New Horned Dinosaurs from Utah Provide Evidence for Intracontinental Dinosaur Endemism

Background

During much of the Late Cretaceous, a shallow, epeiric sea divided North America into eastern and western landmasses. The western landmass, known as Laramidia, although diminutive in size, witnessed a major evolutionary radiation of dinosaurs. Other than hadrosaurs (duck-billed dinosaurs), the most common dinosaurs were ceratopsids (large-bodied horned dinosaurs), currently known only from Laramidia and Asia. Remarkably, previous studies have postulated the occurrence of latitudinally arrayed dinosaur “provinces,” or “biomes,” on Laramidia. Yet this hypothesis has been challenged on multiple fronts and has remained poorly tested.

Methodology/Principal Findings

Here we describe two new, co-occurring ceratopsids from the Upper Cretaceous Kaiparowits Formation of Utah that provide the strongest support to date for the dinosaur provincialism hypothesis. Both pertain to the clade of ceratopsids known as Chasmosaurinae, dramatically increasing representation of this group from the southern portion of the Western Interior Basin of North America. Utahceratops gettyi gen. et sp. nov.—characterized by short, rounded, laterally projecting supraorbital horncores and an elongate frill with a deep median embayment—is recovered as the sister taxon to Pentaceratops sternbergii from the late Campanian of New Mexico. Kosmoceratops richardsoni gen. et sp. nov.—characterized by elongate, laterally projecting supraorbital horncores and a short, broad frill adorned with ten well developed hooks—has the most ornate skull of any known dinosaur and is closely allied to Chasmosaurus irvinensis from the late Campanian of Alberta.

Conclusions/Significance

Considered in unison, the phylogenetic, stratigraphic, and biogeographic evidence documents distinct, co-occurring chasmosaurine taxa north and south on the diminutive landmass of Laramidia. The famous Triceratops and all other, more nested chasmosaurines are postulated as descendants of forms previously restricted to the southern portion of Laramidia. Results further suggest the presence of latitudinally arrayed evolutionary centers of endemism within chasmosaurine ceratopsids during the late Campanian, the first documented occurrence of intracontinental endemism within dinosaurs.     

A longirostrine tyrannosauroid from the Early Cretaceous of China

The fossil record of tyrannosauroid theropods is marked by a substantial temporal and morphological gap between small-bodied, Barremian taxa, and extremely large-bodied taxa from the latest Cretaceous. Here we describe a new tyrannosauroid, Xiongguanlong baimoensis n. gen. et sp., from the Aptian–Albian Xinminpu Group of western China that represents a phylogenetic, morphological, and temporal link between these disjunct portions of tyrannosauroid evolutionary history. Xiongguanlong is recovered in our phylogenetic analysis as the sister taxon to Tyrannosauridae plus Appalachiosaurus, and marks the appearance of several tyrannosaurid hallmark features, including a sharp parietal sagittal crest, a boxy basicranium, a quadratojugal with a flaring dorsal process and a flexed caudal edge, premaxillary teeth bearing a median lingual ridge, and an expanded axial neural spine surmounted by distinct processes at its corners. Xiongguanlong is characterized by a narrow and elongate muzzle resembling that of Alioramus. The slender, unornamented nasals of Xiongguanlong are inconsistent with recent hypotheses of correlated progression in tyrannosauroid feeding mechanics, and suggest more complex patterns of character evolution in the integration of feeding adaptations in tyrannosaurids. Body mass estimates for the full-grown holotype specimen of Xiongguanlong fall between those of Late Cretaceous tyrannosaurids and Barremian tyrannosauroids, suggesting that the trend of increasing body size observed in North American Late Cretaceous Tyrannosauridae may extend through the Cretaceous history of Tyrannosauroidea though further phylogenetic work is required to corroborate this.     

Skull Ecomorphology of Megaherbivorous Dinosaurs from the Dinosaur Park Formation (Upper Campanian) of Alberta,Canada

Megaherbivorous dinosaur coexistence on the Late Cretaceous island continent of Laramidia has long puzzled researchers, owing to the mystery of how so many large herbivores (6–8 sympatric species, in many instances) could coexist on such a small (4–7 million km²) landmass. Various explanations have been put forth, one of which–dietary niche partitioning–forms the focus of this study. Here, we apply traditional morphometric methods to the skulls of megaherbivorous dinosaurs from the Dinosaur Park Formation (upper Campanian) of Alberta to infer the ecomorphology of these animals and to test the niche partitioning hypothesis. We find evidence for niche partitioning not only among contemporaneous ankylosaurs, ceratopsids, and hadrosaurids, but also within these clades at the family and subfamily levels. Consubfamilial ceratopsids and hadrosaurids differ insignificantly in their inferred ecomorphologies, which may explain why they rarely overlap stratigraphically: interspecific competition prevented their coexistence.     

The origin and early evolution of metatherian mammals: the Cretaceous record

Metatherians, which comprise marsupials and their closest fossil relatives, were one of the most dominant clades of mammals during the Cretaceous and are the most diverse clade of living mammals after Placentalia. Our understanding of this group has increased greatly over the past 20 years, with the discovery of new specimens and the application of new analytical tools. Here we provide a review of the phylogenetic relationships of metatherians with respect to other mammals, discuss the taxonomic definition and diagnosis of Metatheria, outline the Cretaceous history of major metatherian clades, describe the paleobiology, biogeography, and macroevolution of Cretaceous metatherians, and provide a physical and climatic background of Cretaceous metatherian faunas. Metatherians are a clade of boreosphendian mammals that must have originated by the Late Jurassic, but the first unequivocal metatherian fossil is from the Early Cretaceous of Asia. Metatherians have the distinctive tightly interlocking occlusal molar pattern of tribosphenic mammals, but differ from Eutheria in their dental formula and tooth replacement pattern, which may be related to the metatherian reproductive process which includes an extended period of lactation followed by birth of extremely altricial young. Metatherians were widespread over Laurasia during the Cretaceous, with members present in Asia, Europe, and North America by the early Late Cretaceous. In particular, they were taxonomically and morphologically diverse and relatively abundant in the Late Cretaceous of western North America, where they have been used to examine patterns of biogeography, macroevolution, diversification, and extinction through the Late Cretaceous and across the Cretaceous-Paleogene (K-Pg) boundary. Metatherian diversification patterns suggest that they were not strongly affected by a Cretaceous Terrestrial Revolution, but they clearly underwent a severe extinction across the K-Pg boundary.     

Diversification shifts in leafroller moths linked to continental colonization and the rise of angiosperms

Tectonic dynamics and niche availability play intertwined roles in determining patterns of diversification. Such drivers explain the current distribution of many clades, whereas events such as the rise of angiosperms can have more specific impacts, such as on the diversification rates of herbivores. The Tortricidae, a diverse group of phytophagous moths, are ideal for testing the effects of these determinants on the diversification of herbivorous clades. To estimate ancestral areas and diversification patterns in Tortricidae, a complete tribal‐level dated tree was inferred using molecular markers (one mitochondrial and five nuclear) and calibrated using fossil constraints. We found that Tortricidae diverged from their sister group c. 120 Myr ago (Ma) and diversified c. 97 Ma, a timeframe synchronous with the rise of angiosperms in the Early–mid Cretaceous. Ancestral areas analysis, based on updated Wallace's biogeographical regions, supports the hypothesis of a Gondwanan origin of Tortricidae in the South American plate. We also detected an increase in speciation rate that coincided with the peak of angiosperm diversification in the Cretaceous. This in turn probably was further heightened by continental colonization of the Palaeotropics when angiosperms became dominant by the end of the Late Cretaceous.     

Explaining large-scale patterns of vertebrate diversity

The major clades of vertebrates differ dramatically in their current species richness, from 2 to more than 32 000 species each, but the causes of this variation remain poorly understood. For example, a previous study noted that vertebrate clades differ in their diversification rates, but did not explain why they differ. Using a time-calibrated phylogeny and phylogenetic comparative methods, I show that most variation in diversification rates among 12 major vertebrate clades has a simple ecological explanation: predominantly terrestrial clades (i.e. birds, mammals, and lizards and snakes) have higher net diversification rates than predominantly aquatic clades (i.e. amphibians, crocodilians, turtles and all fish clades). These differences in diversification rates are then strongly related to patterns of species richness. Habitat may be more important than other potential explanations for richness patterns in vertebrates (such as climate and metabolic rates) and may also help explain patterns of species richness in many other groups of organisms.     

Eutherians experienced elevated evolutionary rates in the immediate aftermath of the Cretaceous–Palaeogene mass extinction

The effect of the Cretaceous–Palaeogene (K–Pg) mass extinction on the evolution of many groups, including placental mammals, has been hotly debated. The fossil record suggests a sudden adaptive radiation of placentals immediately after the event, but several recent quantitative analyses have reconstructed no significant increase in either clade origination rates or rates of character evolution in the Palaeocene. Here we use stochastic methods to date a recent phylogenetic analysis of Cretaceous and Palaeocene mammals and show that Placentalia likely originated in the Late Cretaceous, but that most intraordinal diversification occurred during the earliest Palaeocene. This analysis reconstructs fewer than 10 placental mammal lineages crossing the K–Pg boundary. Moreover, we show that rates of morphological evolution in the 5 Myr interval immediately after the K–Pg mass extinction are three times higher than background rates during the Cretaceous. These results suggest that the K–Pg mass extinction had a marked impact on placental mammal diversification, supporting the view that an evolutionary radiation occurred as placental lineages invaded new ecological niches during the Early Palaeocene.     

Tunicates Illuminate the Enigmatic Evolution of Chordate Metallothioneins by Gene Gains and Losses,Independent Modular Expansions,and Functional Convergences

To investigate novel patterns and processes of protein evolution, we have focused in the metallothioneins (MTs), a singular group of metal-binding, cysteine-rich proteins that, due to their high degree of sequence diversity, still represents a “black hole” in Evolutionary Biology. We have identified and analyzed more than 160 new MTs in nonvertebrate chordates (especially in 37 species of ascidians, 4 thaliaceans, and 3 appendicularians) showing that prototypic tunicate MTs are mono-modular proteins with a pervasive preference for cadmium ions, whereas vertebrate and cephalochordate MTs are bimodular proteins with diverse metal preferences. These structural and functional differences imply a complex evolutionary history of chordate MTs—including de novo emergence of genes and domains, processes of convergent evolution, events of gene gains and losses, and recurrent amplifications of functional domains—that would stand for an unprecedented case in the field of protein evolution.     

Climatic niche evolution in Smilacaceae (Liliales) drives patterns of species diversification and richness between the Old and New World

Geographical variation in species richness in plant groups is determined by the interplay between historical, evolutionary, and ecological processes. However, the processes underlying the striking disparity in species richness between Asia and the Americas remain poorly understood. Here, we synthesize global phylogenetic and macroecological data on the diversification of Smilacaceae, deciphering potential drivers underlying the species diversity pattern biased toward Asia. We compiled global distributions of all Smilacaceae species, and reconstructed the biogeographic history and niche evolution using a new time-calibrated phylogeny (eight genes, 135 species). Integrating these data sets, we estimated evolutionary histories and diversification rates for each region, and tested correlations among species diversification, niche evolution, and niche divergence. Smilacaceae probably originated during the Late Cretaceous/Early Palaeocene and began to diversify in middle to low latitudes in Central America and Eurasia during the Late Eocene. Both the Old and New World clades exhibited a steady, albeit slight, increase of species diversification from the Late Eocene to Early Miocene. However, the Old World clade experienced an abrupt increase in net diversification during the Late Miocene. Our findings also revealed that species diversification rates were positively correlated with ecological niche evolution and niche divergence. Niche shifts and climatic niche evolution since the Middle Miocene played crucial roles in species diversification dynamics within Smilacaceae. The high plant richness in Asia may be explained by greater diversification in this region, potentially promoted by heterogeneous environments.     

A complete skull of an early cretaceous sauropod and the evolution of advanced titanosaurians

Advanced titanosaurian sauropods, such as nemegtosaurids and saltasaurids, were diverse and one of the most important groups of herbivores in the terrestrial biotas of the Late Cretaceous. However, little is known about their rise and diversification prior to the Late Cretaceous. Furthermore, the evolution of their highly-modified skull anatomy has been largely hindered by the scarcity of well-preserved cranial remains. A new sauropod dinosaur from the Early Cretaceous of Brazil represents the earliest advanced titanosaurian known to date, demonstrating that the initial diversification of advanced titanosaurians was well under way at least 30 million years before their known radiation in the latest Cretaceous. The new taxon also preserves the most complete skull among titanosaurians, further revealing that their low and elongated diplodocid-like skull morphology appeared much earlier than previously thought.     

Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds

Birds are the most diverse living tetrapod group and are a model of large-scale adaptive radiation. Neontological studies suggest a radiation within the avian crown group, long after the origin of flight. However, deep time patterns of bird evolution remain obscure because only limited fossil data have been considered. We analyse cladogenesis and limb evolution on the entire tree of Mesozoic theropods, documenting the dinosaur–bird transition and immediate origins of powered flight. Mesozoic birds inherited constraints on forelimb evolution from non-flying ancestors, and species diversification rates did not accelerate in the earliest flying taxa. However, Early Cretaceous short-tailed birds exhibit both phenotypic release of the hindlimb and increased diversification rates, unparalleled in magnitude at any other time in the first 155 Myr of theropod evolution. Thus, a Cretaceous adaptive radiation of stem-group birds was enabled by restructuring of the terrestrial locomotor module, which represents a key innovation. Our results suggest two phases of radiation in Avialae: with the Cretaceous diversification overwritten by extinctions of stem-group birds at the Cretaceous–Palaeogene boundary, and subsequent diversification of the crown group. Our findings illustrate the importance of fossil data for understanding the macroevolutionary processes generating modern biodiversity.     

The patterns and modes of the evolution of disparity in Mesozoic birds

The origin of birds from non-avian theropod dinosaurs is one of the greatest transitions in evolution. Shortly after diverging from other theropods in the Late Jurassic, Mesozoic birds diversified into two major clades—the Enantiornithes and Ornithuromorpha—acquiring many features previously considered unique to the crown group along the way. Here, we present a comparative phylogenetic study of the patterns and modes of Mesozoic bird skeletal morphology and limb proportions. Our results show that the major Mesozoic avian groups are distinctive in discrete character space, but constrained in a morphospace defined by limb proportions. The Enantiornithines, despite being the most speciose group of Mesozoic birds, are much less morphologically disparate than their sister clade, the Ornithuromorpha—the clade that gave rise to living birds, showing disparity and diversity were decoupled in avian history. This relatively low disparity suggests that diversification of enantiornithines was characterized in exhausting fine morphologies, whereas ornithuromorphs continuously explored a broader array of morphologies and ecological opportunities. We suggest this clade-specific evolutionary versatility contributed to their sole survival of the end-Cretaceous mass extinction.     

The First Dinosaur from Washington State and a Review of Pacific Coast Dinosaurs from North America

We describe the first diagnostic dinosaur fossil from Washington State. The specimen, which consists of a proximal left femur, was recovered from the shallow marine rocks of the Upper Cretaceous (Campanian) Cedar District Formation (Nanaimo Group) and is interpreted as pertaining to a large theropod on the basis of its hollow medullary cavity and proximally placed fourth trochanter. The Washington theropod represents one of the northernmost occurrences of a Mesozoic dinosaur on the west coast of the United States and one of only a handful from the Pacific coast of Laramidia during the Cretaceous. Its isolated nature and preservation in marine rocks suggest that the element was washed in from a nearby fluvial system. If the femur pertains to a tyrannosauroid, which seems likely given its size and the widespread occurrence of the group across Laramidia during Late Cretaceous times, then it would represent an earlier occurrence of large body size than previously recognized (complete femur length estimated at 1.2 meters). Uncertainty surrounding the latitude of deposition of the Nanaimo Group (i.e., the Baja-British Columbia hypothesis) precludes assigning the Washington theropod to either of the putative northern or southern biogeographic provinces of Laramidia.     

Dinosaurs and the Cretaceous Terrestrial Revolution

The observed diversity of dinosaurs reached its highest peak during the mid- and Late Cretaceous, the 50 Myr that preceded their extinction, and yet this explosion of dinosaur diversity may be explained largely by sampling bias. It has long been debated whether dinosaurs were part of the Cretaceous Terrestrial Revolution (KTR), from 125-80 Myr ago, when flowering plants, herbivorous and social insects, squamates, birds and mammals all underwent a rapid expansion. Although an apparent explosion of dinosaur diversity occurred in the mid-Cretaceous, coinciding with the emergence of new groups (e.g. neoceratopsians, ankylosaurid ankylosaurs, hadrosaurids and pachycephalosaurs), results from the first quantitative study of diversification applied to a new supertree of dinosaurs show that this apparent burst in dinosaurian diversity in the last 18 Myr of the Cretaceous is a sampling artefact. Indeed, major diversification shifts occurred largely in the first one-third of the group's history. Despite the appearance of new clades of medium to large herbivores and carnivores later in dinosaur history, these new originations do not correspond to significant diversification shifts. Instead, the overall geometry of the Cretaceous part of the dinosaur tree does not depart from the null hypothesis of an equal rates model of lineage branching. Furthermore, we conclude that dinosaurs did not experience a progressive decline at the end of the Cretaceous, nor was their evolution driven directly by the KTR.     

Mountain building triggered late cretaceous north american megaherbivore dinosaur radiation

Prior studies of Mesozoic biodiversity document a diversity peak for dinosaur species in the Campanian stage of the Late Cretaceous, yet have failed to provide explicit causal mechanisms. We provide evidence that a marked increase in North American dinosaur biodiversity can be attributed to dynamic orogenic episodes within the Western Interior Basin (WIB). Detailed fossil occurrences document an association between the shift from Sevier-style, latitudinally arrayed basins to smaller Laramide-style, longitudinally arrayed basins and a well substantiated decreased geographic range/increased taxonomic diversity of megaherbivorous dinosaur species. Dispersal-vicariance analysis demonstrates that the nearly identical biogeographic histories of the megaherbivorous dinosaur clades Ceratopsidae and Hadrosauridae are attributable to rapid diversification events within restricted basins and that isolation events are contemporaneous with known tectonic activity in the region. SymmeTREE analysis indicates that megaherbivorous dinosaur clades exhibited significant variation in diversification rates throughout the Late Cretaceous. Phylogenetic divergence estimates of fossil clades offer a new lower boundary on Laramide surficial deformation that precedes estimates based on sedimentological data alone.     

Evolution of Lycopodiaceae (Lycopsida): estimating divergence times from rbcL gene sequences by use of nonparametric rate smoothing

By use of nonparametric rate smoothing and nucleotide sequences of the rbcL gene, divergence times in Lycopodiaceae are estimated. The results show that much extant species diversity in Lycopodiaceae stems from relatively recent cladogenic events. These results corroborate previous ideas based on paleobotanical and biogeographical data. Previous molecular phylogenetic analyses recognized a split into neotropical and paleotropical clades in Huperzia, which contains 85-90% of all living species. Connecting this biogeographical pattern with continent movements, the diversification of this epiphytic group was suggested to coincide with that of angiosperms in the mid to Late Cretaceous. Results presented here are consistent with this idea, and the diversification of the two clades is resolved as Late Cretacous (78 and 95 Myr). In the related genera Lycopodium and Lycopodiella, the patterns are somewhat different. Here species diversity is scattered among different subgeneric groups. Most of the high-diversity subgeneric groups seem to have diversified very recently (Late Tertiary), whereas the cladogenic events leading to these groups are much older (Early to Late Cretaceous). Our analysis shows that, although much living species diversity stems from relatively recent cladogenesis, the origins of the family (Early Carboniferous) and generic crown groups (Early Permian to Early Jurassic) are much more ancient events.     

FOSSILS AND A LARGE MOLECULAR PHYLOGENY SHOW THAT THE EVOLUTION OF SPECIES RICHNESS,GENERIC DIVERSITY,AND TURNOVER RATES ARE DISCONNECTED

The magnitude and extent of global change during the Cenozoic is remarkable, yet the impacts of these global changes on the biodiversity and evolutionary dynamics of species diversification remain poorly understood. To investigate this question, we combine paleontological and neontological data for the angiosperm order Fagales, an ecologically important clade of about 1370 species of trees with an exceptional fossil record. We show differences in patterns of accumulation of generic diversity, species richness, and turnover rates for Fagales. Generic diversity evolved rapidly since the Late Cretaceous and peaked during the Eocene or Oligocene. Turnover rates were high during periods of extreme global climate change, but relatively low when the climate remained stable. Species richness accumulated gradually throughout the Cenozoic, possibly at an accelerated pace after the Middle Miocene. Species diversification occurred in new environments: Quercoids radiating in Oligocene subtropical seasonally arid habitats, Casuarinaceae in Australian pyrophytic biomes, and Betula in Late Neogene holarctic habitats. These radiations were counterbalanced by regional extinctions in Late Neogene mesic warm‐temperate forests. Thus, the overall diversification at species level is linked to regional radiations of clades with appropriate ecologies exploiting newly available habitats.     

ORIGINS,EVOLUTION, AND DIVERSIFICATION OF CLEPTOPARASITIC LINEAGES IN LONG‐TONGUED BEES

The evolution of parasitic behavior may catalyze the exploitation of new ecological niches yet also binds the fate of a parasite to that of its host. It is thus not clear whether evolutionary transitions from free‐living organism to parasite lead to increased or decreased rates of diversification. We explore the evolution of brood parasitism in long‐tongued bees and find decreased rates of diversification in eight of 10 brood parasitic clades. We propose a pathway for the evolution of brood parasitic strategy and find that a strategy in which a closed host nest cell is parasitized and the host offspring is killed by the adult parasite represents an obligate first step in the appearance of a brood parasitic lineage; this ultimately evolves into a strategy in which an open host cell is parasitized and the host offspring is killed by a specialized larval instar. The transition to parasitizing open nest cells expanded the range of potential hosts for brood parasitic bees and played a fundamental role in the patterns of diversification seen in brood parasitic clades. We address the prevalence of brood parasitic lineages in certain families of bees and examine the evolution of brood parasitism in other groups of organisms.