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.     

Adaptive radiation of multituberculate mammals before the extinction of dinosaurs

The Cretaceous-Paleogene mass extinction approximately 66 million years ago is conventionally thought to have been a turning point in mammalian evolution. Prior to that event and for the first two-thirds of their evolutionary history, mammals were mostly confined to roles as generalized, small-bodied, nocturnal insectivores, presumably under selection pressures from dinosaurs. Release from these pressures, by extinction of non-avian dinosaurs at the Cretaceous-Paleogene boundary, triggered ecological diversification of mammals. Although recent individual fossil discoveries have shown that some mammalian lineages diversified ecologically during the Mesozoic era, comprehensive ecological analyses of mammalian groups crossing the Cretaceous-Paleogene boundary are lacking. Such analyses are needed because diversification analyses of living taxa allow only indirect inferences of past ecosystems. Here we show that in arguably the most evolutionarily successful clade of Mesozoic mammals, the Multituberculata, an adaptive radiation began at least 20 million years before the extinction of non-avian dinosaurs and continued across the Cretaceous-Paleogene boundary. Disparity in dental complexity, which relates to the range of diets, rose sharply in step with generic richness and disparity in body size. Moreover, maximum dental complexity and body size demonstrate an adaptive shift towards increased herbivory. This dietary expansion tracked the ecological rise of angiosperms and suggests that the resources that were available to multituberculates were relatively unaffected by the Cretaceous-Paleogene mass extinction. Taken together, our results indicate that mammals were able to take advantage of new ecological opportunities in the Mesozoic and that at least some of these opportunities persisted through the Cretaceous-Paleogene mass extinction. Similar broad-scale ecomorphological inventories of other radiations may help to constrain the possible causes of mass extinctions.     

Dating the origin of the Orchidaceae from a fossil orchid with its pollinator

Since the time of Darwin, evolutionary biologists have been fascinated by the spectacular adaptations to insect pollination exhibited by orchids. However, despite being the most diverse plant family on Earth, the Orchidaceae lack a definitive fossil record and thus many aspects of their evolutionary history remain obscure. Here we report an exquisitely preserved orchid pollinarium (of Meliorchis caribea gen. et sp. nov.) attached to the mesoscutellum of an extinct stingless bee, Proplebeia dominicana, recovered from Miocene amber in the Dominican Republic, that is 15-20 million years (Myr) old. This discovery constitutes both the first unambiguous fossil of Orchidaceae and an unprecedented direct fossil observation of a plant-pollinator interaction. By applying cladistic methods to a morphological character matrix, we resolve the phylogenetic position of M. caribea within the extant subtribe Goodyerinae (subfamily Orchidoideae). We use the ages of other fossil monocots and M. caribea to calibrate a molecular phylogenetic tree of the Orchidaceae. Our results indicate that the most recent common ancestor of extant orchids lived in the Late Cretaceous (76-84 Myr ago), and also suggest that the dramatic radiation of orchids began shortly after the mass extinctions at the K/T boundary. These results further support the hypothesis of an ancient origin for Orchidaceae.     

Geochemical environmental changes and dinosaur extinction during the Cretaceous-Paleogene (K/T) transition in the Nanxiong Basin, South China: Evidence from dinosaur eggshells

The complex patterns of trace elements including Ir and isotope distributions in the three K/T sections of the Nanxiong Basin prove the existence of two environmental events in the latest Cretaceous and earliest Paleocene. The first geochemical environmental event occurred at about 2 Ma prior to the K/T boundary interval, where the dinosaur diversity was hardly reduced, except that a number of pathological eggshells appeared. The second one was larger and occurred just at and near the Cretaceous-Paleogene (K/T) boundary. The extinction of the dinosaurs spread out within 250 ka with major extinction beginning at the boundary interval. This is even later than their extinction in Montana, North America and in India. The cause of the dinosaur extinction may be the result of a complex multiple events brought about by the coincidence of global environment change marked by multiple Ir and δ¹⁸O anomalies, and environmental poisoning characterized by other trace elements derived from the local source. Successive short- and long-term conditions of geochemically induced environmental stress negatively affected the reproductive process and thus contributed to the extinction of the dinosaurs. Supported by National Natural Science Foundation of China (Grant No. 40472018) and the Chinese Academy of Sciences (Grant No. 21039751)     

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.     

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.     

A new feathered maniraptoran dinosaur fossil that fills a morphological gap in avian origin

Recent fossil discoveries have substantially reduced the morphological gap between non-avian and avian dinosaurs, yet avians including Archaeopteryx differ from non-avian theropods in their limb proportions. In particular, avians have proportionally longer and more robust forelimbs that are capable of supporting a large aerodynamic surface. Here we report on a new maniraptoran dinosaur, Anchiornis huxleyi gen. et sp. nov., based on a specimen collected from lacustrine deposits of uncertain age in western Liaoning, China. With an estimated mass of 110 grams, Anchiornis is the smallest known non-avian theropod dinosaur. It exhibits some wrist features indicative of high mobility, presaging the wing-folding mechanisms seen in more derived birds and suggesting rapid evolution of the carpus. Otherwise, Anchiornis is intermediate in general morphology between non-avian and avian dinosaurs, particularly with regard to relative forelimb length and thickness, and represents a transitional step toward the avian condition. In contrast with some recent comprehensive phylogenetic analyses, our phylogenetic analysis incorporates subtle morphological variations and recovers a conventional result supporting the monophyly of Avialae. Supported by Hundred Talents Project of the Chinese Academy of Sciences, National Natural Science Foundation of China (Grant Nos. 40125006, 40472018), and National Basic Research Program of China (Grant No. 2006CB806400)     

A long-tailed,seed-eating bird from the Early Cretaceous of China

The lacustrine deposits of the Yixian and Jiufotang Formations in the Early Cretaceous Jehol Group in the western Liaoning area of northeast China are well known for preserving feathered dinosaurs, primitive birds and mammals. Here we report a large basal bird, Jeholornis prima gen. et sp. nov., from the Jiufotang Formation. This bird is distinctively different from other known birds of the Early Cretaceous period in retaining a long skeletal tail with unexpected elongated prezygopophyses and chevrons, resembling that of dromaeosaurids, providing a further link between birds and non-avian theropods. Despite its basal position in early avian evolution, the advanced features of the pectoral girdle and the carpal trochlea of the carpometacarpus of Jeholornis indicate the capability of powerful flight. The dozens of beautifully preserved ovules of unknown plant taxa in the stomach represents direct evidence for seed-eating adaptation in birds of the Mesozoic era.     

Forensic palaeontology: The Archaeoraptor forgery

The Archaeoraptor fossil was announced as a 'missing link' and purported to be possibly the best evidence since Archaeopteryx that birds did, in fact, evolve from certain types of carnivorous dinosaur. It reportedly came from Early Cretaceous beds of China that have produced other spectacular fossils transitional between birds and extinct non-avian dinosaurs. But Archaeoraptor was revealed to be a forgery in which bones of a primitive bird and a non-flying dromaeosaurid dinosaur had been combined. Here we use high-resolution X-ray computed tomography (CT) to determine the nature and extent of the forgery, as well as how it was built, by imaging the fracture pattern and distribution of materials through the entire specimen.     

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.     

The smallest known non-avian theropod dinosaur

Non-avian dinosaurs are mostly medium to large-sized animals, and to date all known mature specimens are larger than the most primitive bird, Archaeopteryx. Here we report on a new dromaeosaurid dinosaur, Microraptor zhaoianus gen. et sp. nov., from the Early Cretaceous Jiufotang Formation of Liaoning, China. This is the first mature non-avian dinosaur to be found that is smaller than Archaeopteryx, and it eliminates the size disparity between the earliest birds and their closest non-avian theropod relatives. The more bird-like teeth, the Rahonavis-like ischium and the small number of caudal vertebrae of Microraptor are unique among dromaeosaurids and improve our understanding of the morphological transition to birds. The nearly completely articulated foot shows features, such as distally positioned digit I, slender and recurved pedal claws, and elongated penultimate phalanges, that are comparable to those of arboreal birds. The discovery of these in non-avian theropods provides new insights for studying the palaeoecology of some bird-like theropod dinosaurs.     

Cretaceous eutherians and Laurasian origin for placental mammals near the K/T boundary

Estimates of the time of origin for placental mammals from DNA studies span nearly the duration of the Cretaceous period (145 to 65 million years ago), with a maximum of 129 million years ago and a minimum of 78 million years ago. Palaeontologists too are divided on the timing. Some support a deep Cretaceous origin by allying certain middle Cretaceous fossils (97-90 million years old) from Uzbekistan with modern placental lineages, whereas others support the origin of crown group Placentalia near the close of the Cretaceous. This controversy has yet to be addressed by a comprehensive phylogenetic analysis that includes all well-known Cretaceous fossils and a wide sample of morphology among Tertiary and recent placentals. Here we report the discovery of a new well-preserved mammal from the Late Cretaceous of Mongolia and a broad-scale phylogenetic analysis. Our results exclude Cretaceous fossils from Placentalia, place the origin of Placentalia near the Cretaceous/Tertiary (K/T) boundary in Laurasia rather than much earlier within the Cretaceous in the Southern Hemisphere, and place afrotherians and xenarthrans in a nested rather than a basal position within Placentalia.     

A new troodontid dinosaur from China with avian-like sleeping posture

Discovering evidence of behaviour in fossilized vertebrates is rare. Even rarer is evidence of behaviour in non-avialan dinosaurs that directly relates to stereotypical behaviour seen in extant birds (avians) and not previously predicted in non-avialan dinosaurs. Here we report the discovery of a new troodontid taxon from the Early Cretaceous Yixian Formation of western Liaoning, China. Numerous other three-dimensionally preserved vertebrate fossils have been recovered recently at this locality, including some specimens preserving behavioural information. The new troodontid preserves several features that have been implicated in avialan origins. Notably, the specimen is preserved in the stereotypical sleeping or resting posture found in extant Aves. Evidence of this behaviour outside of the crown group Aves further demonstrates that many bird features occurred early in dinosaurian evolution.     

Extraterrestrial amino acids in Cretaceous/Tertiary boundary sediments at Stevns Klint, Denmark

Since the discovery nearly a decade ago that Cretaceous/Tertiary (K/T) boundary layers are greatly enriched in iridium, a rare element in the Earth's crust, there has been intense controversy on the relationship between this Ir anomaly and the massive extinction of organisms ranging from dinosaurs to marine plankton that characterizes the K/T boundary. Convincing evidence suggests that both the Ir spike and the extinction event were caused by the collision of a large bolide (greater than 10 km in diameter) with the Earth. Alternative explanations claim that extensive, violent volcanism can account for the Ir, and that other independent causes were responsible for the mass extinctions. We surmise that the collision of a massive extraterrestrial object with the Earth may have produced a unique organic chemical signature because certain meteorites, and probably comets, contain organic compounds which are either rare or non-existent on the Earth. In contrast, no organic compounds would be expected to be associated with volcanic processes. Here we find that K/T boundary sediments at Stevns Klint, Denmark, contain both alpha-amino-isobutyric acid [AIB,(CH3)2CNH2COOH] and racemic isovaline [ISOVAL, CH3CH2(CH3)CNH2COOH], two amino acids that are exceedingly rare on the Earth but which are major amino acids in carbonaceous chondrites. An extraterrestrial source is the most reasonable explanation for the presence of these amino acids.     

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.     

Paleornithology of China: A general review

Study of fossil birds in China was first conducted by western scholars in last century, and extensive study of Cenozoic birds by Chinese scholars since the 1970s. However, it is the finding of Mesozoic birds, mostly from northeast China since the 1990s, that has become the focus and highlight of paleornithology of China. Enantiornithine birds from the Late Jurassic-Early Cretaceous of China provide the most complete record of the early evolution of this extinct group. The co-existence of the most primitive ornithurine bird Liaoningornis with the oldest known Confuciusornis indicates an earlier and more significant diversification of birds than previously recognized. Evidence from the Chinese Mesozoic birds seems to support the arboreal hypothesis of the origin of avian flight. Despite the controversy, the recent discovery of various feathered dinosaurs in China may provide the most compelling evidence for the hypothesis of the dinosaurian origin of birds.     

Branched integumental structures in Sinornithosaurus and the origin of feathers

The evolutionary origin of feathers has long been obscured because no morphological antecedents were known to the earliest, structurally modern feathers of Archaeopteryx. It has been proposed that the filamentous integumental appendages on several theropod dinosaurs are primitive feathers; but the homology between these filamentous structures and feathers has been disputed, and two taxa with true feathers (Caudipteryx and Protarchaeopteryx) have been proposed to be flightless birds. Confirmation of the theropod origin of feathers requires documentation of unambiguously feather-like structures in a clearly non-avian theropod. Here we describe our observations of the filamentous integumental appendages of the basal dromaeosaurid dinosaur Sinornithosaurus millenii, which indicate that they are compound structures composed of multiple filaments. Furthermore, these appendages exhibit two types of branching structure that are unique to avian feathers: filaments joined in a basal tuft, and filaments joined at their bases in series along a central filament. Combined with the independent phylogenetic evidence supporting the theropod ancestry of birds, these observations strongly corroborate the hypothesis that the integumental appendages of Sinornithosaurus are homologous with avian feathers. The plesiomorphic feathers of Sinornithosaurus also conform to the predictions of an independent, developmental model of the evolutionary origin of feathers.     

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 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.