Molar morphology and occlusion of the Early Jurassic mammaliaform Erythrotherium parringtoni

Funding Information: We thank Bhart-Anjan Bhullar (Yale University, New Haven, USA) and Roger Smith (ISAM), who kindly provided the scan of Erythrotherium parringtoni, as well as Pip Brewer (Natural History Museum of Denmark, Copenhagen, Denmark), Michael Day, Farah Ahmed, Amin Garbout (all Natural History Museum, London, UK), Robert Asher and Mathew Lowe (both UMZC) for scans and access to comparative material of Morganucodon and Megazostrodon. We are also grateful to Anton Du Plessis (ISAM), Fernando Abdala (Bernard Price Institute for Palaeontological Research, Johannesburg, South Africa) and Amin Garbout (Natural History Museum, London, United Kingdom), who scanned the material used in this study. We also thank Richard Cifelli (Sam Noble Museum, Norman, USA) and David Grossnickle (University of Washington, Seattle, USA) for their kind and helpful reviews. This study was funded by grants MA 1643/15-2 and MA 1643/20-1 of the Deutsche Forschungsgemeinschaft (DFG) to TM. Publisher Copyright: Copyright © 2022 K.R.K. Jäger et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (for details please see http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.The South African Early Jurassic morganucodontan Erythrotherium is considered by some authors to be potentially synonymous with Morganucodon, due to similar tooth morphology. However, despite their similar dental morphology, the occlusal pattern of Erythrotherium parringtoni has been described as embrasure occlusion, close to the mode of Megazostrodon rudnerae, rather than that of Morganucodon. In this study the molars of Erythrotherium were re-examined and the two alternative occlusal hypotheses were tested using the Occlusal Fingerprint Analyser (OFA). Morphological comparison of the molars of Erythrotherium parringtoni to those of Morganucodon watsoni showed similarities in cusp height and shape in lingual/buccal views, but the molars and individual cusps of Erythrotherium parringtoni are considerably narrower linguo-buccally, and more gracile. With cusps a and c close together in Erythrotherium parringtoni, cusp positioning differs from that of Morganucodon watsoni and shows similarities to the pattern in Megazostrodon rudnerae. Also, the upper molars of Erythrotherium parringtoni are aligned in a straight row and lack the angle, relative to the longitudinal axis, between the first and second upper molars that is present in Morganucodon watsoni. This results in embrasure occlusion being the only viable occlusal mode for Erythrotherium parringtoni, which was confirmed by the OFA analysis. A Morganucodon-like occlusion would allow only the main cusps a/A to contact their antagonists and thus major gaps would be present, causing considerable reduction of functionality of the dentition. Based on the morphological evidence and the differing occlusal mode, the perpetuation of Erythrotherium parringtoni as a separate genus is confirmed.Peer reviewe

A reassessment of the postcanine dentition and systematics of the tritylodontid Stereognathus (Cynodontia, Tritylodontidae, Mammaliamorpha), from the Middle Jurassic of the United Kingdom

Tritylodontidae was a successful advanced cynodont clade with a close relationship to mammals, but falling outside the clade Mammaliaformes. Stereognathus ooliticus was the first tritylodontid to be named and described in 1854, but since then no comprehensive description for this species has been produced. A second species, S. hebridicus, was named in 1972 and diagnosed based solely on size difference, being larger than the S. ooliticus holotype. We reexamined all postcanine tooth material attributed to the genus Stereognathus to test the species diagnosis and identify diagnostic morphological characters for this genus. We find no statistical difference in size distribution between S. ooliticus and S. hebridicus postcanine specimens. Specimens previously attributed to the different species fall along an ontogenetic spectrum of size, with no clear clustering. Morphologically, we affirm many previously described features for Stereognathus and identify new morphological features in upper and lower postcanines. We find no morphological features to distinguish these two species, and therefore we synonymize S. hebridicus under S. ooliticus. We reevaluate the scoring of S. ooliticus in previous phylogenetic analyses, generating a new tree using rescored Stereognathus characters. Finally, we suggest that similar reevaluations and redescriptions of other poorly described tritylodontid material are necessary to further clarify relationships among Tritylodontidae and the evolution of characters in derived genera such as Stereognathus.Peer reviewe

Modeling enamel matrix secretion in mammalian teeth

The most mineralized tissue of the mammalian body is tooth enamel. Especially in species with thick enamel, three-dimensional (3D) tomography data has shown that the distribution of enamel varies across the occlusal surface of the tooth crown. Differences in enamel thickness among species and within the tooth crown have been used to examine taxonomic affiliations, life history, and functional properties of teeth. Before becoming fully mineralized, enamel matrix is secreted on the top of a dentine template, and it remains to be explored how matrix thickness is spatially regulated. To provide a predictive framework to examine enamel distribution, we introduce a computational model of enamel matrix secretion that maps the dentine topography to the enamel surface topography. Starting from empirical enamel-dentine junctions, enamel matrix deposition is modeled as a diffusion-limited free boundary problem. Using laboratory microCT and synchrotron tomographic data of pig molars that have markedly different dentine and enamel surface topographies, we show how diffusion-limited matrix deposition accounts for both the process of matrix secretion and the final enamel distribution. Simulations reveal how concave and convex dentine features have distinct effects on enamel surface, thereby explaining why the enamel surface is not a straightforward extrapolation of the dentine template. Human and orangutan molar simulations show that even subtle variation in dentine topography can be mapped to the enamel surface features. Mechanistic models of extracellular matrix deposition can be used to predict occlusal morphologies of teeth. Author summary Teeth of most mammals are covered by a layer of highly mineralized enamel that cannot be replaced or repaired. The enamel layer is not uniform over the underlying dentine, and spatial regulation of enamel formation is critical for making a functional tooth. To explore which kind of mechanisms could underlie the complex patterns of enamel distribution, we present a computational model. Starting from tomography-imaged teeth from which enamel has been digitally removed, enamel is restored on dentine surfaces by simulating diffusion-limited secretion of enamel matrix. Our simulations show how the combination of subtle features of dentine and diffusion-limited secretion of the enamel matrix can substantially increase the complexity of the enamel surface. We propose that the strength of the diffusion-limited process is a key factor in determining enamel distribution among mammalian species.Peer reviewe

Functional tests of the competitive exclusion hypothesis for multituberculate extinction

Multituberculate mammals thrived during the Mesozoic, but their diversity declined from the mid-late Paleocene onwards, becoming extinct in the late Eocene. The radiation of superficially similar, eutherian rodents has been linked to multituberculate extinction through competitive exclusion. However, characteristics providing rodents with a supposed competitive advantage are currently unknown and comparative functional tests between the two groups are lacking. Here, a multifaceted approach to craniomandibular biomechanics was taken to test the hypothesis that superior skull function made rodents more effective competitors. Digital models of the skulls of four extant rodents and the Upper Cretaceous multituberculate Kryptobaatar were constructed and used (i) in finite-element analysis to study feeding-induced stresses, (ii) to calculate metrics of bite force production and (iii) to determine mechanical resistances to bending and torsional forces. Rodents exhibit higher craniomandibular stresses and lower resistances to bending and torsion than the multituberculate, apparently refuting the competitive exclusion hypothesis. However, rodents optimize bite force production at the expense of higher skull stress and we argue that this is likely to have been more functionally and selectively important. Our results therefore provide the first functional lines of evidence for potential reasons behind the decline of multituberculates in the changing environments of the Paleogene.Peer reviewe

A robust, semi-automated approach for counting cementum increments imaged with synchrotron X-ray computed tomography

Cementum, the tissue attaching mammal tooth roots to the periodontal ligament, grows appositionally throughout life, displaying a series of circum-annual incremental features. These have been studied for decades as a direct record of chronological lifespan. The majority of previous studies on cementum have used traditional thin-section histological methods to image and analyse increments. However, several caveats have been raised in terms of studying cementum increments in thin-sections. Firstly, the limited number of thin-sections and the two-dimensional perspective they impart provide an incomplete interpretation of cementum structure, and studies often struggle or fail to overcome complications in increment patterns that complicate or inhibit increment counting. Increments have been repeatedly shown to both split and coalesce, creating accessory increments that can bias increment counts. Secondly, identification and counting of cementum increments using human vision is subjective, and it has led to inaccurate readings in several experiments studying individuals of known age. Here, we have attempted to optimise a recently introduced imaging modality for cementum imaging; X-ray propagation-based phase-contrast imaging (PPCI). X-ray PPCI was performed for a sample of rhesus macaque (Macaca mulatta) lower first molars (n = 10) from a laboratory population of known age. PPCI allowed the qualitative identification of primary/annual versus intermittent secondary increments formed by splitting/coalescence. A new method for semi-automatic increment counting was then integrated into a purpose-built software package for studying cementum increments, to count increments in regions with minimal complications. Qualitative comparison with data from conventional cementochronology, based on histological examination of tissue thin-sections, confirmed that X-ray PPCI reliably and non-destructively records cementum increments (given the appropriate preparation of specimens prior to X-ray imaging). Validation of the increment counting algorithm suggests that it is robust and provides accurate estimates of increment counts. In summary, we show that our new increment counting method has the potential to overcome caveats of conventional cementochronology approaches, when used to analyse three-dimensional images provided by X-ray PPCI.Peer reviewe

Ptch2 is a Potential Regulator of Mesenchymal Stem Cells

Ptch receptors 1 and 2 mediate Hedgehog signaling pivotal for organ development and homeostasis. In contrast to embryonic lethal Ptch1(-/-) phenotype, Ptch2(-/-) mice display no effect on gross phenotype. In this brief report, we provide evidence of changes in the putative incisor mesenchymal stem cell (MSC) niches that contribute to accelerated incisor growth, as well as intriguing changes in the bones and skin which suggest a role for Ptch2 in the regulation of MSCs and their regenerative potential. We employed histological, immunostaining, and computed tomography (mu CT) analyses to analyze morphological differences between Ptch2(-/-) and wild-type incisors, long bones, and skins. In vitro CFU and differentiation assays were used to demonstrate the MSC content and differentiation potential of Ptch2(-/-) bone marrow stromal cells. Wound healing assay was performed in vivo and in vitro on 8-week-old mice to assess the effect of Ptch2 on the wound closure. Loss of Ptch2 causes increases in the number of putative MSCs in the continuously growing incisor, associated with increased vascularization observed in the tooth mesenchyme and the neurovascular bundle. Increased length and volume of Ptch2(-/-) bones is linked with the increased number and augmented in vitro differentiation potential of MSCs in the bone marrow. Dynamic changes in the Ptch2(-/-) skin thickness relate to changes in the mesenchymal compartment and impact the wound closure potential. The effects of Ptch2 abrogation on the postnatal MSCs suggest a crucial role for Ptch2 in Hedgehog signaling regulation of the organ regenerative potential.Peer reviewe

Digital cranial endocast of Riograndia guaibensis (Late Triassic, Brazil) sheds light on the evolution of the brain in non-mammalian cynodonts

A digital cranial endocast of the specimen UFRGS-PV-596-T of Riograndia guaibensis was obtained from μCT scan images. This is a small cynodont, closely related to mammaliaforms, from the Late Triassic of Brazil. Riograndia has large olfactory bulb casts and the cerebral hemispheres region is relatively wider than in other non-mammaliaform cynodonts. Impressions of vessels were observed and a conspicuous mark on the dorsal surface was interpreted as the transverse sinus. The calculated encephalization quotient is greater than the range seen in most other non-mammaliaform cynodonts. The ratios between linear and area measurements of the dorsal surface suggest four evolutionary changes from a basal eucynodont morphology to mammaliaforms, involving an evolutionary increase of the relative size of the olfactory bulbs and the width of the cerebral hemispheres and cerebellum. The data supports the hypothesis of the neurological evolution of the mammalian lineage starting with a trend for an increase of the olfactory bulbs, which is associated with adaptations in the nasal cavity. This trend is suggested to be linked to the selective pressures for small-sized faunivorous, and probably nocturnal, animals, and represents an initial improvement of the sensory receptor system, subsequently leading to further development of the ‘superior’ structures for sensorial processing and integration.Fil: Rodrigues, Pablo Gusmão. Universidade Federal do Rio Grande do Sul; BrasilFil: Martinelli, Agustín Guillermo. Universidade Federal do Rio Grande do Sul; Brasil. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Museo Argentino de Ciencias Naturales "Bernardino Rivadavia"; ArgentinaFil: Schultz, Cesar Leandro. Universidade Federal do Rio Grande do Sul; BrasilFil: Corfe, Ian J.. University of Helsinki; FinlandiaFil: Gill, Pamela G.. University of Bristol; Reino UnidoFil: Soares, Marina. Universidade Federal do Rio Grande do Sul; BrasilFil: Rayfield, Emily J.. University of Bristol; Reino Unid

Reply to: Revisiting life history and morphological proxies for early mammaliaform metabolic rates

Non peer reviewe

Reptile-like physiology in Early Jurassic stem-mammals

Despite considerable advances in knowledge of the anatomy, ecology and evolution of early mammals, far less is known about their physiology. Evidence is contradictory concerning the timing and fossil groups in which mammalian endothermy arose. To determine the state of metabolic evolution in two of the earliest stem-mammals, the Early Jurassic Morganucodon and Kuehneotherium, we use separate proxies for basal and maximum metabolic rate. Here we report, using synchrotron X-ray tomographic imaging of incremental tooth cementum, that they had maximum lifespans considerably longer than comparably sized living mammals, but similar to those of reptiles, and so they likely had reptilian-level basal metabolic rates. Measurements of femoral nutrient foramina show Morganucodon had blood flow rates intermediate between living mammals and reptiles, suggesting maximum metabolic rates increased evolutionarily before basal metabolic rates. Stem mammals lacked the elevated endothermic metabolism of living mammals, highlighting the mosaic nature of mammalian physiological evolution. Modern mammals are endothermic, but it has not been clear when this type of metabolism evolved. Here, Newham et al. analyse tooth and bone structure in Early Jurassic stem-mammal fossils to estimate lifespan and blood flow rates, which inform about basal and maximum metabolic rates, respectively, and show these stem-mammals had metabolic rates closer to modern ectothermic reptiles than to endothermic mammals.Peer reviewe