Embryogenesis and ossification of emydura subglobosa (testudines, pleurodira, chelidae) and patterns of turtle development

Developmental Dynamics

Volumn 238, Issue 11, 2009, Pages 2770-2786

  Werneburg, Ingmar ^a   Hugi, Jasmina ^a   Müller, Johannes ^b   Sánchez Villagra, Marcelo R ^a  

^a PALÄONTOLOGISCHES INSTITUT UND MUSEUM   (Switzerland)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Cryptodira; Embryogenesis; Heterochrony; Parsimov; Pleurodira; Skeletogenesis; Skull, skeleton; Staging system (SES)

Indexed keywords

ARTICLE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EMYDURA SUBGLOBOSA; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; MANDIBLE; MAXILLA; NECK; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; TAXON; TOOTH DEVELOPMENT; TURTLE; VERTEBRA;

ANIMALS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; EXTREMITIES; OSTEOGENESIS; SKULL; SPINE; TURTLES;

CHELIDAE; CRYPTODIRA; EMYDURA SUBGLOBOSA; EPIPLASTRON; PLEURODIRA; TESTUDINES; TETRAPODA; VERTEBRATA;

EID: 70350712295     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22104     Document Type: Article

References (99)

1. Alibardi L, Thompson MB. 1999. Morphogenesis of shell and scutes in the turtle Emydura macquarii. Austral J Zool 47:245-260. (Pubitemid 29375348)
2. Beggs K, Young J, Georges A, West P. 2000. Ageing the eggs and embryos of the pig-nosed turtle, Carettochelys insculpta (Chelonia: Carettochelydidae), from northern Australia. Can J Zool 78:373-392.
3. Bell BA, Spotila JR, Paladino FV, Reina RD. 2003. Low reproductive success of leatherback turtles, Dermochelys coriacea, is due to high embryonic mortality. Biol Conserv 115:131-138.
4. Bona P, Alcalde L. 2009. Chondrocranium and skeletal development of Phrynops hilarii (Pleurodira: Chelidae). Acta Zool 89:301-325.
5. Bonin F, Devaux B, Dupré A. 2006. Turtles of the world. Baltimore: John Hopkins University Press.
6. Boughner JC, Buchtová M, Fu K, Diewert V, Hallgrímsson B, Richman JM. 2007. Embryonic development of Python sebae. I: Staging criteria and macroscopic skeletal morphogenesis of the heads and limbs. Zoology 110:212-230.
7. Boulenger G. 1889. On the characters of the chelonian families Pelomedusidae and Chelydridae. Annu Mag Nat Hist 61:346-347.
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 31:616-627.
9. Cherepanov GO. 1995. Ontogenetic development of the shell in Trionyx sinensis (Trionychidae, Testudinata) and some questions on the nomenclature of bony plates. Russ J Herpetol 2:129-133.
10. Colbert MW, Rowe T. 2008. Ontogenetic sequence analysis: Using parsimony to characterize developmental sequences and sequence polymorphism. J Exp Zool (Mol Dev Evol) 310B.
11. Cretekos CJ, Weatherbee SD, Chen C-H, Badwaik NK, Niswander L, Behringer RR, Rasweiler JJI. 2005. Embryonic staging system for the short-tailed fruit bat, Carollia perspicillata, a model organism for the mammalian order Chiroptera, based upon timed pregnancies in captive-bred animals. Dev Dyn 233:721-738. (Pubitemid 40853449)
12. Danilov IG, Parham JF. 2008. A reassessment of some poorly known turtles from the middle Jurassic of China, with comments on the antiquity of extant turtles. J Vertebr Paleontol 28:306-318.
13. de Jong IML, Witte F, Richardson MK. 2009. Developmental stages until hatching of the Lake Victoria cichlid Haplochromis piceatus (Teleostei: Cichlidae). J Morphol 270:519-535.
14. Edgeworth FH. 1935. The cranial muscles of vertebrates. London: Cambridge University Press.
15. Eßwein S. 1992. Zur phylogenetischen und ontogenetischen Entwicklung des akinetischen Craniums der Schildkrö-ten. Natürliche Konstruktionen - Mitteilungen des SFB 230 751-755
16. Fabrezi M, Manzano A, Abdala V, Zaher H. 2009. Developmental basis of limb homology in pleurodiran turtles, and the identity of the hooked element in the chelonian tarsus. Zool J Linnean Soc 155:845-866.
17. Franz-Odendaal T. 2006. Intramembranous ossification of scleral ossicles in Chelydra serpentina. Zoology 109:75-81.
18. Fröbisch NB. 2008. Ossification patterns in the tetrapod limb-conservation and divergence from morphogenetic events. Biological Reviews 83.
19. Fürbringer M. 1874. Zur vergleichenden Anatomie der Schultermuskeln. II. Theil. Jenaische Z Naturwissenschaften 8:175-280.
20. Gaffney ES. 1977. The side-necked turtle family Chelidae: a theory of relationships using shared derived characters. Am Mus Novitates 2620:1-28.
21. Gaffney ES. 1979. Comparative cranial morphology of recent and fossil turtles. Bull Am Mus Nat Hist 164:67-376.
22. Gaffney ES, Meylan PA. 1988. A phylogeny of turtles. In: Benton MJ, editor. The phylogeny and classification of the tetrapods. Volume 1: Amphibians, reptiles, birds. Oxford: Clarendon Press. p 157-219.
23. Galbraith DA, Brooks DR, Obbard ME. 1989. The influence of growth rate on age and body size at maturity in female snapping turtles (Chelydra serpentina). Copeia: 896-904.
24. Giannini N, Goswami A, Sánchez-Villagra MR. 2006. Development of integumentary structures in Rousettus amplexicaudatus (Mammalia: Chiroptera: Pteropodidae) during late-embryonic and fetal stages. J Mammal 87:993-1001.
25. 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.
26. Gilbert SF, Cebra-Thomas JA, Burke AC. 2008. How the turtle gets its shell. In: Wyneken J, Godfrey MH, Bels V, editors. Biology of turtles. New York:CRC Press. p 1-16.
27. Goodrich ES. 1930. Studies on the structure and development of vertebrates. London: Macmillan and Co.
28. Greenbaum E. 2002. A standardized series of embryonic stages for the emydid turtle Trachemys scripta. Can J Zool 80:1350-1370. (Pubitemid 36048878)
29. Greenbaum E, Carr JL. 2002. Staging criteria for embryos of the spiny softshell turtle, Apalone spinifera (Testudines: Trionychidae). J Morphol 254:272-291. (Pubitemid 35399997)
30. Guyot G, Pieau C, Renous S. 1994. Déáveloppement embryonnaire d'une tortue terrestre, la tortue d'Hermann, Testudo hermanni Gmelin, 1789. Ann Sci Nat Zool Paris 15:115-137.
31. Haeckel, E. 1896. Systematische Phylogenie. Zweiter Theil, Systematische Phylogenie der wirbellosen Thiere (Invertebrata). Berlin: Georg Reimer.
32. Harrison L, Larsson H. 2008. Estimating evolution of temporal sequence changes: a practical approach to inferring ancestral developmental sequences and sequence heterochrony. Systemat Biol 57:378-387. (Pubitemid 351882197)
33. Hennig AS. 2001. Haltung und Nachzucht der Rotbauch- Spitzkopfschildkröte (Emydura subglobosa). Reptilia 9:70-73.
34. Herrel A, O'Reilly JC, Richmond AM. 2002. Evolution of bite performance in turtles. J Evol Biol 15:1083-1094.
35. Herrel A, Van Damme J, Aerts P. 2008. Cervical anatomy and function in turtles. In: Wyneken J, Godfrey MH, Bels V, editors. Biology of turtles. New York: CRC Press. p 163-185.
36. Highfield AC. 1996. Practical encyclopedia of keeping and breeding tortoises and freshwater turtles. London: Carapace Press.
37. Hoffmann CK. 1890. Schildkröten. Leipzig: C.F. Winter'sche Verlagshandlung. 442 p.
38. Hopwood N. 2005. Visual standards and disciplinary change: Normal plates, tables and stages in embryology. Hist Sci 43:239-303. (Pubitemid 41235348)
39. Hopwood N. 2007. A history of normal plates, tables and stages in vertebrate embryology. Int J Dev Biol 51:1-26. (Pubitemid 46182037)
40. Hugi J, Mitgutsch C, Sánchez-Villagra MR. 2009. Chondrogenic and ossification patterns and sequences in White's skink Liopholis whitii (Scincidae, Reptilia). Zoosystemat Evol (in press).
41. Jeffery JE, Bininda-Emonds ORP, Coates MI, Richardson MK. 2005. A new technique for identifying sequence heterochrony. Systemat Biol 54:230-240.
42. Jenner RA, Wills MA. 2007. The choice of model organisms in evo-devo. Nature Rev Genet 8:311-319.
43. Joyce WG. 2007. Phylogenetic relationships of Mesozoic turtles. Bull Peabody Mus Nat Hist 48:3-102.
44. Krefft G. 1876. Notes on Australian animals in New Guinea with description of a new freshwater tortoise belonging to the genus Euchelymys (Gray). Ann Museo Civico Storia Nat Genova 1:390-394.
45. Lakjer T. 1926. Studien über die Trigeminus- versorgte Kaumuskulatur der Sauropsiden. Copenhagen: C.A. Reitsel Buchhandlung.
46. Legler JM, Georges A. 1993. Chapter 21. Family Chelidae. In: Glasby RB, editor. Fauna of Australia 2A: Amphibia and reptilia. Australian Government Publishing Service. http://www.ea.gov. au/biodiversity/abrs/onlineresources/ abif/ fauna/foa/2a-contents.html.
47. Lemell P, Lemell C, Snelderwaard P, Gumpenberger M, Wochesländer R, Weisgram J. 2002. Feeding patterns of Chelus fimbriatus (Pleurodira: Chelidae). J Exp Biol 205:1495-1506. (Pubitemid 34853473)
48. Li C, Wu X-C, Rieppel O, Wang L-T, Zhao L-J. 2008. An ancestral turtle from the Late Triassic of southwestern China. Nature 456:497-501. (Pubitemid 352759012)
49. Maddison DR, Maddison WP. 2001. Mac- Clade 4. In. Sunderland, MA: Sinauer Associates, Inc. Publishers.
50. Mickoleit G. 2004. Phylogenetische Systematik der Wirbeltiere. München: Verlag Dr. Friedrich Pfeil.
51. Miller JD. 1985. Embryology of marine turtles. In: Gans C, Billet F, Maderson PFA, editors. Biology of the reptilian, Vol.14: Development A. New York: John Wiley & Sons. p 269-328.
52. Mitgutsch C. 2003. On Carl Gegenbaur's theory on head metamerism and the selection of taxa for comparisons. Theory Biosci. 122:204-229. (Pubitemid 36781567)
53. Müller J. 2003. Early loss and multiple return of the lower temporal arcade in diapsid reptiles. Naturwissenschaften 90:473-476. (Pubitemid 37363558)
54. Nagashima H, Uchida K, Yamamoto K, Kuraku S, Usuda R, Kuratani S. 2005. Turtle-chicken chimera: an experimental approach to understanding evolutionary innovation in the turtle. Dev Dyn 232:149-161. (Pubitemid 40070867)
55. Nagashima H, Kuraku S, Uchida K, Ohya Y, Narita Y, Kuratani S. 2007. On the carapacial ridge in turtle embryos: its developmental origin, function and the chelonian body plan. Development 134: 2219-2226. (Pubitemid 47010011)
56. 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 325:193-196.
57. Nicol E. 1993. Red-bellied short-necked turtle, Emydura subglobosa. Tortuga Gazette 29:1-3.
58. Nolte MJ, Hockman D, Cretekos CJ, Behringer RR, Rasweiler JJI. 2009. Embryonic staging system for the black mastiff bat, Molossus rufus (Molossidae), correlated with structure-function relationships in the adult. Anat Rec 292:155-168.
59. Ogushi K. 1913. Anatomische Studien an der japanischen dreikralligen Lippenschildkro ̈te (Trionyx japanicus). II. Mitteilung: Muskel- und peripheres Nervensystem. Morphol Jahrbuch 46: 299-562.
60. Olsson L. 1993. Pigment pattern formation in the larval salamander Ambystoma maculatum. J Morphol 215:151-163.
61. O'Steen S. 1998. Embryonic temperature influences juvenile temperature choice and growth rate in snapping turtles Chelydra serpentina. J Exp Biol 201:439-449.
62. Packard GC, Packard MJ, Birchard GF. 2000. Availability of water affects organ growth in prenatal and neonatal snapping turtles (Chelydra serpentina). J Comp Physiol B 170:69-74.
63. Pawlowski S. 2001. Weitere Erkenntnisse zu Reproduktionsvermöö gen und Schlupferfolg zweier Weibchen der Rotbauch- Spitzkopfschildkröte, Emydura subglobosa (KREFFT 1876). Elaphe 12:35-45.
64. Rathke H. 1848. Ueber die Entwickelung der Schildkröten. Braunschweig: Druck und Verlag von Friedrich Vieweg und Sohn.
65. Richardson MK, Jeffery JE, Coates MI, Bininda-Emonds ORP. 2001. Comparative methods in developmental biology. Zoology 104:278-283.
66. Richardson MK, Gobes S, van Leeuwen A, Poelman A, Pieau C, Sánchez-Villagra MR. 2009. Heterochrony in limb evolution: developmental mechanisms and natural selection. J Exp Zool (Mol Dev Evol) 310B:639-664.
67. Rieppel O. 1990. The structure and development of the jaw adductor musculature in the turtle Chelydra serpentina. Zool J Linnean Soc 98:27-62.
68. Rieppel O. 1993. Studies on skeleton formation in reptiles: Patterns of ossification in the skeleton of Chelydra serpentina (Reptilia, Testudines). J Zool 231:487-509. (Pubitemid 23806655)
69. Rieppel O. 2004. Kontroversen innerhalb der Tetrapoda: die Stellung der Schildkröten (Testudines). Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin 43:201-221.
70. Rieppel O. 2008. The relationships of turtles within amniotes. In: Wyneken J, Godfrey MH, Bels V, editors. Biology of turtles. New York: CRC Press. p 345-353.
71. Sánchez-Villagra MR, Winkler JD, Wurst L. 2007. Autopodial skeleton evolution in side-necked turtles (Pleurodira). Acta Zool (Stockholm) 88:199-209. (Pubitemid 46920180)
72. Sánchez-Villagra MR, Goswami A, Weisbecker V, Mock O, Kuratani S. 2008. Conserved relative timing of cranial ossification patterns in early mammalian evolution. Evol Dev 10:519-530.
73. Sánchez-Villagra MR, Müller H, Sheil CA, Scheyer TM, Nagashima H, Kuratani S. 2009. Skeletal development in the Chinese soft-shelled turtle Pelodiscus sinensis (Testudines: Trionychidae). J Morphol [DOI: 10.1002/jmor.10766] (in press).
74. Sanger TJ, Losos JB, Gibson-Brown JJ. 2008. A developmental staging series for the lizard genus Anolis: A new system for the integration of evolution, development, and ecology. J Morphol 269:129-137.
75. Scanlon TC. 1982. Anatomy of the neck of the western painted turtle (Chrysemys picta belli Gray; Reptilia, Testudinata) from the perspective of possible movements in the region. Ann Arbor, MI: The University of Michigan. p 283.
76. Scheyer TM. 2007. Comparative bone histology of the turtle shell (carapace and plastron): implications for turtle systematics, functional morphology and turtle origins. In: Mathematisch-Naturwissenschaftlichen Fakultät, Institut für Paläontologie. Bonn: Rheinischen Friedrich- Wilhelms-Universität Bonn. p 343 [URN: http://nbn-resolving.de/ urn: nbn:de:hbz:5N-12299; URL: http://hss.ulb. uni-bonn.de/diss-online/math-nat- fak/2007/ scheyer-torsten].
77. Scheyer TM, Anquetin J. 2008. Bone histology of the Middle Jurassic turtle shell remains from Kirtlington, Oxfordshire, England. Lethaia 41:85-96. (Pubitemid 351247514)
78. Scheyer TM, Brüüllmann 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 269:1008-1021.
79. Schumacher GH. 1972. Die Kopf- und Halsregion der Lederschildkröte Dermochelys coriacea (LINNEAUS 1766)- Anatomische Untersuchungen im Vergleich zu anderen rezenten Schildkrö-ten-Mit 7 Figuren im Text und 31 Tafeln. Berlin: Akademie-Verlag.
80. Schumacher GH. 1973. The head muscles and hyolaryngeal skeleton of turtles and crocodilians. In: Gans C, editor. Biology of the reptilia. New York:Academic Press. p 101-199.
81. Schwarz AH. 2006. Keeping and breeding the redbelly shortneck turtle, Emydura subglobosa. Reptilia (GB) 45:62-65.
82. Sellier N, Brillard J-P, Dupuy V, Bakst MR. 2006. Comparative staging of embryo development in chicken, turkey, duck, goose, Guinea fowl, and Japanese quail assessed from five hours after fertilization through seventy-two hours of incubation. J Appl Poultry Res 15:219-228.
83. Shah RV. 1963. The neck musculature of a cryptodire (Deirochelys) and a pleurodire (Chelonida) compared. Bull Mus Comp Zool 129:343-368.
84. Sheil CA. 2003. Osteology and skeletal development of Apalone spinifera (Reptilia: Testudines:Trionychidae). J Morphol 256:42-78.
85. Sheil CA. 2005. Skeletal development of Macrochelys temminckii (Reptilia: Testudines: Chelydridae). J Morphol 263:71-106.
86. Sheil CA, Greenbaum E. 2005. Reconsideration of skeletal development of Chelydra serpentina (Reptilia: Testudinata: Chelydridae): evidence for intraspecific variation. J Zool Lond 265:235-267.
87. Smith KK. 1997. Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 51:1663-1678.
88. Tokita M, Kuratani S. 2001. Normal embryonic stages of the Chinese softshelled turtle Pelodiscus sinensis (Trionychidae). Zool Sci 18:705-715. (Pubitemid 33398203)
89. Tzika A, Milinkovitch MC. 2008. A pragmatic approach for selecting evo-devo model species in amniotes. In: Minelli A, Fusco G, editors. Evolving pathways. Key themes in evolutionary developmental biology. Cambridge: Cambridge University Press.
90. Vallois HV. 1922. Les transformationes de la musculature de l'episome chez les vertébrés. Arch Morphol Gen Exp.
91. Velhagen WA Jr. 1997. Analyzing developmental sequences using sequence units. Systemat Biol 46:204-210.
92. Vieira LG, Santos ALQ, Lima FC. 2007. Ontogeny of scleral ossicles of giant amazon river turtles Podocnemis expansa Schweigger, 1812 (Testudines, Podocnemididae). Braz J Morphol Sci 24:220-223.
93. Vieira LG, Santos ALQ, Lima FC, Pinto JGS. 2009. Ontogeny of the plastron of the giant amazon river turtle, Podocnemis expansa (Schweigger, 1812) (Testudines, Podocnemididae). Zool Sci 26:491-495.
94. Weisbecker V, Goswami A, Wroe S, Sánchez- Villagra MR. 2008. Ossification heterochrony in the mammalian postcranial skeleton and the marsupial-placental dichotomy. Evolution 62:2027-2041.
95. Werneburg I. 2009. A standard system to study vertebrate embryos. PLoS One 4:e5887 [DOI: 10.1371/journal.pone. 0005887].
96. Werneburg I, Sánchez-Villagra MR. 2009. Timing of organogenesis support basal position of turtles in the amniote tree of life. BMC Evol Biol 9:82 [DOI: 10.1186/ 1471-2148-9-82].
97. Yntema CL. 1968. A series of stages in the embryonic development of Chelydra serpentina. J Morphol 125:219-251.
98. Zangerl R. 1969. The Turtle Shell. In: Bellairs Ad'A, Parson TS, editors. Biology of the Reptilia. Morphology A. London and New York: Academic Press. pp 311-339.
99. Ziermann JM. 2008. Evolutionäre Entwicklung larvaler Cranialmuskulatur der Anura und der Einfluss von Sequenzheterochronien. In: Biologisch- Pharmazeutische Fakultät. Jena: Friedrich-Schiller- Universität. p 347.