Morphogenetic and constructional differences of the carapace of aquatic and terrestrial turtles and their evolutionary significance

The postembryonic development of the turtle carapace was studied in the aquatic Еmys orbicularis and the terrestrial Тestudo graeca. Differences in the structure of the bony shell in aquatic and terrestrial turtles were shown to be associated with varying degrees of development of epidermal derivatives, namely, the thickness of the scutes and the depth of horny furrows. Sinking of the horny furrows into the dermis causes local changes in the structure of the collagen matrix, which might precondition the acceleration of the ossification. Aquatic turtles possess a relatively thin horny cover, whose derivatives are either weakly developed or altogether absent and thus make no noticeable impact on the growth dynamics of bony plates. Carapace plates of these turtles outgrow more or less evenly around the periphery, which results in uniform costals, relatively narrow and partly reduced neurals, and broad peripherals extending beyond the marginal scutes. In terrestrial turtles (Testudinidae), horny structures are much more developed and exert a considerable impact on the growth of bony elements. As a result, bony plates outgrow unevenly in the dermis, expanding fast in the zones under the horny furrows and slowly outside these zones. This determines the basic features of the testudinid carapace: alternately cuneate shape of costals, an alternation of broad octagonal and narrow tetragonal neurals, and the limitation of the growth of peripherals by pleuro-marginal furrows. The evolutionary significance of morphogenetic and constructional differences in the turtle carapace, and the association of these differences with the turtle habitats are discussed.     

A thin-shelled reptile from the Late Triassic of North America and the origin of the turtle shell

A new, thin-shelled fossil from the Upper Triassic (Revueltian: Norian) Chinle Group of New Mexico, Chinlechelys tenertesta, is one of the most primitive known unambiguous members of the turtle stem lineage. The thin-shelled nature of the new turtle combined with its likely terrestrial habitat preference hint at taphonomic filters that basal turtles had to overcome before entering the fossil record. Chinlechelys tenertesta possesses neck spines formed by multiple osteoderms, indicating that the earliest known turtles were covered with rows of dermal armour. More importantly, the primitive, vertically oriented dorsal ribs of the new turtle are only poorly associated with the overlying costal bones, indicating that these two structures are independent ossifications in basal turtles. These novel observations lend support to the hypothesis that the turtle shell was originally a complex composite in which dermal armour fused with the endoskeletal ribs and vertebrae of an ancestral lineage instead of forming de novo. The critical shell elements (i.e. costals and neurals) are thus not simple outgrowths of the bone of the endoskeletal elements as has been hypothesized from some embryological observations.     

Nature of the turtle shell: Morphogenetic causes of bone variability and its evolutionary implication

The turtle shell is characterized by a high degree of conservatism of the fundamental model and, at the same time, a high variability at the individual level. The components of the bony shell vary in origin. The costal and neural plates of the carapace are modified elements of the axial skeleton (ribs and neural arches) and the plastral plates are transformed dermal ossifications of the shoulder girdle and gastralia, peripheral, pygal, and suprapygal plates are similar to osteoderms of other reptiles. The variability of the structure of particular parts of the turtle shell is manifested differently. Most anomalies have been recorded in the caudal part of the carapace. The plastron is relatively stable in morphology. Variations in the bony shell structure are observed in (1) unusual shape and size of plates combined with normal number of plates, (2) presence of additional plates, and (3) absence of regular plates. Based on the morphogenetic characteris-tics, anomalies are subdivided into (1) variations caused by changes in the number of elements of the axial skeleton or their contacts with the dermis (neurals and costals); (2) variations due to changes in the number of horny scutes (peripherals); (3) variations connected with irregular osteogeny or disturbed growth of bones     

Chondrocranium and skeletal development of Phrynops hilarii (Pleurodira: Chelidae)

The present study represents the first comprehensive contribution to the knowledge of the skeletal development of a pleurodiran turtle, Phrynops hilarii (Pleurodira, Chelidae). The most remarkable features found are: (1) absence of ascending process on pterygoquadrate cartilage; (2) presence of ossification centres for the epiotics; (3) as in other pleurodirans, dorsal ribs IX and X are ‘sacralized’; (4) contact between ilium and carapace occurs later in ontogenetic development; (5) suture between ischia, pubes and plastron occurs in posthatching specimens; (6) contrary to previous interpretations, the phalangeal formula of the pes of P. hilarii is 2 : 3 : 3 : 3 : 5; (7) the hooked bone represents the fifth metatarsal.     

Studies on skeleton formation in reptiles: Patterns of ossification in the skeleton of Chelydra serpentina (Reptilia, Testudines)

Patterns and sequence of ossification are described throughout the skeleton of Chelydra serpentina Linnaeus. Evidence is adduced documenting the decoupling of ossification processes from sequence and patterns of chondrification. Convergence of ontogenetic repatterning in the ossification of the axial skeleton in Chelydra and Squamata is discussed, as are problems of adaptive modification of ossification patterns. The development of a carapace may be correlated with changes of ossification patterns in the postcranial axial skeleton of turtles, but the most striking evidence for the adaptive modification of ossification sequence obtains from a comparison of the limb skeleton and its ossification in Chelydra and in sea turtles     

Paradox segmentation along inter- and intrasomitic borderlines is followed by dysmorphology of the axial skeleton in the open brain (opb) mouse mutant

In open brain (opb) mutant embryos, developmental defects of the trunk spinal cord were spatially correlated with severe defects of the epaxial somite derivatives including sclerotomes, whereas hypaxial somite derivatives are much less affected. Later in development, the neural arches (epaxial sclerotome derivatives) formed but were severely disorganized, and also the distal ribs (hypaxial sclerotome derivatives) were malformed. Adjacent neural arches and vertebral bodies were often fused where joints should have formed suggesting defects of the intrasomitic borderlines. Moreover, neural arches frequently and ribs sometimes were split into halves at distinct levels along the dorso-ventral body axis. This suggests that ‘resegmentation’ of sclerotomes across the somite borders did not completely occur. These prominent skeletal defects were preceded by reduced expression of Pax1 along the intrasomitic borderlines, and incomplete maintenance of somite borders between central sclerotome moieties. The defects of the axial skeleton were accompanied by segmentation defects of the myotomes which were split distally, and also partly fused from adjacent segments across somite borders. The segmentation defects observed suggest that in opb mutants both segmental borderlines, the somite borders and the intrasomitic borderlines (fissures), were affected and behaved paradoxically. Dev. Genet. 22:359–373, 1998. © 1998 Wiley-Liss, Inc.     

Distinctive neural bones in Dipsochelys giant tortoises: Structural and taxonomic characters

The carapace of turtles consists of characteristic dermal bones (neurals, costal, and pleurals) and epidermal scutes. The variation in neural bone configuration in the Indian Ocean giant tortoise genus Dipsochelys is assessed. Study of 42 specimens supports earlier reports that variation is largely restricted to the anterior and posterior bones. Each species of Dipsochelys possesses a distinctive arrangement of neural bones. The configurations are related to the carapace shape with the relative width of the bones and interdigitating processes influencing structural stability. An exceptional configuration is described for the saddle‐backed species D. arnoldi, wherein this configuration arises from musculoskeletal adaptations for browsing in this species. J. Morphol. 240:33–37, 1999. © 1999 Wiley‐Liss, Inc.     

How the turtle forms its shell: a paracrine hypothesis of carapace formation

We propose a two-step model for the evolutionary origin of the turtle shell. We show here that the carapacial ridge (CR) is critical for the entry of the ribs into the dorsal dermis. Moreover, we demonstrate that the maintenance of the CR and its ability to attract the migrating rib precursor cells depend upon fibroblast growth factor (FGF) signaling. Inhibitors of FGF allow the CR to degenerate, with the consequent migration of ribs along the ventral body wall. Beads containing FGF10 can rearrange rib migration in the chick, suggesting that the CR FGF10 plays an important role in attracting the rib rudiments. The co-ordinated growth of the carapacial plate and the ribs may be a positive feedback loop (similar to that of the limbs) caused by the induction of Fgf8 in the distal tips of the ribs by the FGF10-secreting mesenchyme of the CR. Once in the dermis, the ribs undergo endochrondral ossification. We provide evidence that the ribs act as signaling centers for the dermal ossification and that this ossification is due to bone morphogenetic proteins secreted by the rib. Thus, once the ribs are within the dermis, the ossification of the dermis is not difficult to achieve. This relatively rapid means of carapace formation would allow for the appearance of turtles in the fossil record without obvious intermediates.     

化石闭壳龟的新发现

闭壳龟(Cuora)是龟科(Emydidae)中的一个现生属,有6个现生种,分布于东亚和东南亚,我国产4种。为该地区龟类动物中的一个小类群,以前未有化石发现。本文记述的是闭壳龟属的一个化石新种(Cuora pitheca,sp.nov.),时代为上新世早期。这是该属龟类的首次化石记录。它的发现,不仅把闭壳龟属的历史从现代推至上新世早期,并为探讨该龟类的进化和分布提供重要资料。     

湖北南漳早始新世的鳖类

本文记述了湖北南漳走马岭组上段的古鳖属—新种——沐浴古鳖 (Aspideretes muyuensis, sp. nov.),并对其分类位置和时代作了探讨.新种的主要特征是:背甲前、后缘平切;前椎板前部超出在第一对肋板内缘之前;第一对肋板与颈板之间有一对大的孔洞;椎板7块;肋板8对,最后两对在中线处左、右相遇;背甲纹饰较细小,腹甲表面光滑.     

放射纹蛇颈龟的新材料及其有关问题的探讨

放射纹蛇颈龟 (Plesiochelys radiplicatus) 系1953年杨钟健、周明镇所建,由一不完整的背甲和部分腹甲为代表.本文记述了一件可归该种的基本完整的背甲,补充了种的一些特征.并结合目前资料,对龟甲上的某些幼体特征,以及蛇颈龟类的系统分类和我国的蛇颈龟等问题,作了探讨.     

An integrative approach to examining a homology question: shell structures in soft‐shell turtles

Understanding the patterns of shell reduction in turtles is relevant when examining both fossils and living forms. The soft‐shelled turtles (Trionychidae) are characterized by the general reduction of the peripheral bony elements of the carapace, and some species possess structures of contested homology. By examining Remane's ‘principal criteria’, we addressed the primary homology of the prenuchal and the posterior peripheral ossicles (= PPOs) of the Asian flapshell turtles, Lissemys spp., thus evaluating their topological equivalence, their structural quality, and the presence of intermediate forms in ontogeny and phylogeny. We conducted an analysis of gross morphology, bone histology, and ontogeny of these elements in a large sample of living and fossil trionychids and their sister‐group, the carettochelyids. We conclude that the prenuchal comprises a neomorphic structure that does not fulfil any of the homology criteria examined. The assessment of the homology of PPOs is less straightforward because of the presence of partly conflicting evidence. Nevertheless, PPOs and standard peripherals share an antero‐posterior polarity of the ossification pattern, which we interpret as a significant shared underlying developmental pattern. Depending on the phylogenetic position of Lissemys in trionychid phylogeny, the hypothesis of PPOs homology with standard peripherals is a straightforward one or, alternatively, one involving homologous developmental processes at other levels of the hierarchy, resulting in similar microstructural characteristics of these bony shell features. In this respect, we consider the antero‐posterior polarity of the ossification pattern of both PPOs and standard peripherals as providing potential evidence for the homology of the genetic control regulating the expression of both these structures, and therefore we interpret these structures as homologues on the basis of a deeply homologous underlying developmental process. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 462–476.     

The complete mitochondrial genome sequences of <Emphasis Type="Italic">Chelodina rugosa</Emphasis> and <Emphasis Type="Italic">Chelus fimbriata</Emphasis> (Pleurodira: Chelidae): implications of a common absence of initiation sites (O<Subscript>L</Subscript>) in pleurodiran turtles

Within the order Testudines, while phylogenetic analyses have been performed on the suborder Cryptodira with complete mitochondrial genomes (mitogenomes), mitogenomic information from another important suborder Pleurodira has been inadequate. In the present study, complete mitochondrial DNA (mtDNA) sequences of two chelid turtles Chelodina rugosa and Chelus fimbriata were firstly determined, the lengths of which were 16,582 and 16,661 bp respectively. As the typical vertebrate mitogenome, both mtDNAs consist of 13 protein coding genes, 2 ribosomal RNAs (rRNAs), 22 transfer RNAs (tRNAs), and a long noncoding region (control region, CR). However, the initiation sites for light-strand replication (O_L), which has been identified in all reported Cryptodire mitogenomes, were not found in the putative position of the two chelid turtles and African helmeted turtle Pelomedusa subrufa. The results suggested that the absence of mitogenomic initiation sites (O_L) could be a characteristic of Pleurodira. Phylogenetic relationships of chelid turtles and other turtles were reconstructed using the reported mitogenomes. Both maximum likelihood (ML) and Bayesian inference (BI) analyses suggested the monophyly of Pleurodira and Cryptodira as well as a sister group relationship between the two chelid turtles with strong statistical support. This phylogenetic framework was also utilized to estimate divergence dates among lineages using relaxed-clock methods combined with fossil evidence. Divergence estimates revealed that genus Chelodina diverged from genus Chelus in Late Cretaceous (~83 million years ago (mya)), and the time is consistent with the vicariance of the fragments which was caused by Gondwana split.     

The Development and Evolution of the Turtle Body Plan: Inferring Intrinsic Aspects of the Evolutionary Process from Experimental Embryology

The body plan of turtles is unique among tetrapods in the presenceof the shell. The structure of the carapace involves a uniquerelationship between the axial and the appendicular skeletons.A common developmental mechanism, an epithelial-mesenchymalinteraction, has been identified in the early stages of carapacedevelopment by means of basic histological and immunofluorescencetechniques. By analogy to other structures initiated by epithelial-mesenchymalinteractions, it is hypothesized that carapace development isdependent on this interaction in the body wall. Surgical perturbationswere designed to test the causal connection between the epithelial-mesenchymalinteraction in the body wall and the unusual placement of theribs in turtles. By comparison to data available on body wallformation in avian embryos, these experiments also shed lighton the segregation of somitic and lateral plate cell populationsand the embryonic origin of the scapula in turtles. This study specifically addresses the ontogeny of a unique tetrapodbody plan. The ontogenetic information can be used to make inferencesabout the phytogeny of this body plan and how it could haveevolved from the more typical primitive tetrapod. On a moregeneral level this studyexplores the potential role of commondevelopmental mechanisms in the generation of evolutionary novelties,and the developmental incongruities between homologous skeletalelements in different groups of tetrapods.     

Development of the carapacial ridge: implications for the evolution of genetic networks in turtle shell development

SUMMARY Paleontologists and neontologists have long looked to development to understand the homologies of the dermal bones that form the "armor" of turtles, crocodiles, armadillos, and other vertebrates. This study shows molecular evidence supporting a dermomyotomal identity for the mesenchyme of the turtle carapacial ridge. The mesenchyme of the carapace primordium expresses Pax3 , Twist1 , Dermo1 , En1 , Sim1 , and Gremlin at early stages and before overt ossification expresses Pax1 . A hypothesis is proposed that this mesenchyme forms dermal bone in the turtle carapace. A comparison of regulatory gene expression in the primordia of the turtle carapace, the vertebrate limb, and the vertebral column implies the exaptation of key genetic networks in the development of the turtle shell. This work establishes a new role for this mesodermal compartment and highlights the importance of changes in genetic regulation in the evolution of morphology.     

Evolutionary mechanisms of rib loss in anurans: a comparative developmental approach

ABSTRACT The presence of free ribs is presumed to be a primitive morphological character observed only in a few families of Recent anurans, whereas the absence of ribs has been considered to be a derived condition that is widespread within this order. A comparative study of rib development based on representatives of several anuran lineages (Alytes, Bombina, Bufo, Discoglossus, Hyla, Pelobates, Pelodytes, Rana, and Xenopus) reveals a previously undetected diversity of developmental features in the formation and interaction between neural arches and ribs. The absence of free ribs at premetamorphic or later stages is verified in some groups, but we present for the first time evidence of the existence of larval rib rudiments in others, both in the anterior (Rana, Hyla) and posterior (Bufo, Discoglossus, Pelobates) presacral regions. Heterochrony seems to have played a major role in the processes underlying rib reduction. The intracolumnar differences between anterior (V(2)-V(4)) and posterior (V(5)-V(8)) regions are based on perturbations in the timing of early differentiation. Furthermore, a clear shift in the relative timing of ossification among evolutionary lineages was detected. In this respect Xenopus has a highly derived condition. The use of the morphological character of "rib loss" in phylogenetic analyses must be reconsidered due to the different convergent developmental paths described here. The phylogenetic analysis of a "sequence units" matrix of rib development is compared with current anuran phylogenies. Some evolutionary information appears to be clearly present in the ontogenetic data of this "missing morphology," but its value for evolutionary inferences is rather limited.