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Caudata show the plesiomorphic pattern of an early forelimb contra a late hind limb development. But compared to other caudates like Necturus [ 55 ] or Andrias [ 56 ] the axolotl obviously exhibits a delayed development of limbs during maturation [ 51 ]. When discussing the development of the limbs within Amniota this should be kept in mind.

Phylogenetic breadth in the sampling of published information was chosen based on the extent of existing descriptions and the quality of illustrations Table S1. For the echidna, Tachyglossus aculeatus , the staging system of Semon [ 57 ] was used. To expand this information, we examined 21 embryo photographs and drawings of this species Hubrecht collection, Berlin [ 58 ] and ordered them chronologically by the number of somites Table S3.

All taxa analysed are listed in Table S1. Each major tetrapod clade is represented by one species, except for Cryptodira, represented by 14 species Figures 4 and S3. With this in mind we should be careful not to overinterpret character changes [ 29 ]. For example, our preliminary and cautious interpretation on the evolution of the neck length in Testudines vs.

Eastern box turtle | Smithsonian's National Zoo

Sauria could be refuted by including pleurodire turtles with shorter necks Pelomedusidae or birds with elongated necks Struthioniformes. Our examination of the embryology of sensory characters could be extended by including mammal and bird species of nidicolous as well as nidifugous behaviour. Also the ground pattern of neck length and flight behaviour in these groups should be addressed.

When including taxa of different body shape the results could still remain similar to ours and the functional explanations should be rethought. Examples of excluded characters are the shape and development of pigmentation, detailed carapace or scale differentiations — all characters important for staging prehatching embryos of a particular species.

Although pigmentation and colouration are mentioned in most staging tables, some authors refer to first occurrence of pigment cells that are hard to see in photographs and in embryos that have been fixed for a long time. Other authors call an organ "pigmented" when the organ is completely "dark".

In most cases we were not able to interpret the drawings and photographs as mentioned in the descriptions based on their different quality and the subjective view and approach of each author. We also refrained from listing every single somite number because there is high variability in the formation of the mesodermal segments. The presented definition of clusters, five somites each, serves to reflect the variance of somite development but is also an example of subjectivity in character definition — an unavoidable limitation of any morphological study of this kind.

In literature the forelimb development is usually better documented, because in general a more or less simultaneous development of fore- and hind limb is observable as we experienced when observing both limbs.


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When defining events for the limb development we either discuss both limbs separately or only the forelimb was discussed. If there had been an unrecorded "abnormal" temporal shift between fore- and hind limb in one particular species, it would have only reflected a derived feature of this species and would be useless for the approach of this study.

Whereas Gaffney and Meylan [ 59 ] and Shaffer et al. Trionychia are represented in our study Figures 1c and S2c. The interrelationships of the Testudinoidea swamp turtles and tortoises and Trionychia species that we included in our analysis are widely accepted and follow Gaffney and Meylan [ 59 ]. Within Chelonioidea, Dermochelys is generally considered to be the sister group of all remaining marine turtle taxa [ 63 ]; given conflicts of morphological and molecular data [ 64 ], we set Chelonioidea excl. Dermochelys as unresolved for all analyses Figures 4 and S3.

Lee MSY: Correlated progression and the origin of turtles. Meyer A, Zardoya R: Recent advances in the molecular phylogeny of vertebrates. Annual Review of Ecology, Evolution, and Systematics. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin. Joyce WG: Phylogenetic relationships of Mesozoic turtles. Bulletin of the Peabody Museum of Natural History. Lee MSY: Molecules, morphology, and the monophyly of diapsid reptiles.

Contributions to Zoology. Bulletin of the American Museum of Natural History. Molecular Biology and Evolution. Rieppel O: Studies on skeleton formation in reptiles: implications for turtle relationships. Rieppel O, deBraga M: Turtles as diapsid reptiles. Hill RV: Integration of morphological data sets for phylogenetic analysis of Amniota: the importance of integumentary characters and increased taxonomic sampling.

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How turtle shells evolved... twice - Judy Cebra Thomas

Werneburg I: A standard system to study vertebrate embryos. PLoS One. BMC Evolutionary Biology. Phylogenetische Systematik der Wirbeltiere. Friedrich Pfeil. Schoch RR: Skull ontogeny: developmental patterns of fishes conserved across major tetrapod clades. Journal of Anatomy.

Germain D, Laurin M: Evolution of ossification sequences in salamanders and urodele origins assessed through event-pairing and new methods. Smith KK: Heterochrony revisited: the evolution of developmental sequences. Biological Journal of the Linnean Society. Lee MSY: The homologies and early evolution of the shoulder girdle in turtles. Zoological Journal of the Linnean Society.

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Rieppel O: The structure and development of the jaw adductor musculature in the turtle Chelydra serpentina. Developmental Dynamics. Journal of Morphology. Proc Biol Sci. Smith KK: Comparative patterns of craniofacial development in eutherian and metatherian mammals. Version 2. Version 4. Homepage of Olaf R. Bininda-Emonds, currently. Wiens JJ: Character analysis in morphological phylogenetics: Problems and solutions. Velhagen WA: Analyzing developmental sequences using sequence units.

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American Naturalist. Theory Biosci. Journal of Mammalian Evolution. Developmental biology of the Axolotl. Kleinteich T: Cranial musculature in the larva of the caecilian, Ichthyophis kohtaoensis Lissamphibia: Gymnophiona. Gosner KL: A simplified table for staging anuran embryos and larvae with notes on identification.

Semon R: Zur Entwickelungsgeschichte der Monotremen. Denkschriften der Medicinisch-Naturwissenschaftlichen Gesellschaft zu Jena. Edited by: Benton MJ. Molecular Phylogenetics and Evolution. Jamniczky HA: Turtle carotid circulation: a character analysis case study. Hirayama R: Phylogenetic systematics of chelonioid sea turtles. The Island Arc. Vertebrate Zoology. Download references.

Biology of Turtles: From Structures to Strategies of Life

We thank Olaf R. Scheyer, Vera Weisbecker, Laura A. Wilson, and Janine M. Correspondence to Ingmar Werneburg.

Electronic supplementary material

This article is published under license to BioMed Central Ltd. Reprints and Permissions. Search all BMC articles Search. Abstract Background The phylogenetic position of turtles is the most disputed aspect in the reconstruction of the land vertebrate tree of life. Results The timing of events in organogenesis of diverse character complexes in all body regions is not uniform across amniotes and can be analysed using a parsimony-based method. Conclusion The clear signal of a basal position of turtles provided by heterochronic data implies significant convergence in either molecular, adult morphological or developmental timing characters, as only one of the alternative solutions to the phylogenetic conundrum can be right.

Background The controversial phylogenetic position [ 1 — 5 ] of turtles among land vertebrates and their highly derived anatomical features [ 6 — 8 ] have been subject of molecular and morphological investigations. Figure 1. Full size image. Figure 2. Results and discussion The turtle-saurian relationship is clearly the best supported hypothesis using Parsimov [ 19 ], independent of which hypothesis of inner turtle phylogeny is taken as reference.

Figure 3. Figure 4. Conclusion The embryological data and their analysis presented here are in agreement with a basal position of turtles instead of one nested within a saurian clade. Methods Analyses of sequence heterochrony The key methodology for a comparative analysis of developmental sequence data is 'event-pairing' [ 37 ]. Procedures implemented in the analysis The procedures of the heterochrony analysis follow in general Jeffery et al.

On the use of ordered vs. Treatment of event simultaneity The issue of how to treat events scored as simultaneous has been discussed before [ 43 — 47 ]. Taxonomic sampling As an outgroup to all observed amniotes we have chosen the axolotl, Ambystoma mexicanum , based on detailed and comparative description of its developmental stages [ 50 , 51 ]. Remarks on characters excluded from the heterochrony analysis Examples of excluded characters are the shape and development of pigmentation, detailed carapace or scale differentiations — all characters important for staging prehatching embryos of a particular species.

Alternative hypotheses of cryptodire relationships Whereas Gaffney and Meylan [ 59 ] and Shaffer et al. References 1. Article Google Scholar 5. Google Scholar 6. Article Google Scholar 7. Article Google Scholar Google Scholar Article PubMed Google Scholar Friedrich Pfeil Google Scholar Google Scholar Download references. Acknowledgements We thank Olaf R. Electronic supplementary material Additional file 1: Supplementary Information. PDF 4 MB. Additional file 2: turtles. Nexus data file containing the event paired matrix for all observed species open i.

Based on the rank table Table S4 , the event pairs were generated with eventpairsim. With its miserly metabolism and tranquil temperament, its capacity to forgo food and drink for months at a time, its redwood burl of a body shield, so well engineered it can withstand the impact of a stampeding wildebeest, the turtle is one of the longest-lived creatures Earth has known. Individual turtles can survive for centuries, bearing silent witness to epic swaths of human swagger. Last March, a giant tortoise named Adwaita said to be as old as years died in a Calcutta zoo, having been taken to India by British sailors, records suggest, during the reign of King George II.

In June, newspapers around the world noted the passing of Harriet, a Galapagos tortoise that died in the Australia Zoo at age — years after Charles Darwin is said, perhaps apocryphally, to have plucked her from her equatorial home. Christopher J. Raxworthy, the associate curator of herpetology at the American Museum of Natural History, says the liver, lungs and kidneys of a centenarian turtle are virtually indistinguishable from those of its teenage counterpart, a Ponce de Leonic quality that has inspired investigators to begin examining the turtle genome for novel longevity genes.

Raxworthy said. Turtles have the power to almost stop the ticking of their personal clock. George Zug, curator of herpetology at the Smithsonian Institution. Turtles resist growing old, and they resist growing up. Zug and his co-workers recently determined that among some populations of sea turtles, females do not reach sexual maturity until they are in their 40s or 50s, which Dr.

Turtles are also ancient as a family.

The noble chelonian lineage that includes all living turtles and tortoises extends back million years or more, possibly predating other reptiles like snakes and crocodiles, as well as birds, mammals, even the dinosaurs. Yet the clan has evolved a dazzling array of variations on its blockbuster theme, allowing it to colonize every continent save Antarctica and nearly every type of biome nested therein: deserts; rainforests; oceans; rivers; bogs; mountains; New Brunswick, Canada; New Brunswick, N.

Whitfield Gibbons, a professor of ecology at the University of Georgia in Athens. Troubles Foreseen. The iconic turtle likewise has colonized the human heart. People may despise cats or fear dogs, but practically everybody has a soft spot for turtles. Yet such warm and fuzzy feelings have proved cold comfort for turtles, and herpetologists fear that in humans the stalwart survivors from the Mesozoic era may at last have met their mortician.

Turtle habitats are fast disappearing, or are being fragmented and transected by roads on which millions of turtles are crushed each year. Gibbons said. Researchers estimate that at least half of all turtle species are in serious trouble, and that some of them, like the Galapagos tortoise, the North American bog turtle, the Pacific leatherback sea turtle and more than a dozen species in China and Southeast Asia, may effectively go extinct in the next decade if extreme measures are not taken.

Cover said. Box turtles and other forest-dwelling species can spot a lake or pond a mile in the distance, possibly by detecting polarized light glinting off the surface of the water. Female sea turtles migrate across entire oceans every breeding season, unerringly making their way from far-flung feeding grounds right back to the beach where they were born, and where they are instinctively driven to lay their own eggs.

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Timing of organogenesis support basal position of turtles in the amniote tree of life

View all New York Times newsletters. Instinctive does not mean inflexible, however. Should a weary wayfarer arrive at her natal beach in the dead of night and find it has eroded away, Dr. Pritchard said, she can adapt, swimming down the coast until she locates a suitably sandy nesting site. Turtles, it seems, are all ears, all the time.

There is the Indian star tortoise, its shell a vivid basket weave of dark and light veins that dance like spattered sunlight as the tortoise crosses the forest floor; and the Matamata turtle of the Amazon basin, with a flattened, ragged head and neck that look like dead leaves and a bumpy shell that mimics an old log — just try to spot that Matamata at the bottom of a stream, awaiting passing prey; and the massive alligator snapping turtle of the south-central United States, which lures fish right into its open jaw with a red bleb of flesh on the floor of its mouth that jiggles like a chubby worm.

Among the most common questions leveled at turtle researchers is, What is the difference between a turtle and a tortoise? It depends on where you live, researchers reply. In the United States, any reptile with a shell is referred to as a turtle, and the term tortoise is reserved for those turtle species that have elephantine feet and live entirely on land, like the desert tortoise of the American Southwest.

Whatever their group identity badge, turtles vary considerably in size, from the tiny speckled padloper tortoise of South Africa, which in adulthood is no bigger than a computer mouse, to the great leatherback sea turtle, which can measure seven feet long and weigh 2, pounds. Menu plans vary as well.


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Many turtles are omnivores, happily consuming fruits, leaves, insects, mollusks, fish, frogs, ice cream. Gibbons told of a friend whose his pet box turtle would respond to the sound of a spoon being tapped on a glass ice cream bowl by emerging from behind the couch, walking over to its owner, rearing up on its hind legs and waiting to be spoon-fed its just dessert.