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Annual Review of Ecology, Evolution, and Systematics

Volume 51, 2020

Origin and Evolution of the Turtle Body Plan

Abstract

The origin of turtles and their uniquely shelled body plan is one of the longest standing problems in vertebrate biology. The unfulfilled need for a hypothesis that both explains the derived nature of turtle anatomy and resolves their unclear phylogenetic position among reptiles largely reflects the absence of a transitional fossil record. Recent discoveries have dramatically improved this situation, providing an integrated, time-calibrated model of the morphological, developmental, and ecological transformations responsible for the modern turtle body plan. This evolutionary trajectory was initiated in the Permian (>260 million years ago) when a turtle ancestor with a diapsid skull evolved a novel mechanism for lung ventilation. This key innovation permitted the torso to become apomorphically stiff, most likely as an adaption for digging and a fossorial ecology. The construction of the modern turtle body plan then proceeded over the next 100 million years following a largely stepwise model of osteological innovation.

Keyword(s): amniote, anapsid, diapsid, innovation, turtle shell
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2020-11-02
2024-04-16
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Literature Cited

  1. Baur G. 1887. On the morphogeny of the carapace in Testudinata. Am. Nat. 21:89–90
     [Google Scholar]
  2. Bever GS, Lyson TR, Field DF, Bhullar B-AS 2015. Evolutionary origin of the turtle skull. Nature 525:239–43Study of the diapsid skull of Eunotosaurus and a large-scale phylogenetic analysis of early reptiles.
     [Google Scholar]
  3. Bever GS, Lyson TR, Field DF, Bhullar B-AS 2016. The amniote temporal roof and the diapsid origin of the turtle skull. Zoology 119:471–73
     [Google Scholar]
  4. Bhullar B-AS, Bever GS. 2009. An archosaur‐like laterosphenoid in early turtles (Reptilia: Pantestudines). Breviora 518:1–11
     [Google Scholar]
  5. Bojanus LH 1819–1821. Anatome Testudinis Europaeae Vilnius, Lithuania: Zawadzki
  6. Bonin F, Defaux B, Dupré A 2006. Turtles of the World London: A. & C. Black
  7. Burke AC. 1989. Development of the turtle carapace: implications for the evolution of a novel bauplan. J. Morphol. 199:363–78
     [Google Scholar]
  8. Burke AC. 1991. The development and evolution of the turtle body plan: inferring intrinsic aspects of the evolutionary process from experimental embryology. Am. Zool. 31:616–27
     [Google Scholar]
  9. Carrier DR. 1987. The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint. Paleobiology 13:326–41
     [Google Scholar]
  10. Carroll RL. 2013. Problems of the ancestry of turtles. Morphology and Evolution of Turtles DB Brinkman, PA Holroyd, JD Gardner 19–36 New York: Springer
     [Google Scholar]
  11. Cebra-Thomas JA, Betters E, Yin M, Plafkin C, McDow K, Gilbert SF 2007. Evidence that a late-emerging population of trunk neural crest cells forms the plastron bones in the turtle Trachemys scripta. Dev. . Biol 9:267–77
     [Google Scholar]
  12. Cebra-Thomas JA, Tan F, Sistla S, Estes E, Bender G et al. 2005. How the turtle forms its shell: a paracrine hypothesis of carapace formation. J. Exp. Zoolog. B Mol. Dev. Evol. 304:558–69
     [Google Scholar]
  13. Cebra-Thomas JA, Terrell A, Branyan K, Shah S, Rice R et al. 2013. Late-emigrating trunk neural crest cells in turtle embryos generate an osteogenic ectomesenchyme in the plastron. Dev. Dynam. 242:1223–35
     [Google Scholar]
  14. Chen G, Deng C, Li Y-P 2012. TGF-β and BMP signaling in osteoblast differentiation and bone formation. Int. J. Biol. Sci. 8:272–88
     [Google Scholar]
  15. Chiari Y, Cahais V, Galtier N, Delsuc F 2012. Phylogenomic analyses support the position of turtles as sister group of birds and crocodiles (Archosauria). BMC Biol 10:65
     [Google Scholar]
  16. Clark K, Bender G, Murray BP, Panfilio K, Cook S et al. 2001. Evidence for the neural crest origin of turtle plastron bones. Genesis 31:111–17
     [Google Scholar]
  17. Cohen KM, Finney SC, Gibbard PL, Fan J-X 2013. The ICS International Chronostratigraphic Chart. Episodes 36:199–204
     [Google Scholar]
  18. Cordero GA, Quinteros K. 2015. Skeletal remodeling suggests the turtle's shell is not an evolutionary straitjacket. Biol. Lett. 11:20150022
     [Google Scholar]
  19. Cox CB. 1969. The problematic Permian reptile Eunotosaurus. Bull. Brit. Mus. Nat. . Hist 18:165–96
     [Google Scholar]
  20. Crawford NG, Faircloth BC, McCormack JE, Brumfield RT, Winker K, Glenn TC 2012. More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs. Biol. Lett. 8:783–86
     [Google Scholar]
  21. Crawford NG, Parham JF, Sellas AB, Faircloth BC, Glenn TCet al 2015. A phylogenomic analysis of turtles. Mol. Phylogenetics Evol 83:250–57
     [Google Scholar]
  22. deBraga M, Rieppel O. 1997. Reptile phylogeny and the affinities of turtles. Zool. J. Linn. Soc. 120:281–354
     [Google Scholar]
  23. Field DJ, Gauthier JA, King BL, Pizani D, Lyson TR, Peterson KJ 2014. Toward consilience in reptile phylogeny: miRNAs support an archosaur, not lepidosaur, affinity for turtles. Evol. Dev. 16:189–96
     [Google Scholar]
  24. Fong JJ, Brown JM, Fujita MK, Boussau BA 2012. Phylogenomic approach to vertebrate phylogeny supports a turtle archosaur affinity and a possible paraphyletic Lissamphibia. PLOS ONE 7:e48990
     [Google Scholar]
  25. Ford DP, Benson RBJ. 2020. The phylogeny of early amniotes and the affinities of Parareptilia and Varanopidae. Nat. Ecol. Evol. 4:57–65
     [Google Scholar]
  26. Gaffney ES. 1980. Phylogenetic relationships of the major groups of amniotes. The Terrestrial Environment and the Origin of Land Vertebrates AL Panchen 593–610 London: Academic
     [Google Scholar]
  27. Gaffney ES. 1990. The comparative osteology of the triassic turtle Proganochelys. Bull. 194, Am. Mus. Nat. Hist. New York:
  28. Gaffney ES, Meylan PA. 1988. A phylogeny of turtles. The Phylogeny and Classification of the Tetrapods, Vol. 1: Amphibians, Reptiles, Birds MJ Benton 157–219 Oxford, UK: Clarendon
     [Google Scholar]
  29. Gans C, Hughes GM. 1967. The mechanism of lung ventilation in the tortoise Testudo graeca Linne. J. Exp. Biol. 47:1–20
     [Google Scholar]
  30. Gaunt AS, Gans C. 1969. Mechanics of respiration in the snapping turtles, Chelydra serpentina (Linne). J. Morph. 128:195–228
     [Google Scholar]
  31. Gauthier JA, Kluge AG, Rowe T 1988. Amniote phylogeny and the importance of fossils. Cladistics 4:105–209
     [Google Scholar]
  32. Gilbert SF, Bender G, Better E, Yin M, Cebra‐Thomas JA 2007. The contribution of neural crest cells to the nuchal bone and plastron of the turtle shell. Int. Comp. Biol. 47:401–8
     [Google Scholar]
  33. Gilbert SF, Cebra-Thomas JA, Burke AC 2008. How the turtle gets its shell. Biology of Turtles J Wyneken, MH Godfrey, V Bels 1–16 Boca Raton, FL: CRC
     [Google Scholar]
  34. 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. 3:47–58
     [Google Scholar]
  35. Hedges SB, Poling LL. 1999. A molecular phylogeny of reptiles. Science 283:998–1000
     [Google Scholar]
  36. Hill RV. 2005. Integration of morphological data sets for phylogenetic analysis of Amniota: the importance of integumentary characters and increased taxonomic sampling. Syst. Biol. 54:530–47
     [Google Scholar]
  37. Hirasawa T, Nagashima H, Kuratani S 2013. The endoskeletal origin of the turtle carapace. Nat. Commun. 4:2107
     [Google Scholar]
  38. Hirasawa T, Pascual-Anaya J, Kamezaki N, Taniguchi M, Mine K, Kuratani S 2015. The evolutionary origin of the turtle shell and its dependence on the axial arrest of the embryonic rib cage. J. Exp. Zool. B Mol. Dev. Evol. 324:194–207
     [Google Scholar]
  39. Hsiang AY. 2015. Evolutionary origins of major reptile lineages: case studies on phylogenetic incongruence and the importance of fossils PhD Thesis, Yale Univ., New Haven, CT
  40. Hugall AF, Foster R, Lee MSY 2007. Calibration choice, rate smoothing, and the pattern of tetrapod diversification according to the long nuclear gene RAG‐1. Syst. Biol. 56:543–63
     [Google Scholar]
  41. Iwabe N, Hara Y, Kumazawa Y, Shibamoto K, Miyata T, Katoh K 2005. Sister group relationship of turtles to the bird crocodilian clade revealed by nuclear DNA‐coded proteins. Mol. Biol. Evol. 22:810–13
     [Google Scholar]
  42. Jackson DC. 2011. Life in a Shell—A Physiologist's View of a Turtle Cambridge, MA: Harvard Univ. Press
  43. Jenkins FA Jr 1970. Anatomy and function of expanded ribs in certain edentates and primates. J. Mammal. 51:288–301
     [Google Scholar]
  44. Joyce WG. 2007. Phylogenetic relationships of Mesozoic turtles. Bull. Peabody Mus. Nat. Hist. 48:3–102
     [Google Scholar]
  45. Joyce WG. 2017. A review of the fossil record of basal Mesozoic turtles. Bull. Peabody Mus. Nat. Hist. 58:65–113
     [Google Scholar]
  46. Joyce WG, Gauthier JA. 2004. Palaeoecology of Triassic stem turtles sheds new light on turtle origins. Proc. R. Soc. B 271:1–5
     [Google Scholar]
  47. Joyce WG, Lucas SG, Scheyer TM, Heckert AB, Hunt AP 2009. A thin-shelled reptile from the Late Triassic of North America and the origin of the turtle shell. Proc. R. Soc. B 276:507–13
     [Google Scholar]
  48. Joyce WG, Schoch RR, Lyson TR 2013. The girdles of the oldest fossil turtle, Proterochersis robusta, and the age of the turtle crown. BMC Evol. Biol. 13:266
     [Google Scholar]
  49. Kumar S, Stecher G, Suleski M, Hedges SB 2017. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34:1812–19
     [Google Scholar]
  50. Kumazawa Y, Nishida M. 1999. Complete mitochondrial DNA sequences of the green turtle and blue‐tailed mole skink: statistical evidence for archosaurian affinity of turtles. Mol. Biol. Evol. 16:784–92
     [Google Scholar]
  51. Kuraku S, Usuda R, Kuratani S 2005. Comprehensive survey of carapacial ridge-specific genes in turtle implies co-option of some regulatory genes in carapace evolution. Evol. Dev. 7:3–17
     [Google Scholar]
  52. 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. 13:1–14
     [Google Scholar]
  53. Kuratani S, Nagashima H. 2012. A developmental basis for innovative evolution of the turtle shell. From Clone to Bone: The Synergy of Morphological and Molecular Tools in Palaeobiology R Asher, J Müller279–300 Cambridge, UK: Cambridge Univ. PressDevelopmental and fossil data inform an evo-devo model for the origin of the turtle shell.
     [Google Scholar]
  54. Laurin M, Piñeiro G 2017. A reassessment of the taxonomic position of mesosaurs, and a surprising phylogeny of early amniotes. Front. Earth Sci 5:88
     [Google Scholar]
  55. Laurin M, Reisz RR. 1995. A reevaluation of early amniote phylogeny. Zool. J. Linn. Soc. 113:165–223
     [Google Scholar]
  56. Lautenschlager S, Ferreira GS, Werneburg I 2018. Sensory evolution and ecology of early turtles revealed by digital endocranial reconstructions. Front. Ecol. Evol. 6:fevo.2018.00007
     [Google Scholar]
  57. Lee MSY. 1997a. Pareiasaur phylogeny and the origin of turtles. Zool. J. Linn. Soc. 120:197–280
     [Google Scholar]
  58. Lee MSY. 1997b. Reptile relationships turn turtle. Nature 389:245–46
     [Google Scholar]
  59. Lee MSY. 2013. Turtle origins: insights from phylogenetic retrofitting and molecular scaffolds. J. Evol. Biol. 26:2729–38
     [Google Scholar]
  60. Li C, Fraser NC, Rieppel O, Wu X-C 2018. A Triassic stem turtle with an edentulous beak. Nature 560:477–79
     [Google Scholar]
  61. Li C, X‐C Wu, Rieppel O, Wang L‐T, Zhao L‐J 2008. An ancestral turtle from the Late Triassic of southwestern China. Nature 456:497–501Odontochelys description—pivotal fossil that sets the stage for considerable future turtle origins work.
     [Google Scholar]
  62. Lima FC, Santos ALQ, Vieira LG, Da Silva-Junior LM, Romão MF et al. 2011. Ontogeny of the shell bones of embryos of Podocnemis unifilis (Troschel, 1848) (Testudines, Podocnemididae). Anat. Rec. 294:621–32
     [Google Scholar]
  63. Loredo GA, Brukman A, Harris MP, Kagle D, Leclair EE et al. 2001. Development of an evolutionarily novel structure: fibroblast growth factor expression in the carapacial ridge of turtle embryos. J. Exp. Zoo. 291:274–81
     [Google Scholar]
  64. Lu B, Yang W, Dai Q, Fu J 2013. Using genes as characters and a parsimony analysis to explore the phylogenetic position of turtles. PLOS ONE 8:e79348
     [Google Scholar]
  65. Lyson TR, Bever GS, Bhullar B‐AS, Joyce WG, Gauthier JA 2010. Transitional fossils and the origin of turtles. Biol. Lett. 6:830–33
     [Google Scholar]
  66. Lyson TR, Bever GS, Scheyer TM, Hsiang AY, Gauthier JA 2013a. Evolutionary origin of the turtle shell. Curr. Biol. 23:1113–19Eunotosaurus postcranial anatomy and elaboration of evo-devo model for origin of shell/lung ventilatory apparatus.
     [Google Scholar]
  67. Lyson TR, Bhullar B-AS, Bever GS, Joyce WG, de Queiroz K et al. 2013b. Homology of the enigmatic nuchal bone reveals novel reorganization of the shoulder girdle in the evolution of the turtle shell. Evol. Dev. 15:317–25
     [Google Scholar]
  68. Lyson TR, Gilbert SF. 2009. Turtles all the way down: loggerheads at the root of the chelonian tree. Evol. Devo. 11:133–35
     [Google Scholar]
  69. Lyson TR, Joyce WG. 2012. Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage. Biol. Lett. 8:1028–31
     [Google Scholar]
  70. Lyson TR, Rubidge BS, Scheyer TM, Queiroz KD, Schachner ER et al. 2016. Fossorial origin of the turtle shell. Curr. Biol. 26:1887–94Novel hypothesis proposed where the earliest step in construction of shell is adaptation for digging.
     [Google Scholar]
  71. Lyson TR, Schachner ER, Botha-Brink J, Scheyer TM, Lambertz M et al. 2014. Origin of the unique ventilatory apparatus of turtles. Nat. Commun. 5:5211
     [Google Scholar]
  72. Lyson TR, Sperling EA, Heimberg AM, Gauthier JA, King BL, Peterson KJ 2012. MicroRNAs support a turtle+lizard clade. Biol. Lett. 8:104–7
     [Google Scholar]
  73. MacCord K, Caniglia G, Moustakas-Verho JE, Burke AC 2014. The dawn of chelonian research: turtles between comparative anatomy and embryology in the 19th century. J. Exp. Zool. B Mol. Dev. Evol. 324:169–80
     [Google Scholar]
  74. Matsuda Y, Nishida-Umehara C, Tarui H, Kuroiwa A, Yamada K et al. 2005. Highly conserved linkage homology between birds and turtles: Bird and turtle chromosomes are precise counterparts of each other. Chromosome Res 13:601–15
     [Google Scholar]
  75. Mayerl CJ, Capano JG, Moreno AA, Wyneken J, Blob RW, Brainerd EL 2019. Pectoral and pelvic girdle rotations during walking and swimming in a semi-aquatic turtle: testing functional role and constraint. J. Exp. Bio. 222:jeb212688
     [Google Scholar]
  76. Mitchell SW, Morehouse GR. 1863. Researches Upon the Anatomy and Physiology of Respiration in the Chelonia Washington, DC: Smithsonian
  77. Moustakas JE 2008. Development of the carapacial ridge: implications for the evolution of genetic networks in turtle shell development. Evol. Dev 10:29–36
     [Google Scholar]
  78. Moustakas-Verho JE, Cherepanov GO. 2015. The integumental appendages of the turtle shell: an evo-devo perspective. J. Exp. Zool. B Mol. Dev. Evol. 324:221–29
     [Google Scholar]
  79. Müller J. 2003. Early loss and multiple return of the lower temporal arcade in diapsid reptiles. Naturwissenschaften 90:473–76
     [Google Scholar]
  80. Müller J, Scheyer TM, Head JJ, Barrett PM, Werneburg I et al. 2010. Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. PNAS 107:2118–23
     [Google Scholar]
  81. 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 134:2219–26
     [Google Scholar]
  82. 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. 87:1–13
     [Google Scholar]
  83. Nagashima H, Shibata M, Taniguchi M, Ueno S, Kamezaki N, Sato N 2014. Comparative study of the shell development of hard- and soft-shelled turtles. J. Anat. 225:60–70
     [Google Scholar]
  84. Nagashima H, Sugahara F, Takechi M, Ericsson R, Kawashima‐Ohya Y et al. 2009. Evolution of the turtle body plan by the folding and creation of new muscle connections. Science 325:193–96Developmental study describing consequences of shortened/flabellate ribs and folding body wall muscles around shoulder girdle.
     [Google Scholar]
  85. Ogushi K. 1911. Anatomische Studien an der japanischen dreikralligen Lippenschildkröte (Trionyx japonicus). Morpholog. Jahrbuch 43:1–106
     [Google Scholar]
  86. Pascual-Anaya J, Hirasawa T, Sato TI, Kuraku S, Kuratani S 2014. Comparative analysis of pleurodiran and cryptodiran turtle embryos depicts the molecular ground pattern of the turtle carapacial ridge. Int. J. Dev. Biol. 58:743–50
     [Google Scholar]
  87. Piñeiro G, Ferigolo J, Ramos A, Laurin M 2012. Cranial morphology of the Early Permian mesosaurid Mesosaurus tenuidens and the evolution of the lower temporal fenestration reassessed. C. R. Palevol. 11:379–91
     [Google Scholar]
  88. Reisz RR, Laurin M. 1991. Owenetta and the origin of turtles. Nature 349:324–26
     [Google Scholar]
  89. Rice R, Kallonen A, Cebra-Thomas J, Gilbert SF 2016. Development of the turtle plastron, the order-defining skeletal structure. PNAS 113:5317–22
     [Google Scholar]
  90. Rice R, Riccio P, Gilbert SF, Cebra-Thomas J 2015. Emerging from the rib: resolving the turtle controversies. J. Exp. Zool. B Mol. Dev. Evol. 324:208–20
     [Google Scholar]
  91. Rieppel O. 2001. Turtles as hopeful monsters. Bioessays 23:987–91
     [Google Scholar]
  92. Rieppel O. 2013. The evolution of the turtle shell. Morphology and Evolution of Turtles DB Brinkman, PA Holroyd, JD Gardner 51–61 New York: Springer
     [Google Scholar]
  93. Rieppel O. 2017. Turtles as Hopeful Monsters: Origins and Evolution Bloomington: Indiana Univ. Press
  94. Rieppel O, deBraga M. 1996. Turtles as diapsid reptiles. Nature 384:453–55
     [Google Scholar]
  95. Rieppel O, Reisz RR. 1999. The origin and early evolution of turtles. Ann. Rev. Ecol. Syst. 30:1–22
     [Google Scholar]
  96. Romer AS. 1956. Osteology of the Reptiles Chicago: Univ. Chicago Press
  97. Ruckes H. 1929. Studies in chelonian osteology part II: the morphological relationships between the girdles, ribs, and carapace. Ann. N.Y. Acad. Sci. 31:81–120
     [Google Scholar]
  98. Salazar VS, Gamer LW, Rosen V 2016. BMP signalling in skeletal development, disease and repair. Nat. Rev. Endocrinol. 12:203–21
     [Google Scholar]
  99. Sánchez‐Villagra MR, Müller H, Sheil CA, Scheyer TM, Nagashima H, Kuratani S 2009. Skeletal development in the Chinese softshelled turtle Pelodiscus sinensis (Testudines: Trionychidae). J. Morphol. 270:1381–99
     [Google Scholar]
  100. Scheyer TM, Brüllmann B, Sánchez‐Villagra MR 2008. The ontogeny of the shell in side‐necked turtles, with emphasis on the homologies of costal and neural bones. J. Morphol. 269:1008–21
     [Google Scholar]
  101. Scheyer TM, Sander PM. 2007. Shell bone histology indicates terrestrial palaeoecology of basal turtles. Proc. Biol. Sci. 274:1885–93
     [Google Scholar]
  102. Schoch RR, Klein N, Scheyer TM, Sues H-D 2019. Microanatomy of the stem-turtle Pappochelys rosinae indicates a predominantly fossorial mode of life and clarifies early steps in the evolution of the shell. Sci. Rep. 9:10430
     [Google Scholar]
  103. Schoch RR, Sues H-D. 2015. A Middle Triassic stem-turtle and the evolution of the turtle body plan. Nature 523:584–87Pappochelys description—diapsid stem turtle that bridges the temporal/morphological gap between Eunotosaurus and later turtles.
     [Google Scholar]
  104. Schoch RR, Sues H-D. 2016. The diapsid origin of turtles. Zoology 119:159–61
     [Google Scholar]
  105. Schoch RR, Sues H-D. 2017. Osteology of the Middle Triassic stem-turtle Pappochelys rosinae and the early evolution of the turtle skeleton. J. Syst. Palaeontol. 16:927–65
     [Google Scholar]
  106. Schoch RR, Sues H-D. 2020. The origin of the turtle body plan: evidence from fossils and embryos. Palaeontology 63:375–93
     [Google Scholar]
  107. Seeley HG. 1892. On a new reptile from Welte Vreden (Beaufort West), Eunotosaurus africanus (Seeley). Q. J. Geol. Soc. 47:583–85
     [Google Scholar]
  108. Shaffer HB, Minx P, Warren DE, Shedlock Am, Thomson RC et al. 2013. The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol 14:R28Along with Wang et al. (2013), first publication of entire turtle genome, solidifying the turtle-archosaur phylogenetic hypothesis.
     [Google Scholar]
  109. Shearman RM, Burke AC. 2009. The lateral somatic frontier in ontogeny and phylogeny. J. Exp. Zool. B Mol. Dev. Evol. 312:603–12
     [Google Scholar]
  110. Sheil CA. 2005. Skeletal development of Macrochelys temminckii (Reptilia: Testudines: Chelydridae). J. Morphol. 263:71–106
     [Google Scholar]
  111. Sheil CA, Greenbaum E. 2005. Reconsideration of skeletal development of Chelydra serpentina (Reptilia: Testudinata: Chelydridae): evidence for intraspecific variation. J. Zool. 265:235–67
     [Google Scholar]
  112. Shen X‐X, Liang D, Wen J‐Z, Zhang P 2011. Multiple genome alignments facilitate development of NPCL markers: a case study of tetrapod phylogeny focusing on the position of turtles. Mol. Biol. Evol. 12:3237–57
     [Google Scholar]
  113. Smith-Paredes D, Lord A, Meyer D, Bhullar B-AS 2020. A developmental staging system and musculoskeletal development sequence of the Common Musk turtle (Sternotherus odoratus). Dev. Dynam. 2020.dvdy.210
     [Google Scholar]
  114. Sterli J, de la Fuente MS, Rougier GW 2007. Anatomy and relationships of Palaeochersis talampayensis, a Late Triassic turtle from Argentina. Palaeontogr. Abt. A 281:1–61
     [Google Scholar]
  115. Sumida SS, Modesto S. 2001. A phylogenetic perspective on locomotory strategies in early amniotes. Am. Zool. 41:586–97
     [Google Scholar]
  116. Szczygielski T, Sulej T. 2016. Revision of the Triassic European turtles Proterochersis and Murrhardtia (Reptilia, Testudinata, Proterochersidae), with the description of new taxa from Poland and Germany. Zool. J. Linn. Soc. 177:395–427
     [Google Scholar]
  117. Szczygielski T, Sulej T. 2019. The early composition and evolution of the turtle shell (Reptilia, Testudinata). Palaeontology 62:375–415
     [Google Scholar]
  118. Tzika AC, Helaers R, Schramm G, Milinkovitch M 2011. Reptilian‐transcriptome v1.0, a glimpse in the brain transcriptome of five divergent Sauropsida lineages and the phylogenetic position of turtles. Evodevo 2:19
     [Google Scholar]
  119. Vallén E. 1942. Beiträge zur Kenntnis der Ontogenie und der vergleichenden Anatomie des Schildkrötenpanzers. Acta Zool. Stockholm231–127
     [Google Scholar]
  120. von Baer KE. 1828. Über Entwicklungsgeschichte der Thiere: Beobachtung und Reflexion Königsberg, Russia: Bornträger
  121. Walker WF Jr 1979. Locomotion. Turtles, Perspectives and Research M Harless, H Morlock 435–54 New York: John Wiley & Sons
     [Google Scholar]
  122. Wang Z, Pascual-Anaya J, Zadissa A, Li W, Niimura Y et al. 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. 45:701–6Along with Schaffer et al. (2013), first publication of entire turtle genome, solidifying the turtle-archosaur phylogenetic hypothesis.
     [Google Scholar]
  123. Werneburg I, Hinz JK, Gumpenberger M, Volpato V, Natchev N, Joyce WG 2015b. Modeling neck mobility in fossil turtles. J. Exp. Zool. B Mol. Dev. Evol. 324:230–43
     [Google Scholar]
  124. Werneburg I, Wilson LAB, Parr WCH, Joyce WG 2015a. Evolution of neck vertebral shape and neck retraction at the transition to modern turtles: an integrated geometric morphometric approach. Syst. Biol. 64:187–204
     [Google Scholar]
  125. Williams EE. 1950. Variation and selection in the cervical central articulations of living turtles. Bull. Am. Mus. Nat. Hist. 94:509–61
     [Google Scholar]
  126. Zangerl R. 1969. The homology of the shell elements in turtles. J. Morphol. 65:383–406
     [Google Scholar]
  127. Zardoya R, Meyer A. 1998. Complete mitochondrial genome suggests diapsid affinities of turtles. PNAS 95:14226–31
     [Google Scholar]
  128. Zardoya R, Meyer A. 2001. The evolutionary position of turtles revisited. Naturwissenschaften 88:193–200
     [Google Scholar]
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Origin and Evolution of the Turtle Body Plan
Annual Review of Ecology, Evolution, and Systematics 51, 143 (2020); https://doi.org/10.1146/annurev-ecolsys-110218-024746
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