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University of Birmingham Osteology of the archosauromorph Teyujagua paradoxa and the early evolution of the archosauriform skull Pinheiro, Felipe; Oliveira, Daniel; Butler, Richard DOI: 10.1093/zoolinnean/zlz093 License: Other (please specify with Rights Statement) Document Version Peer reviewed version Citation for published version (Harvard): Pinheiro, F, Oliveira, D & Butler, R 2020, 'Osteology of the archosauromorph Teyujagua paradoxa and the early evolution of the archosauriform skull', Zoological Journal of the Linnean Society, vol. 189, no. 1, pp. 378–417. https://doi.org/10.1093/zoolinnean/zlz093 Link to publication on Research at Birmingham portal Publisher Rights Statement: This is a pre-copyedited, author-produced version of an article accepted for publication in Zoological Journal of the Linnean Society following peer review. The version of record Pinheiro, F.L., Oliveira, D & Butler, R.J. (2019) Osteology of the archosauromorph Teyujagua paradoxa and the early evolution of the archosauriform skull, Zoological Journal of the Linnean Society, zlz093 is available online at: https://doi.org/10.1093/zoolinnean/zlz093 General rights Unless a licence is specified above, all rights (including copyright and moral rights) in this document are retained by the authors and/or the copyright holders. 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Oct. 2021 Zoological Journal of the Linnean Society Osteology of the archosauromorph Teyujagua paradoxa Pinheiro et al. 2016 and the early evolution of the archosauriform skull Journal: Zoological Journal of the Linnean Society Manuscript ID ZOJ-03-2019-3638.R1 Manuscript Type:ForOriginal Review Article Only Archosauromorpha < Taxa, Gondwana < Palaeontology, Triassic < Keywords: Palaeontology, phylogeny < Phylogenetics, skull < Anatomy Archosauriformes are a major group of reptiles that include the crown group Archosauria (birds, crocodilians, and their extinct relatives) and closely related taxa. Archosauriformes are characterized by a highly diagnostic skull architecture, which is linked to the predatory habits of their early representatives and the development of extensive cranial pneumaticity associated with the nasal capsule. The evolution of the archosauriform skull from the more plesiomorphic configuration present ancestrally in the broader clade Archosauromorpha was, until recently, elusive. This began to change with the discovery and description of Teyujagua paradoxa, an early archosauromorph from the Lower Triassic Abstract: Sanga do Cabral Formation of Brazil. Here, we provide a detailed osteological description of the holotype and thus far only known specimen of T. paradoxa. In addition to providing new details of the anatomy of T. paradoxa, our study also revealed an early development of skull pneumaticity prior to the emergence of the antorbital fenestra. We use this new data to discuss the evolution of antorbital openings within Archosauriformes. Reappraisal of the phylogenetic position of T. paradoxa supports previous hypotheses of a close relationship with Archosauriformes. The data presented here provide new insights into character evolution during the origin of the archosauriform skull. Page 1 of 98 Zoological Journal of the Linnean Society 1 1 2 3 Archosauriformes are a major group of fossil and living reptiles that include the crown 4 5 6 group Archosauria (birds, crocodilians, and their extinct relatives) and closely related 7 8 taxa. Archosauriformes are characterized by a highly diagnostic skull architecture, 9 10 which is linked to the predatory habits of their early representatives and the 11 12 development of extensive cranial pneumaticity associated with the nasal capsule. The 13 14 15 evolution of the archosauriform skull from the more plesiomorphic configuration 16 17 present ancestrally in the broader clade Archosauromorpha was, until recently, elusive. 18 19 This began to change with the discovery and description of Teyujagua paradoxa, an 20 21 For Review Only 22 early archosauromorph from the Lower Triassic Sanga do Cabral Formation of Brazil. 23 24 Here, we provide a detailed osteological description of the holotype and thus far only 25 26 known specimen of T. paradoxa. In addition to providing new details of the anatomy of 27 28 T. paradoxa, our study also reveals an early development of skull pneumaticity prior to 29 30 31 the emergence of the antorbital fenestra. We use these new data to discuss the evolution 32 33 of antorbital openings within Archosauriformes. Reappraisal of the phylogenetic 34 35 position of T. paradoxa supports previous hypotheses of a close relationship with 36 37 38 Archosauriformes. The data presented here provide new insights into character 39 40 evolution during the origin of the archosauriform skull. 41 42 43 ADDITIONAL KEYWORDS: Archosauromorpha – Brazil – Gondwana – Lower 44 45 Triassic – phylogeny – skull. 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Zoological Journal of the Linnean Society Page 2 of 98 2 1 2 3 INTRODUCTION 4 5 6 Archosauriformes are an extraordinarily diverse clade of diapsid reptiles that originated 7 8 during the Permian and underwent several pulses of adaptive radiation during the 9 10 11 Mesozoic Era (Gauthier, 1986; Brusatte et al., 2008; Claessens et al., 2009; Nesbitt, 12 13 2011; Ezcurra et al., 2014; Ezcurra & Butler, 2018). Representatives of this clade, such 14 15 as non-avian dinosaurs, birds, crocodilians and pterosaurs, have been major components 16 17 18 of tetrapod faunas since the Triassic Period, with birds comprising around a third of 19 20 extant tetrapod diversity (Jetz et al., 2012). Several classic anatomical features, such as 21 For Review Only 22 the external mandibular fenestrae, closed lower temporal bars, serrated teeth and 23 24 25 antorbital fenestrae characterize the archosauriform skull (Gauthier, 1986; Nesbitt, 26 27 2011; Ezcurra et al., 2016). However, the evolution of these characters from the typical 28 29 condition observed in early members of the more inclusive clade Archosauromorpha 30 31 was, until recently, elusive. The recent description of the archosauromorph Teyujagua 32 33 34 paradoxa from the Lower Triassic Sanga do Cabral Formation of Brazil, however, 35 36 started to shed light on this important evolutionary transition. Teyujagua paradoxa was 37 38 recovered by Pinheiro et al. (2016) as the sister-taxon to Archosauriformes, and this 39 40 41 species displays several intermediate character conditions that provide new insights into 42 43 the assembly of the archosauriform skull (Pinheiro et al. 2016). 44 45 46 Teyujagua paradoxa is known only from its holotype, UNIPAMPA 0653, an 47 48 almost complete skull articulated with lower jaws and cervicals I-IV (Figs 1, 2). This 49 50 51 specimen was only briefly described by Pinheiro et al. (2016). Since then, further 52 53 preparation of UNIPAMPA 0653 has exposed key features of the left side of the skull 54 55 and cervical vertebrae. In addition, X-ray micro-computed tomography imaging (µCT 56 57 scans) and 3D modeling of individual bones have revealed anatomical characters which 58 59 60 otherwise would be impossible to access. Here we present a complete description of the Page 3 of 98 Zoological Journal of the Linnean Society 3 1 2 3 holotype of T. paradoxa. We also reassess the phylogenetic relationships of T. paradoxa 4 5 6 using two different phylogenetic frameworks and discuss the early evolution of key 7 8 characters of archosauriform craniomandibular anatomy. 9 10 11 12 13 14 INSTITUTION ABBREVIATIONS 15 16 17 AMNH, American Museum of Natural History, New York, USA; BP, Evolutionary 18 19 Studies Institute (formerly Bernard Price Institute for Palaeontological Research), 20 21 University of the Witwatersrand,For Review Johannesburg, South Only Africa; CAPPA/UFSM, Centro 22 23 24 de Apoio à Pesquisa Paleontológica da Quarta Colônia, São João do Polêsine, Brazil; 25 26 FMNH, Field Museum of Natural History, Chicago, USA; GMPKU, Geological 27 28 Museum of Peking University, Beijing, China; ISIR, Indian Statistical Institute Reptiles, 29 30 Kolkata, India; IVPP, Institute of Vertebrate Paleontology and Paleoanthropology, 31 32 33 Beijing, China; MCN, Museu de Ciências Naturais, Fundação Zoobotânica do Rio 34 35 Grande do Sul, Porto Alegre, Brazil; MCP, Museu de Ciências e Tecnologia da 36 37 Pontifícia Universidade Católica do Rio Grande do Sul,
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  • Resolving Homology in the Face of Shifting Germ Layer Origins

    Resolving Homology in the Face of Shifting Germ Layer Origins

    REVIEW ARTICLE Resolving homology in the face of shifting germ layer origins: Lessons from a major skull vault boundary Camilla S Teng1,2†, Lionel Cavin3, Robert E Maxson Jnr2, Marcelo R Sa´ nchez-Villagra4, J Gage Crump1* 1Department of Stem Cell Biology and Regenerative Medicine, University of Southern California, Los Angeles, United States; 2Department of Biochemistry, Keck School of Medicine, University of Southern California, Los Angeles, United States; 3Department of Earth Sciences, Natural History Museum of Geneva, Geneva, Switzerland; 4Paleontological Institute and Museum, University of Zurich, Zurich, Switzerland Abstract The vertebrate skull varies widely in shape, accommodating diverse strategies of feeding and predation. The braincase is composed of several flat bones that meet at flexible joints called sutures. Nearly all vertebrates have a prominent ‘coronal’ suture that separates the front and back of the skull. This suture can develop entirely within mesoderm-derived tissue, neural crest- derived tissue, or at the boundary of the two. Recent paleontological findings and genetic insights in non-mammalian model organisms serve to revise fundamental knowledge on the development and evolution of this suture. Growing evidence supports a decoupling of the germ layer origins of *For correspondence: the mesenchyme that forms the calvarial bones from inductive signaling that establishes discrete [email protected] bone centers. Changes in these relationships facilitate skull evolution and may create susceptibility to disease. These concepts provide a general framework for approaching issues of homology in Present address: †Department of Cell and Tissue Biology, cases where germ layer origins have shifted during evolution. University of California, San Francisco, San Francisco, United States Introduction Competing interests: The At the beginning of skull vault development, mesenchymal cells of either neural crest or mesoderm authors declare that no origin condense into nascent bone fields.