Tyler R. Lyson

Transitional fossils and the origin of turtles

The origin of turtles is one of the most contentious issues in systematics with three currently viable hypotheses: turtles as the extant sister to (i) the crocodile–bird clade, (ii) the lizard–tuatara clade, or (iii) Diapsida (a clade composed of (i) and (ii)). We reanalysed a recent dataset that allied turtles with the lizard–tuatara clade and found that the inclusion of the stem turtle Proganochelys quenstedti and the ‘parareptile’ Eunotosaurus africanus results in a single overriding morphological signal, with turtles outside Diapsida. This result reflects the importance of transitional fossils when long branches separate crown clades, and highlights unexplored issues such as the role of topological congruence when using fossils to calibrate molecular clocks.

Evolutionary origin of the turtle skull

Transitional fossils informing the origin of turtles are among the most sought-after discoveries in palaeontology. Despite strong genomic evidence indicating that turtles evolved from within the diapsid radiation (which includes all other living reptiles), evidence of the inferred transformation between an ancestral turtle with an open, diapsid skull to the closed, anapsid condition of modern turtles remains elusive. Here we use high-resolution computed tomography and a novel character/taxon matrix to study the skull of Eunotosaurus africanus, a 260-million-year-old fossil reptile from the Karoo Basin of South Africa, whose distinctive postcranial skeleton shares many unique features with the shelled body plan of turtles. Scepticism regarding the status of Eunotosaurus as the earliest stem turtle arises from the possibility that these shell-related features are the products of evolutionary convergence. Our phylogenetic analyses indicate strong cranial support for Eunotosaurus as a critical transitional form in turtle evolution, thus fortifying a 40-million-year extension to the turtle stem and moving the ecological context of its origin back onto land. Furthermore, we find unexpected evidence that Eunotosaurus is a diapsid reptile in the process of becoming secondarily anapsid. This is important because categorizing the skull based on the number of openings in the complex of dermal bone covering the adductor chamber has long held sway in amniote systematics, and still represents a common organizational scheme for teaching the evolutionary history of the group. These discoveries allow us to articulate a detailed and testable hypothesis of fenestral closure along the turtle stem. Our results suggest that Eunotosaurus represents a crucially important link in a chain that will eventually lead to consilience in reptile systematics, paving the way for synthetic studies of amniote evolution and development.

A Divergence Dating Analysis of Turtles Using Fossil Calibrations: An Example of Best Practices

Abstract Turtles have served as a model system for molecular divergence dating studies using fossil calibrations. However, because some parts of the fossil record of turtles are very well known, divergence age estimates from molecular phylogenies often do not differ greatly from those observed directly from the fossil record alone. Also, the phylogenetic position and age of turtle fossil calibrations used in previous studies have not been adequately justified. We provide the first explicitly justified minimum and soft maximum age constraints on 22 clades of turtles following best practice protocols. Using these data we undertook a Bayesian relaxed molecular clock analysis establishing a timescale for the evolution of crown Testudines that we exploit in attempting to address evolutionary questions that cannot be resolved with fossils alone. Some of these questions, such as whether the turtle crown originated in the Triassic or Jurassic, cannot be resolved by our analysis. However, our results generate novel age-of-origination estimates for clades within crown Testudines. Finally, we compare our fossil calibrations and posterior age estimates to those from other studies, revealing substantial differences in results and interpretation.

Calibration uncertainty in molecular dating analyses: there is no substitute for the prior evaluation of time priors

Calibration is the rate-determining step in every molecular clock analysis and, hence, considerable effort has been expended in the development of approaches to distinguish good from bad calibrations. These can be categorized into a priori evaluation of the intrinsic fossil evidence, and a posteriori evaluation of congruence through cross-validation. We contrasted these competing approaches and explored the impact of different interpretations of the fossil evidence upon Bayesian divergence time estimation. The results demonstrate that a posteriori approaches can lead to the selection of erroneous calibrations. Bayesian posterior estimates are also shown to be extremely sensitive to the probabilistic interpretation of temporal constraints. Furthermore, the effective time priors implemented within an analysis differ for individual calibrations when employed alone and in differing combination with others. This compromises the implicit assumption of all calibration consistency methods, that the impact of an individual calibration is the same when used alone or in unison with others. Thus, the most effective means of establishing the quality of fossil-based calibrations is through a priori evaluation of the intrinsic palaeontological, stratigraphic, geochronological and phylogenetic data. However, effort expended in establishing calibrations will not be rewarded unless they are implemented faithfully in divergence time analyses.

Toward consilience in reptile phylogeny: miRNAs support an archosaur, not lepidosaur, affinity for turtles

Understanding the phylogenetic position of crown turtles (Testudines) among amniotes has been a source of particular contention. Recent morphological analyses suggest that turtles are sister to all other reptiles, whereas the vast majority of gene sequence analyses support turtles as being inside Diapsida, and usually as sister to crown Archosauria (birds and crocodilians). Previously, a study using microRNAs (miRNAs) placed turtles inside diapsids, but as sister to lepidosaurs (lizards and Sphenodon) rather than archosaurs. Here, we test this hypothesis with an expanded miRNA presence/absence dataset, and employ more rigorous criteria for miRNA annotation. Significantly, we find no support for a turtle + lepidosaur sister‐relationship; instead, we recover strong support for turtles sharing a more recent common ancestor with archosaurs. We further test this result by analyzing a super‐alignment of precursor miRNA sequences for every miRNA inferred to have been present in the most recent common ancestor of tetrapods. This analysis yields a topology that is fully congruent with our presence/absence analysis; our results are therefore in accordance with most gene sequence studies, providing strong, consilient molecular evidence from diverse independent datasets regarding the phylogenetic position of turtles.

Toward consilience in reptile phylogeny

Understanding the phylogenetic position of crown turtles (Testudines) among amniotes has been a source of particular contention. Recent morphological analyses suggest that turtles are sister to all other reptiles, whereas the vast majority of gene sequence analyses support turtles as being inside Diapsida, and usually as sister to crown Archosauria (birds and crocodilians). Previously, a study using microRNAs (miRNAs) placed turtles inside diapsids, but as sister to lepidosaurs (lizards and Sphenodon) rather than archosaurs. Here, we test this hypothesis with an expanded miRNA presence/absence dataset, and employ more rigorous criteria for miRNA annotation. Significantly, we find no support for a turtle + lepidosaur sister‐relationship; instead, we recover strong support for turtles sharing a more recent common ancestor with archosaurs. We further test this result by analyzing a super‐alignment of precursor miRNA sequences for every miRNA inferred to have been present in the most recent common ancestor of tetrapods. This analysis yields a topology that is fully congruent with our presence/absence analysis; our results are therefore in accordance with most gene sequence studies, providing strong, consilient molecular evidence from diverse independent datasets regarding the phylogenetic position of turtles.

A REVISION OF PLESIOBAENA (TESTUDINES: BAENIDAE) AND AN ASSESSMENT OF BAENID ECOLOGY ACROSS THE K/T BOUNDARY

Abstract Over the course of the last two decades, the baenid taxon Plesiobaena has typically been thought to consist of two named species, Plesiobaena antiqua (Campanian) and Plesiobaena putorius (Paleocene), along with an unnamed species from the Maastrichtian, but the interrelationship of these three taxa was never explored in an explicit phylogenetic context. Herein we present or re-describe a number of relevant specimens and provide a cladistic analysis of Baenidae using species only as terminal taxa. The phylogenetic analysis clearly reveals that Plesiobaena in the traditional sense is a paraphyletic assemblage relative to the clade formed by Gamerabaena sonsalla and Palatobaena spp., thus demanding some nomenclatural adjustments. In particular, Plesiobaena putorius is moved to a new genus, Cedrobaena, and the unnamed taxon from the Maastrichtian is formally named Peckemys brinkman. Many of the new Cedrobaena putorius and Peckemys brinkman specimens described herein were found at the Turtle Graveyard locality in Slope County, North Dakota, along with four other turtle taxa, increasing the turtle diversity of this locality to at least six taxa. Although this indicates that Turtle Graveyard is the worlds most diverse fossil turtle thanatocoenosis, a comparable diversity is found in modern river systems in the southeastern United States today. Our phylogenetic analysis indicates that seven out of nine latest Cretaceous baenid turtle lineages survived into the Paleocene, four of which are interpreted as being durophagous.

Spatial niche partitioning in dinosaurs from the latest cretaceous (Maastrichtian) of North America

We examine patterns of occurrence of associated dinosaur specimens (n = 343) from the North American Upper Cretaceous Hell Creek Formation and equivalent beds, by comparing their relative abundance in sandstone and mudstone. Ceratopsians preferentially occur in mudstone, whereas hadrosaurs and the small ornithopod Thescelosaurus show a strong association with sandstone. By contrast, the giant carnivore Tyrannosaurus rex shows no preferred association with either lithology. These lithologies are used as an indicator of environment of deposition, with sandstone generally representing river environments, and finer grained sediments typically representing floodplain environments. Given these patterns of occurrence, we argue that spatial niche partitioning helped reduce competition for resources between the herbivorous dinosaurs. Within coastal lowlands ceratopsians preferred habitats farther away from rivers, whereas hadrosaurs and Thescelosaurus preferred habitats in close proximity to rivers, and T. rex, the ecosystems sole large carnivore, inhabited both palaeoenvironments. Spatial partitioning of the environment helps explain how several species of large herbivorous dinosaurs coexisted. This study emphasizes that different lithologies can preserve dramatically dissimilar vertebrate assemblages, even when deposited in close proximity and within a narrow window of time. The lithology in which fossils are preserved should be recorded as these data can provide unique insights into the palaeoecology of the animals they preserve.

Homology of the enigmatic nuchal bone reveals novel reorganization of the shoulder girdle in the evolution of the turtle shell

The turtle shell represents a unique modification of the ancestral tetrapod body plan. The homologies of its approximately 50 bones have been the subject of debate for more than 200 years. Although most of those homologies are now firmly established, the evolutionary origin of the dorsal median nuchal bone of the carapace remains unresolved. We propose a novel hypothesis in which the nuchal is derived from the paired, laterally positioned cleithra—dorsal elements of the ancestral tetrapod pectoral girdle that are otherwise retained among extant tetrapods only in frogs. This hypothesis is supported by origin of the nuchal as paired, mesenchymal condensations likely derived from the neural crest followed by a unique two‐stage pattern of ossification. Further support is drawn from the establishment of the nuchal as part of a highly conserved “muscle scaffold” wherein the cleithrum (and its evolutionary derivatives) serves as the origin of the Musculus trapezius. Identification of the nuchal as fused cleithra is congruent with its general spatial relationships to other elements of the shoulder girdle in the adult morphology of extant turtles, and it is further supported by patterns of connectivity and transformations documented by critical fossils from the turtle stem group. The cleithral derivation of the nuchal implies an anatomical reorganization of the pectoral girdle in which the dermal portion of the girdle was transformed from a continuous lateral‐ventral arc into separate dorsal and ventral components. This transformation involved the reduction and eventual loss of the scapular rami of the clavicles along with the dorsal and superficial migration of the cleithra, which then fused with one another and became incorporated into the carapace.

New Material of Gilmoremys lancensis nov. comb. (Testudines: Trionychidae) from the Hell Creek Formation and the Diagnosis of Plastomenid Turtles

Abstract Plastomenidae is a poorly diagnosed clade of extinct soft-shelled turtles (Trionychidae) known from the Campanian to Eocene of North America. Five skulls, a mandible, two carapaces, and numerous plastral remains from the Hell Creek Formation (Late Cretaceous, Maastrichtian) of North Dakota and Montana are referable to Gilmoremys lancensis nov. comb., a taxon previously known from a carapace and xiphiplastron only. Gilmoremys lancensis is diagnosed by a carapace that is covered by elongate sinusoidal grooves, distally expanded second costals, hyoplastral shoulders, an extensive secondary palate with accessory ridges, an extremely elongate mandible, a contribution of the parietal to the wall of the orbit, and a posterior ossified narial canal. A phylogenetic analysis of all well-known plastomenid turtles establishes Gilmoremys lancensis as the most basal known plastomenid and reveals that cranial characters are more reliable in diagnosing plastomenid turtles, in particular the contribution of the parietal to the orbit wall and the extensive secondary palate. All plastomenid turtles with a locked entoplastron are placed in Hutchemys. Assuming that all taxa are monophyletic, the phylogenetic analysis implies that the G. lancensis lineage is the only one to go extinct at the K/T boundary, whereas the four remaining plastomenid lineages survive. Extensive ghost ranges are nevertheless apparent. Taphonomic considerations indicate that G. lancensis was a riverine turtle, whereas more derived plastomenids preferred swampy habitats.