New reptile shows dinosaurs and pterosaurs evolved among diverse precursors.

Dinosaurs and pterosaurs have remarkable diversity and disparity through most of the Mesozoic Era1-3. Soon after their origins, these reptiles diversified into a number of long-lived lineages, evolved unprecedented ecologies (for example, flying, large herbivorous forms) and spread across Pangaea4,5. Recent discoveries of dinosaur and pterosaur precursors6-10 demonstrated that these animals were also speciose and widespread, but those precursors have few if any well-preserved skulls, hands and associated skeletons11,12. Here we present a well-preserved partial skeleton (Upper Triassic, Brazil) of the new lagerpetid Venetoraptor gassenae gen. et sp. nov. that offers a more comprehensive look into the skull and ecology of one of these precursors. Its skull has a sharp, raptorial-like beak, preceding that of dinosaurs by around 80 million years, and a large hand with long, trenchant claws that firmly establishes the loss of obligatory quadrupedalism in these precursor lineages. Combining anatomical information of the new species with other dinosaur and pterosaur precursors shows that morphological disparity of precursors resembles that of Triassic pterosaurs and exceeds that of Triassic dinosaurs. Thus, the 'success' of pterosaurs and dinosaurs was a result of differential survival among a broader pool of ecomorphological variation. Our results show that the morphological diversity of ornithodirans started to flourish among early-diverging lineages and not only after the origins of dinosaurs and pterosaurs.

Functional adaptive landscapes predict terrestrial capacity at the origin of limbs.

The acquisition of terrestrial, limb-based locomotion during tetrapod evolution has remained a subject of debate for more than a century1,2. Our current understanding of the locomotor transition from water to land is largely based on a few exemplar fossils such as Tiktaalik3, Acanthostega4, Ichthyostega5 and Pederpes6. However, isolated bony elements may reveal hidden functional diversity, providing a more comprehensive evolutionary perspective7. Here we analyse 40 three-dimensionally preserved humeri from extinct tetrapodomorphs that span the fin-to-limb transition and use functionally informed ecological adaptive landscapes8-10 to reconstruct the evolution of terrestrial locomotion. We show that evolutionary changes in the shape of the humerus are driven by ecology and phylogeny and are associated with functional trade-offs related to locomotor performance. Two divergent adaptive landscapes are recovered for aquatic fishes and terrestrial crown tetrapods, each of which is defined by a different combination of functional specializations. Humeri of stem tetrapods share a unique suite of functional adaptations, but do not conform to their own predicted adaptive peak. Instead, humeri of stem tetrapods fall at the base of the crown tetrapod landscape, indicating that the capacity for terrestrial locomotion occurred with the origin of limbs. Our results suggest that stem tetrapods may have used transitional gaits5,11 during the initial stages of land exploration, stabilized by the opposing selective pressures of their amphibious habits. Effective limb-based locomotion did not arise until loss of the ancestral 'L-shaped' humerus in the crown group, setting the stage for the diversification of terrestrial tetrapods and the establishment of modern ecological niches12,13.

Origins of mammalian vertebral function revealed through digital bending experiments.

Unravelling the functional steps that underlie major transitions in the fossil record is a significant challenge for biologists owing to the difficulties of interpreting functional capabilities of extinct organisms. New computational modelling approaches provide exciting avenues for testing function in the fossil record. Here, we conduct digital bending experiments to reconstruct vertebral function in non-mammalian synapsids, the extinct forerunners of mammals, to provide insights into the functional underpinnings of the synapsid-mammal transition. We estimate range of motion and stiffness of intervertebral joints in eight non-mammalian synapsid species alongside a comparative sample of extant tetrapods, including salamanders, reptiles and mammals. We show that several key aspects of mammalian vertebral function evolved outside crown Mammalia. Compared to early diverging non-mammalian synapsids, cynodonts stabilized the posterior trunk against lateroflexion, while evolving axial rotation in the anterior trunk. This was later accompanied by posterior sagittal bending in crown mammals, and perhaps even therians specifically. Our data also support the prior hypothesis that functional diversification of the mammalian trunk occurred via co-option of existing morphological regions in response to changing selective demands. Thus, multiple functional and evolutionary steps underlie the origin of remarkable complexity in the mammalian backbone.

Variation in the sacrum of phytosaurs: New evidence from a partial skeleton of Machaeroprosopus mccauleyi.

Phytosaurs are a group of Upper Triassic semi-aquatic archosauriform reptiles. Their variable skull morphology forms the foundation of our understanding of their relationships and paleoecology, while only a few studies have focused on demonstrating the existence of postcranial variation. The numbers of vertebrae in the sacrum are thought to vary from two, the plesiomorphic condition for archosauriforms, to three, with the addition of a sacralized dorsal (i.e., dorsosacral) vertebra. In this study, we demonstrate the presence of a sacralized first caudal (i.e., caudosacral) vertebra in a sacrum belonging to Machaeroprosopus mccauleyi. We rule out taphonomic distortion or pathology as explanations for the inclusion of this element in the sacrum, suggesting instead that it occurred through modifications of the same developmental processes that likely produced dorsosacral vertebrae in phytosaurs. Additionally, we show that a dorsosacral vertebra is common in phytosaur specimens from the Chinle Formation and Dockum Group of the southwestern United States and suggest that it may be widespread among phytosaurs. The addition of sacral vertebrae potentially aided adaptation to larger body sizes or more terrestrial lifestyles in certain taxa.

A new pseudosuchian from the Favret Formation of Nevada reveals that archosauriforms occupied coastal regions globally during the Middle Triassic.

Recent studies suggest that both stem- and crown-group Archosauria encompassed high ecological diversity during their initial Triassic radiation. We describe a new pseudosuchian archosaur, Benggwigwishingasuchus eremicarminis gen. et sp. nov., from the Anisian (Middle Triassic) Fossil Hill Member of the Favret Formation (Nevada, USA), a pelagic setting in the eastern Panthalassan Ocean characterized by the presence of abundant ammonoids and large-bodied ichthyosaurs. Coupled with archosauriforms from the eastern and western Tethys Ocean, Benggwigwishingasuchus reveals that pseudosuchians were also components of Panthalassan ocean coastal settings, establishing that the group occupied these habitats globally during the Middle Triassic. However, Benggwigwishingasuchus, Qianosuchus, and Ticinosuchus (two other pseudosuchians known from marine sediments) are not recovered in a monophyletic group, demonstrating that a nearshore marine lifestyle occurred widely across Archosauriformes during this time. Benggwigwishingasuchus is recovered as part of an expanded Poposauroidea, including several taxa (e.g. Mandasuchus, Mambawakalae) from the Middle Triassic Manda Beds of Tanzania among its basally branching members. This implies a greater undiscovered diversity of poposauroids during the Early Triassic, and supports that the group, and pseudosuchians more broadly, diversified rapidly following the End-Permian mass extinction.

Levels of homology and the problem of neocortex.

The neocortex is found only in mammals, and the fossil record is silent on how this soft tissue evolved. Understanding neocortex evolution thus devolves to a search for candidate homologous neocortex traits in the extant nonmammalian amniotes. The difficulty is that homology is based on similarity, and the six-layered neocortex structure could hardly be more dissimilar in appearance from the nuclear organization that is so conspicuous in the dorsal telencephalon of birds and other reptiles. Recent molecular data have, however, provided new support for one prominent hypothesis, based on neuronal circuits, that proposes the principal neocortical input and output cell types are a conserved feature of amniote dorsal telencephalon. Many puzzles remain, the greatest being understanding the selective pressures and molecular mechanisms that underlie such tremendous morphological variation in telencephalon structure.

Palaeohistology reveals an unusual periodontium and tooth implantation in a filter-feeding pterodactyloid pterosaur, Pterodaustro guinazui, from the Lower Cretaceous of Argentina.

Pterosaurs are an extinct group of Mesozoic flying reptiles, which exhibited high diversity with regard to their dentition. Although morphological features of pterosaur dentition have been described in detail in several contributions, the histology of tooth and tooth attachment tissues (i.e. periodontium) has been scarcely analysed to date for this clade. Here we describe and interpret the microstructure of the tooth and periodontium attachment tissues of Pterodaustro guinazui, a filter-feeding pterodactyloid pterosaur from the Lower Cretaceous of Argentina. The histological analysis of the lower jaw and its filamentous teeth verifies that the geometry of the implantation corresponds to an aulacodont condition (i.e. teeth are set in a groove with no interdental separation). This pattern departs from that recorded in other archosaurs, being possibly also present in other, non-closely related, pterosaurs. Regarding tooth attachment, in contrast to other pterosaurs, there is no direct evidence for gomphosis in Pterodaustro (i.e. the absence of cementum, mineralized periodontal ligamentum and alveolar bone). Nevertheless, the current evidence for ankylosis is still not conclusive. Contrary to that reported for other archosaurs, replacement teeth are absent in Pterodaustro, which is interpreted as evidence for monophyodonty or diphyodonty in this taxon. Most of the microstructural features are possibly related to the complex filter-feeding apparatus of Pterodaustro and does not appear to represent the general pattern of pterosaurs.

Locomotor and postural diversity among reptiles viewed through the prism of femoral microanatomy: Palaeobiological implications for some Permian and Mesozoic taxa.

The water-to-land transition by the first tetrapod vertebrates represents a key stage in their evolution. Selection pressures exerted by this new environment on animals led to the emergence of new locomotor and postural strategies that favoured access to different ecological niches and contributed to their evolutionary success. Today, amniotes show great locomotor and postural diversity, particularly among Reptilia, whose extant representatives include parasagittally locomoting erect and crouched bipeds (birds), sub-parasagittal 'semi-erect' quadrupeds (crocodylians) and sprawling quadrupeds (squamates and turtles). But the different steps leading to such diversity remain enigmatic and the type of locomotion adopted by many extinct species raises questions. This is notably the case of certain Triassic taxa such as Euparkeria and Marasuchus. The exploration of the bone microanatomy in reptiles could help to overcome these uncertainties. Indeed, this locomotor and postural diversity is accompanied by great microanatomical disparity. On land, the bones of the appendicular skeleton support the weight of the body and are subject to multiple constraints that partly shape their external and internal morphology. Here we show how microanatomical parameters measured in cross-section, such as bone compactness or the position of the medullocortical transition, can be related to locomotion. We hypothesised that this could be due to variations in cortical thickness. Using statistical methods that take phylogeny into account (phylogenetic flexible discriminant analyses), we develop different models of locomotion from a sample of femur cross-sections from 51 reptile species. We use these models to infer locomotion and posture in 7 extinct reptile taxa for which they remain debated or not fully clear. Our models produced reliable inferences for taxa that preceded and followed the quadruped/biped and sprawling/erect transitions, notably within the Captorhinidae and Dinosauria. For taxa contemporary with these transitions, such as Terrestrisuchus and Marasuchus, the inferences are more questionable. We use linear models to investigate the effect of body mass and functional ecology on our inference models. We show that body mass seems to significantly impact our model predictions in most cases, unlike the functional ecology. Finally, we illustrate how taphonomic processes can impact certain microanatomical parameters, especially the eccentricity of the section, while addressing some other potential limitations of our methods. Our study provides insight into the evolution of enigmatic locomotion in various early reptiles. Our models and methods could be used by palaeontologists to infer the locomotion and posture in other extinct reptile taxa, especially when considered in combination with other lines of evidence.

Neuroanatomy of the crocodylomorph Portugalosuchus azenhae from the late cretaceous of Portugal.

We present the first detailed braincase anatomical description and neuroanatomical study of Portugalosuchus azenhae, from the Cenomanian (Late Cretaceous) of Portugal. This eusuchian crocodylomorph was originally described as a putative Crocodylia and one of the oldest representatives of this clade; however, its phylogenetic position remains controversial. Based on new data obtained from high resolution Computed Tomography images (by micro-CT scan), this study aims to improve the original description of this taxon and also update the scarce neuroanatomical knowledge of Eusuchia and Crocodylia from this time interval, a key period to understand the origin and evolution of these clades. The resulting three-dimensional models from the CT data allowed a detailed description of its well-preserved neurocranium and internal cavities. Therefore, it was possible to reconstruct the cavities of the olfactory region, nasopharyngeal ducts, brain, nerves, carotid arteries, blood vessels, paratympanic sinus system and inner ear, which allowed to estimate some neurosensorial capabilities. By comparison with other crocodylomorphs, these analyses showed that Portugalosuchus, back in the Cenomanian, already displayed an olfactive acuity, sight, hearing and cognitive skills within the range of that observed in other basal eusuchians and crocodylians, including extant species. In addition, and in order to test its disputed phylogenetic position, these new anatomical data, which helped to correct and complete some of the original observations, were included in one of the most recent morphology-based phylogenies. The position of Portugalosuchus differs slightly from the original publication since it is now located as a "thoracosaurid" within Gavialoidea, but still as a crocodylian. Despite all this, to better contrast these results, additional phylogenetic analyses including this new morphological character coding together with DNA data should be performed.

Creation of forest edges has a global impact on forest vertebrates.

Forest edges influence more than half of the world's forests and contribute to worldwide declines in biodiversity and ecosystem functions. However, predicting these declines is challenging in heterogeneous fragmented landscapes. Here we assembled a global dataset on species responses to fragmentation and developed a statistical approach for quantifying edge impacts in heterogeneous landscapes to quantify edge-determined changes in abundance of 1,673 vertebrate species. We show that the abundances of 85% of species are affected, either positively or negatively, by forest edges. Species that live in the centre of the forest (forest core), that were more likely to be listed as threatened by the International Union for Conservation of Nature (IUCN), reached peak abundances only at sites farther than 200-400 m from sharp high-contrast forest edges. Smaller-bodied amphibians, larger reptiles and medium-sized non-volant mammals experienced a larger reduction in suitable habitat than other forest-core species. Our results highlight the pervasive ability of forest edges to restructure ecological communities on a global scale.

Global ecomorphological restructuring of dominant marine reptiles prior to the Cretaceous-Palaeogene mass extinction.

Mosasaurid squamates were the dominant amniote predators in marine ecosystems during most of the Late Cretaceous. Here, we use a suite of biomechanically rooted, functionally descriptive ratios in a framework adapted from population ecology to investigate how the morphofunctional disparity of mosasaurids evolved prior to the Cretaceous-Palaeogene (K/Pg) mass extinction. Our results suggest that taxonomic turnover in mosasaurid community composition from Campanian to Maastrichtian is reflected by a notable global increase in morphofunctional disparity, especially driving the North American record. Ecomorphospace occupation becomes polarized during the Late Maastrichtian, with morphofunctional disparity plateauing in the Southern Hemisphere and decreasing in the Northern Hemisphere. We show that these changes are not strongly associated with mosasaurid size, but rather with the functional capacities of their skulls. Our novel approach indicates that mosasaurid morphofunctional disparity was in decline in multiple provincial communities before the K/Pg mass extinction, highlighting region-specific patterns of disparity evolution and the importance of assessing vertebrate extinctions both globally and locally. Ecomorphological differentiation in mosasaurid communities, coupled with declines in other formerly abundant marine reptile groups, indicates widespread restructuring of higher trophic levels in marine food webs was well underway when the K/Pg mass extinction took place.

Re-description of the early Triassic diapsid Palacrodon from the lower Fremouw formation of Antarctica.

The rapid radiation and dispersal of crown reptiles following the end-Permian mass extinction characterizes the earliest phase of the Mesozoic. Phylogenetically, this early radiation is difficult to interpret, with polytomies near the crown node, long ghost lineages, and enigmatic origins for crown group clades. Better understanding of poorly known taxa from this time can aid in our understanding of this radiation and Permo-Triassic ecology. Here, we describe an Early Triassic specimen of the diapsid Palacrodon from the Fremouw Formation of Antarctica. While Palacrodon is known throughout the Triassic and exhibits a cosmopolitan geographic range, little is known of its evolutionary relationships. We recover Palacrodon outside of crown reptiles (Sauria) but more crownward than Youngina capensis and other late Permian diapsids. Furthermore, Palacrodon possesses anatomical features that add clarity to the evolution of the stapes within the reptilian lineage, as well as incipient adaptations for arboreality and herbivory during the earliest phases of the Permo-Triassic recovery.

Dietary niche partitioning in Early Jurassic ichthyosaurs from Strawberry Bank.

Jurassic ichthyosaurs dominated upper trophic levels of marine ecosystems. Many species coexisted alongside each another, and it is uncertain whether they competed for the same array of food or divided dietary resources, each specializing in different kinds of prey. Here, we test whether feeding differences existed between species, applying finite element analysis to ichthyosaurs for the first time. We examine two juvenile ichthyosaur specimens, referred to Hauffiopteryx typicus and Stenopterygius triscissus, from the Strawberry Bank Lagerstätte, a shallow marine environment from the Early Jurassic of southern England (Toarcian, ~183 Ma). Snout and cranial robusticity differ between the species, with S. triscissus having a more robust snout and cranium and specializing in slow biting of hard prey, and H. typicus with its slender snout specializing in fast, but weaker bites on fast-moving, but soft prey. The two species did not differ in muscle forces, but stress distributions varied in the nasal area, reflecting differences when biting at different points along the tooth row: the more robustly snouted Stenopterygius resisted increases or shifts in stress distribution when the bite point was shifted from the posterior to the mid-point of the tooth row, but the slender-snouted Hauffiopteryx showed shifts and increases in stress distributions between these two bite points. The differences in cranial morphology, dentition and inferred stresses between the two species suggest adaptations for dietary niche partitioning.

Diphyodont tooth replacement of Brasilodon-A Late Triassic eucynodont that challenges the time of origin of mammals.

Two sets of teeth (diphyodonty) characterise extant mammals but not reptiles, as they generate many replacement sets (polyphyodonty). The transition in long-extinct species from many sets to only two has to date only been reported in Jurassic eucynodonts. Specimens of the Late Triassic brasilodontid eucynodont Brasilodon have provided anatomical and histological data from three lower jaws of different growth stages. These reveal ordered and timed replacement of deciduous by adult teeth. Therefore, this diphyodont dentition, as contemporary of the oldest known dinosaurs, shows that Brasilodon falls within a range of wide variations of typically mammalian, diphyodont dental patterns. Importantly, these three lower jaws represent distinct ontogenetic stages that reveal classic features for timed control of replacement, by the generation of only one replacement set of teeth. This data shows that the primary premolars reveal a temporal replacement pattern, importantly from directly below each tooth, by controlled regulation of tooth resorption and regeneration. The complexity of the adult prismatic enamel structure with a conspicuous intra-structural Schmelzmuster array suggests that, as in the case of extant mammals, this extinct species would have probably sustained higher metabolic rates than reptiles. Furthermore, in modern mammals, diphyodonty and prismatic enamel are inextricably linked, anatomically and physiologically, to a set of other traits including placentation, endothermy, fur, lactation and even parental care. Our analysis of the osteodental anatomy of Brasilodon pushes back the origin of diphyodonty and consequently, its related biological traits to the Norian (225.42 ± 0.37 myr), and around 25 myr after the End-Permian mass extinction event.

Current Status of the Hypothesis of a Claustro-Insular Homolog in Sauropsids.

The author previously worked extensively on the broad problem of the evolution of the vertebrate pallium. He proposed various Bauplan models covering at least gnathostomes, based in the definition of a set of pallial sectors with topologically invariant positional relationships and distinct molecular profiles. Out of one of these models, presented as the "updated tetrapartite pallium model," a modified definition of the earlier lateral pallium sector (LPall) concept emerged, characterizing it in mammals as an unitary claustro-insular transitional (mesocortical) complex intercalated between the neocortex or dorsal pallium (DPall) above and olfactory cortex or ventral pallium (VPall) underneath. A distinctive molecular marker of the early-born deep claustral component of the LPall was found to be the transcription factor Nr4a2, which is not expressed significantly in the overlying insular cortex or in adjoining cortical territories. Given that earlier comparative studies had identified molecularly and topologically comparable VPall, LPall, and DPall sectors in the avian pallium, an avian Nr4a2 probe was applied, aiming to identify the reportedly absent avian claustro-insular complex. An early-born superficial subpopulation of the avian LPall that expresses this marker selectively through development was indeed found. This was proposed to be a claustrum homolog, whereas the remaining Nr4a2-negative avian LPall cells were assumed to represent a possible insular homolog. This last notion was subsequently supported by comparable selective expression of the mouse insular marker Cyp26b, also found restricted to the avian LPall. Some published data suggested that similar molecular properties and structure apply at the reptilian LPall. This analysis was reviewed in Puelles et al. [The pallium in reptiles and birds in the light of the updated tetrapartite pallium model. 2017]. Four years on, the present commentary discusses some international publications accrued in the interval that touch on the claustro-insular homology hypothesis. Some of them are opposed to the hypothesis whereas others corroborate or support it. This raises a number of secondary issues of general interest.

Homology and osteological correlates of pedal muscles among extant sauropsids.

Archosaurs displayed an evolutionary trend toward increasing bipedalism in their evolutionary history, that is, forelimbs tend to be reduced in contrast to the development of hindlimbs becoming major weight-bearing and locomotor appendages. The archosaurian locomotion has been extensively discussed based on their limb morphology because the latter reflects their locomotor modes very well. However, despite some attempts of reconstructing the hindlimb musculature in Archosauria, that of the most distal portion, the pes, has often been neglected. In order to rectify this trend, detailed homologies of pedal muscles among sauropsids were established based on dissections and literature reviews of adult conditions. As a result, homologies of some pedal muscles between non-avian sauropsids and avians were revised, challenging classical hypotheses. The present new hypothesis postulates that the avian m. tibialis cranialis and non-avian m. extensor digitorum longus, as well as the avian m. extensor digitorum longus and non-avian m. tibialis anterior, are homologous with each other, respectively. This is more plausible because it requires no drastical change in the attachment sites between the avian and non-avian homologues unlike the classical hypothesis. Many interosseous muscles in non-archosaurian sauropsids that have long been regarded as a part of short digital extensors or flexors are also divided into multiple distinct muscles so that they can be homologized with short pedal muscles among all sauropsids. In addition, osteological correlates of attachments are identified for most of the pedal muscles, contributing to future attempts of reconstruction of this muscle system in fossil archosaurs.

Interrogating Genomic-Scale Data for Squamata (Lizards, Snakes, and Amphisbaenians) Shows no Support for Key Traditional Morphological Relationships.

Genomics is narrowing uncertainty in the phylogenetic structure for many amniote groups. For one of the most diverse and species-rich groups, the squamate reptiles (lizards, snakes, and amphisbaenians), an inverse correlation between the number of taxa and loci sampled still persists across all publications using DNA sequence data and reaching a consensus on the relationships among them has been highly problematic. In this study, we use high-throughput sequence data from 289 samples covering 75 families of squamates to address phylogenetic affinities, estimate divergence times, and characterize residual topological uncertainty in the presence of genome-scale data. Importantly, we address genomic support for the traditional taxonomic groupings Scleroglossa and Macrostomata using novel machine-learning techniques. We interrogate genes using various metrics inherent to these loci, including parsimony-informative sites (PIS), phylogenetic informativeness, length, gaps, number of substitutions, and site concordance to understand why certain loci fail to find previously well-supported molecular clades and how they fail to support species-tree estimates. We show that both incomplete lineage sorting and poor gene-tree estimation (due to a few undesirable gene properties, such as an insufficient number of PIS), may account for most gene and species-tree discordance. We find overwhelming signal for Toxicofera, and also show that none of the loci included in this study supports Scleroglossa or Macrostomata. We comment on the origins and diversification of Squamata throughout the Mesozoic and underscore remaining uncertainties that persist in both deeper parts of the tree (e.g., relationships between Dibamia, Gekkota, and remaining squamates; among the three toxicoferan clades Iguania, Serpentes, and Anguiformes) and within specific clades (e.g., affinities among gekkotan, pleurodont iguanians, and colubroid families).

A basal ichthyosauriform with a short snout from the Lower Triassic of China.

The incompleteness of the fossil record obscures the origin of many of the more derived clades of vertebrates. One such group is the Ichthyopterygia, a clade of obligatory marine reptiles that appeared in the Early Triassic epoch, without any known intermediates. Here we describe a basal ichthyosauriform from the upper Lower Triassic (about 248 million years ago) of China, whose primitive skeleton indicates possible amphibious habits. It is smaller than ichthyopterygians and had unusually large flippers that probably allowed limited terrestrial locomotion. It also retained characteristics of terrestrial diapsid reptiles, including a short snout and body trunk. Unlike more-derived ichthyosauriforms, it was probably a suction feeder. The new species supports the sister-group relationships between ichthyosauriforms and Hupehsuchia, the two forming the Ichthyosauromorpha. Basal ichthyosauromorphs are known exclusively from south China, suggesting that the clade originated in the region, which formed a warm and humid tropical archipelago in the Early Triassic. The oldest unequivocal record of a sauropterygian is also from the same stratigraphic unit of the region.