Abstract
Because of their unique morphology, turtles have raised profound questions as to their evolutionary origin. In striking contrast to the body plan of other tetrapods, the shoulder girdle of turtles sits inside the rib cage, which comprises the dorsal shell, or carapace. By this topological change of the skeletal elements, the carapace has been regarded as an example of evolutionary novelty that violates the ancestral body plan of tetrapods. In this chapter, we first overview the phylogenetic positioning of turtles, and then review how turtles evolved their unique body plan. In brief, three points have been clarified by recent studies. (1) Turtles have birds/crocodilians (or archosaurians) affinity of evolutionary origin. (2) During embryogenesis, the turtle also establishes the vertebrate basic body plan, as in other vertebrates, followed by the late developmental stages of generating turtle-specific structures, such as folding of the lateral body wall to make the apparent inside-out topology of shoulder girdle against ribs. (3) One of the causal factors of folding appears to be the concentric growth of carapacial margin, which involves an ancestral gene expression cascade in a new location. These reports allow us to hypothesize the stepwise, not necessarily saltatory, evolution of turtles, consistent with the recent finding of a transitional fossil animal, Odontochelys, that did not have the carapace but already possessed the plastron.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bhullar B-AS, Bever GS (2009) An archosaur-like laterosphenoid in early turtles (Reptilia: Pantestudines). Breviora 518:1–11
Burke AC (1989) Development of the turtle carapace: implications for the evolution of a novel bauplan. J Morphol 199:363–378
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
Burke AC (2009) Turtles……again. Evol Dev 11:622–624
Caspers GJ, Reinders GJ, Leunissen JA, Wattel J, de Jong WW (1996) Protein sequences indicate that turtles branched off from the amniote tree after mammals. J Mol Evol 42:580–586
Chen Z-Q, Benton MJ (2012) The timing and pattern of biotic recovery following the end-Permian mass extinction. Nat Geosci 5:375–383
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 8:783–786
Damiani RJ, Modesto JP (2001) The morphology of the pareiasaurian vomer. N Jb Geol Paläont Mh 7:423–434
Duboule D (1994) Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate bauplan and the evolution of morphologies through heterochrony. Development (Camb) 1994:135–142
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
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, Boca Raton, pp 1–16
Hall BK (1998) Evolutionary developmental biology, 2nd edn. Chapman & Hall, London
Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92
Hedges SB (2012) Amniote phylogeny and the position of turtles. BMC Biol 10:64
Hedges SB, Moberg KD, Maxson LR (1990) Tetrapod phylogeny inferred from 18S and 28S ribosomal RNA sequences and a review of the evidence for amniote relationships. Mol Biol Evol 7:607–633
Irie N, Kuratani S (2011) Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat Commun 2:248
Kawashima-Ohya Y, Narita Y, Nagashima H, Usuda U, Kuratani S (2011) Hepatocyte growth factor is crucial for development of the carapace in turtles. Evol Dev 13:260–268
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
Kuratani S, Kuraku S, Nagashima H (2011) Evolutionary developmental perspective for the origin of the turtles: the folding theory for the shell based on the developmental nature of the carapacial ridge. Evol Dev 13:1–14
Li C, Wu X, Rieppel O, Wang L, Zhao L (2008) An ancestral turtle from the Late Triassic of southwestern China. Nature (Lond) 45:497–501
Lyson TR, Sperling EA, Heimberg AM, Gauthier JA, King BL et al (2012) MicroRNAs support a turtle + lizard clade. Biol Lett 8:104–107
Merck JW (1997) A phylogenetic analysis of the euryapsid reptiles. Unpublished Ph.D. dissertation, University of Texas at Austin
Müller J (2003) Early loss and multiple return of the lower temporal arcade in diapsid reptiles. Naturwissenschaften 90:473–476
Müller J, Sterli J, Anquetin J (2011) Carotid circulation in amniotes and its implications for turtle relationships. N Jb Geol Paläont Abh 261:289–297
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
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 (Camb) 134:2219–2226
Nagashima H, Sugahara F, Takechi 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
Nagashima H, Kuraku S, Uchida K, Kawashima-Ohya Y, Narita Y, Kuratani S (2012a) Body plan of turtles: an anatomical, developmental and evolutionary perspective. Anat Sci Int 87:1–13
Nagashima H, Kuraku S, Uchida K, Kawashima-Ohya Y, Narita Y, Kuratani S (2012b) Origin of the turtle body plan: the folding theory to illustrate turtle-specific developmental repatterning. In: Brinkman DB, Holroyd PA, Gardner JD (eds) Morphology and evolution of turtles: origin and early diversification. Springer, Dordrecht
Nelson WJ, Nusse R (2004) Convergence of Wnt, β-catenin, and cadherin pathways. Science 303:1483–1487
Ohya YK, Kuraku S, Kuratani S (2005) Hox code in embryos of Chinese soft-shelled turtle Pelodiscus sinensis correlates with the evolutionary innovation in the turtle. J Exp Zool 304B:107–118
Ohya YK, Usuda R, Kuraku S, Nagashima H, Kuratani S (2006) Unique features of Myf-5 in turtles: nucleotide deletion, alternative splicing and unusual expression pattern. Evol Dev 8:415–423
Raff A (1996) The shape of life: genes, development, and the evolution of animal form. University of Chicago Press, Chicago
Rieppel O (2000) Turtles as diapsid reptiles. Zool Scr 29:199–212
Rieppel O (2001) Turtles as hopeful monsters. Bioessays 23:987–991
Rieppel O, de Braga M (1996) Turtles as diapsid reptiles. Nature (Lond) 384:453–455
Romer AS (1956) Osteology of the reptiles. University of Chicago Press, Chicago
Shaffer HB, Minx P, Warren DE, Shedlock AM, Thomson RC, Valenzuela N 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:R28
Tokita M, Kuratani S (2001) Normal embryonic stages of the Chinese soft-shelled turtle Pelodiscus sinensis. Zool Sci 18:705–715
Tsuji LA, Müller J (2009) Assembling the history of the Parareptilia: phylogeny, diversification, and a new definition of the clade. Fossil Rec 12:71–81
Wang Z, Pascual-Anaya J, Zadissa A, Li W, Niimura Y, Huang Z 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. doi:10.1038/ng.2615
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Japan
About this chapter
Cite this chapter
Irie, N., Nagashima, H., Kuratani, S. (2014). The Turtle Evolution: A Conundrum in Vertebrate Evo-Devo. In: Kondoh, H., Kuroiwa, A. (eds) New Principles in Developmental Processes. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54634-4_23
Download citation
DOI: https://doi.org/10.1007/978-4-431-54634-4_23
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-54633-7
Online ISBN: 978-4-431-54634-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)