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Evolution, Diversity, and Development of the Craniocervical System in Turtles with Special Reference to Jaw Musculature

  • Gabriel S. FerreiraEmail author
  • Ingmar WerneburgEmail author
Chapter
Part of the Fascinating Life Sciences book series (FLS)

Abstract

Turtles are one of the most enigmatic groups of vertebrates with their highly modified “body plan” and, as such, attracted the attention of researchers for a long time. Aside from the unusual turtle shell, the skull in this group shows great changes in comparison to that of other amniote groups. Because the skull has been considered one of most important body regions when analyzing the phylogenetic relationships of amniotes, the distinct turtle skull morphology is one of the key features in defining their position among reptiles. Here, we review the current knowledge of the turtle head, summarizing the general morphology of the skull and neck as well as the different anatomical modifications characteristic of the main lineages of extant and extinct turtles. We explore the main questions that have been raised while studying those issues, for instance, the origin and diversity of the temporal emarginations (dermal bone reductions), the different neck retraction mechanisms and their influence on the shape of the skull, and the anatomy and development of the jaw adductor musculature and its relation to some characteristic features of the turtle skull, such as akinesis and the divergent trochlear mechanisms in cryptodires and pleurodires. Based on 3D reconstructions, we propose a hypothetical model for ancestral states and gross morphology of the jaw adductor musculature in Proganochelys quenstedti (the earliest turtle with a complete shell), an important step toward the understanding of the evolution of those muscles in turtles. Finally, we suggest that more integrative approaches that consider anatomical, developmental, and paleontological data and that employ modern techniques in morphological and functional anatomic analyses (such as μCT scanning and finite element analysis) have a greater potential to answer the still numerous open questions about the evolution of the turtle head.

Keywords

Testudinata Pleurodira Cryptodira Proganochelys quenstedti Diapsida Neck retraction Emargination Fenestration M. zygomaticomandibularis Trochlear mechanism 

Notes

Acknowledgments

Janine Ziermann, Raul Diaz Jr., and Rui Diogo are thanked for the invitation to write this chapter. We would like to thank Juliane Hinz (Tübingen) for help with the 3D models and Wolfgang Maier for access to the histological sections. We also thank two anonymous reviewers for their suggestions. GSF was supported by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) grants 2016/03934-2 and 2014/2539-5. IW was supported by SNF advanced postdoc mobility grant P300PA_164720.

References

  1. Anderson NJ (2009) Biomechanics of feeding and neck motion in the Softshell turtle, Apalone spinifera, Rafinesque [doctor of arts thesis in the Department of Biology, Idaho state university]. ProQuest, Ann ArborGoogle Scholar
  2. Anquetin J, Tong H, Claude J (2017) A Jurassic stem pleurodire sheds light on the functional origin of neck retraction in turtles. Sci Rep 7:42376.  https://doi.org/10.1038/srep42376 http://www.nature.com/articles/srep42376#supplementary-information CrossRefPubMedPubMedCentralGoogle Scholar
  3. Araújo R, Polcyn MJ (2013) A biomechanical analysis of the skull and adductor chamber muscles in the Late Cretaceous plesiosaur Libonectes. Palaeontologica Electronica 16(2:10A):25Google Scholar
  4. Baur G (1889) On the morphology of the vertebrate skull. J Morphol 3:471–474Google Scholar
  5. de Beer GR (1937) The development of the vertebrate skull. The University of Chicago Press, ChicagoGoogle Scholar
  6. Bels VL, Davenport J, Delheusy V (1997) Kinematic analysis of the feeding behavior in the box turtle Terrapene carolina (L.), (Reptilia: Emydidae). J Exp Zool 277:198–212CrossRefGoogle Scholar
  7. Bels V, Baussart S, Davenport J, Shorten M, O’Riordan RM, Renous S, Davenport JL (2008) Functional evolution of feeding behavior in turtles. In: Wyneken J, Godfrey MH, Bels V (eds) Biology of turtles. CRC Press, Boca Raton, pp 187–212Google Scholar
  8. Bever GS, Lyson TR, Field DJ, Bhullar B-AS (2015) Evolutionary origin of the turtle skull. Nature 525:239–242PubMedCrossRefGoogle Scholar
  9. Bever GS, Lyson TR, Field DJ, Bhullar B-AS (2016) The amniote temporal roof and the diapsid origin of the turtle skull. Zoology 119:471–473.  https://doi.org/10.1016/j.zool.2016.04.005 CrossRefPubMedGoogle Scholar
  10. Bojanus LH (1819) Anatome testudinis europaeae. Isis 11:1766–1769 1762 platesGoogle Scholar
  11. Boulenger GA (1918) Sur la place des cheloniens dans la classification, vol 167. Comptes Tendues A l’Academie Des Sciences, Paris, pp 614–618Google Scholar
  12. deBraga M, Rieppel O (1997) Reptile phylogeny and the interrelationships of turtles. Zool J Linnean Soc 120:281–354CrossRefGoogle Scholar
  13. Bramble DM (1974) Occurrence and significance of the os transiliens in gopher tortoises. Copeia:102–109Google Scholar
  14. Broom R (1924) On the classification of the reptiles. Bull Am Mus Nat Hist 51:39–65Google Scholar
  15. Burke AC (1989) Development of the turtle carapace: implications for the evolution of a novel Bauplan. J Morphol 199:363–378PubMedCrossRefGoogle Scholar
  16. Cebra-Thomas J, Tan F, Sistla S, Estes E, Bender G, Kim C, Riccio P, Gilbert SF (2005) How the turtle forms its shell: a paracrine hypothesis of carapace formation. J Exp Zool B Mol Dev Evol 304B:558–569CrossRefGoogle Scholar
  17. Clark K, Bender G, Murray BP, Panfilio K, Cook S, Davis R, Murnen K, Tuan RS, Gilbert SF (2001) Evidence for the neural crest origin of turtle plastron bones. Genesis 31:111–117PubMedCrossRefGoogle Scholar
  18. Claude J, Pritchard P, Tong H, Paradis E, Auffray JC (2004) Ecological correlates and evolutionary divergence in the skull of turtles: a geometric morphometric assessment. Syst Biol 53:933–948PubMedCrossRefGoogle Scholar
  19. Cope E (1896) The ancestry of the Testudinata. Am Nat 30:398–400Google Scholar
  20. Cordero GA, Quinteros K (2015) Skeletal remodelling suggests the turtle’s shell is not an evolutionary straitjacket. Biol Lett 11:20150022.  https://doi.org/10.1098/rsbl.2015.0022 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Crawford NG, Parham JF, Sellas AB, Faircloth BC, Glenn TC, Papenfuss TJ, Henderson JB, Hanson MH, Simison WB (2015) A phylogenomic analysis of turtles. Mol Phylogenet Evol 83:250–257PubMedCrossRefGoogle Scholar
  22. Dalrymple GH (1975) Variation in the cranial feeding mechanism of turtles of the genus Trionyx Geoffroy. PhD thesis, University of Toronto, TorontoGoogle Scholar
  23. Dalrymple GH (1977) Intraspecific variation in the cranial feeding mechanism of turtles of the genus Trionyx (Reptilia, Testudines, Trionychidae). J Herpetol 11:255–285CrossRefGoogle Scholar
  24. Daza JD, Diogo R, Johnston P, Abdala V (2011) Jaw adductor muscles across lepidosaurs: a reappraisal. Anat Rec 294:1765–1782.  https://doi.org/10.1002/ar.21467 CrossRefGoogle Scholar
  25. Diogo R, Abdala V (2010) Muscles of vertebrates. CRC Press/Science Publishers, Boca Bacon, New York; Oxon/EnfieldGoogle Scholar
  26. Diogo R, Abdala V, Lonergan N, Wood BA (2008) From fish to modern humans–comparative anatomy, homologies and evolution of the head and neck musculature. J Anat 213:391–424PubMedPubMedCentralCrossRefGoogle Scholar
  27. Edgeworth FH (1935) The cranial muscles of vertebrates. Cambridge University Press, LondonGoogle Scholar
  28. Eger SC (2006) Morphologische und phylogenetische Untersuchungen an der Nickhautmuskulatur bei Sauropsiden (unter besonderer Berücksichtigung der Chelonia). Universität Tübingen, TübingenGoogle Scholar
  29. Ernst CH, Barbour RW (1992) Turtles of the world. Smithsonian Institution Scholarly Press, Washington, DCGoogle Scholar
  30. Eßwein SE (1992) Zur phylogenetischen und ontogenetischen Entwicklung des akinetischen Craniums der Schildkröten. Natürliche Konstruktionen-Mitteilungen des SFB 230 7 (Proceedings of the II. International Symposium of the Sonderforschungsbereich 230, Stuttgart, 1.-4.10.1991):51–55Google Scholar
  31. Ferreira GS (2016) Abordagens convergentes, novidades evolutivas e a origem da carapaça das tartarugas. Revista da Biologia 16:6CrossRefGoogle Scholar
  32. Ferreira GS, Lautenschlager S, Langer MC, Evers SW, Rabi M, Werneburg I (2018) Biomechanical analyses suggest relation between neck-retraction and the trochlear mechanism in extant turtles. In: Turtle evolution symposium. Scidinge Hall, Tübingen, pp 38–40Google Scholar
  33. Foffa D, Cuff AR, Sassoon J, Rayfield EJ, Mavrogordato MN, Benton MJ (2014) Functional anatomy and feeding biomechanics of a giant Upper Jurassic pliosaur (Reptilia: Sauropterygia) from Weymouth Bay, Dorset, UK. J Anat 225:209–219.  https://doi.org/10.1111/joa.12200 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Frazzetta TH (1968) Adaptive problems and possibilities in the temporal fenestration of tetrapod skulls. J Morphol 125:145–157PubMedCrossRefGoogle Scholar
  35. Frolich LM (1997) The role of the skin in the origin of amniotes: permeability barrier, protective covering and mechanical support. In: Sumida SS, Martin KLM (eds) Amniote origins. Completing the transition to land. Academic Press, San DiegoGoogle Scholar
  36. Fuchs H (1915) Über den Bau und die Entwicklung des Schädels der Chelone imbricata. Ein Beitrag zur Entwicklungsgeschichte und vergleichenden Anatomie des Wirbeltierschädels. Erster Teil: Das Primordialskelett des Neurocraniums und des Kieferbogens. In: Voeltzkow A (ed) Reise in Ostafrika in den Jahren 1903–1905, Wissenschaftliche Ergebnisse, vol 5. Schweizerbart, Stuttgart, pp 1–325Google Scholar
  37. Fuchs H (1931) Von dem Ductus angularis oris der Arrauschildkröte (Podocnemis expansa). (Ein neues Organ?). Nachrichten von der Gesellschaft der Wissenschaften zu Göttingen. Mathematisch-Physikalische Klasse:131–147Google Scholar
  38. Gaffney ES (1975) A phylogeny and classification of the higher categories of turtles. Bull Am Mus Nat Hist 155:387–436Google Scholar
  39. Gaffney ES (1977) The side-necked turtle family Chelidae: a theory of relationships using shared derived characters. Am Mus Novit 2620:1–28Google Scholar
  40. Gaffney ES (1979) Comparative cranial morphology of recent and fossil turtles. Bull Am Mus Nat Hist 164:67–376Google Scholar
  41. Gaffney ES (1980) Phylogenetic relationships of the major groups of amniotes. In: Panchen AL (ed) The terrestrial environment and the origin of land vertebrates, Systematic Association, vol 15. Academic Press, LondonGoogle Scholar
  42. Gaffney ES (1985) The cervical and caudal vertebrae of the cryptodiran turtle, Meiolania platyceps, from the Pleistocene of Lord Howe Island. Australia American Museum Novitates 2805:1–29Google Scholar
  43. Gaffney ES (1990) The comparative osteology of the Triassic turtle Proganochelys. Bull Am Mus Nat Hist 194:1–263Google Scholar
  44. Gaffney ES, Jenkins FA Jr (2010) The cranial morphology of Kayentachelys, an early Jurassic cryptodire, and the early history of turtles. Acta Zool 91:335–368Google Scholar
  45. Gaffney ES, Kitching JW (1994) The most ancient African turtle. Nature 369:55–58CrossRefGoogle Scholar
  46. Gaffney ES, Kitching JW (1995) The morphology and relationships of Australochelys, and early Jurassic turtle from South Africa. Am Musem Novitates 3130:29Google Scholar
  47. Gaffney ES, Meylan PA (1988) A phylogeny of turtles. In: Benton MJ (ed) The phylogeny and classification of the Tetrapods. Volume 1: Amphibians, reptiles, birds, vol 35A. Clarendon Press, Oxford, pp 157–219Google Scholar
  48. Gaffney ES, Hutchison JH, Jenkins AF, Meeker LJ (1987) Modern turtle origins: the oldest known cryptodire. Science 237:289–291PubMedCrossRefGoogle Scholar
  49. Gaffney ES, Tong H, Meylan PA (2006) Evolution of the side-necked turtles: the families Bothremydidae, Euraxemydidae, and Araripemydidae. Bull Am Mus Nat Hist 300:700CrossRefGoogle Scholar
  50. Gardiner BG (1993) Haematothermia: warm-blooded amniotes. Cladistics 9:369–395CrossRefGoogle Scholar
  51. Gasc JP (1981) Axial musculature. In: Gans C, Parsons TS, Parsons TS (eds) Biology of the Reptilia, (Morphology F). morphology D, vol 11. Academic Press, London, pp 355–435Google Scholar
  52. Gaupp E (1895) Zur vergleichenden Anatomie der Schläfengegend am knöchernen Wirbeltierschädel. Morphologische Arbeiten 4:77–131Google Scholar
  53. Gauthier J, Kluge AG, Rowe T (1988) Amniote phylogeny and the importance of fossils. Cladistics 4:105–209CrossRefGoogle Scholar
  54. Gauthier JA, Kearney M, Anderson Maisano J, Rieppel O, Behlke ADB (2012) Assembling the Squamate Tree of Life: Perspectives from the Phenotype and the Fossil Record. Bulletin of the Peabody Museum of Natural History 53(1):3–308CrossRefGoogle Scholar
  55. George JC, Shah RV (1955) The myology of the head and the neck of the common Indian pond turtle, Lissemys punctata granosa Schoepff. J Anim Morphol Physiol 1:1–12Google Scholar
  56. Gilbert SF, Loredo GA, Brukman A, Burke AC (2001) Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution. Evol Dev 3:47–58PubMedCrossRefGoogle Scholar
  57. Gilbert SF, Bender G, Betters E, Yin M, Cebra-Thomas JA (2007) The contribution of neural crest cells to the nuchal bone and plastron of the turtle shell. Integr Comp Biol 47:401–408.  https://doi.org/10.1093/icb/icm020 CrossRefPubMedGoogle Scholar
  58. Gilbert SF, Cebra-Thomas JA, Burke AC (2008) How the turtle gets its shell. In: Wyneken J, Godfrey MH, Bels V (eds) Biology of turtles. CRC Press, Boca Raton, pp 1–16Google Scholar
  59. Goodrich ES (1916) On the classification of the Reptilia. Proc R Soc London Ser B, Containing Papers of a Biological Character 89:261–276CrossRefGoogle Scholar
  60. Goodrich ES (1930) Studies on the structure and development of vertebrates. Macmillan and Co, LondonCrossRefGoogle Scholar
  61. Gregory WK (1946) Pareiasaurs versus placodonts as near ancestors to the turtles. Bull Am Mus Nat Hist 86:277–326Google Scholar
  62. Gregory WK, Adams LA (1915) The temporal fossæ of vertebrates in relation to the jaw muscles. Science 41:763–765PubMedCrossRefGoogle Scholar
  63. Guillon JM, Guéry L, Hulin V, Girondot M (2012) A large phylogeny of turtles (Testudines) using molecular data. Contrib Zool 81:147–158Google Scholar
  64. Hacker G (1954) Über Kiefermuskulatur und Mundfascien bei Testudo graeca. PhD thesis, Ernst-Moritz-Arndt-Universität, GreifswaldGoogle Scholar
  65. Hay OP (1905) On the group of fossil turtles known as the Amphichelydia; with remarks on the origin and relationships of the suborders, superfamilies, and families of Testudines. Bull Am Mus Nat Hist 21:137–175Google Scholar
  66. Hedges SB (2012) Amniote phylogeny and the position of turtles. BMC Biol 10:64PubMedPubMedCentralCrossRefGoogle Scholar
  67. Hedges SB, Poling LL (1999) A molecular phylogeny of reptiles. Science 283:998–1001PubMedCrossRefGoogle Scholar
  68. Heiss E, Plenk H, Weisgram J (2008) Microanatomy of the palatal mucosa of the semiaquatic Malayan box turtle, Cuora amboinensis, and functional implications. Anat Rec 291:10CrossRefGoogle Scholar
  69. Herrel A, O’Reilly JC, Richmond AM (2002) Evolution of bite performance in turtles. J Evol Biol 15:1083–1094CrossRefGoogle Scholar
  70. Herrel A, Van Damme J, Aerts P (2008) Cervical anatomy and function in turtles. In: Wyneken J, Godfrey MH, Bels V (eds) Biology of turtles. CRC Press, Boca Raton, pp 163–185Google Scholar
  71. Hoffmann CK (1890) Reptilien. 1. Schildkröten, 6(3). Dr. H.G. Bronn’s Klassen und Ordnungen des Thier-Reichs, wissenschaftlich dargestellt in Wort und Bild. C.F. Winter’sche Verlagshandlung, LeipzigGoogle Scholar
  72. Hofsten N (1941) On the phylogeny of the Reptilia. Zool Bidrag Fran Uppsala 20:501–521Google Scholar
  73. Holliday CM, Witmer LM (2007) Archosaur adductor chamber evolution: integration of musculoskeletal and topological criteria in jaw muscle homology. J Morphol 268:457–484.  https://doi.org/10.1002/Jmor.10524 CrossRefPubMedGoogle Scholar
  74. Iordansky NN (1987) Morphological and functional features of mandibular apparatus in turtles (Reptilia, Chelonia) and the problem of their origin [in Russian] (English abstract), МОРФО-ФУНКЦИОНАЛЬНЫЕ ОСОБЕННОСТИ ЧЕЛЮСТНОГО АППАРАТА ЧЕРЕПАХ (REPТlLIA, CHELONIA) И ПРОБЛЕМА ИХ ПРОИСХОЖДЕНИЯ. Zoologichesky Zhurnal 66:1716–1729Google Scholar
  75. Iordansky NN (1994) Tendons of jaw muscles in Amphibia and Reptilia: homology and evolution. Russ J Herpetol 1:13–20Google Scholar
  76. Iordansky NN (1996) Jaw musculature of turtles: structure, functions, and evolutionary conservatism. Russ J Herpetol 3:49–57Google Scholar
  77. Iordansky NN (2010) Pterygoideus muscles and other jaw adductors in amphibians and reptiles Biol Bull 37:905–914. [English version of Russian original text]CrossRefGoogle Scholar
  78. Jannel A (2015) Neck mobility, grazing habits, and intraspecific combat behaviour in the Giant Pleistocene horned turtle Meiolania platyceps. Uppsala UniversitetGoogle Scholar
  79. Jones MEH, Curtis N, O’Higgins P, Fagan M, Evans SE (2009) The head and neck muscles accociated with feeding on Sphenodon (Reptilia: Lepidosauria: Rynchocephalia). Palaeontologia Electronica 12(7A):56 http://palaeo-electronica.org/2009_2002/2179/index.html Google Scholar
  80. Jones MEH, Werneburg I, Curtis N, Penrose R, O’Higgins P, Fagan MJ, Evans SE (2012) The head and neck anatomy of sea turtles (Cryptodira: Chelonioidea) and skull shape in Testudines. PLoS One 7:e47852.  https://doi.org/10.1371/journal.pone.0047852 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Joyce WG (2007) Phylogenetic relationships of Mesozoic turtles. Bull Peabody Mus Nat Hist 48:3–102CrossRefGoogle Scholar
  82. Joyce WG (2015) The origin of turtles: a paleontological perspective. J Exp Zool B Mol Dev Evol 324:181–193PubMedCrossRefGoogle Scholar
  83. Joyce WG, Lyson TR (2015) A review of the fossil record of turtles of the clade Baenidae. Bull Peabody Mus Nat Hist 56:147–183.  https://doi.org/10.3374/014.056.0203 CrossRefGoogle Scholar
  84. Joyce WG, Sterli J (2012) Congruence, non-homology, and the phylogeny of basal turtles. Acta Zool 93:149–159.  https://doi.org/10.1111/j.1463-6395.2010.00491.x CrossRefGoogle Scholar
  85. Joyce WG, Parham JF, Gauthier JA (2004) Developing a protocol for the conversion of rank-based taxon names to phylogenetically defined clade names, as exemplified by turtles. J Paleontol 78:989–1013CrossRefGoogle Scholar
  86. Joyce WG, Werneburg I, Lyson TR (2013a) The hooked element in the pes of turtles (Testudines): a global approach to exploring homology. J Anat 223:421–441PubMedPubMedCentralGoogle Scholar
  87. Joyce WG, Parham JF, Lyson TR, Warnock RCM, Donoghue PCJ (2013b) A divergence dating analysis of turtles using fossil calibrations: an example of best practice. J Paleontol 87:612–634CrossRefGoogle Scholar
  88. Joyce WG, Rabi M, Clark JM, Xu X (2016) A toothed turtle from the late Jurassic of China and the global biogeographic history of turtles. BMC Evol Biol 16:236.  https://doi.org/10.1186/s12862-016-0762-5 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Karl HV (1997) Zur Taxonomie und Morphologie einiger tertiärer Weichschildkröten unter besonderer Berücksichtigung von Trionychinae Zentraleuropas (Testudines: Trionychidae). PhD thesis, Universität Salzburg, SalzburgGoogle Scholar
  90. Kilias R (1957) Die funktionell-anatomische und systematische Bedeutung der Schläfenreduktion bei Schildkröten. Mitteilungen aus dem Zoologischen Museum in Berlin 33:307–354CrossRefGoogle Scholar
  91. Kuratani S, Kuraku S, Nagashima H (2011) Evolutionary developmental perspective for the origin of turtles: the folding theory for the shell based on the developmental nature of the carapacial ridge. Evol Dev 13:1–14PubMedCrossRefGoogle Scholar
  92. Lakjer T (1926) Studien über die Trigeminus-versorgte Kaumuskulatur der Sauropsiden. C.A. Reitsel Buchhandlung, CopenhagenGoogle Scholar
  93. Lambertz M, Böhme W, Perry SF (2010) The anatomy of the respiratory system in Platysternon megacephalum Gray, 1831 (Testudines: Cryptodira) and related species, and its phylogenetic implications. Comp Biochem Physiol A Mol Integr Physiol 156:7.  https://doi.org/10.1016/j.cbpa.2009.12.016 CrossRefGoogle Scholar
  94. Laurin M (2002) Tetrapod phylogeny, amphibian origins, and the definition of the name Tetrapoda. Syst Biol 51:6CrossRefGoogle Scholar
  95. Laurin M, Piñeiro GH (2017) A reassessment of the taxonomic position of mesosaurs, and a surprising phylogeny of early amniotes. Front Earth Sci 5:88CrossRefGoogle Scholar
  96. Laurin M, Reisz RR (1995) A reevaluation of early amniote phylogeny. Zool J Linnean Soc 113:165–223CrossRefGoogle Scholar
  97. Lautenschlager S, Witzmann F, Werneburg I (2016) Palate anatomy and morphofunctional aspects of interpterygoid vacuities in temnospondyl cranial evolution. Sci Nat 103:79.  https://doi.org/10.1007/s00114-016-1402-z CrossRefGoogle Scholar
  98. Lee MSY (1993) The origin of the turtle body plan: bridging a famous morphological gap. Science 261:1716–1720PubMedCrossRefGoogle Scholar
  99. Lee MSY (1995) Historical burden in systematics and the interrelationships of ‘parareptiles’. Biol Rev 70:459–547CrossRefGoogle Scholar
  100. Lee MSY (1997) Pareiasaur phylogeny and the origin of turtles. Zool J Linnean Soc 120:197–280CrossRefGoogle Scholar
  101. Lee MSY (2013) Turtle origins: insights from phylogenetic retrofitting and molecular scaffolds. J Evol Biol 26:2729–2738PubMedCrossRefGoogle Scholar
  102. Lemell C, Weisgram J (1997) Feeding patterns of Pelusios castaneus (Chelonia: Pleurodira). Neth J Zool 47:429–441CrossRefGoogle Scholar
  103. Lemell P, Lemell C, Snelderwaard P, Gumpenberger M, Wochesländer R, Weisgram J (2002) Feeding patterns of Chelus fimbriatus (Pleurodira: Chelidae). J Exp Biol 205:1495–1506PubMedGoogle Scholar
  104. Lemell P, Beisser CJ, Gumpenberger M, Snelderwaard P, Gemel R, Weisgram J (2010) The feeding apparatus of Chelus fimbriatus (Pleurodira; Chelidae)–adaptation perfected? Amphibia-Reptilia 31:97–107CrossRefGoogle Scholar
  105. Li C, Wu XC, Rieppel O, Wang LT, Zhao LJ (2008) An ancestral turtle from the Late Triassic of southwestern China. Nature 456:497–501PubMedCrossRefGoogle Scholar
  106. Li C, Fraser NC, Rieppel O, Wu X-C (2018) A Triassic stem turtle with an edentulous beak. Nature 560:476–479  https://doi.org/10.1038/s41586-018-0419-1 PubMedCrossRefGoogle Scholar
  107. Loredo GA, Brukman A, Harris MP, Kagle D, Leclair EE, Gutman R, Denney E, Henkelman E, Murray BP, Fallon JF, Tuan RS, Gilbert SF (2001) Development of an evolutionarily novel structure: fibroblast growth factor expression in the carapacial ridge of turtle embryos. J Exp Zool Mol Dev Evol 291:274–281CrossRefGoogle Scholar
  108. Løvtrup S (1977) The phylogeny of Vertebrata. John Wiley, LondonGoogle Scholar
  109. Løvtrup S (1985) On the classification of the taxon Tetrapoda. Syst Zool 34:463–470CrossRefGoogle Scholar
  110. Luther A (1914) Über die vom N. trigeminus versorgte Muskulatur der Amphibien mit einem vergleichenden Ausblick über den Adductor mandibulae der Gnathostomen, und einem Beitrag zum Verständnis der Organisation der Anurenlarven. Acta Societatis Scientiarum Fenniciae 44:1–151Google Scholar
  111. Lyson TR, Joyce WG (2012) Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage. Biol Lett 8:1028–1031PubMedPubMedCentralCrossRefGoogle Scholar
  112. Lyson T, Bever GS, Bhullar BAS, Joyce WG, Gauthier JA (2010) Transitional fossils and the origin of turtles. Biol Lett 6:830–833.  https://doi.org/10.1098/rsbl.2010.0371 CrossRefPubMedPubMedCentralGoogle Scholar
  113. Lyson TR, Bever GS, Scheyer TM, Hsiang AY, Gauthier JA (2013) Evolutionary origin of the turtle shell. Curr Biol 23:1–7CrossRefGoogle Scholar
  114. Lyson TR, Schachner ER, Botha-Brink J, Scheyer TM, Lambertz M, Bever GS, Rubidge BS, Queiroz K (2014) Origin of the unique ventilatory apparatus of turtles. Nat Commun 5:1–11CrossRefGoogle Scholar
  115. Lyson TR, Rubidge Bruce S, Scheyer TM, de Queiroz K, Schachner Emma R, Smith Roger MH, Botha-Brink J, Bever GS (2016) Fossorial origin of the turtle shell. Curr Biol 26:1887–1894.  https://doi.org/10.1016/j.cub.2016.05.020 CrossRefPubMedGoogle Scholar
  116. MacDougall MJ, Modesto SP, Brocklehurst N, Verrière A, Reisz RR, Fröbisch J (2018) Response: a reassessment of the taxonomic position of mesosaurs, and a surprising phylogeny of early amniotes. Front Earth Sci 6:99CrossRefGoogle Scholar
  117. Maier W, Werneburg I (2014) Schlüsselereignisse der organismischen Makroevolution. Scidinge Hall, TübingenGoogle Scholar
  118. Mannen H, Li SSL (1999) Molecular evidence for a clade of turtles. Mol Phylogenet Evol 13:144–148PubMedCrossRefGoogle Scholar
  119. Matsumoto R, Evans SE (2017) The palatal dentition of tetrapods and its functional significance. J Anat 230:47–65.  https://doi.org/10.1111/joa.12534 CrossRefPubMedGoogle Scholar
  120. Mulcahy DG, Noonan BP, Moss T, Townsend TM, Reeder TW, Sites JW Jr, Wiens JJ (2012) Estimating divergence dates and evaluating dating methods using phylogenomic and mitochondrial data in squamate reptiles. Mol Phylogenet Evol 65:974–991.  https://doi.org/10.1016/j.ympev.2012.08.018 CrossRefPubMedGoogle Scholar
  121. Mulisch M, Welsch U (2015) Romeis-Mikroskopische Technik. Springer, BerlinCrossRefGoogle Scholar
  122. Müller J (2003) Early loss and multiple return of the lower temporal arcade in diapsid reptiles. Naturwissenschaften 90:473–476PubMedCrossRefGoogle Scholar
  123. Müller J, Sterli J, Anquentin J (2011) Carotid circulation in amniotes and its implications for turtle relationships. Neues Jahrbuch der Gelogie und Paläontologie, Abhandlungen 261:289–297CrossRefGoogle Scholar
  124. Nagashima H, Kuraku S, Uchida K, Ohya YK, Narita Y, Kuratani S (2007) On the carapacial ridge in turtle embryos: its developmental origin, function and the chelonian body plan. Development 134:2219–2226PubMedCrossRefGoogle Scholar
  125. Nagashima H, Sugahara F, Takeshi M, Ericsson R, Kawashima-Ohya Y, Narita Y, Kuratani S (2009) Evolution of the turtle body plan by the folding and creation of new muscle connections. Science 325:193–196PubMedCrossRefGoogle Scholar
  126. Nagashima H, Kuraku S, Uchida K, Kawashima-Ohya Y, Narita Y, Kuratani S (2012) Body plan of turtles: an anatomical, developmental and evolutionary perspective. Anat Sci Int 87:1–13PubMedCrossRefGoogle Scholar
  127. Nagashima H, Kuraku S, Uchida K, Kawashima-Ohya Y, Narita Y, Kuratani S (2013) Origin of the turtle body plan: the folding theory to illustrate turtle-specific developmental repatterning. In: Morphology and evolution of turtles. Springer, Dordrecht, pp 37–50CrossRefGoogle Scholar
  128. Nagashima H, Sugahara F, Takechi M, Sato N, Kuratani S (2015) On the homology of the shoulder girdle in turtles. J Exp Zool B Mol Dev Evol 324(3):244–254PubMedCrossRefGoogle Scholar
  129. Natchev N, Heiss E, Lemell P, Stratev D, Weisgram J (2009) Analysis of prey capture and food transport kinematics in two Asian box turtles, Cuora amboinensis and Cuora flavomarginata (Chelonia, Geoemydidae), with emphasis on terrestrial feeding patterns. Zoology 112:113–127PubMedCrossRefGoogle Scholar
  130. Natchev N, Lemell P, Heiss E, Beisser C, Weisgram J (2010) Aquatic feeding in a terrestrial turtle: a functional-morphological study of the feeding apparatus in the Indochinese box turtle Cuora galbinifrons (Testudines, Geoemydidae). Zoomorphology 129:111–119CrossRefGoogle Scholar
  131. Natchev N, Tzankov N, Werneburg I, Heiss E (2015) Feeding behaviour in a ‘basal’ tortoise provides insights on the transitional feeding mode at the dawn of modern land turtle evolution. PeerJ 3:e1172.  https://doi.org/10.7717/peerj.1172 CrossRefPubMedPubMedCentralGoogle Scholar
  132. Neenan JM, Klein N, Scheyer TM (2013) European origin of placodont marine reptiles and the evolution of crushing dentition in Placodontia. Nat Commun 4:1621.  https://doi.org/10.1038/ncomms2633 CrossRefPubMedGoogle Scholar
  133. Nick L (1912) Das Kopfskelett von Dermochelys coriacea L. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere 33:1–238Google Scholar
  134. Ogushi K (1911) Anatomische Studien an der japanischen dreikralligen Lippenschildkröte (Trionyx japanicus). I. Mitteilung. Morphologisches Jahrbuch 43:1–106Google Scholar
  135. Ogushi K (1913a) Anatomische Studien an der japanischen dreikralligen Lippenschildkröte (Trionyx japanicus). II. Mitteilung: Muskel- und peripheres Nervensystem. Morphologisches Jahrbuch 46:299–562Google Scholar
  136. Ogushi K (1913b) Zur Anatomie der Hirnnerven und des Kopfsympathicus von Trionyx japonicus nebst einigen kritischen Bemerkungen. Morphologisches Jahrbuch 45:441–480Google Scholar
  137. Ogushi K (1914) Der Kehlkopf von Trionyx japonicus. Anat Anz 45:481–503Google Scholar
  138. Olson EC (1947) The family Diadectidae and its nearing on the classification of turtles. Fieldiana Geology 11:1–53Google Scholar
  139. Osborn HF (1903) On the primary division of the Reptilia into two sub-classes, Synapsida and Diapsida. Science 17:275–276PubMedCrossRefGoogle Scholar
  140. Poglayen-Neuwall I (1953) Untersuchungen der Kiefermuskulatur und deren Innervation bei Schildkröten. Acta Zool 34:241–292CrossRefGoogle Scholar
  141. Poglayen-Neuwall I (1954) Die Kiefermuskulatur der Eidechsen und ihre Innervation. Z Wiss Zool 158:79–132Google Scholar
  142. Poglayen-Neuwall I (1966) Bemerkungen zur Morphologie und Innervation der Trigeminusmuskulatur von Chelus fimbriatus (Schneider). Zoologische Beiträge 12:43–65Google Scholar
  143. Pritchard PCH (1984) Piscivory in turtles, and evolution of long-necked Chelidae. In: Ferguson MWJ (ed) The structure, development and evolution of Reptiles. A Festschrift in honour of Professor A.d’A. Bellairs on the occasion of his retirement, Symposia of the Zoological Society of London, vol 52. Academic Press, LondonGoogle Scholar
  144. Rabi M, Zhou C-F, Wings O, Ge S, Joyce WG (2013) A new xinjiangchelyid turtle from the middle Jurassic of Xinjiang, China and the evolution of the basipterygoid process in Mesozoic turtles. BMC Evol Biol 13:1–28CrossRefGoogle Scholar
  145. Rabi M, Sukanov VB, Egorova VN, Danilov I, Joyce WG (2014) Osteology, relationships, and ecology of Annemys (Testudines, Eucryptodira) from the Late Jurassic of Shar Teg, Mongolia and phylogenetic definitions for Xinjiangchelyidae, Sinemydidae, and Macrobaenidae. J Vertebr Paleontol 34:327–352CrossRefGoogle Scholar
  146. Ray CE (1959) A sesamoid bone in the jaw musculature of Gopherus polyphemus (Reptilia: Testudininae). Anat Anz 107:85–91PubMedGoogle Scholar
  147. Reisz RR, Head JJ (2008) Turtle origins out to sea. Nature 456:450–451PubMedCrossRefGoogle Scholar
  148. Rhodin AGJ, Iverson JB, Bour R, Fritz U, Georges A, Shaffer HB, van Dijk PPJ (2017) Turtles of the world: annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status. In: AGJ R, Iverson JB, van Dijk PP, Saumure RA, Buhlmann KA, Pritchard PCH, Mittermeier RA (eds) Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group, vol 7, 8th edn. Chelonian Research Monographs, Lunenburg, pp 1–292Google Scholar
  149. Rice R, Kallonen A, Cebra-Thomas J, Gilbert SF (2016) Development of the turtle plastron, the order-defining skeletal structure. Proc Natl Acad Sci U S A 113:6.  https://doi.org/10.1073/pnas.1600958113 CrossRefGoogle Scholar
  150. Rieppel O (1980) The trigeminal jaw adductor musculature of Tupinambis, with comments on the phylogenetic relationship of the Teiidae (Reptilia, Lacertilia). Zool J Linnean Soc 69:1–29CrossRefGoogle Scholar
  151. Rieppel O (1984) The structure of the skull and jaw adductor musculature in the Gekkota, with comments on the phylogenetic-relationships of the Xantusiidae (Reptilia, Lacertilia). Zool J Linnean Soc 82:291–318CrossRefGoogle Scholar
  152. Rieppel O (1987) The development of the trigeminal jaw adductor musculature and associated skull elements in the lizard Podarcis sicula. J Zool 212:131–150CrossRefGoogle Scholar
  153. Rieppel O (1990) The structure and development of the jaw adductor musculature in the turtle Chelydra serpentina. Zool J Linnean Soc 98:27–62CrossRefGoogle Scholar
  154. Rieppel O (1993) Patterns of diversity in the reptilian skull. In: Hanken J, Hall BK (eds) The skull, patterns of structural and systematic diversity, vol 2. University of Chicago Press, Chicago, pp 344–389Google Scholar
  155. Rieppel O (2000) Turtles as diapsid reptiles. Zool Scr 29:199–212CrossRefGoogle Scholar
  156. Rieppel O (2004) Kontroversen innerhalb der Tetrapoda—die Stellung der Schildkröten (Testudines). Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin 43:201–221Google Scholar
  157. Rieppel O (2008) The relationships of turtles within amniotes. In: Wyneken J, Godfrey MH, Bels V (eds) Biology of turtles. CRC Press, Boca Raton, pp 345–353Google Scholar
  158. Rieppel O (2013) The evolution of the turtle shell. In: Gardner J, Brinkman D, Holroyd P (eds) Vertebrate paleobiology and paleoanthropology series, Morphology and evolution of turtles. Springer, Dordrecht, pp 51–61Google Scholar
  159. Rieppel O, Reisz RR (1999) The origin and early evolution of turtles. Annu Rev Ecol Syst 30:1–22CrossRefGoogle Scholar
  160. Robert McNeel & Associates (2003) Rhinoceros 3D. Version 3.0 SR3, November. BarcelonaGoogle Scholar
  161. Romer AS (1956) Osteology of the reptiles. The University of Chicago Press, ChicagoGoogle Scholar
  162. Rougier GW, De La Fuente MS, Arcucci AB (1995) Late Triassic turtles from South America. Science 268:855–858PubMedCrossRefGoogle Scholar
  163. Scheyer TM, Sander PM (2007) Shell bone histology indicates terrestrial palaeoecology of basal turtles. Proc R Soc B Biol Sci 274:1885–1893.  https://doi.org/10.1098/rspb.2007.0499 CrossRefGoogle Scholar
  164. Scheyer TM, Werneburg I, Mitgutsch C, Delfino M, Sánchez-Villagra MR (2013) Three ways to tackle the turtle: integrating fossils, comparative embryology and microanatomy. In: Gardner J, Brinkman D, Holroyd P (eds) Vertebrate paleobiology and paleoanthropology series. Springer, Dordrecht, pp 63–70Google Scholar
  165. Schoch RR, Sues HD (2015) A middle Triassic stem-turtle and the evolution of the turtle body plan. Nature 523:584–587.  https://doi.org/10.1038/nature14472 CrossRefPubMedGoogle Scholar
  166. Schoch RR, Sues HD (2016) The diapsid origin of turtles. Zoology 119:3.  https://doi.org/10.1016/j.zool.2016.01.004 CrossRefGoogle Scholar
  167. Schulman H (1906) Vergleichende Untersuchungen über die Trigeminus-Muskulatur der Monotremen, sowie die dabei in Betracht kommenden Nerven und Knochen. In: Jenaische Denkschriften, Zoologische Forschungsreisen in Australien und dem Malayischen Archipel. Mit Unterstützung des Herrn Dr. Paul von Ritter ausgeführt in den Jahren 1891–1893 (III. 2. Teil), vol 2, vol 6. G. Fischer, Jena, pp 297–400Google Scholar
  168. Schumacher GH (1954/55) Beiträge zur Kiefermuskulatur der Schildkröten: II. Mitteilung. Bau des M. adductor mandibularis unter spezieller Berücksichtigung der Fascien des Kopfes bei Platysternon megacephalum, Emys orbicularis, Testudo graeca, Pelomedusa subrufa, Clemmys caspica riculata, Graptemys geographica, Hardella thurrjii, Macrochelys temminckii, Emydura krefftii, Hydromedusa tectifera, Chelodina longicollis, Trionyx punctatus, Amyda sinensis und Dogania subplana. Wissenschaftliche Zeitschrift der Ernst Moritz Arndt-Universität Greifswald—Mathematisch-naturwissenschaftliche Reihe 4:501–518Google Scholar
  169. Schumacher GH (1954a) Beiträge zur Kiefermuskulatur der Schildkröten. I. Mitteilung. Bau des M. adductor mandibularis unter spezieller Berücksichtigung des M. pterygoideus bei Chelone, Podocnemis, Sternothaerus und Testudo elephantopus. PhD thesis, Ernst-Moritz-Arndt-Universität, GreifswaldGoogle Scholar
  170. Schumacher GH (1954b) Beiträge zur Kiefermuskulatur der Schildkröten: III. Mitteilung. Bau des M. Adductor mandibularis bei Macrochelys temminckii, Platysternon megacephalum, Clemmys caspica rivulata, Emys orbicularis, Graptemys geographica, Hardella thurjii, Testudo graeca, Amyda sinensis, Dogania subplana, Trionyx punctatus, Pelomedusa subrufa, Chelodina longicollis, Hydromedusa tectifera und Emydura krefftii. Wissenschaftliche Zeitschrift der Ernst Moritz Arndt-Universität Greifswald—Mathematisch-naturwissenschaftliche Reihe 4:559–588Google Scholar
  171. Schumacher GH (1956) Morphologische Studie zum Gleitmechanismus des M. adductor mandibulae externus bei Schildkröten. Anat Anz 103:1–12PubMedGoogle Scholar
  172. Schumacher GH (1972) Die Kopf- und Halsregion der Lederschildkröte Dermochelys coriacea (LINNAEUS 1766)—Anatomische Untersuchungen im Vergleich zu anderen rezenten Schildkröten—Mit 7 Figuren im Text und 31 Tafeln, Abhandlungen der Akademie der Wissenschaften der DDR, vol 2. Akademie, BerlinGoogle Scholar
  173. Schumacher GH (1973) The head muscles and hyolaryngeal skeleton of turtles and crocodilians. In: Gans C, Parsons TS (eds) Biology of the Reptilia, morphology D, vol 4. Academic Press, London, pp 101–199Google Scholar
  174. Seeley HG (1892) On a new reptile from Welte Vreden (Beaufort West) Eunotosaurus africanus (Seeley). Quat J Geol Soc 48:3Google Scholar
  175. Shaffer HB (2009) Turtles (Testudines). In: Hedges SB, Kumar S (eds) The TimeTree of life. Oxford University Press, New York, pp 398–401Google Scholar
  176. Stayton CT (2011) Terrestrial feeding in aquatic turtles: environment-dependent feeding behavior modulation and the evolution of terrestrial feeding in Emydidae. J Exp Biol 214:4083–4091PubMedCrossRefGoogle Scholar
  177. Sterli J (2010) Phylogenetic relationships among extinct and extant turtles: the position of Pleurodira and the effects of the fossils on rooting crown-group turtles. Contrib Zool 79:93–106Google Scholar
  178. Sterli J, de la Fuente M (2010) Anatomy of Condorchelys antiqua STERLI, 2008, and the origin of the modern jaw closure mechanism in turtles. J Vertebr Paleontol 30:351–366CrossRefGoogle Scholar
  179. Sterli J, Joyce WG (2007) The cranial anatomy of the early Jurassic turtle Kayentachelys aprix. Acta Palaeontol Pol 52:675–694Google Scholar
  180. Sterli J, Müller J, Anquetin J, Hilger A (2010) The parapasisphenoid complex in Mesozoic turtles and the evolution of the testudinate basicranium. Can J Earth Sci 47:1337–1346CrossRefGoogle Scholar
  181. Summers AP, Darouian KF, Richmond AM, Brainerd EL (1998) Kinematics of aquatic and terrestrial prey capture in Terrapene carolina, with implications for the evolution of feeding in cryptodire turtles. J Exp Zool 281:280–287PubMedCrossRefGoogle Scholar
  182. Tarsitano SF, Oelofsen B, Frey E, Riess J (2001) The origin of temporal fenestra. S Afr J Sci 97:334–336Google Scholar
  183. Thomson JT (1932) The anatomy of the tortoise. Sci Proc R Dublin Soc New Series 20:359–461 324 platesGoogle Scholar
  184. Tokita M (2004) Morphogenesis of parrot jaw muscles: understanding the development of an evolutionary novelty. J Morphol 259:69–81.  https://doi.org/10.1002/Jmor.10172 CrossRefPubMedGoogle Scholar
  185. Tsai HP, Holliday CM (2011) Ontogeny of the Alligator cartilago transiliens and its significance for sauropsid jaw muscle evolution. PLoS One 6:e24935PubMedPubMedCentralCrossRefGoogle Scholar
  186. Tsuji LA, Müller J (2009) Assembling the history of the Parareptilia: phylogeny, diversification, and a new definition of the clade. Fossil Record 12:71–81CrossRefGoogle Scholar
  187. Tvarožková B (2006) Development of the temporal emargination in turtles and the temporal fenestration in crocodilians: the origin of an anapsid-like chelonian skull. Masters thesis, Charles University in Prague, PragueGoogle Scholar
  188. Underwood G (1970) The eye. In: Gans C, Parsons TS (eds) Biology of the Reptilia, morphology D, vol 2. Academic Press, London, pp 1–97Google Scholar
  189. Versluys J (1919) Über die Phylogenie der Schläfengruben und Jochbogen bei den Reptilia. Sitzungsberichte der Heidelberger Akademie der Wissenschaften, Mathematisch-naturwissenschaftliche Klasse, Abteilung B, Biologische Wissenschaften 13:1–29Google Scholar
  190. Vitek NS, Joyce W (2015) A review of the fossil record of new world turtles of the clade pan-Trionychidae. Bull Peabody Mus Nat Hist 56:185–244CrossRefGoogle Scholar
  191. Walker WF Jr (1973) The locomotor apparatus of Testudinines. In: Gans C, Parsons TS (eds) Biology of the Reptilia, morphology D, vol 4. Academic Press, London, pp 1–100Google Scholar
  192. Wang Z, Pascual-Anaya J, Zadissa A, Li W, Niimura Y, Huang Z, Li C, White S, Xiong Z, Fang D, Wang B, Ming Y, Chen Y, Zheng Y, Kuraku S, Pignatelli M, Herrero J, Beal K, Nozawa M, Li Q, Wang J, Zhang H, Yu L, Shigenobu S, Wang J, Liu J, Flicek P, Searle S, Wang J, Kuratani S, Yin Y, Aken B, Zhang G, Irie N (2013) The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nat Genet 45:701–706.  https://doi.org/10.1038/ng.2615 CrossRefPubMedPubMedCentralGoogle Scholar
  193. Watson DMS (1914) Eunotosaurus africanus Seeley, and the ancestry of the Chelonia. Proc Zool Soc London 11:1011–1020Google Scholar
  194. Weisgram J (1985) Feeding mechanisms of Claudius angustatus COPE 1865. In: Dunker HR, Fleischer G (eds) Fortschritte der Zoologie: Functional morphology in vertebrates, vol 30. Gustav Fischer, Stuttgart, pp 256–260Google Scholar
  195. Werneburg I (2011) The cranial musculature in turtles. Palaeontol Electron 14:15a 99 pagesGoogle Scholar
  196. Werneburg I (2012) Temporal bone arrangements in turtles: an overview. J Exp Zool B Mol Dev Evol 318:235–249PubMedCrossRefGoogle Scholar
  197. Werneburg I (2013a) Jaw musculature during the dawn of turtle evolution. Org Divers Evol 13:225–254CrossRefGoogle Scholar
  198. Werneburg I (2013b) The tendinous framework in the temporal skull region of turtles and considerations about its morphological implications in amniotes: a review. Zool Sci 31:141–153CrossRefGoogle Scholar
  199. Werneburg I (2015) Neck motion in turtles and its relation to the shape of the temporal skull region. Comptes Rendus Palevol 14:527–548CrossRefGoogle Scholar
  200. Werneburg I, Maier W (2018) Considerations on the development of the akinetic skull in pleurodire and cryptodire turtles. In: Turtle Evolution Symposium. Scidinge Hall, Tübingen, pp 90–91Google Scholar
  201. Werneburg I, Sánchez-Villagra MR (2009) Timing of organogenesis support basal position of turtles in the amniote tree of life. BMC Evol Biol 9:1–9.  https://doi.org/10.1186/1471-2148-9-82 CrossRefGoogle Scholar
  202. Werneburg I, Maier W, Joyce WG (2013) Embryonic remnants of intercentra and cervical ribs in turtles. Biol Open 2:1103–1107PubMedPubMedCentralCrossRefGoogle Scholar
  203. Werneburg I, Hinz JK, Gumpenberger M, Volpato V, Natchev N, Joyce WG (2015a) Modeling neck mobility in fossil turtles. J Exp Zool B Mol Dev Evol 324:230–243PubMedCrossRefGoogle Scholar
  204. Werneburg I, Wilson LAB, Parr WCH, Joyce WG (2015b) Evolution of neck vertebral shape and neck retraction at the transition to modern turtles: an integrated geometric morphometric approach. Syst Biol 64:187–204PubMedCrossRefGoogle Scholar
  205. Williams EE (1950) Variation and selection in the cervical central articulations of living turtles. Bull Am Mus Nat Hist 94:509–561Google Scholar
  206. Williston SW (1917) The phylogeny and classification of reptiles. J Geol 25:411–421CrossRefGoogle Scholar
  207. Witzmann F, Werneburg I (2017) The palatal interpterygoid vacuities of temnospondyls and the implications for the associated eye- and jaw musculature. Anat Rec 300:1240–1269.  https://doi.org/10.1002/ar.23582 CrossRefGoogle Scholar
  208. Wochesländer R, Hilgers H, Weisgram J (1999) Feeding mechanism of Testudo hermanni boettgeri (Chelonia, Cryptodira). Neth J Zool 49:1–13CrossRefGoogle Scholar
  209. Yntema CL (1968) A series of stages in the embryonic development of Chelydra serpentina. J Morphol 125:219–251PubMedCrossRefGoogle Scholar
  210. Zangerl R (1948) The methods of comparative anatomy and its contribution to the study of evolution. Evolution 2:351–374PubMedCrossRefGoogle Scholar
  211. Zardoya R, Meyer A (1998) Complete mitochondrial genome suggests diapsid affinities of turtles. Proc Natl Acad Sci U S A 95:14226–14231PubMedPubMedCentralCrossRefGoogle Scholar
  212. Zardoya R, Meyer A (2001) The evolutionary position of turtles revised. Naturwissenschaften 88:193–200PubMedCrossRefGoogle Scholar
  213. Zdansky O (1923) Über die Temporalregion des Schildkrötenschädels. Bull Geol Inst Univ Upsala 19:89–114Google Scholar
  214. Zhou C-F, Rabi M (2015) A sinemydid turtle from the Jehol Biota provides insights into the basal divergence of crown turtles. Sci Rep 5:16299.  https://doi.org/10.1038/srep16299 CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Senckenberg Center for Human Evolution and PalaeoenvironmentEberhard Karls UniversitätTübingenGermany
  2. 2.Fachbereich GeowissenschaftenEberhard-Karls-UniversitätTübingenGermany
  3. 3.Laboratório de Paleontologia de Ribeirão Preto, FFCLRPUniversidade de São PauloRibeirão PretoBrazil
  4. 4.Museum für Naturkunde, Leibniz-Institut für Evolutions- und BiodiversitätsforschungHumboldt-Universität zu BerlinBerlinGermany

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