: Discussionmentioning

confidence: 99%

The TMJ disc is a common ancestral feature in all mammals, as evidenced by the presence of a rudimentary disc during monotreme development

Anthwal

Tucker

2020

Preprint

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“…While varanid and iguanian lizards have traditionally been used as models of plesiomorphic amniote posture and locomotion (Jenkins & Goslow, 1983;Padian & Olsen, 1984;Ritter, 1996;Blob & Biewener, 1999;Blob, 2000;Farlow & Pianka, 2000;Clemente et al, 2011;Dick & Clemente, 2016), tegus were chosen here to represent a more shallowly-nested clade of terrestrial generalists (Sheffield et al, 2011;Simões et al, 2018) of growing importance as laboratory animals (Bennett & John-Alder, 1984;Montero et al, 2004;Toledo et al, 2008;Sheffield et al, 2011). In comparison, among extant mammals, didelphid opossums are a well-established plesiomorphic model for therian development, anatomy, and locomotion (Broom, 1899;Jenkins, 1971b;Hiiemae & Crompton, 1985;Klima, 1985;Parchman, Reilly & Biknevicius, 2003;Sánchez-Villagra & Maier, 2003;Gosnell et al, 2011;Hübler et al, 2013;Diogo et al, 2016;Bhullar et al, 2019).…”

Section: Two Study Speciesmentioning

confidence: 99%

Broad similarities in shoulder muscle architecture and organization across two amniotes: implications for reconstructing non-mammalian synapsids

Fahn-Lai

Biewener

Pierce

2020

PeerJ

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The evolution of upright limb posture in mammals may have enabled modifications of the forelimb for diverse locomotor ecologies. A rich fossil record of non-mammalian synapsids holds the key to unraveling the transition from "sprawling" to "erect" limb function in the precursors to mammals, but a detailed understanding of muscle functional anatomy is a necessary prerequisite to reconstructing postural evolution in fossils. Here we characterize the gross morphology and internal architecture of muscles crossing the shoulder joint in two morphologically-conservative extant amniotes that form a phylogenetic and morpho-functional bracket for non-mammalian synapsids: the Argentine black and white tegu Salvator merianae and the Virginia opossum Didelphis virginiana. By combining traditional physical dissection of cadavers with nondestructive three-dimensional digital dissection, we find striking similarities in muscle organization and architectural parameters. Despite the wide phylogenetic gap between our study species, distal muscle attachments are notably similar, while differences in proximal muscle attachments are driven by modifications to the skeletal anatomy of the pectoral girdle that are well-documented in transitional synapsid fossils. Further, correlates for force production, physiological cross-sectional area (PCSA), muscle gearing (pennation), and working range (fascicle length) are statistically indistinguishable for an unexpected number of muscles. Functional tradeoffs between force production and working range reveal muscle specializations that may facilitate increased girdle mobility, weight support, and active stabilization of the shoulder in the opossum-a possible signal of postural transformation. Together, these results create a foundation for reconstructing the musculoskeletal anatomy of the non-mammalian synapsid pectoral girdle with greater confidence, as we demonstrate by inferring shoulder muscle PCSAs in the fossil non-mammalian cynodont Massetognathus pascuali.How to cite this article Fahn-Lai P, Biewener AA, Pierce SE. 2020. Broad similarities in shoulder muscle architecture and organization across two amniotes: implications for reconstructing non-mammalian synapsids. PeerJ 8:e8556

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“…For example, if a study is constrained to a small number of trials, noise inherent to DeepLabCut’s predictions can have a magnified impact and thus more stringent error tolerances are appropriate. Likewise, in a study that seeks to quantify subtle motions (e.g., hemimandible wiggle, Bhullar et al, 2019), extra care must be taken when establishing the error tolerance.…”

Section: Discussionmentioning

confidence: 99%

Integrating XMALab and DeepLabCut for high-throughput XROMM

Laurence-Chasen

Manafzadeh

Hatsopoulos

et al. 2020

Preprint

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23Marker tracking is a major bottleneck in studies involving X-ray Reconstruction of 24Moving Morphology (XROMM). Here, we tested whether DeepLabCut, a new deep 25 learning package built for markerless tracking, could be applied to videoradiographic 26 data to improve data processing throughput. Our novel workflow integrates XMALab, 27 the existing XROMM marker tracking software, and DeepLabCut while retaining each 28 program's utility. XMALab is used for generating training datasets, error correction, and 29 3D reconstruction, whereas the majority of marker tracking is transferred to 30 DeepLabCut for automatic batch processing. In the two case studies that involved an in 31 vivo behavior, our workflow achieved a 6 to 13-fold increase in data throughput. In the 32 third case study, which involved an acyclic, post mortem manipulation, DeepLabCut 33 struggled to generalize to the range of novel poses and did not surpass the throughput 34 of XMALab alone. Deployed in the proper context, this new workflow facilitates large 35 scale XROMM studies that were previously precluded by software constraints. 36 37 Data processing in kinematics workflows can be a time-consuming and laborious 38 task, especially when three-dimensional (3D) reconstruction requires the integration of 39 data from multiple cameras. In marker-based XROMM (X-ray Reconstruction of Moving 40 Morphology; Brainerd et al., 2010), every radiopaque marker in every frame of two X-41 ray videos must be accurately tracked. This step has been streamlined by the open-42 source program XMALab (Knörlein et al., 2016), which offers a suite of features for 43 marker detection, visualization, and tracking. Marker tracking remains a major 44bottleneck in the XROMM workflow, however, limiting the feasibility of studies that 45 require large sample sizes across multiple individuals or species (cf. Gintof et al., 2010; 46 Granatosky et al., 2019; Iriarte-Diaz et al., 2017; Martinez et al., 2018). 47 126 Network training and analysis 127Once the training dataset is generated, the standard DeepLabCut workflow is 128 followed. The functions create_training_dataset and train_network were used to train a 129 single neural network whose weights were optimized for both camera-1 and camera-2 130 videos. In all cases, we used ResNet-101. We allowed training to run until 131DeepLabCut's native cross-entropy loss function plateaued, typically between 200,000 132 and 500,000 iterations. DLCTools supports the use of separate neural networks for 133 each camera plane, if the user chooses. This would double the amount of training but 134 may improve performance. The DLCTools function analyze_xromm_videos calls the 135 native analyze_videos function to predict points for new trials. It automatically detects

show abstract

Rolling of the jaw is essential for mammalian chewing and tribosphenic molar function

Cited by 59 publications

References 27 publications

The TMJ disc is a common ancestral feature in all mammals, as evidenced by the presence of a rudimentary disc during monotreme development

The TMJ disc is a common ancestral feature in all mammals, as evidenced by the presence of a rudimentary disc during monotreme development

Broad similarities in shoulder muscle architecture and organization across two amniotes: implications for reconstructing non-mammalian synapsids

Integrating XMALab and DeepLabCut for high-throughput XROMM

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