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Resolving the phylogenetic relationships of early amniotes, in particular stem reptiles, remains a difficult problem. Three-dimensional morphological analysis of well-preserved stem-reptile specimens can reveal important anatomical data and clarify regions of phylogeny. Here, we present the first thorough description of the unusual early Permian stem reptile Bolosaurus major, including the first comprehensive description of a bolosaurid braincase. We describe previously obscured details of the palate, allowing for insight into bolosaurid feeding mechanics. Aspects of the rostrum, palate, mandible, and neurocranium suggest that B. major had a particularly strong bite. We additionally found B. major has a surprisingly slender stapes, similar to that of the middle Permian stem reptile Macroleter poezicus, which may suggest enhanced hearing abilities compared to other Paleozoic amniotes (e.g., captorhinids). We incorporated our new anatomical information into a large phylogenetic matrix (150 OTUs, 590 characters) to explore the relationship of Bolosauridae among stem reptiles. Our analyses generally recovered a paraphyletic "Parareptilia," and found Bolosauridae to diverge after Captorhinidae + Araeoscelidia. We also included B. major within a smaller matrix (10 OTUs, 27 characters) designed to explore the interrelationships of Bolosauridae and found all species of Bolosaurus to be monophyletic. While reptile relationships still require further investigation, our phylogeny suggests repeated evolution of impedance-matching ears in Paleozoic stem reptiles.

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Paleozoic synapsids represent the first chapter in the evolution of this large clade that includes mammals. These fascinating terrestrial vertebrates were the first amniotes to successfully adapt to a wide range of feeding strategies, reflected by their varied dental morphologies. Evolution of the marginal dentition on the mammalian side of amniotes is characterized by strong, size and shape heterodonty, with the late Permian therapsids showing heterodonty with the presence of incisiform, caniniform, and multicuspid molariform dentition. Rarity of available specimens has previously prevented detailed studies of dental anatomy and evolution in the initial chapter of synapsid evolution, when synapsids were able to evolve dentition for insectivory, herbivory, and carnivory. Numerous teeth, jaw elements, and skulls of the hypercarnivorous varanopid Mesenosaurus efremovi have been recently discovered in the cave systems near Richards Spur, Oklahoma, permitting the first detailed investigation of the dental anatomy of a Paleozoic tetrapod using multiple approaches, including morphometric and histological analyses. As a distant stem mammal, Mesenosaurus is the first member of this large and successful clade to exhibit a type of dental heterodonty that combines size and morphological (shape) variation of the tooth crowns. Here we present the first evidence of functional differentiation in the dentition of this early synapsid, with three distinct dental regions having diverse morphologies and functions. The quality and quantity of preserved materials has allowed us to identify the orientation and curvature of the carinae (cutting edges), and the variation and distribution of the ziphodonty (serrations) along the carinae. The shape-related heterodonty seen in this taxon may have contributed to this taxon's ability to be a successful mid-sized predator in the taxonomically diverse community of early Permian carnivores, but may have also extended the ecological resilience of this clade of mid-sized predators across major faunal and environmental transitions.

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Detailed description of the holotype skeleton of Delorhynchus cifellii, made possible through the use of neutron tomography, has yielded important new information about the cranial and postcranial anatomy of this early Permian acleistorhinid parareptile. Hitherto unknown features of the skull include a sphenethmoid, paired epipterygoids and a complete neurocranium. In addition, the stapes has been exposed in three dimensions for the first time in an early parareptile. Postcranial material found in articulation with the skull in this holotype allows for the first detailed description of vertebrae, ribs, shoulder girdle and humerus of an acleistorhinid parareptile, allowing for a reevaluation of the phylogenetic relationships of this taxon with other acleistorhinids, and more broadly among parareptiles. Results show that Delorhynchus is recovered as the sister taxon of Colobomycter, and 'acleistorhinids' now include Lanthanosuchus.

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A ubiquitous feature of the auditory organ in amniotes is the longitudinal mapping of neuronal characteristic frequencies (CFs), which increase exponentially with distance along the organ. The exponential tonotopic map reflects variation in hair cell properties according to cochlear location and is thought to stem from concentration gradients in diffusible morphogenic proteins during embryonic development. While in all amniotes the spatial gradient is initiated by sonic hedgehog (SHH), released from the notochord and floorplate, subsequent molecular pathways are not fully understood. In chickens, BMP7 is one such morphogen, secreted from the distal end of the cochlea. In mammals, the developmental mechanism differs from birds and may depend on cochlear location. A consequence of exponential maps is that each octave occupies an equal distance on the cochlea, a spacing preserved in the tonotopic maps in higher auditory brain regions. This may facilitate frequency analysis and recognition of acoustic sequences.

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Seymouria is among the best-known stem amniotes and holds an important phylogenetic position for discussions of amniote evolution. Previous work has focused primarily on the osteology of Seymouria, with recent interest turning to the application of computed tomography (CT) to study the internal features. We utilized neutron CT to reconstruct the first virtual cranial endocast and the first complete otic endocasts of Seymouria, revealing previously unrecognized details of its palaeoneuroanatomy. The brain and inner ear of Seymouria are largely plesiomorphic relative to later-diverging crown amniotes, showing no indication of increased encephalization or braincase ossification. Our results also clarify the plesiomorphic condition for carotid artery morphology in amniotes, with Seymouria showing a similar condition to basal members of both the synapsid and sauropsid lineages. The reconstructed neuroanatomy also indicates that Seymouria did not possess any particular neuroanatomical specializations, despite the probable presence of an impedance matching hearing system.

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The exquisite preservation of maxillary and mandibular fragments of Seymouria has allowed us to examine for the first time in detail the dental anatomy and patterns of development in this stem amniote. The results obtained through histological examination show that Seymouria has pleurodont implantation with ankylosis of the tooth to the labial side of the jawbone. The dentary and maxillary teeth exhibit similar dental characteristics, such as the attachment bone (alveolar bone) and cementum rising above the jawbone on the base of the tooth, and smooth carinae extending lingually toward the tooth apex. Additionally, the clear presence of plicidentine, infolding of dentine into the pulp cavity, was found within the tooth root extending into the tooth crown. Lastly, the tooth replacement pattern is alternating, illustrating that Seymouria retains the classic primitive condition for tetrapods, a pattern that is continued in amniotes. Our results provide an important basis for comparison with other stem amniotes and with amniotes.

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The whole-body (tachymetabolic) endothermy seen in modern birds and mammals is long held to have evolved independently in each group, a reasonable assumption when it was believed that its earliest appearances in birds and mammals arose many millions of years apart. That assumption is consistent with current acceptance that the non-shivering thermogenesis (NST) component of regulatory body heat originates differently in each group: from skeletal muscle in birds and from brown adipose tissue (BAT) in mammals. However, BAT is absent in monotremes, marsupials, and many eutherians, all whole-body endotherms. Indeed, recent research implies that BAT-driven NST originated more recently and that the biochemical processes driving muscle NST in birds, many modern mammals and the ancestors of both may be similar, deriving from controlled 'slippage' of Ca2+ from the sarcoplasmic reticulum Ca2+ -ATPase (SERCA) in skeletal muscle, similar to a process seen in some fishes. This similarity prompted our realisation that the capacity for whole-body endothermy could even have pre-dated the divergence of Amniota into Synapsida and Sauropsida, leading us to hypothesise the homology of whole-body endothermy in birds and mammals, in contrast to the current assumption of their independent (convergent) evolution. To explore the extent of similarity between muscle NST in mammals and birds we undertook a detailed review of these processes and their control in each group. We found considerable but not complete similarity between them: in extant mammals the 'slippage' is controlled by the protein sarcolipin (SLN), in birds the SLN is slightly different structurally and its role in NST is not yet proved. However, considering the multi-millions of years since the separation of synapsids and diapsids, we consider that the similarity between NST production in birds and mammals is consistent with their whole-body endothermy being homologous. If so, we should expect to find evidence for it much earlier and more widespread among extinct amniotes than is currently recognised. Accordingly, we conducted an extensive survey of the palaeontological literature using established proxies. Fossil bone histology reveals evidence of sustained rapid growth rates indicating tachymetabolism. Large body size and erect stature indicate high systemic arterial blood pressures and four-chambered hearts, characteristic of tachymetabolism. Large nutrient foramina in long bones are indicative of high bone perfusion for rapid somatic growth and for repair of microfractures caused by intense locomotion. Obligate bipedality appeared early and only in whole-body endotherms. Isotopic profiles of fossil material indicate endothermic levels of body temperature. These proxies led us to compelling evidence for the widespread occurrence of whole-body endothermy among numerous extinct synapsids and sauropsids, and very early in each clade's family tree. These results are consistent with and support our hypothesis that tachymetabolic endothermy is plesiomorphic in Amniota. A hypothetical structure for the heart of the earliest endothermic amniotes is proposed. We conclude that there is strong evidence for whole-body endothermy being ancient and widespread among amniotes and that the similarity of biochemical processes driving muscle NST in extant birds and mammals strengthens the case for its plesiomorphy.

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The transition of amniotes to a fully terrestrial lifestyle involved the adaptation of major molecular innovations to the epidermis, often in the form of epidermal appendages such as hair, scales and feathers. Feathers are diverse epidermal structures of birds, and their evolution has played a key role in the expansion of avian species to a wide range of lifestyles and habitats. As with other epidermal appendages, feather development is a complex process which involves many different genetic and protein elements. In mammals, many of the genetic elements involved in epidermal development are located at a specific genetic locus known as the epidermal differentiation complex (EDC). Studies have identified a homologous EDC locus in birds, which contains several genes expressed throughout epidermal and feather development. A family of avian EDC genes rich in aromatic amino acids that also contain MTF amino acid motifs (EDAAs/EDMTFs), that includes the previously reported histidine-rich or fast-protein (HRP/fp), an important marker in feather development, has expanded significantly in birds. Here, we characterize the EDAA gene family in birds and investigate the evolutionary history and possible functions of EDAA genes using phylogenetic and sequence analyses. We provide evidence that the EDAA gene family originated in an early archosaur ancestor, and has since expanded in birds, crocodiles and turtles, respectively. Furthermore, this study shows that the respective amino acid compositions of avian EDAAs are characteristic of structural functions associated with EDC genes and feather development. Finally, these results support the hypothesis that the genes of the EDC have evolved through tandem duplication and diversification, which has contributed to the evolution of the intricate avian epidermis and epidermal appendages.

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Amniotes, a clade of terrestrial vertebrates, which includes all of the descendants of the last common ancestor of the reptiles (including dinosaurs and birds) and mammals, is one of the most successful group of animals on our planet. In addition to having an egg equipped with an amnion, an adaptation to lay eggs on land, amniotes possess a number of other major morphological characteristics. Chief among them is the amniote skull, which can be classified into several major types distinguished by the presence and number of temporal fenestrae (windows) in the posterior part. Amniotes evolved from ancestors who possessed a skull composed of a complex mosaic of small bones separated by sutures. Changes in skull composition underlie much of the large-scale evolution of amniotes with many lineages showing a trend in reduction of cranial elements known as the "Williston's Law." The skull of amniotes is also arranged into a set of modules of closely co-evolving bones as revealed by modularity and integration tests. One of the most consistently recovered and at the same time most versatile modules is the "face," anatomically defined as the anterior portion of the head. The faces of amniotes display extraordinary amount of variation, with many adaptive radiations showing parallel tendencies in facial scaling, e.g., changes in length or width. This review explores the natural history of the amniote face and discusses how a better understanding of its anatomy and developmental biology helps to explain the outstanding scale of adaptive facial diversity. We propose a model for facial evolution in the amniotes, based on the differential rate of cranial neural crest cell proliferation and the timing of their skeletal differentiation.

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Evolution of the terrestrial egg of amniotes (reptiles, birds, and mammals) is often considered to be one of the most significant events in vertebrate history. Presence of an eggshell, fetal membranes, and a sizeable yolk allowed this egg to develop on land and hatch out well-developed, terrestrial offspring. For centuries, morphologically-based studies have provided valuable information about the eggs of amniotes and the embryos that develop from them. This review explores the history of such investigations, as a contribution to this special issue of Journal of Morphology, titled Developmental Morphology and Evolution of Amniote Eggs and Embryos. Anatomically-based investigations are surveyed from the ancient Greeks through the Scientific Revolution, followed by the 19th and early 20th centuries, with a focus on major findings of historical figures who have contributed significantly to our knowledge. Recent research on various aspects of amniote eggs is summarized, including gastrulation, egg shape and eggshell morphology, eggs of Mesozoic dinosaurs, sauropsid yolk sacs, squamate placentation, embryogenesis, and the phylotypic phase of embryonic development. As documented in this review, studies on amniote eggs and embryos have relied heavily on morphological approaches in order to answer functional and evolutionary questions.

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Recent studies have demonstrated a mechanism of embryonic yolk processing in lizards, snakes and turtles that differs markedly from that of birds. In the avian pattern, cells that line the inside of the yolk sac take up products of yolk digestion and deliver nutrients into the vitelline circulation. In contrast, in squamates and turtles, proliferating endodermal cells invade and fill the yolk sac cavity, forming elongated strands of yolk-filled cells that surround small blood vessels. This arrangement provides a means by which yolk material becomes cellularized, digested, and transported for embryonic use. Ultrastructural observations on late-stage Alligator mississippiensis eggs reveal elongated, vascular strands of endodermal cells within the yolk sac cavity. The strands of cells are intermixed with free yolk spheres and clumps of yolk-filled endodermal cells, features that reflect early phases in the yolk-processing pattern. These observations indicate that yolk processing in Alligator is more like the pattern of other reptiles than that of birds.

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Evolution of the terrestrial, amniotic egg of vertebrates required new mechanisms by which yolk material could be processed for embryonic use. Recent studies on each of the major extant reptile groups have revealed elaborate morphological specializations for yolk processing, features that differ dramatically from those of birds. In the avian pattern, liquid yolk is housed in a yolk sac whose endodermal lining absorbs and digests yolk material and sends resultant nutrients into the blood circulation. In snakes, lizards, turtles, and crocodilians, as documented herein, the yolk sac becomes invaded by endodermal cells that proliferate and phagocytose yolk material. Blood vessels then invade, and the endodermal cells become arranged around them, forming elongated "spaghetti-like" strands that fill the yolk sac cavity. This pattern provides an effective means by which yolk material is cellularized, digested, and transported by vitelline vessels to the developing embryo. Phylogenetically, the (non-avian) "reptilian" pattern was ancestral for sauropsids and was modified or replaced in ancestors to birds. This review postulates that evolution of the "avian" pattern involved increased reliance on extracellular digestion of yolk, allowing embryonic development to occur more rapidly than in typical reptiles. Comparative studies of yolk processing that draw on morphological, biochemical, molecular approaches are needed to explain how and why the "reptilian" pattern was replaced in birds or their archosaurian ancestors.

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Longevity, an important life-history trait, is determined by extrinsic and/or intrinsic causing mortality. Here, we used body mass (BM), field metabolic rate (FMR), longevity, and female maturity data reported from 300 amniote species to test whether 1) longevity was related to BM, FMR and female maturity, and 2) FMR, female maturity, or both, had a direct effect on longevity and whether an indirect effect of FMR on female maturity improved model fit. The results showed that BM was positively correlated with longevity and FMR, but negatively correlated with mass-specific FMR (mFMR) in amniotes. Phylogenetic confirmatory path analysis showed that, in the best model, longevity had a direct negative correlation with mFMR in lizards, and an indirect negative correlation with mFMR through female maturity in mammals. However, longevity had a direct positive correlation with mFMR in birds. Furthermore, longevity was positively correlated with female maturity in endotherms (birds and mammals) but weakly correlated with female maturity in ectotherms (lizards). Thus, our results are consistent with the life-history theory and the "rate-of-living" hypothesis in lizards and mammals but not support them in birds.

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Reptiles are notable for the extensive genomic diversity and species richness among amniote classes, but there is nevertheless a need for detailed genome-scale studies. Although the monophyletic amniotes have recently been a focus of attention through an increasing number of genome sequencing projects, the abundant repetitive portion of the genome, termed the "repeatome", remains poorly understood across different lineages. Consisting predominantly of transposable elements or mobile and satellite sequences, these repeat elements are considered crucial in causing chromosomal rearrangements that lead to genomic diversity and evolution. Here, we propose major repeat landscapes in representative reptilian species, highlighting their evolutionary dynamics and role in mediating chromosomal rearrangements. Distinct karyotype variability, which is typically a conspicuous feature of reptile genomes, is discussed, with a particular focus on rearrangements correlated with evolutionary reorganization of micro- and macrochromosomes and sex chromosomes. The exceptional karyotype variation and extreme genomic diversity of reptiles are used to test several hypotheses concerning genomic structure, function, and evolution.

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Genetic variation in the enzymes that catalyze posttranslational modification of proteins is a potentially important source of phenotypic variation during evolution. Ubiquitination is one such modification that affects turnover of virtually all of the proteins in the cell in addition to roles in signaling and epigenetic regulation. UBE2D3 is a promiscuous E2 enzyme, which acts as an ubiquitin donor for E3 ligases that catalyze ubiquitination of developmentally important proteins. We have used protein sequence comparison of UBE2D3 orthologs to identify a position in the C-terminal α-helical region of UBE2D3 that is occupied by a conserved serine in amniotes and by alanine in anamniote vertebrate and invertebrate lineages. Acquisition of the serine (S138) in the common ancestor to modern amniotes created a phosphorylation site for Aurora B. Phosphorylation of S138 disrupts the structure of UBE2D3 and reduces the level of the protein in mouse embryonic stem cells (ESCs). Substitution of S138 with the anamniote alanine (S138A) increases the level of UBE2D3 in ESCs as well as being a gain of function early embryonic lethal mutation in mice. When mutant S138A ESCs were differentiated into extraembryonic primitive endoderm, levels of the PDGFRα and FGFR1 receptor tyrosine kinases were reduced and primitive endoderm differentiation was compromised. Proximity ligation analysis showed increased interaction between UBE2D3 and the E3 ligase CBL and between CBL and the receptor tyrosine kinases. Our results identify a sequence change that altered the ubiquitination landscape at the base of the amniote lineage with potential effects on amniote biology and evolution.

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Varanopids were a group of small to medium-sized synapsids whose fossil record spans the Carboniferous through middle Permian. Although their phylogenetic relationships have received some interest in recent years, little is known about other aspects of their palaeobiology, including their skeletal growth, allometry and habitat preference. Here, we describe varanopid long bone histology based on a sample of well-preserved femora from the lower Permian Richards Spur fissure fill locality, Comanche County, Oklahoma, USA. The sample includes five femora from at least two varanopid taxa-Mycterosaurus and the large varanodontine Varanops brevirostris-and four additional mycterosaurine femora not diagnosed to genus. Prior work on femoral bone compactness provided a baseline to make lifestyle inferences and evaluate whether varanopids were ancestrally terrestrial. Moreover, the large availability of specimens spanning different sizes made possible an assessment of size-related ontogenetic histovariability. All specimens revealed moderately dense cortical bone tissues composed of sparsely vascularized parallel-fibred and lamellar bone with radially arranged rows of longitudinal canals (mostly simple), and many preserved regularly spaced growth marks (annuli and lines of arrested growth) as in modern varanids. We show that bone histology has the potential to explain how ballast was shed and the skeleton lightened for terrestrial mobility in ancestral synapsids and their basal amniote kin, as well as how adjustments in postnatal growth influenced the evolution of larger body sizes in the terrestrial frontier. This article is part of the theme issue 'Vertebrate palaeophysiology'.

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Artificial athletic turf containing crumb rubber (CR) from shredded tires is a growing environmental and public health concern. However, the associated health risk is unknown due to the lack of toxicity data for higher vertebrates. We evaluated the toxic effects of CR in a developing amniote vertebrate embryo. CR water leachate was administered to fertilized chicken eggs via different exposure routes, i.e., coating by dropping CR leachate on the eggshell; dipping the eggs into CR leachate; microinjecting CR leachate into the air cell or yolk. After 3 or 7 d of incubation, embryonic morphology, organ development, physiology, and molecular pathways were measured. The results showed that CR leachate injected into the yolk caused mild to severe developmental malformations, reduced growth, and specifically impaired the development of the brain and cardiovascular system, which were associated with gene dysregulation in aryl hydrocarbon receptor, stress-response, and thyroid hormone pathways. The observed systematic effects were probably due to a complex mixture of toxic chemicals leaching from CR, such as metals (e.g., Zn, Cr, Pb) and amines (e.g., benzothiazole). This study points to a need to closely examine the potential regulation of the use of CR on playgrounds and artificial fields.

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The amniote jaw complex is a remarkable amalgamation of derivatives from distinct embryonic cell lineages. During development, the cells in these lineages experience concerted movements, migrations, and signaling interactions that take them from their initial origins to their final destinations and imbue their derivatives with aspects of form including their axial orientation, anatomical identity, size, and shape. Perturbations along the way can produce defects and disease, but also generate the variation necessary for jaw evolution and adaptation. We focus on molecular and cellular mechanisms that regulate form in the amniote jaw complex, and that enable structural and functional integration. Special emphasis is placed on the role of cranial neural crest mesenchyme (NCM) during the species-specific patterning of bone, cartilage, tendon, muscle, and other jaw tissues. We also address the effects of biomechanical forces during jaw development and discuss ways in which certain molecular and cellular responses add adaptive and evolutionary plasticity to jaw morphology. Overall, we highlight how variation in molecular and cellular programs can promote the phenomenal diversity and functional morphology achieved during amniote jaw evolution or lead to the range of jaw defects and disease that affect the human condition.

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Evolution of the large-yolked, amniotic egg required mechanisms by which extracellular yolk could be made available for embryonic development. In birds, the endodermal lining of the yolk sac absorbs and digests the yolk. In contrast, recent studies on lizards and snakes (squamates) have revealed that yolk is processed by means of a proliferating mass of "spaghetti-like" strands formed by endodermal cells attached to anastomosing blood vessels. To clarify the method of yolk processing in chelonians, we applied electron microscopy to an extensive series of embryos of the pond slider turtle, Trachemys scripta. Our findings demonstrate that proliferating endodermal cells phagocytose yolk spheres. These cells remain attached to one another following mitosis, thereby forming clumps that progressively occupy the yolk sac cavity. Upon invasion of blood vessels, the cells become organized into elongated, vascularized "spaghetti-like" strands of cells like those found in squamates. Residual yolk found in the body cavity of new hatchlings chiefly consists of these vascularized strands. Such strands of cells also develop in the false map turtle, Graptemys pseudographica (Emydidae). We infer that the developmental pattern by which yolk is processed is ancestral for both Chelonia and Reptilia, and therefore must have been modified or abandoned in birds or their archosaur ancestors.

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BACKGROUND: The pharyngeal arches are a series of bulges found on the lateral surface of the head of vertebrate embryos, and it is within these segments that components of the later anatomy are laid down. In most vertebrates, the post-otic pharyngeal arches will form the branchial apparatus, while in amniotes these segments are believed to generate the larynx. It has been unclear how the development of these segments has been altered with the emergence of the amniotes. RESULTS: In this study, we examined the development of pharyngeal arches in amniotes and show that the post-otic pharyngeal arches in this clade are greatly diminished. We find that the post-otic segments do not undergo myogenesis or skeletogenesis, but are remodelled before these processes occur. We also find that nested DLX expression, which is a feature of all the pharyngeal arches in anamniotes, is associated with the anterior segments but less so with the posterior arches in amniotes. We further show that the posterior arches of the mouse embryo fail to properly delineate, which demonstrates the lack of function of these posterior segments in later development. CONCLUSION: In amniotes, there has been a loss of the ancestral "branchial" developmental programme that is a general feature of gnathostomes; myogenesis and skeletogenesis This is likely to have facilitated the emergence of the larynx as a new structure not constrained by the segmental organisation of the posterior pharyngeal region.