Peter J. Makovicky

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.

Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs

How evolutionary changes in body size are brought about by variance in developmental timing and/or growth rates (also known as heterochrony) is a topic of considerable interest in evolutionary biology. In particular, extreme size change leading to gigantism occurred within the dinosaurs on multiple occasions. Whether this change was brought about by accelerated growth, delayed maturity or a combination of both processes is unknown. A better understanding of relationships between non-avian dinosaur groups and the newfound capacity to reconstruct their growth curves make it possible to address these questions quantitatively. Here we study growth patterns within the Tyrannosauridae, the best known group of large carnivorous dinosaurs, and determine the developmental means by which Tyrannosaurus rex, weighing 5,000 kg and more, grew to be one of the most enormous terrestrial carnivorous animals ever. T. rex had a maximal growth rate of 2.1 kg d-1, reached skeletal maturity in two decades and lived for up to 28 years. T. rexs great stature was primarily attained by accelerating growth rates beyond that of its closest relatives.

The earliest dromaeosaurid theropod from South America

The evolutionary history of Maniraptora, the clade of carnivorous dinosaurs that includes birds and the sickle-clawed Dromaeosauridae, has hitherto been largely restricted to Late Jurassic and Cretaceous deposits on northern continents. The stunning Early Cretaceous diversity of maniraptorans from Liaoning, China, coupled with a longevity implied by derived Late Jurassic forms such as Archaeopteryx, pushes the origins of maniraptoran lineages back to Pangaean times and engenders the possibility that such lineages existed in Gondwana. A few intriguing, but incomplete, maniraptoran specimens have been reported from South America, Africa and Madagascar. Their affinities remain contested, however, and they have been interpreted as biogeographic anomalies relative to other faunal components of these land-masses. Here we describe a near-complete, small dromaeosaurid that is both the most complete and the earliest member of the Maniraptora from South America, and which provides new evidence for a unique Gondwanan lineage of Dromaeosauridae with an origin predating the separation between northern and southern landmasses.

A basal troodontid from the Early Cretaceous of China.

Troodontid dinosaurs form one of the most avian-like dinosaur groups. Their phylogenetic position is hotly debated, and they have been allied with almost all principal coelurosaurian lineages. Here we report a basal troodontid dinosaur, Sinovenator changii gen. et sp. nov., from the lower Yixian Formation of China. This taxon has several features that are not found in more derived troodontids, but that occur in dromaeosaurids and avialans. The discovery of Sinovenator and the examination of character distributions along the maniraptoran lineage indicate that principal structural modifications toward avians were acquired in the early stages of maniraptoran evolution.

A Review of Dromaeosaurid Systematics and Paravian Phylogeny

Abstract Coelurosauria is the most diverse clade of theropod dinosaurs. Much of this diversity is present in Paraves—the clade of dinosaurs containing dromaeosaurids, troodontids, and avialans. Paraves has over 160 million years of evolutionary history that continues to the present day. The clade represents the most diverse living tetrapod group (there are over 9000 extant species of Aves—a word used here as synonomous with “bird”), and it is at the root of the paravian radiation, when dromaeosaurids, troodontids, and avialans were diverging from one another, that we find the morphology and soft tissue changes associated with the origin of modern avian flight. Within the first 15 million years of known paravian evolutionary history members of this clade exhibited a difference of nearly four orders of magnitude in body size, a value that is similar to the extreme body size disparity present today in mammalian carnivorans, avians, and varanoid squamates. In this respect, Paraves is an important case study in characterizing the patterns, processes, and dynamics of evolutionary size change. This last point is of particular interest because of the historical significance placed on the role of body size reduction in the origin of powered avian flight. Our study reviews and revises the membership of Dromaeosauridae and provides an apomorphy-based diagnosis for all valid taxa. Of the currently 31 named dromaeosaurid species, we found 26 to be valid. We provide the most detailed and comprehensive phylogenetic analysis of paravians to date in order to explore the phylogenetic history of dromaeosaurid taxa. The general pattern of paravian relationships is explored within the broader context of Coelurosauria with an emphasis on sampling basal avialans, because of their importance for character optimizations at the base of Paraves. A large dataset was constructed by merging two datasets, one examining coelurosaur relationships broadly (based on previous TWiG datasets) and the other examining avialan relationships specifically (Clarke et al., 2006). This merged dataset was then significantly revised and supplemented with novel character analysis focusing on paravian taxa. During character analysis, particular attention was given to basal members of Dromaeosauridae, enigmatic basal paravians such as Jinfengopteryx elegans and Anchiornis huxleyi, and the incorporation of new morphological information from two undescribed troodontid species from the Late Cretaceous of Mongolia. A final dataset of 474 characters scored for 111 taxa was used to address paravian evolution. This dataset is important in that it bridges a phylogenetic gap that had persisted between studies on birds and studies on all other coelurosaurs. Most scorings in this matrix were based on the direct observation of specimens. All most parsimonious trees recovered in the cladistic analysis support the monophyly of Paraves, Troodontidae, Dromaeosauridae, and Deinonychosauria. A new clade of basal troodontids is discovered including two undescribed Mongolian troodontids and Jinfengopteryx elegans. Xiaotingia and Anchiornis form a clade at the base of Troodontidae. Recently proposed relationships within Dromaeosauridae are further supported and a succession of clades from Gondwana and Asia form sister taxa to a clade of Laurasian dromaeosaurids. Avialan monophyly is strongly supported with Archaeopteryx, Sapeornis, Jeholornis, and Jixiangornis forming the successive sister taxa to the Confuciusornis node. This topology supports a more basal position for Sapeornis than previous phylogenetic analyses and indicates a progressive acquisition of a fully “avian” shoulder morphology.

Tyrannosaur Paleobiology: New Research on Ancient Exemplar Organisms

Tyrannosaurs Revisited Tyrannosaurs represent some of the most successful and largest carnivores in Earths history. An expanding fossil record has allowed studies of their evolution and behavior that now allow broader comparisons with other groups, not just dinosaurs. Brusatte et al. (p. 1481) review the biology and evolutionary history of tyrannosaurs and update their phylogenetic relations to include several new fossils. The analysis suggests that tyrannosaurs remained relatively small (less than about 5 meters long) until the Late Cretaceous (about 80 million years ago). Tyrannosaurs, the group of dinosaurian carnivores that includes Tyrannosaurus rex and its closest relatives, are icons of prehistory. They are also the most intensively studied extinct dinosaurs, and thanks to large sample sizes and an influx of new discoveries, have become ancient exemplar organisms used to study many themes in vertebrate paleontology. A phylogeny that includes recently described species shows that tyrannosaurs originated by the Middle Jurassic but remained mostly small and ecologically marginal until the latest Cretaceous. Anatomical, biomechanical, and histological studies of T. rex and other derived tyrannosaurs show that large tyrannosaurs could not run rapidly, were capable of crushing bite forces, had accelerated growth rates and keen senses, and underwent pronounced changes during ontogeny. The biology and evolutionary history of tyrannosaurs provide a foundation for comparison with other dinosaurs and living organisms.

A New Dromaeosaurid Theropod from Ukhaa Tolgod (Ömnögov, Mongolia)

Abstract We describe a new dromaeosaurid theropod from the Upper Cretaceous Djadokhta Formation of Ukhaa Tolgod, Mongolia. The new taxon, Tsaagan mangas, consists of a well-preserved skull and cervical series. This specimen marks only the second dromaeosaurid taxon from a formation that has otherwise yielded numerous specimens of Velociraptor mongoliensis, and Tsaagan mangas is the only dromaeosaurid known from Ukhaa Tolgod beyond sporadic occurrences of isolated teeth. Tsaagan mangas differs from other dromaeosaurids in the possession of a straight, untwisted, and pendulous paroccipital process, a large and anteriorly located maxillary fenestra, and a jugal–squamosal contact that excludes the postorbital from the margin of the infratemporal fenestra. The phylogenetic affinities of Tsaagan mangas are determined through a comprehensive phylogenetic analysis of Coelurosauria, confirming its position within Dromaeosauridae. This new specimen, coupled with CT imaging, provides new information on the skull and braincase anatomy of dromaeosaurids.

An Early Ostrich Dinosaur and Implications for Ornithomimosaur Phylogeny

Abstract A new ornithomimosaur from the Yixian Formation of Liaoning Province Peoples Republic of China is described. These beds are near the Jurassic-Cretaceous boundary. This specimen is interesting because it has several primitive characters for ornithomimosaurs such as teeth and a short first metacarpal. This taxon is placed in a phylogenetic analysis of Coelurosauria and shown to be near the base of the ornithomimosaur clade. Using this phylogeny we comment on the biogeographic history of this group.

A Ceratopsian dinosaur from China and the early evolution of Ceratopsia

Ceratopsians (horned dinosaurs) represent one of the last and the most diverse radiations of non-avian dinosaurs. Although recent systematic work unanimously supports a basal division of Ceratopsia into parrot-like psittacosaurids and frilled neoceratopsians, the early evolution of the group remains poorly understood, mainly owing to its incomplete early fossil record. Here we describe a primitive ceratopsian from China. Cladistic analysis posits this new species as the most basal neoceratopsian. This new taxon demonstrates that some neoceratopsian characters evolved in a more incremental fashion than previously known and also implies mosaic evolution of characters early in ceratopsian history.

Osteology and Relationships of Byronosaurus jaffei (Theropoda: Troodontidae)

Abstract The troodontid Byronosaurus jaffei is known from two specimens from adjacent localities in the Nemegt basin, Ömnögov Aimag, Mongolia. These specimens are composed of well-preserved cranial material and fragmentary postcrania. All of these elements are described here. Byronosaurus jaffei is included in a comprehensive phylogenetic analysis of Coelurosauria to ascertain its relationships. Several interesting characters of Byronosaurus jaffei have implications both for theropod relationships and for understanding patterns of variation within coelurosaurian theropods. These include the position of a foramen that marks the exit of the supra-alveolar canal (which we suggest is homologous with the subnarial foramen), the flattened internarial bar, the unusual interfenestral bar, and the unserrated teeth. Additionally, the well-preserved braincase allows detailed comparison with other troodontid taxa.