Nathan D. Smith

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.

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.

Rethinking the Phylogeny of Scleractinian Corals: A Review of Morphological and Molecular Data

Scleractinian corals, which include the architects of coral reefs, are found throughout the worlds oceans and have left a rich fossil record over their 240 million year history. Their classification has been marked by confusion but recently developed molecular and morphological tools are now leading to a better understanding of the evolutionary history of this important group. Although morphological characters have been the basis of traditional classification in the group, they are relatively few in number. In addition, our current understanding of skeletal growth and homology is limited, and homoplasy is rampant, limiting the usefulness of morphological phylogenetics. Molecular phylogenetic hypotheses for the order, which have been primarily focused on reef-building corals, differ significantly from traditional classification. They suggest that the group is represented by two major lineages and do not support the monophyly of traditional suborders and most traditional families. It appears that once a substantial number of azooxanthellate taxa are included in molecular phylogenetic analyses, basal relationships within the group will be clearly defined. Understanding of relationships at lower taxonomic levels will be best clarified by combined analyses of morphological and molecular characters. Molecular phylogenies are being used to inform our understanding of the evolution of morphological characters in the Scleractinia. Better understanding of the evolution of these characters will help to integrate the systematics of fossil and extant taxa. We demonstrate how the combined use of morphological and molecular tools holds great promise for ending confusion in scleractinian systematics.

Phylogenetic Analysis of Pelecaniformes (Aves) Based on Osteological Data: Implications for Waterbird Phylogeny and Fossil Calibration Studies

Background Debate regarding the monophyly and relationships of the avian order Pelecaniformes represents a classic example of discord between morphological and molecular estimates of phylogeny. This lack of consensus hampers interpretation of the groups fossil record, which has major implications for understanding patterns of character evolution (e.g., the evolution of wing-propelled diving) and temporal diversification (e.g., the origins of modern families). Relationships of the Pelecaniformes were inferred through parsimony analyses of an osteological dataset encompassing 59 taxa and 464 characters. The relationships of the Plotopteridae, an extinct family of wing-propelled divers, and several other fossil pelecaniforms (Limnofregata, Prophaethon, Lithoptila, ?Borvocarbo stoeffelensis) were also assessed. The antiquity of these taxa and their purported status as stem members of extant families makes them valuable for studies of higher-level avian diversification. Methodology/Principal Findings Pelecaniform monophyly is not recovered, with Phaethontidae recovered as distantly related to all other pelecaniforms, which are supported as a monophyletic Steganopodes. Some anatomical partitions of the dataset possess different phylogenetic signals, and partitioned analyses reveal that these discrepancies are localized outside of Steganopodes, and primarily due to a few labile taxa. The Plotopteridae are recovered as the sister taxon to Phalacrocoracoidea, and the relationships of other fossil pelecaniforms representing key calibration points are well supported, including Limnofregata (sister taxon to Fregatidae), Prophaethon and Lithoptila (successive sister taxa to Phaethontidae), and ?Borvocarbo stoeffelensis (sister taxon to Phalacrocoracidae). These relationships are invariant when ‘backbone’ constraints based on recent avian phylogenies are imposed. Conclusions/Significance Relationships of extant pelecaniforms inferred from morphology are more congruent with molecular phylogenies than previously assumed, though notable conflicts remain. The phylogenetic position of the Plotopteridae implies that wing-propelled diving evolved independently in plotopterids and penguins, representing a remarkable case of convergent evolution. Despite robust support for the placement of fossil taxa representing key calibration points, the successive outgroup relationships of several “stem fossil + crown family” clades are variable and poorly supported across recent studies of avian phylogeny. Thus, the impact these fossils have on inferred patterns of temporal diversification depends heavily on the resolution of deep nodes in avian phylogeny.

Morphology's role in phylogeny reconstruction: perspectives from paleontology.

A recent article by Scotland et al. (2003; hereafter referred to as SEA) purporting to examine the value of morphological data in phylogeny reconstruction has been received critically by several systematists (Jenner, 2004; Wiens, 2004). As paleontologists—and in an area of systematics restricted solely to morphological data—we take exception to many of the arguments put forward by SEA and feel we may provide a unique perspective in the debate. In their paper, SEA argued for a redefined role for morphology in phylogeny reconstruction, one in which “rigorous and critical anatomical studies of fewer morphological characters, in the context of molecular phylogenies, is a more fruitful approach to integrating the strengths of morphological data with those of sequence data” (p. 539). Such a statement is bold and therefore warrants a critical analysis, as it would effectively neuter the ability of morphological data to generate novel phylogenies. Though issues such as accuracy, support, character coding, and character conceptualization were discussed by SEA, in all cases these discussions resorted to a “too few characters” argument. As the authors characterized it, the “main constraint of morphology-based phylogenetic inference concerns the limited number of unambiguous characters available for analysis in a transformational framework” (p. 539). Additionally, the merits of increased taxon sampling in the context of morphological data were discussed by SEA, and found to be lacking. Though several of the views presented by SEA are not novel (see Hedges and Sibley, 1994, and Hedges and Maxson, 1996), they provide the most detailed recent discussion of this position. We agree with many of the points made by SEA, especially the call for more critical and rigorous analysis of morphology; however, we draw different conclusions from the data. It is our goal to reexamine some of the arguments put forward by SEA, in order to illustrate that a much more optimistic conclusion exists regarding the current and future role of morphology in phylogeny reconstruction.

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.

A Megaraptor-like theropod (Dinosauria: Tetanurae) in Australia: support for faunal exchange across eastern and western Gondwana in the Mid-Cretaceous

The fossil record of Australian dinosaurs in general, and theropods in particular, is extremely sparse. Here we describe an ulna from the Early Cretaceous Eumeralla Formation of Australia that shares unique autapomorphies with the South American theropod Megaraptor. We also present evidence for the spinosauroid affinities of Megaraptor. This ulna represents the first Australian non-avian theropod with unquestionable affinities to taxa from other Gondwanan landmasses, suggesting faunal interchange between eastern and western Gondwana during the Mid-Cretaceous. This evidence counters claims of Laurasian affinities for Early Cretaceous Australian dinosaur faunas, and for the existence of a geographical or climatic barrier isolating Australia from the other Gondwanan continents during this time. The temporal and geographical distribution of Megaraptor and the Eumeralla ulna is also inconsistent with traditional palaeogeographic models for the fragmentation of Gondwana, but compatible with several alternative models positing connections between South America and Antarctica in the Mid-Cretaceous.

Body mass and foraging ecology predict evolutionary patterns of skeletal pneumaticity in the diverse "waterbird" clade.

Extensive skeletal pneumaticity (air‐filled bone) is a distinguishing feature of birds. The proportion of the skeleton that is pneumatized varies considerably among the >10,000 living species, with notable patterns including increases in larger bodied forms, and reductions in birds employing underwater pursuit diving as a foraging strategy. I assess the relationship between skeletal pneumaticity and body mass and foraging ecology, using a dataset of the diverse “waterbird” clade that encompasses a broad range of trait variation. Inferred changes in pneumaticity and body mass are congruent across different estimates of phylogeny, whereas pursuit diving has evolved independently between two and five times. Phylogenetic regressions detected positive relationships between body mass and pneumaticity, and negative relationships between pursuit diving and pneumaticity, whether independent variables are considered in isolation or jointly. Results are generally consistent across different estimates of topology and branch lengths. “Predictive” analyses reveal that several pursuit divers (loons, penguins, cormorants, darters) are significantly apneumatic compared to their relatives, and provide an example of how phylogenetic information can increase the statistical power to detect taxa that depart from established trait correlations. These findings provide the strongest quantitative comparative support yet for classical hypotheses regarding the evolution of avian skeletal pneumaticity.

Anatomy and Affinities of Large Archosauromorphs from the Lower Fremouw Formation (Early Triassic) of Antarctica

ABSTRACT The vertebrate assemblage of the lower Fremouw Formation has been studied for nearly 50 years, but many components remain poorly known. We describe a partial presacral vertebra and the distal end of a left humerus collected just above the Permian—Triassic boundary in the Shackleton Glacier region of the central Transantarctic Mountains. Our identification of these specimens as archosauromorphs that represent at least one taxon of large-bodied archosauriform increases the known reptile diversity of the Fremouw Formation considerably, and provides the first definitive evidence for the presence of Archosauriformes in the Early Triassic of Antarctica. These records increase faunal similarities between the lower Fremouw Formation and other Early Triassic assemblages. Although the lower Fremouw assemblage is typically considered a subset of the coeval Lystrosaurus Assemblage Zone (LAZ) of South Africa, the discrepancy in inferred body size between the Antarctic specimens and Proterosuchus fergusi, coupled with the fact that the LAZ of the Karoo Basin has been sampled much more thoroughly, suggests a real disparity in the maximum body size of apex carnivores between the lower Fremouw assemblage and the LAZ. The lower Fremouw specimens also demonstrate that one or more lineages of archosauriform had attained the large body size characteristic of later members of the clade very soon after the end-Permian mass extinction. This offers a point of contrast with the global pattern of post-extinction terrestrial communities, which are typified by a marked reduction in body size (the ‘Lilliput effect’).

A new species of Threskiornithidae-like bird (Aves, Ciconiiformes) from the Green River Formation (Eocene) of Wyoming

ABSTRACT A new avian species from the late early Eocene Fossil Butte Member of the Green River Formation is described based on a nearly complete postcranial skeleton. The new species, Vadaravis brownae, gen. et sp. nov., can be diagnosed by a unique combination of characters, including the following autapomorphies, which are unique among Aves: two (cranial and caudal) small and discrete pneumatopores on the lateral sides of the caudal-most thoracic centra; and a caudoventrally located pisiform process of the carpometacarpus that projects only weakly cranially. Phylogenetic analyses recover Vadaravis as a member of the waterbird assemblage (including, e.g., penguins, storks, pelicans), closely related to taxa traditionally placed within the avian order Ciconiiformes (storks, flamingos, herons, the hamerkop, ibises, and spoonbills). Additional morphological features and a phylogenetic analysis constrained by a recently recovered waterbird topology suggest close affinities between Vadaravis and Threskiornithidae. This new species represents the first proposed part of Ciconiiformes (and possibly stem-Threskiornithidae) in the Green River Formation of North America. Its discovery increases the known taxonomic and ecological diversity of this diverse fossil avifauna. Vadaravis also represents one of the oldest members of Ciconiiformes (and possibly stem-Threskiornithidae), and implies that additional lineages within the waterbird assemblage had diverged by the late early Eocene.