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      A Triassic plesiosaurian skeleton and bone histology inform on evolution of a unique body plan

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          Abstract

          The first plesiosaur skeleton from the Triassic informs about the evolutionary success of four-flippered marine reptile.

          Abstract

          Secondary marine adaptation is a major pattern in amniote evolution, accompanied by specific bone histological adaptations. In the aftermath of the end-Permian extinction, diverse marine reptiles evolved early in the Triassic. Plesiosauria is the most diverse and one of the longest-lived clades of marine reptiles, but its bone histology is least known among the major marine amniote clades. Plesiosaurians had a unique and puzzling body plan, sporting four evenly shaped pointed flippers and (in most clades) a small head on a long, stiffened neck. The flippers were used as hydrofoils in underwater flight. A wide temporal, morphological, and morphometric gap separates plesiosaurians from their closest relatives (basal pistosaurs, Bobosaurus). For nearly two centuries, plesiosaurians were thought to appear suddenly in the earliest Jurassic after the end-Triassic extinctions. We describe the first Triassic plesiosaurian, from the Rhaetian of Germany, and compare its long bone histology to that of later plesiosaurians sampled for this study. The new taxon is recovered as a basal member of the Pliosauridae, revealing that diversification of plesiosaurians was a Triassic event and that several lineages must have crossed into the Jurassic. Plesiosaurian histology is strikingly uniform and different from stem sauropterygians. Histology suggests the concurrent evolution of fast growth and an elevated metabolic rate as an adaptation to cruising and efficient foraging in the open sea. The new specimen corroborates the hypothesis that open ocean life of plesiosaurians facilitated their survival of the end-Triassic extinctions.

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          Faunal turnover of marine tetrapods during the Jurassic-Cretaceous transition.

          Marine and terrestrial animals show a mosaic of lineage extinctions and diversifications during the Jurassic-Cretaceous transition. However, despite its potential importance in shaping animal evolution, few palaeontological studies have focussed on this interval and the possible climate and biotic drivers of its faunal turnover. In consequence evolutionary patterns in most groups are poorly understood. We use a new, large morphological dataset to examine patterns of lineage diversity and disparity (variety of form) in the marine tetrapod clade Plesiosauria, and compare these patterns with those of other organisms. Although seven plesiosaurian lineages have been hypothesised as crossing the Jurassic-Cretaceous boundary, our most parsimonious topology suggests the number was only three. The robust recovery of a novel group including most Cretaceous plesiosauroids (Xenopsaria, new clade) is instrumental in this result. Substantial plesiosaurian turnover occurred during the Jurassic-Cretaceous boundary interval, including the loss of substantial pliosaurid, and cryptoclidid diversity and disparity, followed by the radiation of Xenopsaria during the Early Cretaceous. Possible physical drivers of this turnover include climatic fluctuations that influenced oceanic productivity and diversity: Late Jurassic climates were characterised by widespread global monsoonal conditions and increased nutrient flux into the opening Atlantic-Tethys, resulting in eutrophication and a highly productive, but taxonomically depauperate, plankton. Latest Jurassic and Early Cretaceous climates were more arid, resulting in oligotrophic ocean conditions and high taxonomic diversity of radiolarians, calcareous nannoplankton and possibly ammonoids. However, the observation of discordant extinction patterns in other marine tetrapod groups such as ichthyosaurs and marine crocodylomorphs suggests that clade-specific factors may have been more important than overarching extrinsic drivers of faunal turnover during the Jurassic-Cretaceous boundary interval.
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            The many adaptations of bone.

            J.D Currey (2003)
            Studies concerned with the "adaptations" in bones usually deal with modelling taking place during the individual's lifetime. However, many adaptations are produced over evolutionary time. This survey samples some adaptations of bone that may occur over both length scales, and tries to show whether short- or long-term adaptation is important. (a) Woven and lamellar bone. Woven bone is less mechanically competent than lamellar bone but is frequently found in bones that grow quickly. (b) Stress concentrations in bone. Bone is full of cavities that potentially may act as stress concentrators. Usually these cavities are oriented to minimise their stress-concentrating effect. Furthermore, the "flow" of lamellae round the cavities will still further reduce their stress-concentrating effect, but the elastic anisotropy of bone will, contrarily, tend to enhance it in normal loading situations. (c) Stiffness versus toughness. The mineral content of bone is the main determinant of differences in mechanical properties. Different bones have different mineral contents that optimise the mix of stiffness and toughness needed. (d) Synergy of whole bone architecture and material properties. As bone material properties change during growth the architecture of the whole bone is modified concurrently, to produce an optimum mechanical behaviour of the whole bone. (e) Secondary remodelling. The formation of secondary osteones in general weakens bone. Various suggestions that have been put forward to account for secondary remodelling: enabling mineral homeostasis; removing dead bone; changing the grain of the bone; taking out microcracks. (f) The hollowness of bones. It is shown how the degree of hollowness is adapted to the life of the animal.
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              Mesozoic marine tetrapod diversity: mass extinctions and temporal heterogeneity in geological megabiases affecting vertebrates.

              The fossil record is our only direct means for evaluating shifts in biodiversity through Earth's history. However, analyses of fossil marine invertebrates have demonstrated that geological megabiases profoundly influence fossil preservation and discovery, obscuring true diversity signals. Comparable studies of vertebrate palaeodiversity patterns remain in their infancy. A new species-level dataset of Mesozoic marine tetrapod occurrences was compared with a proxy for temporal variation in the volume and facies diversity of fossiliferous rock (number of marine fossiliferous formations: FMF). A strong correlation between taxic diversity and FMF is present during the Cretaceous. Weak or no correlation of Jurassic data suggests a qualitatively different sampling regime resulting from five apparent peaks in Triassic-Jurassic diversity. These correspond to a small number of European formations that have been the subject of intensive collecting, and represent 'Lagerstätten effects'. Consideration of sampling biases allows re-evaluation of proposed mass extinction events. Marine tetrapod diversity declined during the Carnian or Norian. However, the proposed end-Triassic extinction event cannot be recognized with confidence. Some evidence supports an extinction event near the Jurassic/Cretaceous boundary, but the proposed end-Cenomanian extinction is probably an artefact of poor sampling. Marine tetrapod diversity underwent a long-term decline prior to the Cretaceous-Palaeogene extinction.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                December 2017
                13 December 2017
                : 3
                : 12
                : e1701144
                Affiliations
                [1 ]Bereich Paläontologie, Steinmann-Institut für Geologie, Mineralogie und Paläontologie, Universität Bonn, Nussallee 8, 53115 Bonn, Germany.
                [2 ]Osaka Museum of Natural History, Nagai Park 1-23, Higashi-Sumiyoshi-ku, Osaka 546-0034, Japan.
                [3 ]Division of Materials and Manufacturing Science, Graduate School of Engineering, Osaka University, 2-1 Yamada-Oka, Suita, Osaka 565-0871, Japan.
                [4 ]UMR 7179 CNRS/Muséum National d’Histoire Naturelle, Départment Adaptations du Vivant, 57 rue Cuvier CP-55, 75005 Paris, France.
                [5 ]Atmosphere and Ocean Research Institute, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa-shi, Chiba 277-8564, Japan.
                [6 ]Dinosaur Institute, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, CA 90007, USA.
                Author notes
                [*]

                Present address: Biosphere-Geosphere Science, Okayama University of Science, Ridai-cho 1-1, Kita-ku, Okayama 700-0005, Japan.

                []Corresponding author. Email: martin.sander@ 123456uni-bonn.de
                Author information
                http://orcid.org/0000-0002-1157-8604
                http://orcid.org/0000-0001-9162-4860
                http://orcid.org/0000-0003-4981-4307
                Article
                1701144
                10.1126/sciadv.1701144
                5729018
                29242826
                a679c415-f27b-400f-a00c-8a3cb576620f
                Copyright © 2017 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                : 04 April 2017
                : 16 November 2017
                Funding
                Funded by: doi http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: award338968
                Award ID: SA 469/47-1
                Funded by: doi http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: award341030
                Award ID: project no. 27/659 and 26800270
                Funded by: LWL Museum fur Naturkunde;
                Award ID: award341031
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Life Sciences
                Paleontology
                Custom metadata
                Jeanelle Ebreo

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