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Squamates present a unique challenge to our understanding of dental evolution in amniotes because they are the only extant tooth-bearing group for which a ligamentous tooth attachment is considered to be absent. This has led to the assumption that mammals and crocodilians have convergently evolved a ligamentous tooth attachment, composed of root cementum, periodontal ligament, and alveolar bone, whereas squamates are thought to possess a single bone of attachment tissue that fuses teeth to the jaws. The identity and homology of tooth attachment tissues between squamates, crocodilians, and mammals have thus been a focal point of debate for decades. We provide a novel interpretation of the mineralized attachment tissues in two focal taxa in this debate, mosasaurids and snakes, and compare dental tissue histology with that of the extant crocodilian Caiman sclerops. We identify a periodontal ligament in these squamates that usually exists temporarily as a soft connective tissue anchoring each tooth to the alveolar bone. We also identify two instances where complete calcification of the periodontal ligament does not occur: in a durophagous mosasaur, and in the hinged teeth of fossil and modern snakes. We propose that the periodontal ligament rapidly calcifies in the majority of mosasaurids and snakes, ankylosing the tooth to the jaw. This gives the appearance of a single, bone-like tissue fusing the tooth to the jaw in ankylosed teeth, but is simply the end stage of dental tissue ontogeny in most snakes and mosasaurids., (© 2017 Anatomical Society.)

Background: Lepidosauria (lizards, snakes, tuatara) is a globally distributed and ecologically important group of over 9,000 reptile species. The earliest fossil records are currently restricted to the Late Triassic and often dated to 227 million years ago (Mya). As these early records include taxa that are relatively derived in their morphology (e.g. Brachyrhinodon), an earlier unknown history of Lepidosauria is implied. However, molecular age estimates for Lepidosauria have been problematic; dates for the most recent common ancestor of all lepidosaurs range between approximately 226 and 289 Mya whereas estimates for crown-group Squamata (lizards and snakes) vary more dramatically: 179 to 294 Mya. This uncertainty restricts inferences regarding the patterns of diversification and evolution of Lepidosauria as a whole., Results: Here we report on a rhynchocephalian fossil from the Middle Triassic of Germany (Vellberg) that represents the oldest known record of a lepidosaur from anywhere in the world. Reliably dated to 238-240 Mya, this material is about 12 million years older than previously known lepidosaur records and is older than some but not all molecular clock estimates for the origin of lepidosaurs. Using RAG1 sequence data from 76 extant taxa and the new fossil specimens two of several calibrations, we estimate that the most recent common ancestor of Lepidosauria lived at least 242 Mya (238-249.5), and crown-group Squamata originated around 193 Mya (176-213)., Conclusion: A Early/Middle Triassic date for the origin of Lepidosauria disagrees with previous estimates deep within the Permian and suggests the group evolved as part of the faunal recovery after the end-Permain mass extinction as the climate became more humid. Our origin time for crown-group Squamata coincides with shifts towards warmer climates and dramatic changes in fauna and flora. Most major subclades within Squamata originated in the Cretaceous postdating major continental fragmentation. The Vellberg fossil locality is expected to become an important resource for providing a more balanced picture of the Triassic and for bridging gaps in the fossil record of several other major vertebrate groups.

The rudimentary characteristic of the eyes of fossorial animals raises some questions regarding its evolution and functionality. Would these eyes result from atrophy or from stagnated development? How would its visual function work? Anatomical investigations of these organs are the fundamental preamble to answer those questions, which are still little explored by the literature. In this article we have studied anatomical aspects of the eyes of three species of fossorial reptiles, within the suborder Amphisbaena (Amphisbaena alba, Amphisbaena mertensi, Leposternon infraorbitale), as well as a species within the ophidian suborder (Typhlops brongersmianus). The minuscule eyes (1-2 mm diameter) were visualized through a scale, a translucent area which corresponds to the spectacle. This spectacle is a thinner and transparent scale, covering a conjunctival sac. The retrobulbar space was filled with the harderian gland. The eyes of Typhlops presented an oval shape, whereas Amphisbaena specimens presented cup-shaped eyes. In Amphisbaenian sclera is comprised of cartilage, while the thin sclera of Typhlops consists of connective tissue and striated muscle fibers. The retina presented all the typical layers found in vertebrates, regardless the species. The characteristics involved in the fossil adaptation of these species include: reduced size of the eyeball, rudimentary cornea, absence of the anterior chamber, presence of a complex iris-ciliary body, and lens with amorphous nucleate cells. The analysis of the eye morphology of these animals suggests that there might be a specific function concerning light perception., (2009 Wiley-Liss, Inc.)

Squamate reptiles are uniquely suited to study of evolution of reproductive mode and pattern of embryonic nutrition. Viviparous species have evolved from oviparous ancestors on numerous occasions, patterns of nutritional provision to embryos range widely from lecithotrophy, at one end of a continuum, to placentotrophy at the other, and structure and function of the maternal-embryonic relationship is highly constrained resulting in parallel evolutionary trajectories among taxa. Embryos of oviparous species primarily receive nourishment from yolk, but also mobilize a significant quantity of calcium from the eggshell. Most viviparous species also are predominantly lecithotrophic, yet all viviparous species are placentotrophic to some degree. Similarities in embryonic development and nutritional pattern between oviparous species and most viviparous species suggest that the pattern of nutrition of oviparous squamates is an exaptation for the evolution of viviparity and that placentotrophy and viviparity evolve concomitantly. The few species of squamates that rely substantially on placentotrophy have structural modifications of the interface between the embryo and mother that are interpreted as adaptations to enhance nutritional exchange. Recent studies have extended understanding of the diversity of embryonic nutrition and placental structure and have resulted in hypotheses for transitions in the evolution of placentotrophy, yet data are available for few species. Indirect tests of these hypotheses, by comparison of structural-functional relationships among clades in which viviparity has evolved, awaits further study of the reproductive biology of squamates.

Squamate reptiles represent an ideal group for studies of viviparity, because they have evolved this reproductive pattern frequently, relatively recently, and at low taxonomic levels. A phylogenetic approach shows particular promise in helping us interpret anatomical, physiological, and ecological diversity. This review summarizes four major categories of active investigation: (1) reproductive anatomy and physiology; (2) placental structure and function; (3) reproductive endocrinology; and (4) reproductive and physiological ecology. Evolutionary reconstructions suggest that on many occasions viviparity has evolved concomitantly with functional placentation, through reduction of the shell membrane and hormonal modifications that prolong gestation. Studies of placentotrophic clades as well as reproductively bimodal species offer great potential for explaining the evolution of viviparity and placentation. However, live-bearing squamates are reproductively diverse, and appear to have solved physiological problems associated with viviparity by a variety of mechanisms. Consequently, studies on one or a few squamate species appear increasingly unlikely to yield all-inclusive explanations. Future studies and analyses should abandon assumptions of universal physiological mechanisms and a single historical sequence, in favor of the documentation of diversity in phylogenetic and quantitative terms.

The occurrence, distribution and the possible cellular co-localizations of chromogranin A (CgA) and of two synthetic secretogranin II-peptides (SgIIC23-3 and SgIIC26-3) with several enteric neuropeptides and serotonin have been investigated immunohistochemically in turtles, lizards and snakes. The distribution of CgA-immunoreactivity was restricted only to the enteroendocrine cells in all the reptiles studied. SgII-immunoreactivity--absent in turtle--revealed nerve cells and fibers, besides enteroendocrine cells in lizard and snake guts. Moreover, the two antisera (C23-3 and C26-3) raised against the different regions of the SgII-molecule yielded distinct distribution patterns of immunoreactivity both in the lizard and snake organs. Small amounts of enteric serotonin cells co-stored CgA or SgIIC23-3 in lizards and snakes and only SgIIC26-3-peptide in snakes. CgA was found co-stored with somatostatin in a few enterocytes of the turtle duodenum. In the same gut segment of lizards and throughout the snake organ, neurotensin and the SgIIC23-3-peptide co-existed in a small number of endocrine cells. The pancreatic polypeptide-containing cells were devoid of immunoreactivity both for CgA and SgII. Bombesin immunopositive cells were absent throughout the intestines of the reptiles investigated. The above findings entirely support the heterogenous distribution of granins in neuroendocrine organs and tissues and also within the same neuroendocrine cell population. They further support the concept of a good conservation of granins during phylogeny.

The classical phylogeny of living reptiles pairs crocodilians with birds, tuataras with squamates, and places turtles at the base of the tree. New evidence from two nuclear genes, and analyses of mitochondrial DNA and 22 additional nuclear genes, join crocodilians with turtles and place squamates at the base of the tree. Morphological and paleontological evidence for this molecular phylogeny is unclear. Molecular time estimates support a Triassic origin for the major groups of living reptiles.

The intention of this review is to compare studies on the morphology and histology (light and electron microscopic) of ultimobranchial glands of various groups of reptiles. Moreover, experiments (including our investigations) on suppression or stimulation of the ultimobranchial gland are included. Adult reptiles possess one (on the left side) or two ultimobranchial glands (UBG). The UBG lie just anterior to the heart. Light as well as electron microscopically, the gland has been shown to contain follicles and cell cords (cell aggregates). The follicular epithelium is lined by simple cuboidal or pseudostratified columnar cells. Ciliated and goblet cells may be present in the follicular epithelia in some groups. The lumen may contain a colloid-like substance with desquamated cells or debris. The UBG of reptiles seem to be an active secretory organ with influence on calcium regulation. Other functions of calcitonin have also been suggested in reptiles for example in neurotransmission, in volume regulation, phosphate balance and promotion of bone calcification (at least in juveniles).

Coronal arteries were injected with lead carbonate suspension and with Indian ink and cleared preparations 150--300 mkm thick were made in 195 hearts of fish, amphibians and reptiles and studied roentgenographically. It was stated that in Chondrichthyes (shark, skate) and in Chondrostei (beluga, stellate sturgeon, sturgeon), as well as in alligator both compact and spongy myocardium of the cardiac ventricle possess blood vessels. In teleostei, amphibians and reptiles (except alligator) spongy myocardium is avascular and receives its nutrition from the ventricle. In view of the data on the presence of blood vessels in the spongy myocardium in some vertebrates, it is impossible to accept the theory suggested by Grant and Regnier according to which vessels in the heart walls appear only in connection with compactization of the myocardium. Vascularization of the spongy myocardium is closely connected with oxygen saturation of the blood flowing through the heart. When this saturation is not satisfactory, the spongy myocardium has blood vessels. In alligator, vascularization of the spongy myocardium is connected with the fact that the heart has four chambers and there are arterial and venous blood streams.

Submicroscopic structural peculiarities in the cornea are described in some reptiles (grass-snake, lizard, turtle). Certain stages in histogenesis of the grass-snake cornea are presented. Poor differentiation of epithelium and its resemblance to endothelium is demonstrated in the grass-snake cornea. In cytoplasm of cornea cells of lizard and turtle a high content of mitochondria is noted. Great majority of mitochondria compactly arranged in the middle part of cytoplasm provide the appearance of zones. There is a middle zone of mitochondrial arrangement, there are also two zones in cytoplasm (internal-perinuclear and peripheral) without mitochondria but with supporting structures.

Microdissectional studies on the kidneys of 24 reptilian species living in different habitats show that the relative length of the distal tubuli is higher in animals adapted to a limited water supply and to fresh-water basins, as compared to animals which have unlimited access to water. No regular changes in the length of proximal, intermediate and connective parts were observed. The increase in the length of the distal tubuli occurs simultaneously among different taxonomic groups of reptiles, indicating the existence of parallelism in evolution of their kidneys.

Vascularization of the spectacle or brille of the reptile was demonstrated by biomicroscopy, histology, fluorescein (in vivo), and Microfil silicone rubber (in situ) injections. This unusual vascularity provides new evidence for reassessment of the origin and development of this structure, and a useful tool with which to do so.

The brainstem reticular formation has been studied in 16 genera representing 11 families of reptiles. Measurements of Nissl-stained reticular neurons revealed that they are distributed along a continuum, ranging in length from 10 micrometer to 95 micrometer. Reticular neurons in crocodilians and snakes tend to be larger than those found in lizards and turtles. Golgi studies revealed that reticular neurons possess long, rectilinear, sparsely branching dendrites. Small reticular neurons (less than 31 micrometers length) possess fusiform or triangular somata which bear two or three primary dendrites. These dendrites have a somewhat simpler ramification pattern when compared with those of large reticular neurons ( greater than 30 micrometers length). Large reticular neurons generally possess perikarya which are triangular or polygonal in shape. The somata of large reticular neurons bear an average of four primary dendrites. The dendrites of reptilian reticular neurons ramify predominantly in the transverse plane and are devoid of spines or excrescences. The dendritic ramification patterns observed in the various repitilian reticular nuclei were correlated with known input and output connections of these nuclei. Nissl and golgi techniques were used to divide the reticular formation into seven nuclei. A nucleus reticularis inferior (RI) is found in the myelencephalon, a reticularis medius (RM) in the caudal two-thirds of the metencephalon, and a reticularis superior (RS) in the rostral metencephalon and caudal mesencephalon. Reticularis inferior can be subdivided into a dorsal portion (RID) and a ventral portion (RIV). All reptilian groups possess RID and RM but RIV is lacking in turtles. Reticularis superior can be subdivided into a large-celled lateral portion (RSL) and a small-celled medial portion (RSM). All reptilian groups possess RSM and RSL, but RSL is quite variable in appearance, being best developed in snakes and crocodilians. The myelencephalic raphe nucleus is also quite variable in its morphology among the different reptilian families. A seventh reticular nucleus, reticularis ventrolateralis (RVL), is found only in snakes and in teiid lizards. It was noted that the reticular formation is simpler (fewer numbers of nuclei) in the representative of older reptilian lineages and more complex (greater numbers of nuclei) in the more modern lineages. Certain reticular nuclei are present or more extensive in those families which have prominent axial musculature.

The taste buds in tortoises (Clemmys japonica and Geoclemys reevesii), lizards (Takydromus tachydromoides) and snakes (Elaphe quadrivirgata) were examined by both ultrastructural and histochemical methods. The taste buds consisted of at least three types of cells: the type I, II and III cells. The type I cells were characterized by the presence of secretory dense granules containing polysaccharides which were demonstrated by periodic acid-chromic acid-silver methenamine technique. The type II cells contained numerous tubular, vesicular and lamellated structures. The type III cells were characterized by dense cored vesicles and afferent synaptic contacts. Besides these cells, basally located cells which resembled the basal cells of other lower vertebrates were sometimes found in the tortoises. After administration of L-DOPA following nialamide, some taste bud cells of the tortoises, Clemmys japonica, showed weak yellowish green fluorescence by monoamine fluorescence histochemistry and the dense-cored vesicles in the type III cells increased in number. Acetylcholine esterase activity was not observed in tortoise taste buds. It is suggested that the three types of cells which compose the taste buds of the reptiles may correspond to the three types of cells in mammalian, and the type III cells represent the gustatory cells which are able to potentially produce biogenic monoamines. From these results, the taste buds of the reptiles may hold an intermediate position between those of mammals and amphibia or fishes.

Ascending spinal projections in the caiman (Caiman crocodilus) were demonstrated with Nauta and Fink-Heimer methods following hemisections of the third spinal segment in a series of twelve animals. These results were compared with earlier data in the literature obtained from a turtle, a snake, and a lizard using the same experimental and histological procedures. The results show remarkable similarities considering that each species represents a different reptilian order with different evolutionary history and habitat. However, the caiman displays several important peculiarities. Although the dorsal funiculus of the caiman contains the largest number of ascending spinal projections of the four species examined, this funiculus has not differentiated into cuneate and gracile fasciculi as is the case in the tegu lizard. The ventro-lateral ascending spinal projections follow a fundamentally similar general morphologic pattern in the four species with only minor variations. The anatomical arrangement in the caiman and tegu lizard appears most similar in the high cervical and the medullary regions; however, this is not the case in midbrain and thalamic regions where considerably more extensive projections are seen in the caiman. In the caiman an extensive spinal connection to the ventro-lateral nucleus of the dorsal thalamus is present; this connection is reminiscent of the mammalian spinal projection to the ventro-basal complex. The caiman has in common with the other three reptilian species a small projection to another dorsal thalamic region that is apparently homologous to the mammalian intralaminar nuclei, which are the destination of the mammalian paleospinothalamic tract.

The course and termination of the pathways descending from the brain stem to the spinal cord have been studied by tracing the ensuing anterograde fiber degeneration, following appropriate lesions in the reptiles Testudo hermanni, Tupinambis nigropunctatus and Python reticulatus. In these reptiles the presence of interstitiospinal, vestibulospinal and reticulospinal pathways has been demonstrated. A crossed rubrospinal tract has been shown in the turtle and lizard, but could not be demonstrated in the Python. The presence of a tectospinal pathway of any importance could not be shown. However, the tectum mesencephali has been found to project profusely to the brain stem reticular formation. The interstitiospinal tract projects predominantly to the ipsilateral side of the spinal cord. The vestibulospinal projection, arising from the large-celled nucleus vestibularis ventrolateralis, comprises a large uncrossed and a small decussating component. The rubrospinal pathway terminates in a particular area of the spinal gray, i.e., the intermediate zone, whereas the interstitiospainal, reticulospinal and vestibulospinal tracts all terminate in the medial part of the ventral horn. It appeared that the classification of descending pathways as advocated in mammals by Kuypers ('64) into lateral and medial systems can be readily applied to reptiles. The lateral system terminates in the dorsal and lateral parts of the intermediate zone, the medial system predominantely in the dorsomedial part of the ventral horn. This classification renders it likely that the absence of a lateral focus of termination as well as the absence of a rubrospinal tract in the Python, is correlated to the absence of limbs. A comparison of experimental data concerning the systems descending from the brain stem to the spinal cord in amphibians, reptiles, birds and mammals suggests that these systems with regard to origin, course and termination have a basic pattern in common.

Chromaffin, small granule-containing (SGC)-cells, neurons and the innervation of these cells was studied in the adrenal gland of three species of reptiles (Testudo graeca, Lacerta dugesi, Natrix natrix). 1. After fixation with glutaraldehyde and osmium-tetroxide adrenaline (A)- and noradrenaline (NA)-storing cells can be distinguished by means of the different electron density of their granules: A-granules are moderately electron-dense, while NA-granules show a core of high electron density. The unusually high electron density of a few A-granules in Testudo occasionally required viewing of unstained sections which facilitated the discrimination of the two cell types in this species. In all species studied NA-granules display a remarkable polymorphism which is most pronounced in the tortoise. In this species A-granules are polymorphic, too. Both types of granules show wide variations in size, which are particularly great in the tortoise. This species also exhibits the largest average sizes for A-granules (285 nm), and NA-granules (354 nm). The corresponding parameters for Lacerta and Natrix, are 255 and 179 nm for A- and 323 and 304 nm for NA-granules, respectively. The rough ER in A-cells of the tortoise regularly occurs in the form of circular dilations ('ergastosomes', Kanerva and Hervonen, 1973). Mitochondria sometimes contain longitudinal cristae with a crystalloid internal pattern. Large dense bodies which incorporate granules are abundant in NA-cells. Smaller dense bodies containing a few dense patches and membranes are present in both A- and NA-cells. Intermediate stages between dense bodies and what appear to be A- or NA-granules (if the latter have lost some of their amine-content) are frequently observed.

In the present study of the origin of the pathways descending from the brain stem to the spinal cord has been investigated in the reptiles Testudo hermanni, Pseudemys scripta elegans, Tupinambis nigropunctatus and Python reticulatus. These reptiles, using highly different types of progression, have been selected, because fundamental variations in the organization of the central motor apparatus are to be expected. The origin of the descending pathways has been demonstrated by recording the occurrence of retrograde cell changes following hemicordotomies and by searching for labeled cells following injection into the spinal cord of the enzyme horseradish peroxidase. In the reptiles studies the presence of interstitiospinal, vestibulospinal and reticulospinal pathways could be demonstrated. A crossed rubrospinal tract has been shown in the turtles and in the lizard, but could not be demonstrated in the Python. The presence of a direct tectospinal pathway could not be shown.

Morphometric measurements were made from serial sections of the vestibular system in four classes of vertebrates: Reptilia, Aves, Amphibia, and Pisces. Representative species of reptile studied were the lizard (Gekko gecko), the common garter snake (Thamnophis sp.), and the common turtle (Chelonia sp.). The budgie (Melopsittacus undulatas), the common pigeon (Columba domestica), the yellow-bellied sapsucker (Sphyrapicus varius), and the horned owl (Bubo virginianus) were chosen as representative of the bird. For the amphibian, the leopard frog (Rana pipiens), and the mud puppy (Necturus maculatus) were chosen for study. As representative of the fish, the goldfish (Carassius auratus), the tilapia (Tilapia mossambica), the guppy (Lebistes sp.), and the sea horse (Hippocampus sp.) were used in these measurements. The morphometric data obtained were then used in estimates of the time constants in the Steinhausen equation which describes the biophysics of fluid flow in the semicircular canals. In general, the time constants (theta/II in the Steinhausen equation) of these representatives of Reptilia, Aves, and Amphibia were of magnitude similar to those reported in mammals, despite the dissimilarities in the diameters of the ducts, the duct radii of curvature, the dimensions of the cristae ampullares and the utricle, and volumes of endolymph within the vestibular system. However, the short-time constants in Pisces were larger (therefore providing a slower response) than those in other vertebrates, and were similar to that of the turtle and the mud puppy.