Bhart-Anjan S. Bhullar

Birds have paedomorphic dinosaur skulls

The interplay of evolution and development has been at the heart of evolutionary theory for more than a century. Heterochrony—change in the timing or rate of developmental events—has been implicated in the evolution of major vertebrate lineages such as mammals, including humans. Birds are the most speciose land vertebrates, with more than 10,000 living species representing a bewildering array of ecologies. Their anatomy is radically different from that of other vertebrates. The unique bird skull houses two highly specialized systems: the sophisticated visual and neuromuscular coordination system allows flight coordination and exploitation of diverse visual landscapes, and the astonishing variations of the beak enable a wide range of avian lifestyles. Here we use a geometric morphometric approach integrating developmental, neontological and palaeontological data to show that the heterochronic process of paedomorphosis, by which descendants resemble the juveniles of their ancestors, is responsible for several major evolutionary transitions in the origin of birds. We analysed the variability of a series of landmarks on all known theropod dinosaur skull ontogenies as well as outgroups and birds. The first dimension of variability captured ontogeny, indicating a conserved ontogenetic trajectory. The second dimension accounted for phylogenetic change towards more bird-like dinosaurs. Basally branching eumaniraptorans and avialans clustered with embryos of other archosaurs, indicating paedomorphosis. Our results reveal at least four paedomorphic episodes in the history of birds combined with localized peramorphosis (development beyond the adult state of ancestors) in the beak. Paedomorphic enlargement of the eyes and associated brain regions parallels the enlargement of the nasal cavity and olfactory brain in mammals. This study can be a model for investigations of heterochrony in evolutionary transitions, illuminating the origin of adaptive features and inspiring studies of developmental mechanisms.

Mass extinction of lizards and snakes at the Cretaceous–Paleogene boundary

The Cretaceous–Paleogene (K-Pg) boundary is marked by a major mass extinction, yet this event is thought to have had little effect on the diversity of lizards and snakes (Squamata). A revision of fossil squamates from the Maastrichtian and Paleocene of North America shows that lizards and snakes suffered a devastating mass extinction coinciding with the Chicxulub asteroid impact. Species-level extinction was 83%, and the K-Pg event resulted in the elimination of many lizard groups and a dramatic decrease in morphological disparity. Survival was associated with small body size and perhaps large geographic range. The recovery was prolonged; diversity did not approach Cretaceous levels until 10 My after the extinction, and resulted in a dramatic change in faunal composition. The squamate fossil record shows that the end-Cretaceous mass extinction was far more severe than previously believed, and underscores the role played by mass extinctions in driving diversification.

A transitional snake from the Late Cretaceous period of North America

Snakes are the most diverse group of lizards, but their origins and early evolution remain poorly understood owing to a lack of transitional forms. Several major issues remain outstanding, such as whether snakes originated in a marine or terrestrial environment and how their unique feeding mechanism evolved. The Cretaceous Coniophis precedens was among the first Mesozoic snakes discovered, but until now only an isolated vertebra has been described and it has therefore been overlooked in discussions of snake evolution. Here we report on previously undescribed material from this ancient snake, including the maxilla, dentary and additional vertebrae. Coniophis is not an anilioid as previously thought; a revised phylogenetic analysis of Ophidia shows that it instead represents the most primitive known snake. Accordingly, its morphology and ecology are critical to understanding snake evolution. Coniophis occurs in a continental floodplain environment, consistent with a terrestrial rather than a marine origin; furthermore, its small size and reduced neural spines indicate fossorial habits, suggesting that snakes evolved from burrowing lizards. The skull is intermediate between that of lizards and snakes. Hooked teeth and an intramandibular joint indicate that Coniophis fed on relatively large, soft-bodied prey. However, the maxilla is firmly united with the skull, indicating an akinetic rostrum. Coniophis therefore represents a transitional snake, combining a snake-like body and a lizard-like head. Subsequent to the evolution of a serpentine body and carnivory, snakes evolved a highly specialized, kinetic skull, which was followed by a major adaptive radiation in the Early Cretaceous period. This pattern suggests that the kinetic skull was a key innovation that permitted the diversification of snakes.

A molecular mechanism for the origin of a key evolutionary innovation, the bird beak and palate, revealed by an integrative approach to major transitions in vertebrate history

The avian beak is a key evolutionary innovation whose flexibility has permitted birds to diversify into a range of disparate ecological niches. We approached the problem of the mechanism behind this innovation using an approach bridging paleontology, comparative anatomy, and experimental developmental biology. First, we used fossil and extant data to show the beak is distinctive in consisting of fused premaxillae that are geometrically distinct from those of ancestral archosaurs. To elucidate underlying developmental mechanisms, we examined candidate gene expression domains in the embryonic face: the earlier frontonasal ectodermal zone (FEZ) and the later midfacial WNT‐responsive region, in birds and several reptiles. This permitted the identification of an autapomorphic median gene expression region in Aves. To test the mechanism, we used inhibitors of both pathways to replicate in chicken the ancestral amniote expression. Altering the FEZ altered later WNT responsiveness to the ancestral pattern. Skeletal phenotypes from both types of experiments had premaxillae that clustered geometrically with ancestral fossil forms instead of beaked birds. The palatal region was also altered to a more ancestral phenotype. This is consistent with the fossil record and with the tight functional association of avian premaxillae and palate in forming a kinetic beak.

AN ARCHOSAUR-LIKE LATEROSPHENOID IN EARLY TURTLES (REPTILIA: PANTESTUDINES)

Abstract Turtles are placed with increasing consistency by molecular phylogenetic studies within Diapsida as sister to Archosauria, but published gross morphology–based phylogenetic analyses do not recover this position. Here, we present a previously unrecognized unique morphological character offering support for this hypothesis: the presence in stem turtles of a laterosphenoid ossification identical to that in Archosauriformes. The laterosphenoid is a tripartite chondrocranial ossification, consisting of an ossified pila antotica, pila metoptica, and taenia medialis + planum supraseptale. It forms the anterior border of the exit for the trigeminal nerve (V) and partially encloses the exits for cranial nerves III, IV, and II. This ossification is unique to turtles and Archosauriformes within Vertebrata. It has been mistakenly dismissed as anatomically dissimilar in these two groups in the past, so we provide a complete description and detailed analysis of correspondence between turtles and Archosauriformes in each of its embryologically distinct components. A preliminary phylogenetic analysis suggests other potential synapomorphies of turtles and archosaurs, including a row or rows of mid-dorsal dermal ossifications.

The Euro-American genus Eopelobates, and a re-definition of the family Pelobatidae (Amphibia, Anura)

The extinct Eopelobates (Eocene of western North America; Eocene–Pliocene of Europe) and Pelobates (Oligocene–Recent of Europe; Recent of northern Africa and the Middle East) are superficially toad-like anurans that are united within the family Pelobatidae mainly on the basis of a unique, tripartite frontoparietal complex. Both genera have a relatively good fossil record consisting of isolated bones, skeletons, and developmental series of tadpoles through adults, all of which are potentially informative for tracing the evolutionary history of the family. Eopelobates is of interest for several reasons. Of the two pelobatid genera, Eopelobates appears earlier in the fossil record (early Eocene vs. late Oligocene) and it is more primitive in lacking many of the features associated with fossoriality in extant Pelobates. The taxonomic composition of Eopelobates has been contentious and at least one putative new species has long been recognised, but never formally named. Here, we provide updated taxonomic accounts for Pelobatoidea, Pelobatidae, Pelobates, and Eopelobates and document development within a series of tadpoles and juveniles of E. bayeri from Bechlejovice (late Oligocene in age), Czech Republic. We also provide updated accounts for the five previously named and currently accepted species of Eopelobates. For the European congeners, E. anthracinus (late Oligocene) and E. bayeri (early Oligocene–middle Miocene) can confidently be regarded as separate species; although the distinction between E. hinschei and E. wagneri (both middle Eocene) is less certain, we provisionally maintain them as separate species. Micro-CT scans for the holotype skeleton of E. grandis (latest Eocene, USA) help resolve some problematic features, most notably showing that the cranial sculpture is of the pit-and-ridge style that is typical for Eopelobates. A sixth congener is named and described based on two skeletons from the middle Eocene portion of the Green River Formation, in Wyoming, USA. We caution that reports of Eopelobates-like anurans from the pre-Eocene of western North America and the early Eocene of India are based on isolated bones that cannot be assigned with confidence to that genus. The presence of Eopelobates in both North America and Europe may be explained by dispersal via the high latitude land bridge that connected those two continents during the late Paleocene through Eocene. The pelobatid fossil record is informative for documenting the nature and timing of changes in cranial features (e.g. ornament patterns, shape of nasals, pattern of frontoparietal–squamosal contact) from the inferred primitive condition seen in most Eopelobates to the more derived condition seen in extant Pelobates, but it is less informative for tracing the evolution of fossoriality, which is a key attribute of extant Pelobates.

A Phylogenetic Approach to Ontogeny and Heterochrony in the Fossil Record: Cranial Evolution and Development in Anguimorphan Lizards (Reptilia: Squamata)

The incorporation of ontogeny into the interpretation of the vertebrate fossil record promises major advances in palaeontology, systematics, and macroevolution. Here, a key additional component, the incorporation of phylogenetic bracketing into ontogenetic considerations, is demonstrated using cranial anatomy in anguimorphan lizards, a diverse modern clade with an extensive fossil record. The obstacles of fragmentary disarticulated fossil material and low representation in museum collections are overcome by using detailed analysis of individual elements and binning into broad ontogenetic stages, respectively. Results indicate the prevalence of classical macroevolutionary phenomena, notably heterochrony and homoplasy (convergence), throughout anguimorphan evolution. Furthermore, two problematic fossil anguimorph taxa are examined, both of which are unusually small for their clades, suggesting either immaturity or dwarfism. Using extant phylogenetic brackets of ontogenetic trajectories to distinguish between these hypotheses, it is shown that the holotype of one of these taxa is indeed a juvenile (also calling into question its taxonomy) and that the other is a dwarf. It is expected that a phylogenetic approach to ontogeny will yield similar insights across a broad range of fossil and extant organisms.

Molecular characterization of dental development in a toothed archosaur, the American alligator Alligator mississippiensis

Few skeletal structures are as informative of the adaptive natural history of vertebrate animals as their teeth. Understanding principles of tooth development is key to understanding evolution of the vertebrate dentition in general and emergence of multiple specialized tooth types in particular. Morphological and phylogenetic considerations suggest that crocodilians have the most primitive mode of dentition within extant tetrapods, displaying simple, conical, socketed, and continuously replaced teeth. Previous histological studies revealed several dental fates, including functional and non‐functional teeth (rudiments) in the developing alligator embryos. We analyze expression of key odontogenic regulators and markers to better characterize the molecular patterning of crocodilian dentition. Importantly, we demonstrate that the morphologically distinct tooth types in Alligator mississippiensis are distinguishable by differences in their developmental programs. We also present evidence showing that tooth maturation is accompanied by dynamic gene expression in the epithelial and mesenchymal cells involved in tooth development. Our data reveal a significant morphological and genetic variation in early dental fates. We believe that this underlying developmental variation reflects modularity, or the ability of teeth to develop semi‐autonomously along the alligator jaw. We propose that such modularity may have been a crucial for adaptive evolution within Amniota, allowing for the progressive modifications to tooth replacement, number, and shape.

Postnatal development of the skull of Dinilysia patagonica (Squamata-stem Serpentes).

The snake skull represents a profound transformation of the ancestral squamate cranium in which dermal skull roof bones were integrated with the braincase, in a manner convergent with that which occurred during the origin of mammals. However, the ontogeny of snake characters at the origin of the clade has until now been inaccessible. Here we describe a postnatal ontogenetic series of the Late Cretaceous stem snake Dinilysia patagonica and compare it to that of extant lizards and snakes. Comparative analysis indicates notable ontogenetic changes, including advanced state of ossification, isometric growth of the otic capsule, fusion of the stylohyal to the quadrate, and great posterior elongation of the supratemporal. Of these transformations, the unfused condition of braincase bones and the retention of a large otic capsule in adults are examples of paedomorphic and peramorphic processes, respectively. Some ontogenetic transformations detected, in particular those present in middle ear, skull roof and suspensorium, are strikingly similar to those present in extant snakes. Nevertheless, Dinilysia retains a lizard‐like paroccipital process without an epiphyseal extremity, and a calcified epiphysis that caps the sphenoccipital tubercle. Finally, the integration of the dermal skull roof with the braincase is similar to that seen in mammals with regard to the overall closure of the braincase, but the two evolutionary and developmental modules appear less integrated in snakes in that the parietal bone of the dermal skull roof progressively overlaps the supraoccipital of the chondrocranial braincase. Anat Rec, 297:560–573, 2014.

A reevaluation of the unusual abdominal musculature of squamate reptiles (Reptilia: Squamata).

The abdominal muscles of lizards and snakes (Squamata) have been the subject of periodic attention from anatomists, embryologists, and systematists. Until now, the presence of a superficial portion of the m. rectus abdominis, named the m. rectus abdominis lateralis, has been considered a key synapomorphy of the clade Autarchoglossa, which includes all extant squamates save Gekkota and Iguania. However, the precise anatomical relations of the m. rectus abdominis lateralis have never been fully investigated. Here, I show that the m. rectus abdominis lateralis is present in Iguania. Its absence in Gekkota represents rare gross anatomical support for recent molecular‐structure‐based hypotheses of squamate relationships placing geckoes as sister to the remaining squamates. Where present, it is the most superficial trunk muscle, exterior to the m. obliquus externus. The separation of the m. rectus abdominis lateralis from the m. rectus abdominis occurs as the m. obliquus externus aponeurosis and part of the m. obliquus internus aponeurosis emerge superficially to form the outer portion of the rectus sheath. In Autarchoglossa, the contralateral mm. recti abdomines laterales meet at the midline and are attached to the imbricae of the transverse scale rows characteristic of the clade, suggesting developmental, functional, and evolutionary association. Because the m. rectus abdominis lateralis is sometimes continuous with the pectoralis, its exclusive association with the m. rectus abdominis is questionable. It may be a neomorphic layer that is part of the abaxial developmental system, comprising those muscles whose connective tissue is largely derived from lateral plate as opposed to somatic mesoderm. Anat Rec, 292:1154–1161, 2009.