Modern Reptiles Research Articles

Three-dimensional dental microwear in type-Maastrichtian mosasaur teeth (Reptilia, Squamata)

Mosasaurs (Squamata, Mosasauridae) were large aquatic reptiles from the Late Cretaceous that filled a range of ecological niches within marine ecosystems. The type-Maastrichtian strata (68–66 Ma) of the Netherlands and Belgium preserve remains of five species that seemed to have performed different ecological roles (carnivores, piscivores, durophages). However, many interpretations of mosasaur diet and niche partitioning are based on qualitative types of evidence that are difficult to test explicitly. Here, we apply three-dimensional dental microwear texture analysis (DMTA) to provide quantitative dietary constraints for type-Maastrichtian mosasaurs, and to assess levels of niche partitioning between taxa. DMTA indicates that these mosasaurs did not exhibit neatly defined diets or strict dietary partitioning. Instead, we identify three broad groups: (i) mosasaurs Carinodens belgicus and Plioplatecarpus marshi plotting in the space of modern reptiles that are predominantly piscivorous and/or consume harder invertebrate prey, (ii) Prognathodon saturator and Prognathodon sectorius overlapping with extant reptiles that consume larger amounts of softer invertebrate prey items, and (iii) Mosasaurus hoffmanni spanning a larger plot area in terms of dietary constraints. The clear divide between the aforementioned first two groups in texture-dietary space indicates that, despite our small sample sizes, this method shows the potential of DMTA to test hypotheses and provide quantitative constraints on mosasaur diets and ecological roles.

Some Morphofunctional Features of the Tail of Early Archosaurs in Relation to Swimming Adaptation

In ancient and modern aquatic and semi-aquatic tetrapods, several types of structure of the locomotor apparatus are presented, providing various styles of swimming. In the course of evolutionary adaptation to swimming, an important role was played by the morphological transformations of the tail, which often performs the main propulsion function. Modern reptiles (except turtles) swim mainly with the help of horizontal tail bends, while mammals swim either vertical or horizontal ones. Among extinct reptiles, Sauropterygia probably used vertical tail mobility when swimming. In most archosauromorphs, the tail became high, laterally compressed, and they swam mainly with the help of its horizontal movements. Among early archosaurs, Proterohampsians and Doswelliids are distinguished by their wide and dorsoventrally flat tails, which may indicate an adaptation to swimming using its vertical mobility.

Condition and Coloration of Lingual Lures of Alligator Snapping Turtles

The lingual lures of Macrochelys (alligator snapping turtles) are believed to be the only prey-capturing lures within the mouths of modern reptiles. To date, no formal assessment of lure condition in Macrochelys has been published, and few researchers record lure data. Herein, we report damaged or missing lures from 25 Macrochelys temminckii (Alligator Snapping Turtle; 7 adults, 18 juveniles) from a sample of more than 2000 lure assessments in 4 states, indicating this is a rare occurrence. We also describe lingual lure color observed in these assessments and introduce standardized terminology and color categories. We suggest researchers record data on the condition and coloration of the lingual lure to further our understanding of this ecological and evolutionary adaptation.

Soft tissue preservation in the Triassic pachypleurosaur Keichousaurus hui: evidence for digestive tract anatomy, diet, and feeding behavior

Keichousaurus hui is the most abundant and representative species in the Xingyi biota in South China. K. hui has been studied in many aspects, including its functional morphology, osteology, ontogeny, allometric growth, sexual dimorphism, and reproduction. Previous studies have assumed that Keichousaurus’ anteriorly curved teeth were used to impale prey and to tear and swallow either the whole or partially fragmented prey. Prey items have been assumed to be small fish or soft-bodied invertebrates, such as squid and shrimp, that were also present in the Xingyi biota. However, there has been no direct evidence for the anatomy of the digestive tract or the diet of the Keichousaurus. There are few reports of the soft tissue preservation of K. hui. In this study, we present relatively complete preservation of the digestive tract with food remains in several well-preserved specimens of K. hui. By comparing with modern reptiles, we reconstructed the internal distribution and organ composition of the digestive tract of K. hui. Through the analysis of the alimentary canal remnants by microscope and X-ray computed microtomography, we infer that K. hui was a frequently piscivorous species that usually swallowed its prey whole.

Evidence for heterothermic endothermy and reptile-like eggshell mineralization in Troodon, a non-avian maniraptoran theropod

The dinosaur-bird transition involved several anatomical, biomechanical, and physiological modifications of the theropod bauplan. Non-avian maniraptoran theropods, such as Troodon, are key to better understand changes in thermophysiology and reproduction occurring during this transition. Here, we applied dual clumped isotope (Δ47 and Δ48) thermometry, a technique that resolves mineralization temperature and other nonthermal information recorded in carbonates, to eggshells from Troodon, modern reptiles, and modern birds. Troodon eggshells show variable temperatures, namely 42 and 29 ± 2 °C, supporting the hypothesis of an endothermic thermophysiology with a heterothermic strategy for this extinct taxon. Dual clumped isotope data also reveal physiological differences in the reproductive systems between Troodon, reptiles, and birds. Troodon and modern reptiles mineralize their eggshells indistinguishable from dual clumped isotope equilibrium, while birds precipitate eggshells characterized by a positive disequilibrium offset in Δ48. Analyses of inorganic calcites suggest that the observed disequilibrium pattern in birds is linked to an amorphous calcium carbonate (ACC) precursor, a carbonate phase known to accelerate eggshell formation in birds. Lack of disequilibrium patterns in reptile and Troodon eggshells implies these vertebrates had not acquired the fast, ACC-based eggshell calcification process characteristic of birds. Observation that Troodon retained a slow reptile-like calcification suggests that it possessed two functional ovaries and was limited in the number of eggs it could produce; thus its large clutches would have been laid by several females. Dual clumped isotope analysis of eggshells of extinct vertebrates sheds light on physiological information otherwise inaccessible in the fossilrecord.

Evolution of eggshell structure in relation to nesting ecology in non-avian reptiles.

Amniotic eggs are multifunctional structures that enabled early tetrapods to colonize the land millions of years ago, and are now the reproductive mode of over 70% of all terrestrial amniotes. Eggshell morphology is at the core of animal survival, mediating the interactions between embryos and their environment, and has evolved into a massive diversity of forms and functions in modern reptiles. These functions are critical to embryonic survival and may serve as models for new antimicrobial and/or breathable membranes. However, we still lack critical data on the basic structural and functional properties of eggs, particularly of reptiles. Here, we first characterized egg shape, shell thickness, porosity, and mineralization of eggs from 91 reptile species using optical images, scanning electron microscopy, and micro computed tomography, and collected data on nesting ecology from the literature. We then used comparative analyses to test hypotheses on the selective pressures driving their evolution. We hypothesized that eggshell morphology has evolved to protect shells from physical damage and desiccation, and, in support, found a positive relationship between thickness and precipitation, and a negative relationship between porosity and temperature. Although mineralization varied extensively, it was not correlated with nesting ecology variables. Ancestral state reconstructions show thinning and increased porosity over evolutionary time in squamates, but the opposite in turtles and crocodilians. Egg shape, size, porosity and calcification were correlated, suggesting potential structural or developmental tradeoffs. This study provides new data and insights into the morphology and evolution of reptile eggs, and raises numerous questions for additional research.

Epidermal complexity in the theropod dinosaur Juravenator from the Upper Jurassic of Germany

AbstractEpidermal scales among modern reptiles are morphologically diverse and serve a variety of functions ranging from moisture balance to chemoreception. Despite being predominantly squamous‐skinned (scaly), the functional implications of this type of integument have never before been explored for a dinosaur. Re‐examination of the holotype of the theropod Juravenator starki (Kimmeridgian, Late Jurassic) reveals previously unseen diversity in its epidermal covering. In addition to the presence of short monofilaments on the dorsal and ventral parts of the tail, we identify distinctive scale patterns corresponding to discrete longitudinal bands of scutate, tuberculate and ornamented scales along the length of the tail. In modern squamous‐skinned amniotes, variation in scale architecture can be linked to functional differences between scale types. In Juravenator, distinctive circular nodes associated with the ornamented scales have recently been interpreted as integumentary sense organs. We also suggest that it is likely that the snake‐like scutate scales on the underside of the tail fulfilled a role related to mechanical protection rather than locomotory function. Whereas the literature on theropod epidermal structures has been dominated by discussions on the evolution and diversity of feathers, this study highlights the complexity of squamous integument in Juravenator, which is revealed as one of the most complex among known theropods. An exploration of the epidermal structures found in Juravenator and other non‐avian theropods reveals great complexity in the type and distribution of these structures across the clade, suggesting potential for the future inquiry into their taxonomic and biological importance.

The tuatara genome reveals ancient features of amniote evolution

The tuatara (Sphenodon punctatus)—the only living member of the reptilian order Rhynchocephalia (Sphenodontia), once widespread across Gondwana1,2—is an iconic species that is endemic to New Zealand2,3. A key link to the now-extinct stem reptiles (from which dinosaurs, modern reptiles, birds and mammals evolved), the tuatara provides key insights into the ancestral amniotes2,4. Here we analyse the genome of the tuatara, which—at approximately 5 Gb—is among the largest of the vertebrate genomes yet assembled. Our analyses of this genome, along with comparisons with other vertebrate genomes, reinforce the uniqueness of the tuatara. Phylogenetic analyses indicate that the tuatara lineage diverged from that of snakes and lizards around 250 million years ago. This lineage also shows moderate rates of molecular evolution, with instances of punctuated evolution. Our genome sequence analysis identifies expansions of proteins, non-protein-coding RNA families and repeat elements, the latter of which show an amalgam of reptilian and mammalian features. The sequencing of the tuatara genome provides a valuable resource for deep comparative analyses of tetrapods, as well as for tuatara biology and conservation. Our study also provides important insights into both the technical challenges and the cultural obligations that are associated with genome sequencing.

Anatomy of a dinosaur-Clarification of vertebrae in vertebrate anatomy.

The flat-end surfaces of dinosaur vertebral centra led to the presumption that intervertebral discs occupied the space between their vertebrae. A set of fused hadrosaur vertebrae allowed that hypothesis to be tested. The Tyrannosaurus rex responsible for this pathology did not escape unscathed. It left behind a tooth crown that had fractured. Fragments of that tooth were scattered through the intervertebral space, evidencing that there was no solid structure to impede its movement. That eliminates the possibility of an intervertebral disc and instead proves the presence of an articular space, similar to that in modern reptiles, but at variance to what is noted in birds. While avian cervical vertebral centra appear to be separated by diarthrodial joints, the preponderance of their thoracic vertebral centra is not separated by synovial joints.

Investigation of a bone lesion in a gorgonopsian (Synapsida) from the Permian of Zambia and periosteal reactions in fossil non-mammalian tetrapods.

While only distantly related to mammals, the anatomy of Permian gorgonopsians has shed light on the functional biology of non-mammalian synapsids and on the origins of iconic 'mammal-like' anatomical traits. However, little is known of gorgonopsian behaviour or physiology, which would aid in reconstructing the paleobiological context in which familiar mammalian features arose. Using multi-modal imaging, we report a discrete osseous lesion in the forelimb of a late Permian-aged gorgonopsian synapsid, recording reactive periosteal bone deposition and providing insights into the origins and diversity of skeletal healing responses in premammalian synapsids. We suggest that the localized lesion on the anterolateral (preaxial) shaft of the left radius represents acute periostitis and, conservatively, most likely developed as a subperiosteal haematoma with subsequent bone deposition and limited internal remodelling. The site records an inner zone of reactive cortical bone forming irregular to radial bony spicules and an outer, denser zone of slowed subperiosteal bone apposition, all of which likely occurred within a single growing season. In surveys of modern reptiles-crocodylians, varanids-such haematomas are rare compared to other documented osteopathologies. The extent and rapidity of the healing response is reminiscent of mammalian and dinosaurian bone pathologies, and may indicate differing behaviour or bone physiology compared to non-dinosaurian reptiles. This report adds to a growing list of putative disease entities recognized in early synapsids and broadens comparative baselines for pathologies and the evolution of bone response to disease in mammalian forebears. This article is part of the theme issue 'Vertebrate palaeophysiology'.

Peculiarities of the Structure and Locomotor Function of the Tail in Sauropterygia

Among ancient and modern marine reptiles, several structural types of the locomotor apparatus were or are present, supporting different styles of swimming. Ichthyosaurs, mosasaurs, saltwater crocodiles, and representatives of many other groups swam or swim with horizontal undulations of the body primarily using the tail with a vertical caudal fin. Sea turtles with a reduced tail and their body completely immobilized by the shell use only limbs transformed into flippers for swimming. Sauropterygians had a substantially immobilized trunk and a horizontal caudal fin. They used a unique type of subaquatic locomotion with the leading role of two pairs of powerful flippers and vertical undulations of the tail, partial analogs of which are found in sea turtles, sirens, cetaceans, and some semi-aquatic mammals.

Integumentary structure and composition in an exceptionally well-preserved hadrosaur (Dinosauria: Ornithischia).

Preserved labile tissues (e.g., skin, muscle) in the fossil record of terrestrial vertebrates are increasingly becoming recognized as an important source of biological and taphonomic information. Here, we combine a variety of synchrotron radiation techniques with scanning electron and optical microscopy to elucidate the structure of 72 million-year-old squamous (scaly) skin from a hadrosaurid dinosaur from the Late Cretaceous of Alberta, Canada. Scanning electron and optical microscopy independently reveal that the three-dimensionally preserved scales are associated with a band of carbon-rich layers up to a total thickness of ∼75 microns, which is topographically and morphologically congruent with the stratum corneum in modern reptiles. Compositionally, this band deviates from that of the surrounding sedimentary matrix; Fourier-transform infrared spectroscopy and soft X-ray spectromicroscopy analyses indicate that carbon appears predominantly as carbonyl in the skin. The regions corresponding to the integumentary layers are distinctively enriched in iron compared to the sedimentary matrix and appear with kaolinite-rich laminae. These hosting carbonyl-rich layers are apparently composed of subcircular bodies resembling preserved cell structures. Each of these structures is encapsulated by calcite/vaterite, with iron predominantly concentrated at its center. The presence of iron, calcite/vaterite and kaolinite may, independently or collectively, have played important roles in the preservation of the layered structures.

An Intermediate Incubation Period and Primitive Brooding in a Theropod Dinosaur

Non-avian dinosaurs such as oviraptorosaurs and troodontids share several important reproductive characters with modern birds, including eggshell microstructure and iterative egg production. Nevertheless, debate exists concerning their incubation strategies. Here we estimate incubation period for the troodontid, Troodon formosus, by examining a near-term embryonic tooth. Synchrotron scanning and histologic thin sections allowed counting of daily (von Ebner) growth lines. The tooth preserves 31 intact lines with an average spacing of 3.3 ± 0.96 μm. Adding 8 more for the missing crown tip gives a total age of 39 days. Modern crocodilians begin to establish their functional dentition at approximately 47% through incubation. Thus, this tooth age suggests a Troodon incubation period of 74 days, falling midway between avian (44.4 days) and reptilian (107.3 days) values predicted by the Troodon egg mass (314 g). An accelerated incubation relative to modern reptiles supports brooding and concurs with a suite of features in oviraptorosaurs and troodontids (sequential laying, large complex clutches, and precocial young) that appear dependent upon both adult body and incubation temperatures elevated over ambient conditions. However, the largely buried condition of Troodon clutches may have prohibited efficient brooding, necessitating longer incubation than that of modern birds with fully exposed eggs.

A Briefly Argued Case That Asgard Archaea Are Part of the Eukaryote Tree.

The recent discovery of the Lokiarchaeota and other members of the Asgard superphylum suggests that closer analysis of the cell biology and evolution of these groups may help shed light on the origin of the eukaryote cell. Asgard lineages often appear in molecular phylogenies as closely related to eukaryotes, and possess “Eukaryote Signature Proteins” coded by genes previously thought to be unique to eukaryotes. This phylogenetic affinity to eukaryotes has been widely interpreted as indicating that Asgard lineages are “eukaryote-like archaea,” with eukaryotes evolving from within a paraphyletic Archaea. Guided by the established principles of systematics, we examine the potential implications of the monophyly of Asgard lineages and Eukarya. We show that a helpful parallel case is that of Synapsida, a group that includes modern mammals and their more “reptile-like” ancestors, united by shared derived characters that evolved in their common ancestor. While this group contains extinct members that share many similarities with modern reptiles and their extinct relatives, they are evolutionarily distinct from Sauropsida, the group which includes modern birds, reptiles, and all other amniotes. Similarly, Asgard lineages and eukaryotes are united by shared derived characters to the exclusion of all other groups. Consequently, the Asgard group is not only highly informative for our understanding of eukaryogenesis, but may be better understood as being early diverging members of a broader group including eukaryotes, for which we propose the name “Eukaryomorpha.” Significantly, this means that the relationship between Eukarya and Asgard lineages cannot, on its own, resolve the debate over 2 vs. 3 Domains of life; instead, resolving this debate depends upon identifying the root of Archaea with respect to Bacteria.

The Evolution and Fossil History of Sensory Perception in Amniote Vertebrates

Sensory perception is of crucial importance for animals to interact with their biotic and abiotic environment. In amniotes, the clade including modern mammals (Synapsida), modern reptiles (Reptilia), and their fossil relatives, the evolution of sensory perception took place in a stepwise manner after amniotes appeared in the Carboniferous. Fossil evidence suggests that Paleozoic taxa had only a limited amount of sensory capacities relative to later forms, with the majority of more sophisticated types of sensing evolving during the Triassic and Jurassic. Alongside the evolution of improved sensory capacities, various types of social communication evolved across different groups. At present there is no definitive evidence for a relationship between sensory evolution and species diversification. It cannot be excluded, however, that selection for improved sensing was partially triggered by biotic interactions, e.g., in the context of niche competition, whereas ecospace expansion, especially during the Mesozoic, might also have played an important role.

Caudal autotomy as anti-predatory behaviour in Palaeozoic reptiles

Many lizards can drop a portion of their tail in response to an attack by a predator, a behaviour known as caudal autotomy. The capacity for intravertebral autotomy among modern reptiles suggests that it evolved in the lepidosaur branch of reptilian evolution, because no such vertebral features are known in turtles or crocodilians. Here we present the first detailed evidence of the oldest known case of caudal autotomy, found only among members of the Early Permian captorhinids, a group of ancient reptiles that diversified extensively and gained a near global distribution before the end-Permian mass extinction event of the Palaeozoic. Histological and SEM evidence show that these early reptiles were the first amniotes that could autotomize their tails, likely as an anti-predatory behaviour. As in modern iguanid lizards, smaller captorhinids were able to drop their tails as juveniles, presumably as a mechanism to evade a predator, whereas larger individuals may have gradually lost this ability. Caudal autotomy in captorhinid reptiles highlights the antiquity of this anti-predator behaviour in a small member of a terrestrial community composed predominantly of larger amphibian and synapsid predators.

A Model Explaining Infantile Esotropia: Dissociated Strabismus as a Result of Sensory Interhemispheric Dissociation and Crossed Dominance in the Brainstem

Over 150 million years, modern reptiles, birds and mammals evolved. Predatory birds and mammals have eyes on the front of their heads. In these animals, binocular correspondence, voluntary eye movements, eye-hand coordination, partial decussation at the optic chiasm and cortical interhemispheric pathways could develop at the cost of a smaller visual field. The subsequent enlargement of the cerebral neocortex and the hemispheric pathways are of central importance in binocular vision, sensory fusion and infantile strabismus. To investigate visual interhemispheric fibers, tractography was used in subjects with infantile esotropia (IE), callosal agenesis and control subjects with normal binocularity. In human callosal agenesis, normal binocularity could be explained by a different interhemispheric connection. In subjects with infantile esotropia, the analyses starting from the primary visual area on one side appeared different from the analysis from the other side. The distribution areas are asymmetrical between sides. Binocularity and alignment not only rely on correspondence between crossed and uncrossed hemi-representations but, in addition the corpus callosum, the most important interhemispheric pathway in placental mammals, seems important in the development of human binocularity. When correspondence is possible between the hemi-representations of the crossed and the uncrossed pathway on both sides of the cortex, the uncrossed pathway finds its way via the corpus callosum toward the contralateral hemi-representation of the same eye. A vertical midline must come out of this process. Meanwhile, however, the other uncrossed pathway strives to find the vertical midline of the other eye. Likely, the corpus callosum is important during the tuning of the pathways involved in sensory fusion. The anterior commissure might be an alternative in callosal agenesis. A failure in the offset will result in strabismus and crossed dominance after V1. Consequently, the normal binocular development of the brainstem (i.e., the superior colliculus), will not take place and latent nystagmus, as well as dissociated divergence, may ensue.

Pathological pitting in ankylosaur (Dinosauria) osteoderms

Large ulcerative pits on the external surface of ankylosaur (Dinosauria) osteoderms have been recognized for many years. They have been ascribed without supporting evidence to damage by predator teeth or to disease. The discovery of numerous examples of pitted osteoderms in a monospecific ankylosaur (Gastonia n.sp.) bone bed in eastern Utah (USA) provided a unique opportunity to study these pits in greater detail. The pits typically are characterized by smooth-walled depressions that disrupt the bone surface, with 43% focal lesions and 57% multifocal. Because ankylosaur osteoderms are analogous to crocodile osteoderms, the possible etiology of the pits was sought among today’s crocodile dermatoses. A modified version of the Istanbul Protocol was used to indicate the degree of certainty for the possible causes. This technique in context of the limited range of response to infection of reptile bone, allows us to narrow the possible causes of pit formation to two. One is ulceration by bacterial or mycological dermatosis; the other is through pressure erosion of the bone surface (cortex) by granuloma formation in the thin skin or at the skin-osteoderm interface. Unfortunately, the biopsies that are critical for differential diagnosis of diseases in modern reptiles cannot be performed on the ankylosaur osteoderms. Therefore, a single definitive etiology for pits in ankylosaurs cannot be identified.

Growth patterns and life-history strategies in Placodontia (Diapsida: Sauropterygia).

Placodontia is a clade of durophagous, near shore marine reptiles from Triassic sediments of modern-day Europe, Middle East and China. Although much is known about their primary anatomy and palaeoecology, relatively little has been published regarding their life history, i.e. ageing, maturation and growth. Here, growth records derived from long bone histological data of placodont individuals are described and modelled to assess placodont growth and life-history strategies. Growth modelling methods are used to confirm traits documented in the growth record (age at onset of sexual maturity, age when asymptotic length was achieved, age at death, maximum longevity) and also to estimate undocumented traits. Based on these growth models, generalized estimates of these traits are established for each taxon. Overall differences in bone tissue types and resulting growth curves indicate different growth patterns and life-history strategies between different taxa of Placodontia. Psephoderma and Paraplacodus grew with lamellar-zonal bone tissue type and show growth patterns as seen in modern reptiles. Placodontia indet. aff. Cyamodus and some Placodontia indet. show a unique combination of fibrolamellar bone tissue regularly stratified by growth marks, a pattern absent in modern sauropsids. The bone tissue type of Placodontia indet. aff. Cyamodus and Placodontia indet. indicates a significantly increased basal metabolic rate when compared with modern reptiles. Double lines of arrested growth, non-annual rest lines in annuli, and subcycles that stratify zones suggest high dependence of placodont growth on endogenous and exogenous factors. Histological and modelled differences within taxa point to high individual developmental plasticity but sexual dimorphism in growth patterns and the presence of different taxa in the sample cannot be ruled out.

Developmental genetic bases behind the independent origin of the tympanic membrane in mammals and diapsids.

The amniote middle ear is a classical example of the evolutionary novelty. Although paleontological evidence supports the view that mammals and diapsids (modern reptiles and birds) independently acquired the middle ear after divergence from their common ancestor, the developmental bases of these transformations remain unknown. Here we show that lower-to-upper jaw transformation induced by inactivation of the Endothelin1-Dlx5/6 cascade involving Goosecoid results in loss of the tympanic membrane in mouse, but causes duplication of the tympanic membrane in chicken. Detailed anatomical analysis indicates that the relative positions of the primary jaw joint and first pharyngeal pouch led to the coupling of tympanic membrane formation with the lower jaw in mammals, but with the upper jaw in diapsids. We propose that differences in connection and release by various pharyngeal skeletal elements resulted in structural diversity, leading to the acquisition of the tympanic membrane in two distinct manners during amniote evolution.