Randall B. Irmis

Best Practices for Justifying Fossil Calibrations

Our ability to correlate biological evolution with climate change, geological evolution, and other historical patterns is essential to understanding the processes that shape biodiversity. Combining data from the fossil record with molecular phylogenetics represents an exciting synthetic approach to this challenge. The first molecular divergence dating analysis (Zuckerkandl and Pauling 1962) was based on a measure of the amino acid differences in the hemoglobin molecule, with replacement rates established (calibrated) using paleontological age estimates from textbooks (e.g., Dodson 1960). Since that time, the amount of molecular sequence data has increased dramatically, affording ever-greater opportunities to apply molecular divergence approaches to fundamental problems in evolutionary biology. To capitalize on these opportunities, increasingly sophisticated divergence dating methods have been, and continue to be, developed. In contrast, comparatively, little attention has been devoted to critically assessing the paleontological and associated geological data used in divergence dating analyses. The lack of rigorous protocols for assigning calibrations based on fossils raises serious questions about the credibility of divergence dating results (e.g., Shaul and Graur 2002; Brochu et al. 2004; Graur and Martin 2004; Hedges and Kumar 2004; Reisz and Muller 2004a, 2004b; Theodor 2004; van Tuinen and Hadly 2004a, 2004b; van Tuinen et al. 2004; Benton and Donoghue 2007; Donoghue and Benton 2007; Parham and Irmis 2008; Ksepka 2009; Benton et al. 2009; Heads 2011). The assertion that incorrect calibrations will negatively influence divergence dating studies is not controversial. Attempts to identify incorrect calibrations through the use of a posteriori methods are available (e.g., Near and Sanderson 2004; Near et al. 2005; Rutschmann et al. 2007; Marshall 2008; Pyron 2010; Dornburg et al. 2011). We do not deny that a posteriori methods are a useful means of evaluating calibrations, but there can be no substitute for a priori assessment of the veracity of paleontological data. Incorrect calibrations, those based upon fossils that are phylogenetically misplaced or assigned incorrect ages, clearly introduce error into an analysis. Consequently, thorough and explicit justification of both phylogenetic and chronologic age assessments is necessary for all fossils used for calibration. Such explicit justifications will help to ensure that divergence dating studies are based on the best available data. Unfortunately, the majority of previously published calibrations lack explicit explanations and justifications of the age and phylogenetic position of the key fossils. In the absence of explicit justifications, it is difficult to distinguish between correct and incorrect calibrations, and it becomes difficult to reevaluate previous claims in light of new data. Paleontology is a dynamic science, with new data and perspectives constantly emerging as a result of new discoveries (see Kimura 2010 for a recent case where the age of the earliest known record of a clade was more than doubled). Calibrations based upon the best available evidence at a given time can become inappropriate as the discovery of new specimens, new phylogenetic analyses, and ongoing stratigraphic and geochronologic revisions refine our understanding of the fossil record. Our primary goals in this paper are to establish the best practices for justifying fossils used for the temporal calibration of molecular phylogenies. Our examples derive mainly, but not exclusively, from the vertebrate fossil record. We hope that our recommendations will lead to more credible calibrations and, as a result, more reliable divergence dates throughout the tree of life. A secondary goal is to help the community (researchers, editors, and reviewers) who might be unfamiliar with fossils to understand and overcome the challenges associated with using paleontological data. In order to accomplish these goals, we present a specimen-based protocol for selecting and documenting relevant fossils and discuss future directions for evaluating and utilizing phylogenetic and temporal data from the fossil record. We likewise encourage biologists relying on nonfossil calibrations for molecular divergence estimates (e.g., ages of island or mountain range formations, continental drift, and biomarkers) to develop their own set of rigorous guidelines so that their calibrations may also be evaluated in a systematic way.

AXIAL SKELETON ONTOGENY IN THE PARASUCHIA (ARCHOSAURIA: PSEUDOSUCHIA) AND ITS IMPLICATIONS FOR ONTOGENETIC DETERMINATION IN ARCHOSAURS

Abstract The sequence of neurocentral suture closure is one criterion for the determination of ontogenetic stage in extant crocodylians. This pattern is frequently used to assess ontogeny for a variety of fossil archosaurs that may or may not follow the same sequence and timing of suture closure. Phytosaurs are one of the few basal archosaur groups with a sample size large enough to help test whether the crocodylian pattern of suture closure is plesiomorphic for Pseudosuchia and Archosauria. Analysis of a large sample of North American phytosaur specimens confirms that phytosaurs share the crocodylian state of closure, and so this pattern is probably plesiomorphic for the Pseudosuchia. An additional independent ontogenetic trend observed in phytosaurs is that the lateral fossae on cervical vertebrae in phytosaurs deepen with ontogeny. A preliminary survey indicates that there is considerable variation of both the sequence and timing of neurocentral suture closure in other archosaur clades. Therefore, it is unwise to apply a priori the crocodylian pattern to other archosaur groups to determine ontogenetic stage. Currently, apart from histological data, there are few if any reliable independent criteria for determining ontogenetic stage. I propose that histology be integrated with independent ontogenetic criteria (such as neurocentral suture closure) and morphometric data to provide a better understanding of archosaur ontogeny.

Ecologically distinct dinosaurian sister group shows early diversification of Ornithodira.

The early evolutionary history of Ornithodira (avian-line archosaurs) has hitherto been documented by incomplete (Lagerpeton) or unusually specialized forms (pterosaurs and Silesaurus). Recently, a variety of Silesaurus-like taxa have been reported from the Triassic period of both Gondwana and Laurasia, but their relationships to each other and to dinosaurs remain a subject of debate. Here we report on a new avian-line archosaur from the early Middle Triassic (Anisian) of Tanzania. Phylogenetic analysis places Asilisaurus kongwe gen. et sp. nov. as an avian-line archosaur and a member of the Silesauridae, which is here considered the sister taxon to Dinosauria. Silesaurids were diverse and had a wide distribution by the Late Triassic, with a novel ornithodiran bauplan including leaf-shaped teeth, a beak-like lower jaw, long, gracile limbs, and a quadrupedal stance. Our analysis suggests that the dentition and diet of silesaurids, ornithischians and sauropodomorphs evolved independently from a plesiomorphic carnivorous form. As the oldest avian-line archosaur, Asilisaurus demonstrates the antiquity of both Ornithodira and the dinosaurian lineage. The initial diversification of Archosauria, previously documented by crocodilian-line archosaurs in the Anisian, can now be shown to include a contemporaneous avian-line radiation. The unparalleled taxonomic diversity of the Manda archosaur assemblage indicates that archosaur diversification was well underway by the Middle Triassic or earlier.

A Complete Skeleton of a Late Triassic Saurischian and the Early Evolution of Dinosaurs

Early Dinosaur Discovery Our understanding of the evolution of early dinosaurs is hampered by limited material, especially compared to the many Jurassic and Cretaceous samples. Nesbitt et al. (p. 1530) provide a complete view of a Late Triassic theropod based on several nearly complete skeletons from New Mexico. The dinosaur elucidates the likely relationships between early theropods and shows that some prominent features were already derived by this time. Comparison among Triassic dinosaur fauna and other early species suggests that Triassic North American fauna were diverse but not endemic, perhaps arising from earlier migrants from South America. A complete theropod from New Mexico implies that early dinosaurs dispersed widely, perhaps originating from South America. Characterizing the evolutionary history of early dinosaurs is central to understanding their rise and diversification in the Late Triassic. However, fossils from basal lineages are rare. A new theropod dinosaur from New Mexico is a representative of the early North American diversification. Known from several nearly complete skeletons, it reveals a mosaic of plesiomorphic and derived features that clarify early saurischian dinosaur evolution and provide evidence for the antiquity of novel avian character systems including skeletal pneumaticity. The taxon further reveals latitudinal differences among saurischian assemblages during the Late Triassic, demonstrates that the theropod fauna from the Late Triassic of North America was not endemic, and suggests that intercontinental dispersal was prevalent during this time.

Early ornithischian dinosaurs: the Triassic record

Abstract Ornithischian dinosaurs are one of the most taxonomically diverse dinosaur clades during the Mesozoic, yet their origin and early diversification remain virtually unknown. In recent years, several new Triassic ornithischian taxa have been proposed, mostly based upon isolated teeth. New discoveries of skeletal material of some of these tooth taxa indicate that these teeth can no longer be assigned to the Ornithischia using unambiguous synapomorphies. The Triassic record of ornithischian dinosaurs now comprises only three probable occurrences: Pisanosaurus and an unnamed heterodontosaurid from Argentina, and an unnamed specimen from the uppermost Triassic of South Africa. This revised Triassic record suggests that ornithischians were not very diverse or abundant through the Triassic, and there are large gaps in the Triassic ornithischian fossil record. Moreover, traditional living analogues for interpreting the feeding ecology of early ornithischians from their tooth morphology are generally inappropriate, and “herbivorous” archosaur teeth such as those found in early ornithischians are not necessarily diagnostic of herbivorous feeding.

A critical re‐evaluation of the Late Triassic dinosaur taxa of North America

Synopsis The North American Triassic dinosaur record has been repeatedly cited as one of the most complete early dinosaur assemblages. The discovery of Silesaurus from Poland and the recognition that Herrerasaurus and Eoraptor may not be theropods have forced a re‐evaluation of saurischian and theropod synapomorphies. Here, we re‐evaluate each purported Triassic dinosaur from North America on a specimen by specimen basis using an apomorphy‐based approach. We attempt to assign specimens to the most exclusive taxon possible. Our revision of purported Late Triassic dinosaur material from North America indicates that dinosaurs were rarer and less diverse in these strata than previously thought. This analysis concludes that non‐dinosaurian dinosauriforms were present in North America in the Late Triassic. Most of the proposed theropod specimens are fragmentary and/or indistinguishable from corresponding elements in the only well‐known Triassic theropod of North America, Coelophysis bauri. No Triassic material from North America can be assigned to Sauropodomorpha, because none of the purported ‘prosauropod’ material is diagnostic. Recent discovery of the skull and skeleton of Revueltosaurus callenderi from Arizona shows that it is a pseudosuchian archosaur, not an ornithischian dinosaur. As a result, other purported North American ornithischian teeth cannot be assigned to the Ornithischia and therefore, there are no confirmed North American Triassic ornithischians. Non‐tetanuran theropods and possible basal saurischians are the only identifiable dinosaurs recognised in North America until the beginning of the Jurassic Period.

The Late Triassic pseudosuchian Revueltosaurus callenderi and its implications for the diversity of early ornithischian dinosaurs

A new discovery of skeletons of Revueltosaurus callenderi from the Upper Triassic Chinle Formation of Petrified Forest National Park, Arizona clearly shows that Revueltosaurus is not an ornithischian dinosaur as previously supposed. Features such as the presence of a postfrontal, crocodile-normal ankle and paramedian osteoderms with anterior bars place R. callenderi within the Pseudosuchia, closer to crocodylomorphs than to dinosaurs. Therefore, dental characters previously used to place Revueltosaurus within the Ornithischia evolved convergently among other archosaur taxa, and cannot be used to diagnose ornithischian dinosaur teeth. As a result, all other putative North American Late Triassic ornithischians, which are all based exclusively on teeth, are cast into doubt. The only reasonably well-confirmed Late Triassic ornithischians worldwide are Pisanosaurus mertii and an unnamed heterodontosaurid from Argentina. This considerably changes the understanding of early dinosaur diversity, distribution and evolution in the Late Triassic.

Evaluating hypotheses for the early diversification of dinosaurs

Many hypotheses have been proposed for the rise of dinosaurs, but their early diversification remains poorly understood. This paper examines the occurrences, species diversity and abundance of early dinosaurs at both regional and global scales to determine patterns of their early evolutionary history. Four main patterns are clear: (1) sauropodomorph dinosaurs became abundant during the late Norian–Rhaetian of Gondwana and Europe; (2) Triassic dinosaurs of North America have low species diversity and abundance until the beginning of the Jurassic; (3) sauropodomorphs and ornithischians are absent in the Triassic of North America; and (4) ornithischian dinosaurs maintain low species diversity, relative abundance and small body size until the Early Jurassic. No one hypothesis fully explains these data. There is no evidence for a Carnian–Norian extinction event, but sauropodomorphs did become abundant during the Norian in some assemblages. No clear connection exists between palaeoenvironment and early dinosaur diversity, but environmental stress at the Triassic–Jurassic boundary is consistent with changes in North American dinosaur assemblages. Elevated growth rates in dinosaurs are consistent with the gradual phyletic increase in body size. This study demonstrates that early dinosaur diversification was a complex process that was geographically diachronous and probably had several causes.

Hindlimb Osteology and Distribution of Basal Dinosauromorphs from the Late Triassic of North America

ABSTRACT The recent discovery of early dinosauromorphs from North America demonstrates that they were contemporaries with dinosaurs and other basal archosaurs during a substantial portion of the Late Triassic Period. Hindlimb material (femora, tibiae, a fibula, astragalocalcanea, and phalanges) of Dromomeron romeri, a non-dinosauriform dinosauromorph from the Petrified Forest Member of the Chinle Formation from north-central New Mexico, is described. A new species of Dromomeron from the lower portion of the Chinle Formation (eastern Arizona) and Dockum Group (northern Texas) is also described, based on several disarticulated femora and tibiae. D. romeri, Lagerpeton, and the new taxon form the sister group to all other dinosauromorphs and demonstrate that this clade, Lagerpetidae, persisted well into the Norian. Lagerpetidae is supported by several synapomorphies: femoral head hook-shaped in medial and lateral views; ventral emargination on the anterolateral side of the femoral head; an enlarged posteromedial tuber of the proximal end of the femur; femoral crista tibiofibularis larger than the medial condyle; anteromedial corner of the distal end of the femur forms 90° or acute (>90°) angle; and a posterior ascending process of the astragalus. An ontogenetic series of the femur of Dromomeron indicates that some character states previously used in phylogenetic analyses of early dinosaurs may be ontogenetically variable.

The precise temporal calibration of dinosaur origins.

Significance Many hypotheses have been put forth to explain the origin and early radiation of dinosaurs, but poor age constraints for constituent fossil assemblages make these scenarios difficult to test. Using precise radioisotopic ages, we demonstrate that the temporal gap between assemblages containing only dinosaur precursors and those with the first dinosaurs was 5–10 million years shorter than previously thought. Thus, these data suggest that the origin of dinosaurs was a relatively rapid evolutionary event. Combined with our synthesis of paleoecological data, we demonstrate there was little compositional difference between the dinosaur precursor assemblages and the earliest dinosaur assemblages, and thus, the initial appearance of dinosaurs was not associated with a fundamental shift in ecosystem composition, as classically stated. Dinosaurs have been major components of ecosystems for over 200 million years. Although different macroevolutionary scenarios exist to explain the Triassic origin and subsequent rise to dominance of dinosaurs and their closest relatives (dinosauromorphs), all lack critical support from a precise biostratigraphically independent temporal framework. The absence of robust geochronologic age control for comparing alternative scenarios makes it impossible to determine if observed faunal differences vary across time, space, or a combination of both. To better constrain the origin of dinosaurs, we produced radioisotopic ages for the Argentinian Chañares Formation, which preserves a quintessential assemblage of dinosaurian precursors (early dinosauromorphs) just before the first dinosaurs. Our new high-precision chemical abrasion thermal ionization mass spectrometry (CA-TIMS) U–Pb zircon ages reveal that the assemblage is early Carnian (early Late Triassic), 5- to 10-Ma younger than previously thought. Combined with other geochronologic data from the same basin, we constrain the rate of dinosaur origins, demonstrating their relatively rapid origin in a less than 5-Ma interval, thus halving the temporal gap between assemblages containing only dinosaur precursors and those with early dinosaurs. After their origin, dinosaurs only gradually dominated mid- to high-latitude terrestrial ecosystems millions of years later, closer to the Triassic–Jurassic boundary.