Turtles as hopeful monsters

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What the papers say Figure 3. The relationship of the shoulder blade to the carapace in turtles (Graptemys geographica). later developmental stages. In the turtle carapace, therefore, the distinction of endoskeleton versus exoskeleton becomes problematic. It had been recognized earlier that the endoskeleton versus exoskeleton cannot be distinguished on the basis of histogenesis, but must be defined with reference to a phylogenetic framework. (17,18) Exoskeletal elements are homologous to structures that in the ancestral condition combine bone, dentine and enamel, i.e., develop at the ectoderm±mesoderm interface. Thus, the bony scales of a trout, or the osteoderms of a crocodile, are exoskeletal, because these are structures that ultimately can be traced back (are homologous) to the heavy scales of early fishes that combine bone, dentine and enamel in a three-layered scale. By contrast, endoskeletal elements are elements that in the ancestral condition are preformed in cartilage, while the cartilaginous stage may be deleted in the descendant (membrane bone). In the turtle carapace, the neural and costal plates ossify from, and in continuity with, the periost of their endoskeletal component. This pattern of ossification corresponds to the definition of Zuwachsknochen, (18) i.e., bone that complements an endoskeletal element that is itself preformed in cartilage. As such, neural and costal plates are endoskeletal components of the turtle carapace, and cannot be derived from a hypothetical ancestral condition by fusion of exoskeletal osteoderms. All other parts of the turtle carapace are exoskeletal, however. The origin of a new body plan The turtle body plan is evidently highly derived, indeed unique among tetrapods. The problem for an evolutionary biologist is to explain these transformations in the context of a gradualistic process. Given the recently obtained developmental evidence, (1,11,13) the theory of ``correlated progression'' (10) presents an incomplete explanation of the turtle body plan: formation of the carapace is not simply the consequence of a fusion of osteoderms, and the location of the scapula inside the rib cage is not the result of a backward migration of the pectoral girdle. Early in the 19th century, EÂ tienne Geoffroy Saint-Hilaire raised the question of how the lung of a reptile could be transformed into the lung of a bird? He found it impossible to postulate that the lung of a reptile, specialized in its own way, could transform into an even more specialized lung of a bird. But he recognized that both reptiles and birds share similar early embryonic rudiments of the lung, and he hypothesized that these could develop along different trajectories in the two groups due to a minor change in early ontogenetic development: ``It only required an `accident' [a change] that 990 BioEssays 23.11
What the papers say is viable and of small magnitude in its origin, but which could be of unpredictable importance with respect to its effects''. (19) The same can be said with respect to the axial skeleton of turtles. The initial segmentation of the paraxial mesoderm is the same in turtles as in all other tetrapods, but further development of structures derived from the somites (dermis, vertebrae and ribs) proceeds along a different trajectory in turtles compared to all other tetrapods. Ribs can only be located either deep to, or superficial to, the scapula. There are no intermediates, and there is only one way to get from one condition to the other, which is the redirection of the migration, through the embryonic body, of the precursor cells that will form the ribs. The study of such complex problems as the evolution of the turtle body plan highlights the important role that development can play in the origin of evolutionary novelties. References 1. Gilbert SF, Loredo GA, Brukman A, Burke AC. Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution. Evol Dev 2001;3:47±58. 2. Hay OP. On Protostega, the systematic position of Dermochelys, and the morphogeny of the chelonian carapace and plastron. Amer Nat 1898;32:929±948. 3. Kaelin J. Zur Morphogenese des Panzers bei den SchildkroÈten. Acta Anat 1945;1:144±176. 4. ValleÂn E. BeitraÈge zur Kenntnis der Ontogenie und der vergleichenden Anatomie des SchildkroÈtenpanzers. Acta Zool Stockholm 1942;23:1± 127. 5. VoÈlker H. UÈ ber das Stamm- Gliedmassen-, und Hautskelett von Dermochelys coriacea L. Zool Jb Anat 1913;33:431±552. 6. Zangerl R. The homology of the shell elements in turtles. J Morphol 1939;65:383±406. 7. Zangerl R. The turtle shell. In: Gans C, Bellairs Ad'A, Parsons TS, editors. Biology of the Reptilia Vol. 1, London: Academic Press; 1969.p. 311± 339. 8. Versluys J. UÈ ber die Phylogenie des Panzers der SchildkroÈten und uÈber die Verwandtschaft der LederschildkroÈte (Dermochelys coriacea). PalaÈont. Z 1914;1:321±347. 9. Gaffney ES. The comparative osteology of the Triassic turtle Proganochelys. Bull. Amer Mus Nat Hist 1990;194:1±263. 10. Lee MSY. Correlated progression and the origin of turtles. Nature 1996;379:811±815. 11. Burke AC. The development and evolution of the turtle body plan: inferring intrinsic aspects of the evolutionary process from experimental embryology. Amer Zool 1991;31:616±627. 12. Ruckes H. Studies in chelonian osteology. Part II. The morphological relationships between girdles, ribs and carapace. Ann NY Acad Sci 1929;31:81±120. 13. Burke AC. Development of the turtle carapace: implications for the evolution of a novel bauplan. J. Morphol 1989;199:363±378. 14. Yntema CL. Extirpation experiments on the embryonic rudiments of the carapace of Chelydra serpentina. J Morphol 1970;132:235±244. 15. Goette A. UÈ ber die Entwicklung des knoÈchernen RuÈckenschildes (Carapax) der SchildkroÈten. Z wiss Zool 1899;66:407±434. 16. Hoffstetter R, Rage J-C. Vertebrae and ribs of modern reptiles. In: Gans C, Bellairs Ad'A, Parsons TS, editors. Biology of the Reptilia Vol. 1 London: Academic Press; 1969. p. 201±310. 17. Patterson C. Cartilage bones, dermal bones and membrane bones, or the exoskeleton versus the endoskeleton. In: Andrews SM, Miles RS, Walker AD, editors. Problems in Vertebrate Evolution. London: Academic Press; 1977. p. 77±121. 18. Starck D. Vergleichende Anatomie der Wirbeltiere auf evolutionsbiologischer Grundlage, Vol 2 Berlin: Springer Verlag; 1979. 19. Geoffroy Saint-Hilaire E. Le deÂgreÂ d'influence du monde ambiant pour modiifier les formes animales; question inteÂressant l'origine des espeÂces teÂleÂosauriennes et successivement celle des animaux de l'eÂpoque actuelle. MeÂm Acad R Sci Inst. France 1833;12:63±92. (The quote is from p. 80). BioEssays 23.11 991
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