Definitive fossil evidence for the extant avian radiation in the Cretaceous

Long-standing controversy surrounds the question of whether living bird lineages emerged after non-avian dinosaur extinction at the Cretaceous/Tertiary (K/T) boundary or whether these lineages coexisted with other dinosaurs and passed through this mass extinction event. Inferences from biogeography and molecular sequence data (but see ref. 10) project major avian lineages deep into the Cretaceous period, implying their 'mass survival' at the K/T boundary. By contrast, it has been argued that the fossil record refutes this hypothesis, placing a 'big bang' of avian radiation only after the end of the Cretaceous. However, other fossil data--fragmentary bones referred to extant bird lineages--have been considered inconclusive. These data have never been subjected to phylogenetic analysis. Here we identify a rare, partial skeleton from the Maastrichtian of Antarctica as the first Cretaceous fossil definitively placed within the extant bird radiation. Several phylogenetic analyses supported by independent histological data indicate that a new species, Vegavis iaai, is a part of Anseriformes (waterfowl) and is most closely related to Anatidae, which includes true ducks. A minimum of five divergences within Aves before the K/T boundary are inferred from the placement of Vegavis; at least duck, chicken and ratite bird relatives were coextant with non-avian dinosaurs.     

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.     

Fossil that fills a critical gap in avian evolution

Despite the discoveries of well-preserved Mesozoic birds, a key part of avian evolution, close to the radiation of all living birds (Aves), remains poorly represented. Here we report on a new taxon from the Late Cretaceous locality of Ukhaa Tolgod, Mongolia, that offers insight into this critically unsampled period. Apsaravis and the controversial alvarezsaurids are the only avialan taxa known from the continental deposits at Ukhaa Tolgod, which have produced hundreds of fossil mammals, lizards and other small dinosaurs. The new taxon, Apsaravis ukhaana, is the best-preserved specimen of a Mesozoic ornithurine bird discovered in over a century. It provides data important for assessing morphological evolution across Avialae, with implications for, first, the monophyly of Enantiornithes and Sauriurae; second, the proposition that the Mesozoic sister taxa of extant birds, as part of an 'ecological bottleneck', inhabited exclusively near-shore and marine environments; and third, the evolution of flight after its origin.     

Fine structure of bone in dinosaurs, birds and mammals

After observation of detailed structural evidence for the origin of birds from dinosaurs, and in light of evidence that dinosaur bone tissue resembles the histology in mammals, the histology of bone has become one of the focal points in discussions of the physiology of dinosaurs and Mesozoic birds. Most of this microstructural information has focused on features related to the vascular organization and the amount of remodelled bone around vascular canals. However, the finer structures have received less attention, although differences in such structures have been observed among modern vertebrates. Here we present evidence that canaliculi--the submicrometre-sized channels that interconnect bone cells and vascular canals--and the collagen fibre bundles in bone are differently organized among certain dinosaur lineages. Ornithomimid dinosaurs are more like birds than mammals in these features. In canalicular structure, and to some extent in fibre bundle arrangement, ornithischian dinosaurs are more like mammals. These differences in both canalicular and lamellar structure are probably linked to differences in the process and rate of bone formation.     

A pug-nosed crocodyliform from the Late Cretaceous of Madagascar

Although the image of crocodyliforms as 'unchanged living fossils' is naive, several morphological features of the group are thought to have varied only within narrow limits during the course of evolution. These include an elongate snout with an array of conical teeth, a dorsoventrally flattened skull and a posteriorly positioned jaw articulation, which provides a powerful bite force. Here we report an exquisitely preserved specimen of a new taxon from the Late Cretaceous of Madagascar that deviates profoundly from this Bauplan, possessing an extremely blunt snout, a tall, rounded skull, an anteriorly shifted jaw joint and clove-shaped, multicusped teeth reminiscent of those of some ornithischian dinosaurs. This last feature implies that the diet of the new taxon may have been predominantly if not exclusively herbivorous. A close relationship with notosuchid crocodyliforms, particularly Uruguaysuchus (Late Cretaceous, Uruguay) is suggested by several shared derived features; this supports a biogeographical hypothesis that Madagascar and South America were linked during the Late Cretaceous.     

A new carnivorous dinosaur from the Late Jurassic Solnhofen archipelago

Small Late Jurassic theropod dinosaurs are rare worldwide. In Europe these carnivorous dinosaurs are represented primarily by only two skeletons of Compsognathus, neither of which is well preserved. Here we describe a small new theropod dinosaur from the Late Jurassic period of Schamhaupten in southern Germany. Being exquisitely preserved and complete from the snout to the distal third of the tail, the new fossil is the best-preserved predatory, non-avian dinosaur in Europe. It possesses a suite of characters that support its identification as a basal coelurosaur. A cladistic analysis indicates that the new taxon is closer to maniraptorans than to tyrannosauroids, grouping it with taxa often considered to be compsognathids. Large portions of integument are preserved along its tail. The absence of feathers or feather-like structures in a fossil phylogenetically nested within feathered theropods indicates that the evolution of these integumentary structures might be more complex than previously thought.     

Dinosaurian growth patterns and rapid avian growth rates

Did dinosaurs grow in a manner similar to extant reptiles, mammals or birds, or were they unique? Are rapid avian growth rates an innovation unique to birds, or were they inherited from dinosaurian precursors? We quantified growth rates for a group of dinosaurs spanning the phylogenetic and size diversity for the clade and used regression analysis to characterize the results. Here we show that dinosaurs exhibited sigmoidal growth curves similar to those of other vertebrates, but had unique growth rates with respect to body mass. All dinosaurs grew at accelerated rates relative to the primitive condition seen in extant reptiles. Small dinosaurs grew at moderately rapid rates, similar to those of marsupials, but large species attained rates comparable to those of eutherian mammals and precocial birds. Growth in giant sauropods was similar to that of whales of comparable size. Non-avian dinosaurs did not attain rates like those of altricial birds. Avian growth rates were attained in a stepwise fashion after birds diverged from theropod ancestors in the Jurassic period.     

Earliest evidence for efficient oral processing in a terrestrial herbivore

Herbivores can increase their digestion rate by mechanically reducing particle size through oral trituration. Groups of terrestrial vertebrates with the greatest capacity to reduce tough plant foods orally are also the most abundant and diverse, as exemplified by ornithopod dinosaurs during the Mesozoic and extant artiodactyl and perissodactyl mammals. Thus, the effective oral processing of high-fibre plant material seems to represent an evolutionary innovation of both functional and macroevolutionary significance. However, evidence for oral processing is poorly documented in the fossil record, especially during the initial stages of terrestrial vertebrate diversification. Here we report on the basal anomodont Suminia getmanovi, the only known Palaeozoic vertebrate in which unequivocal specializations in its cranium and teeth for high-fibre herbivory are well preserved. We propose that the capacity to comminute tough plant foods was critical to the diversification of anomodonts, the most diverse, widely dispersed and abundant group of Palaeozoic terrestrial vertebrates, and to the onset of modern terrestrial ecosystems.     

Skull of the large non-macrostomatan snake Yurlunggur from the Australian Oligo-Miocene

Understanding the origin and early evolution of snakes from lizards depends on accurate morphological knowledge of the skull in basal lineages, but fossil specimens of archaic snakes have been rare, and either fragmentary or difficult to study as a result of compression by enclosing sediments. A number of Cenozoic fossil snakes from Australia have vertebral morphology diagnostic of an extinct group, Madtsoiidae, that was widespread in Gondwana from mid-Cretaceous (Cenomanian) to Eocene times, and also reached Europe in the late Cretaceous period. Despite this long history, only about half the skull is known from the best-known species Wonambi naracoortensis, and the few known cranial elements of other species have added little further evidence for phylogenetic relationships. Conflicting hypotheses have been proposed for their relationships and evolutionary significance, either as basal ophidians with many ancestral (varanoid- or mosasaur-like) features, or advanced (macrostomatan) alethinophidians of little relevance to snake origins. Here I report two partial skeletons referred to Yurlunggur, from the late Oligocene and early Miocene of northern Australia, which together represent almost the complete skull and mandible. The exceptionally preserved skulls provide new evidence linking Yurlunggur with Wonambi and other madtsoiids, falsifying predictions of the macrostomatan hypothesis, and supporting the exclusion of Madtsoiidae from the clade including all extant snakes.     

Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs

Birds are unique among living vertebrates in possessing pneumaticity of the postcranial skeleton, with invasion of bone by the pulmonary air-sac system. The avian respiratory system includes high-compliance air sacs that ventilate a dorsally fixed, non-expanding parabronchial lung. Caudally positioned abdominal and thoracic air sacs are critical components of the avian aspiration pump, facilitating flow-through ventilation of the lung and near-constant airflow during both inspiration and expiration, highlighting a design optimized for efficient gas exchange. Postcranial skeletal pneumaticity has also been reported in numerous extinct archosaurs including non-avian theropod dinosaurs and Archaeopteryx. However, the relationship between osseous pneumaticity and the evolution of the avian respiratory apparatus has long remained ambiguous. Here we report, on the basis of a comparative analysis of region-specific pneumaticity with extant birds, evidence for cervical and abdominal air-sac systems in non-avian theropods, along with thoracic skeletal prerequisites of an avian-style aspiration pump. The early acquisition of this system among theropods is demonstrated by examination of an exceptional new specimen of Majungatholus atopus, documenting these features in a taxon only distantly related to birds. Taken together, these specializations imply the existence of the basic avian pulmonary Bauplan in basal neotheropods, indicating that flow-through ventilation of the lung is not restricted to birds but is probably a general theropod characteristic.     

Cannibalism in the Madagascan dinosaur Majungatholus atopus

Many lines of evidence have been brought to bear on the question of theropod feeding ecology, including functional and physiological considerations, morphological constraints, taphonomic associations, and telling--although rare--indications of direct ingestion. Tooth marks of theropods, although rarely described and generally left unassigned to a particular taxon, can provide unique clues into predator-prey interaction, and can also yield insights into the extent of carcass utilization. Here we describe a sample of tooth-marked dinosaur bone recovered from three well-documented localities in the Upper Cretaceous Maevarano Formation of Madagascar that provides insights into the feeding ecology of the abelisaurid theropod Majungatholus atopus. Intensely tooth-marked elements from multiple individuals show that Majungatholus defleshed dinosaur carcasses. Furthermore, Majungatholus clearly fed upon the remains of not only sauropods, but also conspecifics, and thus was a cannibal. Cannibalism is a common ecological strategy among extant carnivores, but until now the evidence in relation to carnivorous dinosaurs has been sparse and anecdotal.     

Palaeontology. The beaks of ostrich dinosaurs

Primitive ornithomimids, a ubiquitous group of specialized Cretaceous dinosaurs nested within a clade of predominantly carnivorous theropods, are known to have had teeth, whereas derived ornithomimids had an edentulous beak, which has prompted speculation about their dietary habits. Here we describe two new ornithomimid specimens in which soft-tissue structures of the beak have been preserved. These creatures probably used their beaks to strain food sediment in an aqueous environment, rather than for predation on large animals.     

The distribution of integumentary structures in a feathered dinosaur

Non-avian theropod dinosaurs with preserved integumentary coverings are becoming more common; but apart from the multiple specimens of Caudipteryx, which have true feathers, animals that are reasonably complete and entirely articulated that show these structures in relation to the body have not been reported. Here we report on an enigmatic small theropod dinosaur that is covered with filamentous feather-like structures over its entire body.     

Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation

Bats (Chiroptera) represent one of the largest and most diverse radiations of mammals, accounting for one-fifth of extant species. Although recent studies unambiguously support bat monophyly and consensus is rapidly emerging about evolutionary relationships among extant lineages, the fossil record of bats extends over 50 million years, and early evolution of the group remains poorly understood. Here we describe a new bat from the Early Eocene Green River Formation of Wyoming, USA, with features that are more primitive than seen in any previously known bat. The evolutionary pathways that led to flapping flight and echolocation in bats have been in dispute, and until now fossils have been of limited use in documenting transitions involved in this marked change in lifestyle. Phylogenetically informed comparisons of the new taxon with other bats and non-flying mammals reveal that critical morphological and functional changes evolved incrementally. Forelimb anatomy indicates that the new bat was capable of powered flight like other Eocene bats, but ear morphology suggests that it lacked their echolocation abilities, supporting a 'flight first' hypothesis for chiropteran evolution. The shape of the wings suggests that an undulating gliding-fluttering flight style may be primitive for bats, and the presence of a long calcar indicates that a broad tail membrane evolved early in Chiroptera, probably functioning as an additional airfoil rather than as a prey-capture device. Limb proportions and retention of claws on all digits indicate that the new bat may have been an agile climber that employed quadrupedal locomotion and under-branch hanging behaviour.     

Doushantuo embryos preserved inside diapause egg cysts

Phosphatized microfossils in the Ediacaran (635-542 Myr ago) Doushantuo Formation, south China, have been interpreted as the embryos of early animals. Despite experimental demonstration that embryos can be preserved, microstructural evidence that the Doushantuo remains are embryonic and an unambiguous record of fossil embryos in Lower Cambrian rocks, questions about the phylogenetic relationships of these fossils remain. Most recently, some researchers have proposed that Doushantuo microfossils may be giant sulphur-oxidizing bacteria comparable to extant Thiomargarita sp. Here we report new observations that provide a test of the bacterial hypothesis. The discovery of embryo-like Doushantuo fossils inside large, highly ornamented organic vesicles (acritarchs) indicates that these organisms were eukaryotic, and most probably early cleavage stage embryos preserved within diapause egg cysts. Large acanthomorphic microfossils of the type observed to contain fossil embryos first appear in rocks just above a 632.5 +/- 0.5-Myr-old ash bed, suggesting that at least stem-group animals inhabited shallow seas in the immediate aftermath of global Neoproterozoic glaciation.     

The delayed rise of present-day mammals

Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals.     

Origin of avian genome size and structure in non-avian dinosaurs

Avian genomes are small and streamlined compared with those of other amniotes by virtue of having fewer repetitive elements and less non-coding DNA. This condition has been suggested to represent a key adaptation for flight in birds, by reducing the metabolic costs associated with having large genome and cell sizes. However, the evolution of genome architecture in birds, or any other lineage, is difficult to study because genomic information is often absent for long-extinct relatives. Here we use a novel bayesian comparative method to show that bone-cell size correlates well with genome size in extant vertebrates, and hence use this relationship to estimate the genome sizes of 31 species of extinct dinosaur, including several species of extinct birds. Our results indicate that the small genomes typically associated with avian flight evolved in the saurischian dinosaur lineage between 230 and 250 million years ago, long before this lineage gave rise to the first birds. By comparison, ornithischian dinosaurs are inferred to have had much larger genomes, which were probably typical for ancestral Dinosauria. Using comparative genomic data, we estimate that genome-wide interspersed mobile elements, a class of repetitive DNA, comprised 5-12% of the total genome size in the saurischian dinosaur lineage, but was 7-19% of total genome size in ornithischian dinosaurs, suggesting that repetitive elements became less active in the saurischian lineage. These genomic characteristics should be added to the list of attributes previously considered avian but now thought to have arisen in non-avian dinosaurs, such as feathers, pulmonary innovations, and parental care and nesting.     

A gigantic feathered dinosaur from the lower cretaceous of China

Numerous feathered dinosaur specimens have recently been recovered from the Middle-Upper Jurassic and Lower Cretaceous deposits of northeastern China, but most of them represent small animals. Here we report the discovery of a gigantic new basal tyrannosauroid, Yutyrannus huali gen. et sp. nov., based on three nearly complete skeletons representing two distinct ontogenetic stages from the Lower Cretaceous Yixian Formation of Liaoning Province, China. Y. huali shares some features, particularly of the cranium, with derived tyrannosauroids, but is similar to other basal tyrannosauroids in possessing a three-fingered manus and a typical theropod pes. Morphometric analysis suggests that Y. huali differed from tyrannosaurids in its growth strategy. Most significantly, Y. huali bears long filamentous feathers, thus providing direct evidence for the presence of extensively feathered gigantic dinosaurs and offering new insights into early feather evolution.     

Bird-like fossil footprints from the Late Triassic

The study of fossilized footprints and tracks of dinosaurs and other vertebrates has provided insight into the origin, evolution and extinction of several major groups and their behaviour; it has also been an important complement to their body fossil record. The known history of birds starts in the Late Jurassic epoch (around 150 Myr ago) with the record of Archaeopteryx, whereas the coelurosaurian ancestors of the birds date back to the Early Jurassic. The hind limbs of Late Triassic epoch theropods lack osteological evidence for an avian reversed hallux and also display other functional differences from birds. Previous references to suggested Late Triassic to Early Jurassic bird-like footprints have been reinterpreted as produced by non-avian dinosaurs having a high angle between digits II and IV and in all cases their avian affinities have been challenged. Here we describe well-preserved and abundant footprints with clearly avian characters from a Late Triassic redbed sequence of Argentina, at least 55 Myr before the first known skeletal record of birds. These footprints document the activities, in an environment interpreted as small ponds associated with ephemeral rivers, of an unknown group of Late Triassic theropods having some avian characters.     

Biomechanics (Communication arising): prey attack by a large theropod dinosaur

Prey-capture strategies in carnivorous dinosaurs have been inferred from the biomechanical features of their tooth structure, the estimated bite force produced, and their diet. Rayfield et al. have used finite-element analysis (FEA) to investigate such structure-function relationships in Allosaurus fragilis, and have found that the skull was designed to bear more stress than could be generated by simple biting. They conclude that this large theropod dinosaur delivered a chop-and-slash 'hatchet' blow to its prey, which it approached with its mouth wide open before driving its upper tooth row downwards. We argue that this mode of predation is unlikely, and that the FEA results, which relate to an 'overengineered' skull, are better explained by the biomechanical demands of prey capture. Understanding the mechanics of predation is important to our knowledge of the feeding habits of carnivorous dinosaurs and for accurate reconstruction their lifestyles.