Computed tomographic analysis of the dental system of three Jurassic ceratopsians and implications for the evolution of tooth replacement pattern and diet in early-diverging ceratopsians

  1. Jinfeng Hu
  2. Catherine A Forster
  3. Xing Xu
  4. Qi Zhao
  5. Yiming He
  6. Fenglu Han

  • Curated by eLife

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    Evaluation Summary:

    Using micro-CT approaches, the authors provide a thorough investigation of dental morphology and development in some of the rarest and earliest representatives of three early ceratopsian dinosaur genera from China. The innovative approaches employed and nuanced inferences, including about the dental anatomy and replacement patterns in these early-diverging ceratopsians, make the manuscript interesting to mainstream researchers as well as the public.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

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Abstract

The dental system of ceratopsids is among the most specialized structure in Dinosauria by the presence of tooth batteries and high-angled wear surfaces. However, the origin of this unique dental system is poorly understood due to a lack of relevant knowledge in early-diverging ceratopsians. Here, we study the dental system of three earliest-diverging Chinese ceratopsians: Yinlong and Hualianceratops from the early Late Jurassic of Xinjiang and Chaoyangsaurus from the Late Jurassic of Liaoning Province. By micro-computed tomographic analyses, our study has revealed significant new information regarding the dental system, including no more than five replacement teeth in each jaw quadrant; at most one replacement tooth in each alveolus; nearly full resorption of the functional tooth root; and occlusion with low-angled, concave wear facets. Yinlong displays an increase in the number of maxillary alveoli and a decrease in the number of replacement teeth during ontogeny as well as the retention of functional tooth remnants in the largest individual. Chaoyangsaurus and Hualianceratops have slightly more replacement teeth than Yinlong . In general, early-diverging ceratopsians display a relatively slow tooth replacement rate and likely use gastroliths to triturate foodstuffs. The difference in dietary strategy might have influenced the tooth replacement pattern in later-diverging ceratopsians.

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  1. Version published to 10.7554/elife.76676 on eLife
  2. eLife

    Author Response:

    Reviewer #1:

    Hu and colleagues employ computed-tomography methods and provide a detailed description of and inferences about the dental system in three early-diverging ceratopsian dinosaur genera represented by rare specimens from China. Their study identifies nuanced tooth replacement rates and patterns. Furthermore, combined with the analysis of dental wear patterns, their study not only elucidates ontogenetic aspects of these early ceratopsians but also explores the implication of such patterns for dietary adaptations among these taxa. The manuscript, therefore, provides unique insights into the anatomical and ecological contexts of ceratopsians in such deep time.

    The manuscript is rich in data that are summarized in multiple tables and figures. It is also well-written and easy to follow. The inference and conclusions made are also overall well supported by the data presented.

    Thank you for your positive comments!

    The only main comment I have concerns the inference made about the dietary adaptation of Yinlong, which is inferred to be characterized by "feeding strategies other than only grinding food with their teeth." I think that this could be expanded a bit more to incorporate dietary breadth as an additional possible explanation, particularly given the lack of conclusive evidence for the predominance of a single plant species. As it stands, the inference (made across lines 475 through 485) may only imply processing the same food resource using non-chewing methods (e.g., gastroliths to triturate fern). Could the incorporation of other, less abrasive plat foods--in addition to the fibrous ferns--in the diet of Yinlong be a possible, additional explanation for the relatively slow tooth replacement and lack of a heavy tooth wear from chewing-related stress?

    We have provided more explanations and discussion for feeding strategies based on analysing the environmental condition and internal features. Firstly, we analyzed the flora of the Shishugou Formation and the environment that Yinlong lived. Then its feeding strategy can be inferred from its body size and tooth characters. The relatively small body length implies that Yinlong likely feeds on some low plants. The morphology of dentitions, the primitive jaw morphology, and the low tooth replacement rate suggest that Yinlong is unlikely to grind tough foods like derived ceratopsians. Yinlong possibly has other feeding strategies such as processing the foodstuffs by gastroliths, which have been found in some other dinosaurs. We have added more comparison with other dinosaurs (i.e., an armoured dinosaur preserved stomach contents and gastroliths). We suggest that ferns such as Angiopteris, Osmunda, and Coniopteris are suitable to be food choices of Yinlong. Some low and tender leaf and other less abrasive plant foods could also be possible.

    Reviewer #2:

    The authors of the present work aimed to describe tooth replacement in early ceratopsian species from the Lower Jurassic of China, and with this novel information, discuss new hypotheses of successive changes in jaw evolution that led to the highly specialized replacement and jaw function of derived ceratopsids. Major strengths of this study include not only the use of microCT-scans and 3D reconstructions to address tooth replacement in three different species of early ceratopsians (Yinlong, Hualianceratops, and Chaoyangsaurus), but also the observation of wear development, pulp cavity development, zahnreihen, and z-spacing and replacement rate to compare between taxa and address the succession of mandibular and replacement changes in the phylogeny of ceratopsian dinosaurs. The aims were achieved and the conclusions are strongly supported by the evidence discussed and the cited bibliography. Figures are clear and captions are concise. The presented information gives evidence for the comparison and discussion of the order of acquisition of different craniomandibular adaptations that lead to a specialized herbivorous diet, useful not only for ceratopsians and ornithischians, but also for other lineages of dinosaurs in the Mesozoic, and further for comparing with extant and extinct lineages of mammals. Dinosaurs not only were fantastic creatures from the past but also achieved different morphologic, physiologic, and behavioral traits unknown to any other creature, even mammals. For ceratopsians, the appearance of dental batteries corresponds to a unique trait only functionally similar to that in hadrosaurs and some sauropods, and understanding the steps that led to that specialized structure allows us to also understand the drivers that later guided their diversification during the Late Cretaceous.

    Thank you for your positive comments!

    Reviewer #3:

    The major strengths of the paper are its thorough level of detail, rich dataset, and easy readability. The figures are excellent and clear.

    One shortcoming of the paper is the lack of measurements -- a table of measurement for each functional and replacement tooth's length, mesiodistal width, and linguolabial width should be provided.

    We thank the reviewer for pointing out this. We have provided each functional and replacement tooth’s total height, maximum mesiodistal width, maximum labiolingual width of all specimens presented in TABLE S1. These data help to support our conclusions.

    Unfortunately the manuscript is not publishable in its current form because the conclusions are not testable based on the limited data provided. The authors stated "All data generated or analysed during this study are included in the manuscript and supporting file." This is not true. Only the 3D models derived from segmentations are provided, not the raw scans. Segmentation-derived models are interpretations, akin to publishing a drawing of a fossil instead of a photograph, which is not generally acceptable under today's publishing standards (drawings can be published alongside photographs). Please upload the raw scans to an appropriate repository such as Morphosource, Dryad, or Morphobank. Scans can be cropped to the dentigerous regions only, so long as scaling information is preserved.

    We have added raw micro-CT scans of all scanned specimens (all cropped to the dentigerous regions) in Dryad as .TIF or .BMP file format. The file object details are also provided in a TXT file ‘README_file.txt’ saved in Dryad, at https://doi.org/10.5061/dryad.9ghx3ffk0.

  3. eLife

    Evaluation Summary:

    Using micro-CT approaches, the authors provide a thorough investigation of dental morphology and development in some of the rarest and earliest representatives of three early ceratopsian dinosaur genera from China. The innovative approaches employed and nuanced inferences, including about the dental anatomy and replacement patterns in these early-diverging ceratopsians, make the manuscript interesting to mainstream researchers as well as the public.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

  4. eLife

    Reviewer #1 (Public Review):

    Hu and colleagues employ computed-tomography methods and provide a detailed description of and inferences about the dental system in three early-diverging ceratopsian dinosaur genera represented by rare specimens from China. Their study identifies nuanced tooth replacement rates and patterns. Furthermore, combined with the analysis of dental wear patterns, their study not only elucidates ontogenetic aspects of these early ceratopsians but also explores the implication of such patterns for dietary adaptations among these taxa. The manuscript, therefore, provides unique insights into the anatomical and ecological contexts of ceratopsians in such deep time.

    The manuscript is rich in data that are summarized in multiple tables and figures. It is also well-written and easy to follow. The inference and conclusions made are also overall well supported by the data presented.

    The only main comment I have concerns the inference made about the dietary adaptation of Yinlong, which is inferred to be characterized by "feeding strategies other than only grinding food with their teeth." I think that this could be expanded a bit more to incorporate dietary breadth as an additional possible explanation, particularly given the lack of conclusive evidence for the predominance of a single plant species. As it stands, the inference (made across lines 475 through 485) may only imply processing the same food resource using non-chewing methods (e.g., gastroliths to triturate fern). Could the incorporation of other, less abrasive plat foods--in addition to the fibrous ferns--in the diet of Yinlong be a possible, additional explanation for the relatively slow tooth replacement and lack of a heavy tooth wear from chewing-related stress?

  5. eLife

    Reviewer #2 (Public Review):

    The authors of the present work aimed to describe tooth replacement in early ceratopsian species from the Lower Jurassic of China, and with this novel information, discuss new hypotheses of successive changes in jaw evolution that led to the highly specialized replacement and jaw function of derived ceratopsids. Major strengths of this study include not only the use of microCT-scans and 3D reconstructions to address tooth replacement in three different species of early ceratopsians (Yinlong, Hualianceratops, and Chaoyangsaurus), but also the observation of wear development, pulp cavity development, zahnreihen, and z-spacing and replacement rate to compare between taxa and address the succession of mandibular and replacement changes in the phylogeny of ceratopsian dinosaurs. The aims were achieved and the conclusions are strongly supported by the evidence discussed and the cited bibliography. Figures are clear and captions are concise. The presented information gives evidence for the comparison and discussion of the order of acquisition of different craniomandibular adaptations that lead to a specialized herbivorous diet, useful not only for ceratopsians and ornithischians, but also for other lineages of dinosaurs in the Mesozoic, and further for comparing with extant and extinct lineages of mammals. Dinosaurs not only were fantastic creatures from the past but also achieved different morphologic, physiologic, and behavioral traits unknown to any other creature, even mammals. For ceratopsians, the appearance of dental batteries corresponds to a unique trait only functionally similar to that in hadrosaurs and some sauropods, and understanding the steps that led to that specialized structure allows us to also understand the drivers that later guided their diversification during the Late Cretaceous.

  6. eLife

    Reviewer #3 (Public Review):

    The major strengths of the paper are its thorough level of detail, rich dataset, and easy readability. The figures are excellent and clear.

    One shortcoming of the paper is the lack of measurements -- a table of measurement for each functional and replacement tooth's length, mesiodistal width, and linguolabial width should be provided.

    Unfortunately the manuscript is not publishable in its current form because the conclusions are not testable based on the limited data provided. The authors stated "All data generated or analysed during this study are included in the manuscript and supporting file." This is not true. Only the 3D models derived from segmentations are provided, not the raw scans. Segmentation-derived models are interpretations, akin to publishing a drawing of a fossil instead of a photograph, which is not generally acceptable under today's publishing standards (drawings can be published alongside photographs). Please upload the raw scans to an appropriate repository such as Morphosource, Dryad, or Morphobank. Scans can be cropped to the dentigerous regions only, so long as scaling information is preserved.

  7. Version published to 10.1101/2022.01.16.476516v1 on bioRxiv