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Reassessing the Permian Saurian Fossil Record and the Timing of the Crocodile-Lizard Divergence Ezcurra, Martin; Scheyer, Torsten M.; Butler, Richard

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Reassessing the Permian Saurian Fossil Record and the Timing of the Crocodile-Lizard Divergence Ezcurra, Martin; Scheyer, Torsten M.; Butler, Richard The Origin and Early Evolution of Sauria: Reassessing the Permian Saurian Fossil Record and the Timing of the Crocodile-Lizard Divergence Ezcurra, Martin; Scheyer, Torsten M.; Butler, Richard DOI: 10.1371/journal.pone.0089165 License: Creative Commons: Attribution (CC BY) Document Version Publisher's PDF, also known as Version of record Citation for published version (Harvard): Ezcurra, MD, Scheyer, TM & Butler, RJ 2014, 'The Origin and Early Evolution of Sauria: Reassessing the Permian Saurian Fossil Record and the Timing of the Crocodile-Lizard Divergence', PLoS ONE, vol. 9, no. 2, e89165. https://doi.org/10.1371/journal.pone.0089165 Link to publication on Research at Birmingham portal 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. The express permission of the copyright holder must be obtained for any use of this material other than for purposes permitted by law. •Users may freely distribute the URL that is used to identify this publication. •Users may download and/or print one copy of the publication from the University of Birmingham research portal for the purpose of private study or non-commercial research. •User may use extracts from the document in line with the concept of ‘fair dealing’ under the Copyright, Designs and Patents Act 1988 (?) •Users may not further distribute the material nor use it for the purposes of commercial gain. Where a licence is displayed above, please note the terms and conditions of the licence govern your use of this document. When citing, please reference the published version. Take down policy While the University of Birmingham exercises care and attention in making items available there are rare occasions when an item has been uploaded in error or has been deemed to be commercially or otherwise sensitive. If you believe that this is the case for this document, please contact [email protected] providing details and we will remove access to the work immediately and investigate. Download date: 01. Feb. 2019 The Origin and Early Evolution of Sauria: Reassessing the Permian Saurian Fossil Record and the Timing of the Crocodile-Lizard Divergence Martı´n D. Ezcurra1,2*, Torsten M. Scheyer3, Richard J. Butler1,2 1 School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom, 2 GeoBio-Center, Ludwig-Maximilian- Universita¨tMu¨nchen, Munich, Germany, 3 Pala¨ontologisches Institut und Museum, Universita¨tZu¨rich, Zurich, Switzerland Abstract Sauria is the crown-group of Diapsida and is subdivided into Lepidosauromorpha and Archosauromorpha, comprising a high percentage of the diversity of living and fossil tetrapods. The split between lepidosauromorphs and archosauromorphs (the crocodile-lizard, or bird-lizard, divergence) is considered one of the key calibration points for molecular analyses of tetrapod phylogeny. Saurians have a very rich Mesozoic and Cenozoic fossil record, but their late Paleozoic (Permian) record is problematic. Several Permian specimens have been referred to Sauria, but the phylogenetic affinity of some of these records remains questionable. We reexamine and review all of these specimens here, providing new data on early saurian evolution including osteohistology, and present a new morphological phylogenetic dataset. We support previous studies that find that no valid Permian record for Lepidosauromorpha, and we also reject some of the previous referrals of Permian specimens to Archosauromorpha. The most informative Permian archosauromorph is Protorosaurus speneri from the middle Late Permian of Western Europe. A historically problematic specimen from the Late Permian of Tanzania is redescribed and reidentified as a new genus and species of basal archosauromorph: Aenigmastropheus parringtoni. The supposed protorosaur Eorasaurus olsoni from the Late Permian of Russia is recovered among Archosauriformes and may be the oldest known member of the group but the phylogenetic support for this position is low. The assignment of Archosaurus rossicus from the latest Permian of Russia to the archosauromorph clade Proterosuchidae is supported. Our revision suggests a minimum fossil calibration date for the crocodile-lizard split of 254.7 Ma. The occurrences of basal archosauromorphs in the northern (30uN) and southern (55uS) parts of Pangea imply a wider paleobiogeographic distribution for the group during the Late Permian than previously appreciated. Early archosauromorph growth strategies appear to be more diverse than previously suggested based on new data on the osteohistology of Aenigmastropheus. Citation: Ezcurra MD, Scheyer TM, Butler RJ (2014) The Origin and Early Evolution of Sauria: Reassessing the Permian Saurian Fossil Record and the Timing of the Crocodile-Lizard Divergence. PLoS ONE 9(2): e89165. doi:10.1371/journal.pone.0089165 Editor: Valerio Ketmaier, Institute of Biochemistry and Biology, Germany Received September 9, 2013; Accepted January 14, 2014; Published February 27, 2014 Copyright: ß 2014 Ezcurra 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. Funding: Funding was provided by the Synthesys Programm (to MDE), DFG Emmy Noether Programme (BU 2587/3-1 to RJB), and Swiss National Science Foundation (31003A_146440/1 to TS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: Richard Butler is a PLOS ONE Editorial Board member. However, this does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials. * E-mail: [email protected] Introduction The best source of information on the early history of Sauria comes from the numerous fossils of the well-known basal Saurians, or crown group diapsids, are highly taxonomically archosauromorph Protorosaurus speneri from the Late Permian of and morphologically diverse in extant ecosystems, with around Germany and England [19–21]. Multiple less completely known 9,400 lepidosaur (snakes, lizards and rhynchocephalians) and specimens have been also argued to be Permian members of 10,000 archosaur (birds and crocodilians) species, including Sauria (e.g. Parrington’s ‘‘problematic reptile’’ from Tanzania, cursorial, semi-aquatic, marine, fossorial and volant forms [1,2]. UMZC T836 [9]). A better understanding of the Permian saurian The stem-groups of Lepidosauria (non-lepidosaurian Lepidosaur- record is fundamental for providing more accurate fossil omorpha) and Archosauria (non-archosaurian Archosauromor- constraints on the calibration of the crocodile-lizard ( = bird- pha) also include several morphologically disparate saurian lizard) divergence, a major split within vertebrates that is of keen lineages that were mostly restricted in time to the Triassic. These interest to molecular and evolutionary biologists and vertebrate lineages formed important components of Triassic continental paleontologists alike [22–25]. A better knowledge of Permian assemblages, and include kuehneosaurids, rhynchosaurs, proter- saurians is also necessary to improve understanding of phyloge- osuchids, erythrosuchids, euparkeriids, doswelliids and protero- netic relationships within early members of Diapsida, an area of champsids [3–8]. However, the earliest (i.e. pre-Mesozoic) key interest because of the controversial systematic affinities of evolutionary history of Sauria is poorly known and there has several possible saurian lineages including turtles, choristoderans been substantial debate regarding the late Paleozoic (i.e. Permian) and sauropterygians (e.g. [26–39]). New information on the record of the group (e.g. [3,9–18]). Permian saurian record may also yield fresh insights into survivorship of this clade across the Permian-Triassic mass PLOS ONE | www.plosone.org 1 February 2014 | Volume 9 | Issue 2 | e89165 Revisting the Permian Saurian Record extinction and the dynamics of the dramatic saurian radiation in browni, Noteosuchus colletti, Paliguana whitei, Proterosuchus fergusi, post-extinction ecosystems. Protorosaurus speneri, Tanystropheus longobardicus). Eorasaurus olsoni and Here, we revisit and reexamine the Permian record of Sauria to Noteosuchus colletti are included for the first time in a quantitative provide new information on the diversity, phylogeny, morphology, phylogenetic analysis. The hypothesis of Dilkes [4] that Noteosuchus geographic distribution and physiology of Permian members of the colletti is a junior synonym of Mesosuchus browni was not followed clade, and the timing of the crocodile-lizard (or bird-lizard) split. here because this proposal was based on generalized plesio- We fully or partially redescribe some Permian saurian specimens morphic similarities rather than autapomorphies and the temporal (e.g. UMZC T836; BP/1/4220; Eorasaurus olsoni) and we erect a gap between the two species spans most of the Early Triassic [11]. new genus and species of archosauromorph, Aenigmastropheus As a result, Noteosuchus colletti was scored as an independent parringtoni, for a specimen from the middle Late Permian of operational taxonomic unit (OTU) because of its potential to shed Tanzania. Our new data provides an improved understanding of light on the minimal divergence time of Rhynchosauria. The early saurian
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