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      A new Heterodontosaurus specimen elucidates the unique ventilatory macroevolution of ornithischian dinosaurs

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          Abstract

          Ornithischian dinosaurs were ecologically prominent herbivores of the Mesozoic Era that achieved a global distribution by the onset of the Cretaceous. The ornithischian body plan is aberrant relative to other ornithodiran clades, and crucial details of their early evolution remain obscure. We present a new, fully articulated skeleton of the early branching ornithischian Heterodontosaurus tucki. Phase-contrast enhanced synchrotron data of this new specimen reveal a suite of novel postcranial features unknown in any other ornithischian, with implications for the early evolution of the group. These features include a large, anteriorly projecting sternum; bizarre, paddle-shaped sternal ribs; and a full gastral basket – the first recovered in Ornithischia. These unusual anatomical traits provide key information on the evolution of the ornithischian body plan and suggest functional shifts in the ventilatory apparatus occurred close to the base of the clade. We complement these anatomical data with a quantitative analysis of ornithischian pelvic architecture, which allows us to make a specific, stepwise hypothesis for their ventilatory evolution.

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          The fossilised skeletons of long extinct dinosaurs are more than just stones. By comparing these remains to their living relatives such as birds and crocodiles, palaeontologists can reveal how dinosaurs grew, moved, ate and socialised. Previous research indicates that dinosaurs were likely warm-blooded and also more active than modern reptiles. This means they would have required breathing mechanisms capable of supplying enough oxygen to allow these elevated activity levels.

          So far, much of our insight into dinosaur breathing biology has been biased towards dinosaur species more closely related to modern birds, such as Tyrannosaurus rex, as well as the long-necked sauropods. The group of herbivorous dinosaurs known as ornithischians, which include animals with head ornamentation, spikes and heavy body armour, like that found in Triceratops and Stegosaurus, have often been overlooked. As a result, there are still significant gaps in ornithischian biology, especially in understanding how they breathed.

          Radermacher et al. used high-powered X-rays to study a new specimen of the most primitive ornithischian dinosaur, Heterodontosaurus tucki, and discovered that this South African dinosaur has bones researchers did not know existed in this species. These include bones that are part of the breathing system of extant reptiles and birds, including toothpick-shaped bones called gastralia, paired sternal bones and sternal ribs shaped like tennis rackets.

          Together, these new pieces of anatomy form a complicated chest skeleton with a large range of motion that would have allowed the body to expand during breathing cycles. But this increased motion of the chest was only possible in more primitive ornithischians. More advanced species lost much of the anatomy that made this motion possible. Radermacher et al. show that while the chest was simpler in advanced species, their pelvis was more specialised and likely played a role in breathing as it does in modern crocodiles.

          This new discovery could inform the work of biologists who study the respiratory diversity of both living and extinct species. Differences in breathing strategies might be one of the underlying reasons that some lineages of animals go extinct. It could explain why some species do better than others under stressful conditions, like when the climate is warmer or has less oxygen.

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            APE: Analyses of Phylogenetics and Evolution in R language.

            Analysis of Phylogenetics and Evolution (APE) is a package written in the R language for use in molecular evolution and phylogenetics. APE provides both utility functions for reading and writing data and manipulating phylogenetic trees, as well as several advanced methods for phylogenetic and evolutionary analysis (e.g. comparative and population genetic methods). APE takes advantage of the many R functions for statistics and graphics, and also provides a flexible framework for developing and implementing further statistical methods for the analysis of evolutionary processes. The program is free and available from the official R package archive at http://cran.r-project.org/src/contrib/PACKAGES.html#ape. APE is licensed under the GNU General Public License.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                06 July 2021
                2021
                : 10
                : e66036
                Affiliations
                [1 ]Evolutionary Studies Institute, University of the Witwatersrand JohannesburgSouth Africa
                [2 ]Department of Earth and Environmental Sciences, University of Minnesota MinneapolisUnited States
                [3 ]European Synchrotron Radiation Facility GrenobleFrance
                [4 ]Natural History Museum, Imaging and Analysis Centre LondonUnited Kingdom
                [5 ]Department of Cell Biology & Anatomy, School of Medicine, Louisiana State University Health Sciences Center New OrleansUnited States
                [6 ]School of Geography, Earth and Environmental Sciences, University of Birmingham BirminghamUnited Kingdom
                [7 ]Department of Geological Sciences, University of Cape Town Cape TownSouth Africa
                [8 ]Department of Biological Sciences, University of Alberta EdmontonCanada
                [9 ]Department of Earth Sciences, Albany Museum GrahamstownSouth Africa
                [10 ]Division of Paleontology, American Museum of Natural History New YorkUnited States
                Flinders University Australia
                Pennsylvania State University United States
                Flinders University Australia
                George washington University United States
                Author information
                https://orcid.org/0000-0001-6524-7811
                http://orcid.org/0000-0002-8315-1458
                https://orcid.org/0000-0002-8636-925X
                https://orcid.org/0000-0003-2136-7541
                https://orcid.org/0000-0003-4699-0823
                https://orcid.org/0000-0003-0215-7792
                https://orcid.org/0000-0002-9991-0439
                https://orcid.org/0000-0002-1008-0687
                Article
                66036
                10.7554/eLife.66036
                8260226
                34225841
                ebfd423e-048c-45d9-b34b-327922ba347a
                © 2021, Radermacher et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 22 December 2020
                : 24 May 2021
                Funding
                Funded by: DST-NRF Centre of Excellence in Palaeosciences;
                Award Recipient :
                Funded by: Palaeontological Scientific Trust;
                Award Recipient :
                Funded by: Durand Foundation for Evolutionary Biology and Phycology;
                Award ID: No. DFEBP00001/16
                Award Recipient :
                Funded by: DST-NRF-African Origins Platform;
                Award ID: 98800
                Award Recipient :
                Funded by: DST-NRF-African Origins Platform;
                Award ID: 98825
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Evolutionary Biology
                Custom metadata
                A new specimen of Heterodontosaurus elucidates how ornithischian dinosaurs evolved a body plan substantially different from that of other dinosaurs and what these differences meant for their breathing.

                Life sciences
                ornithodira,dinosauria,ornithischia,other
                Life sciences
                ornithodira, dinosauria, ornithischia, other

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