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      Osteology of an exceptionally well-preserved tapejarid skeleton from Brazil: Revealing the anatomy of a curious pterodactyloid clade

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          Abstract

          A remarkably well-preserved, almost complete and articulated new specimen (GP/2E 9266) of Tupandactylus navigans is here described for the Early Cretaceous Crato Formation of Brazil. The new specimen comprises an almost complete skeleton, preserving both the skull and post-cranium, associated with remarkable preservation of soft tissues, which makes it the most complete tapejarid known thus far. CT-Scanning was performed to allow the assessment of bones still covered by sediment. The specimen can be assigned to Tupa. navigans due to its vertical supra-premaxillary bony process and short and rounded parietal crest. It also bears the largest dentary crest among tapejarine pterosaurs and a notarium, which is absent in other representatives of the clade. The new specimen is here regarded as an adult individual. This is the first time that postcranial remains of Tupa. navigans are described, being also an unprecedented record of an articulated tapejarid skeleton from the Araripe Basin.

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          Most cited references82

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          TNT version 1.5, including a full implementation of phylogenetic morphometrics

          Version 1.5 of the computer program TNT completely integrates landmark data into phylogenetic analysis. Landmark data consist of coordinates (in two or three dimensions) for the terminal taxa; TNT reconstructs shapes for the internal nodes such that the difference between ancestor and descendant shapes for all tree branches sums up to a minimum; this sum is used as tree score. Landmark data can be analysed alone or in combination with standard characters; all the applicable commands and options in TNT can be used transparently after reading a landmark data set. The program continues implementing all the types of analyses in former versions, including discrete and continuous characters (which can now be read at any scale, and automatically rescaled by TNT). Using algorithms described in this paper, searches for landmark data can be made tens to hundreds of times faster than it was possible before (from T to 3T times faster, where T is the number of taxa), thus making phylogenetic analysis of landmarks feasible even on standard personal computers.
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            The ontogeny of Pteranodon and other pterosaurs

            S. Bennett (1993)
            Immature specimens of the Late Cretaceous pterosaur Pteranodon were identified using three size-independent criteria: (1) fusion of various cranial and postcranial elements; (2) degree of epiphyseal ossification; and (3) bone grain or degree of ossification of limb-bone shafts. Immature individuals make up 15% of available specimens of Pteranodon and do not differ significantly in size from mature individuals. This and the extensive fusion of the mature skeleton suggest that Pteranodon had determinate growth. The bone of limb-bone shafts of immature individuals is fibro-lamellar bone, which suggests that they grew rapidly to adult size. The size-independent criteria can also be used to identify immature and mature individuals of other pterosaur taxa, and other large pterodactyloids also probably exhibited rapid determinate growth.
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              The earliest pterodactyloid and the origin of the group.

              The pterosaurs were a diverse group of Mesozoic flying reptiles that underwent a body plan reorganization, adaptive radiation, and replacement of earlier forms midway through their long history, resulting in the origin of the Pterodactyloidea, a highly specialized clade containing the largest flying organisms. The sudden appearance and large suite of morphological features of this group were suggested to be the result of it originating in terrestrial environments, where the pterosaur fossil record has traditionally been poor [1, 2], and its many features suggested to be adaptations to those environments [1, 2]. However, little evidence has been available to test this hypothesis, and it has not been supported by previous phylogenies or early pterodactyloid discoveries. We report here the earliest pterosaur with the diagnostic elongate metacarpus of the Pterodactyloidea, Kryptodrakon progenitor, gen. et sp. nov., from the terrestrial Middle-Upper Jurassic boundary of Northwest China. Phylogenetic analysis confirms this species as the basalmost pterodactyloid and reconstructs a terrestrial origin and a predominantly terrestrial history for the Pterodactyloidea. Phylogenetic comparative methods support this reconstruction by means of a significant correlation between wing shape and environment also found in modern flying vertebrates, indicating that pterosaurs lived in or were at least adapted to the environments in which they were preserved.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                25 August 2021
                2021
                : 16
                : 8
                : e0254789
                Affiliations
                [1 ] Instituto de Biociências, Universidade de São Paulo, São Paulo, São Paulo, Brazil
                [2 ] Faculdade de Ciências e Tecnologia, FCT, GeoBioTec, Department of Earth Sciences, Universidade Nova de Lisboa, Caparica, Portugal
                [3 ] Museu da Lourinhã, Lourinhã, Portugal
                [4 ] Laboratório de Paleobiologia, Universidade Federal do Pampa, São Gabriel, Rio Grande do Sul, Brazil
                [5 ] Instituto de Biociências, Laboratório de Herpetologia (LHERP), Universidade Estadual Paulista, São Vicente, São Paulo, Brazil
                [6 ] Instituto de Geociências, Universidade de São Paulo, Cidade Universitária, São Paulo, São Paulo, Brazil
                [7 ] Centro de Ciências Naturais e Humanas, Laboratório de Paleontologia de Vertebrados e Comportamento Animal (LAPC), Universidade Federal do ABC, São Paulo, São Paulo, Brazil
                Università degli Studi di Torino, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0003-2657-5702
                https://orcid.org/0000-0003-1253-3616
                Article
                PONE-D-20-38270
                10.1371/journal.pone.0254789
                8386889
                34432814
                5336b420-5e11-4d15-ba36-0163ef84464c
                © 2021 Beccari et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 December 2020
                : 4 July 2021
                Page count
                Figures: 19, Tables: 5, Pages: 43
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 407969/2016-0, 305758/2017-9
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004263, Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul;
                Award ID: 16/2551-0000271-1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001871, Fundação para a Ciência e a Tecnologia;
                Award ID: UIDB/04035/2020
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 421772/2018-2
                Award Recipient :
                FLP is supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq process numbers 407969/2016-0, 305758/2017-9) and Fundacão de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS process number 16/2551-0000271-1). OM is supported by grants from GeoBioTec-GeoBioSciences, GeoTechnologies and GeoEngineering NOVA [GeoBioCiências, GeoTecnologias e GeoEngenharias], grant UIDB/04035/2020 by the Fundação para a Ciência e Tecnologia. FRC is supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for support (grant No. 421772/2018-2).
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                Musculoskeletal System
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                Custom metadata
                The Supplemental Files include the dataset adopted for the phylogenetic analysis. The specimen described in this study is stored in the collection of the Coleção de Paleontologia Sistemática of the Geosciences Institute of Universidade de São Paulo under reference number: GP/2E 9266. Data inquiries may be sent to the data curator Juliana de Moraes Leme at leme@ 123456usp.br . The raw 3D data for the specimen can be found in the online repository of MorphoSource at: ark:/87602/m4/369632.

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