Osteology of the axial skeleton of Aucasaurus garridoi: phylogenetic and paleobiological inferences.

Aucasaurus garridoi is an abelisaurid theropod from the Anacleto Formation (lower Campanian, Upper Cretaceous) of Patagonia, Argentina. The holotype of Aucasaurus garridoi includes cranial material, axial elements, and almost complete fore- and hind limbs. Here we present a detailed description of the axial skeleton of this taxon, along with some paleobiological and phylogenetic inferences. The presacral elements are somewhat fragmentary, although these show features shared with other abelisaurids. The caudal series, to date the most complete among brachyrostran abelisaurids, shows several autapomorphic features including the presence of pneumatic recesses on the dorsal surface of the anterior caudal neural arches, a tubercle lateral to the prezygapophysis of mid caudal vertebrae, a marked protuberance on the lateral rim of the transverse process of the caudal vertebrae, and the presence of a small ligamentous scar near the anterior edge of the dorsal surface in the anteriormost caudal transverse process. The detailed study of the axial skeleton of Aucasaurus garridoi has also allowed us to identify characters that could be useful for future studies attempting to resolve the internal phylogenetic relationships of Abelisauridae. Computed tomography scans of some caudal vertebrae show pneumatic traits in neural arches and centra, and thus the first reported case for an abelisaurid taxon. Moreover, some osteological correlates of soft tissues present in Aucasaurus and other abelisaurids, especially derived brachyrostrans, underscore a previously proposed increase in axial rigidity within Abelisauridae.

Symbiosis between Cretaceous dinosaurs and feather-feeding beetles.

Extant terrestrial vertebrates, including birds, have a panoply of symbiotic relationships with many insects and arachnids, such as parasitism or mutualism. Yet, identifying arthropod-vertebrate symbioses in the fossil record has been based largely on indirect evidence; findings of direct association between arthropod guests and dinosaur host remains are exceedingly scarce. Here, we present direct and indirect evidence demonstrating that beetle larvae fed on feathers from an undetermined theropod host (avian or nonavian) 105 million y ago. An exceptional amber assemblage is reported of larval molts (exuviae) intimately associated with plumulaceous feather and other remains, as well as three additional amber pieces preserving isolated conspecific exuviae. Samples were found in the roughly coeval Spanish amber deposits of El Soplao, San Just, and Peñacerrada I. Integration of the morphological, systematic, and taphonomic data shows that the beetle larval exuviae, belonging to three developmental stages, are most consistent with skin/hide beetles (family Dermestidae), an ecologically important group with extant keratophagous species that commonly inhabit bird and mammal nests. These findings show that a symbiotic relationship involving keratophagy comparable to that of beetles and birds in current ecosystems existed between their Early Cretaceous relatives.

Fossil basicranium clarifies the origin of the avian central nervous system and inner ear.

Among terrestrial vertebrates, only crown birds (Neornithes) rival mammals in terms of relative brain size and behavioural complexity. Relatedly, the anatomy of the avian central nervous system and associated sensory structures, such as the vestibular system of the inner ear, are highly modified with respect to those of other extant reptile lineages. However, a dearth of three-dimensional Mesozoic fossils has limited our knowledge of the origins of the distinctive endocranial structures of crown birds. Traits such as an expanded, flexed brain, a ventral connection between the brain and spinal column, and a modified vestibular system have been regarded as exclusive to Neornithes. Here, we demonstrate all of these 'advanced' traits in an undistorted braincase from an Upper Cretaceous enantiornithine bonebed in southeastern Brazil. Our discovery suggests that these crown bird-like endocranial traits may have originated prior to the split between Enantiornithes and the more crownward portion of avian phylogeny over 140 Ma, while coexisting with a remarkably plesiomorphic cranial base and posterior palate region. Altogether, our results support the interpretation that the distinctive endocranial morphologies of crown birds and their Mesozoic relatives are affected by complex trade-offs between spatial constraints during development.

Ontogenetic niche shifts in the Mesozoic bird Confuciusornis sanctus.

Paleontological evidence reveals that the rapid growth characteristic of living birds evolved close to the origin of the crown-group Neornithes, as more stemward birds experienced protracted growth until becoming fully grown.1 Research on Mesozoic confuciusornithids, the earliest divergence of fully beaked birds, has revealed a complex life cycle in which these birds experienced multiple growth phases.2-4 Such a life-history pattern calls for the exploration of the role that ontogenetic niche shifts may have played in size-structuring confuciusornithid populations.5,6 Here, by analyzing the skeletal morphometrics of a dense sample of fossil individuals of Confuciusornis sanctus (n = 171, all fledged), we show that the youngest individuals of this confuciusornithid species experienced a precocious burst of beak growth, probably facilitating access to novel food resources that helped them meet the high energetic demands of their initial growth spurt. Such an early burst of facial (i.e., snout) growth resembles that of young crocodilians.7 However, in these reptiles, facial growth slows down soon thereafter, and the matching of snout scaling between mid-sized and larger individuals instigates demographic competence and the dispersion of the former.8 In contrast, our results reveal that beak growth in C. sanctus continued steadily. We hypothesized that the protracted facial growth of older individuals led to ontogenetic niche shifts by dietary segregation among size classes within populations. Our study thus confirms that the life cycle of C. sanctus was notably different from that of modern birds, and it reveals that beak size allometry may have facilitated population cohesiveness between coinhabiting age classes.

Exceptionally simple, rapidly replaced teeth in sauropod dinosaurs demonstrate a novel evolutionary strategy for herbivory in Late Jurassic ecosystems.

BACKGROUND: Dinosaurs dominated terrestrial environments for over 100 million years due in part to innovative feeding strategies. Although a range of dental adaptations was present in Late Jurassic dinosaurs, it is unclear whether dinosaur ecosystems exhibited patterns of tooth disparity and dietary correlation similar to those of modern amniotes, in which carnivores possess simple teeth and herbivores exhibit complex dentitions. To investigate these patterns, we quantified dental shape in Late Jurassic dinosaurs to test relationships between diet and dental complexity. RESULTS: Here, we show that Late Jurassic dinosaurs exhibited a disparity of dental complexities on par with those of modern saurians. Theropods possess relatively simple teeth, in spite of the range of morphologies tested, and is consistent with their inferred carnivorous habits. Ornithischians, in contrast, have complex dentitions, corresponding to herbivorous habits. The dentitions of macronarian sauropods are similar to some ornithischians and living herbivorous squamates but slightly more complex than other sauropods. In particular, all diplodocoid sauropods investigated possess remarkably simple teeth. The existence of simple teeth in diplodocoids, however, contrasts with the pattern observed in nearly all known herbivores (living or extinct). CONCLUSIONS: Sauropod dinosaurs exhibit a novel approach to herbivory not yet observed in other amniotes. We demonstrate that sauropod tooth complexity is related to tooth replacement rate rather than diet, which contrasts with the results from mammals and saurians. This relationship is unique to the sauropod clade, with ornithischians and theropods displaying the patterns observed in other groups. The decoupling of herbivory and tooth complexity paired with a correlation between complexity and replacement rate demonstrates a novel evolutionary strategy for plant consumption in sauropod dinosaurs.

Dental replacement in Mesozoic birds: evidence from newly discovered Brazilian enantiornithines.

Polyphyodonty-multiple tooth generations-in Mesozoic birds has been confirmed since the nineteenth century. Their dental cycle had been assessed through sparse data from tooth roots revealed through broken jawbones and disattached teeth. However, detailed descriptions of their tooth cycling are lacking, and the specifics of their replacement patterns remain largely unknown. Here we present unprecedented µCT data from three enantiornithine specimens from the Upper Cretaceous of southeastern Brazil. The high resolution µCT data show an alternating dental replacement pattern in the premaxillae, consistent with the widespread pattern amongst extinct and extant reptiles. The dentary also reveals dental replacement at different stages. These results strongly suggest that an alternating pattern was typical of enantiornithine birds. µCT data show that new teeth start lingually within the alveoli, resorb roots of functional teeth and migrate labially into their pulp cavities at an early stage, similar to modern crocodilians. Our results imply that the control mechanism for tooth cycling is conserved during the transition between non-avian reptiles and birds. These first 3D reconstructions of enantiornithine dental replacement demonstrate that 3D data are essential to understand the evolution and deep homology of archosaurian tooth cycling.

Independent origins of powered flight in paravian dinosaurs?

Feathered dinosaurs discovered during the last decades have illuminated the transition from land to air in these animals, underscoring a significant degree of experimentation in wing-assisted locomotion around the origin of birds. Such evolutionary experimentation led to lineages achieving either wing-assisted running, four-winged gliding, or membrane-winged gliding. Birds are widely accepted as the only dinosaur lineage that achieved powered flight, a key innovation for their evolutionary success. However, in a recent paper in Current Biology, Pei and colleagues1 disputed this view. They concluded that three other lineages of paravian dinosaurs (those more closely related to birds than to oviraptorosaurs) - Unenlagiinae, Microraptorinae and Anchiornithinae - could have evolved powered flight independently. While we praise the detailed phylogenetic framework of Pei and colleagues1 and welcome a new attempt to understand the onset of flight in dinosaurs, we here expose a set of arguments that significantly weaken their evidence supporting a multiple origin of powered flight. Specifically, we maintain that the two proxies used by Pei and colleagues1 to assess powered flight potential in non-avian paravians - wing loading and specific lift - fail to discriminate between powered flight (thrust generated by flapping) and passive flight (gliding).

Specialized Craniofacial Anatomy of a Titanosaurian Embryo from Argentina.

The first dinosaur embryos found inside megaloolithid eggs from Auca Mahuevo, Patagonia, were assigned to sauropod dinosaurs that lived approximately 80 million years ago. Discovered some 25 years ago, these considerably flattened specimens still remain the only unquestionable embryonic remains of a sauropod dinosaur providing an initial glimpse into titanosaurian in ovo ontogeny. Here we describe an almost intact embryonic skull, which indicates the early development of stereoscopic vision, and an unusual monocerotic face for a sauropod. The new fossil also reveals a neurovascular sensory system in the premaxilla and a partly calcified braincase, which potentially refines estimates of its prenatal stage. The embryo was found in an egg with thicker eggshell and a partly different geochemical signature than those from the egg-bearing layers described in Auca Mahuevo. The cranial bones are comparably ossified as in previously described specimens but differ in facial anatomy and size. The new specimen reveals significant heterochrony in cranial ossifications when compared with non-sauropod sauropodomorph embryos, and demonstrates that the specialized craniofacial morphology preceded the postnatal transformation of the skull anatomy in adults of related titanosaurians.

Retraction Note: Hummingbird-sized dinosaur from the Cretaceous period of Myanmar.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Anatomy of Parahesperornis: Evolutionary Mosaicism in the Cretaceous Hesperornithiformes (Aves).

The Hesperornithiformes constitute the first known avian lineage to secondarily lose flight in exchange for the evolution of a highly derived foot-propelled diving lifestyle, thus representing the first lineage of truly aquatic birds. First unearthed in the 19th century, and today known from numerous Late Cretaceous (Cenomanian-Maastrichtian) sites distributed across the northern hemisphere, these toothed birds have become icons of early avian evolution. Initially erected as a taxon in 1984 by L. D. Martin, Parahesperornis alexi is known from the two most complete hesperornithiform specimens discovered to date and has yet to be fully described. P. alexi thus contributes significantly to our understanding of hesperornithiform birds, despite often being neglected in favor of the iconic Hesperornis. Here, we present a full anatomical description of P. alexi based upon the two nearly complete specimens in the collections of the University of Kansas Natural History Museum, as well as an extensive comparison to other hesperornithiform taxa. This study reveals P. alexi to possess a mosaic of basal and derived traits found among other hesperornithiform taxa, indicating a transitional form in the evolution of these foot-propelled diving birds. This study describes broad evolutionary patterns within the Hesperornithiformes, highlighting the significance of these birds as not only an incredible example of the evolution of ecological specializations, but also for understanding modern bird evolution, as they are the last known divergence of pre-modern bird diversification.

Hummingbird-sized dinosaur from the Cretaceous period of Myanmar.

Skeletal inclusions in approximately 99-million-year-old amber from northern Myanmar provide unprecedented insights into the soft tissue and skeletal anatomy of minute fauna, which are not typically preserved in other depositional environments1-3. Among a diversity of vertebrates, seven specimens that preserve the skeletal remains of enantiornithine birds have previously been described1,4-8, all of which (including at least one seemingly mature specimen) are smaller than specimens recovered from lithic materials. Here we describe an exceptionally well-preserved and diminutive bird-like skull that documents a new species, which we name Oculudentavis khaungraae gen. et sp. nov. The find appears to represent the smallest known dinosaur of the Mesozoic era, rivalling the bee hummingbird (Mellisuga helenae)-the smallest living bird-in size. The O. khaungraae specimen preserves features that hint at miniaturization constraints, including a unique pattern of cranial fusion and an autapomorphic ocular morphology9 that resembles the eyes of lizards. The conically arranged scleral ossicles define a small pupil, indicative of diurnal activity. Miniaturization most commonly arises in isolated environments, and the diminutive size of Oculudentavis is therefore consistent with previous suggestions that this amber formed on an island within the Trans-Tethyan arc10. The size and morphology of this species suggest a previously unknown bauplan, and a previously undetected ecology. This discovery highlights the potential of amber deposits to reveal the lowest limits of vertebrate body size.

Anatomy and Flight Performance of the Early Enantiornithine Bird Protopteryx fengningensis: Information from New Specimens of the Early Cretaceous Huajiying Formation of China.

The Early Cretaceous (∼131 Million Years Ago) Protopteryx fengningensis is one of the oldest and most primitive enantiornithine birds; however, knowledge of its anatomy has largely been limited to the succinct description of two specimens (holotype and paratype). This study describes two new specimens of P. fengningensis preserving most of the skeleton and plumage, and it therefore adds significantly to understanding the morphology of this important species and the character evolution of enantiornithine birds. The well-preserved plumage of these specimens also affords a quantitative assessment of the flight performance of P. fengningensis. Our aerodynamic considerations indicate that this early enantiornithine was capable of intermittent flight (bounding or flap-gliding), thus marking the earliest occurrence of such energy-saving aerial strategy. Anat Rec, 303:716-731, 2020. © 2019 American Association for Anatomy.

Osteohistology and Life History of the Basal Pygostylian, Confuciusornis sanctus.

More than a thousand specimens of Confuciusornis sanctus have been recovered from the Early Cretaceous Jehol Group of Northeastern China. Here, we investigate the bone microstructure of 33 long bones sampled from 14 C. sanctus specimens in an attempt to assess the life history patterns of this basal pygostylian bird. Analysis of the histology of various skeletal elements (femur, humerus, tibia, radius, and ulna) revealed differences in the histology of their bone walls. Based on the osteohistology, we coded the examined specimens into five histology age classes. We found that histological age was not strictly correlated with body size. The variability in the histology of multiple bones from single skeletons suggests differences in the growth rate of the skeleton in response to allometry, functional demands, and pathology. We show that although fibrolamellar bone is widespread across birds, the extent and duration of this rapid phase of bone deposition is highly variable. Comparisons among Mesozoic birds confirm that early ontogenetic growth was rapid, but that later post-hatching growth was strongly influenced by the ontogenetic age of the individual, body size, and local environment, as well as taxonomy. Our findings indicate that C. sanctus experienced rapid growth from early ontogeny until almost fully grown, and thereafter transitioned to slow, episodic growth (for at least 3-4 years) to reach skeletal maturity. Anat Rec, 303:949-962, 2020. © 2019 American Association for Anatomy.

Mid-Cretaceous amber inclusions reveal morphogenesis of extinct rachis-dominated feathers.

We describe three-dimensionally preserved feathers in mid-Cretaceous Burmese amber that share macro-morphological similarities (e.g., proportionally wide rachis with a "medial stripe") with lithic, two-dimensionally preserved rachis-dominated feathers, first recognized in the Jehol Biota. These feathers in amber reveal a unique ventrally concave and dorsoventrally thin rachis, and a dorsal groove (sometimes pigmented) that we identify as the "medial stripe" visible in many rachis-dominated rectrices of Mesozoic birds. The distally pennaceous portion of these feathers shows differentiated proximal and distal barbules, the latter with hooklets forming interlocking barbs. Micro-CT scans and transverse sections demonstrate the absence of histodifferentiated cortex and medullary pith of the rachis and barb rami. The highly differentiated barbules combined with the lack of obvious histodifferentiation of the barb rami or rachis suggests that these feathers could have been formed without the full suite and developmental interplay of intermediate filament alpha keratins and corneous beta-proteins that is employed in the cornification process of modern feathers. This study thus highlights how the development of these feathers might have differed from that of their modern counterparts, namely in the morphogenesis of the ventral components of the rachis and barb rami. We suggest that the concave ventral surface of the rachis of these Cretaceous feathers is not homologous with the ventral groove of modern rachises. Our study of these Burmese feathers also confirms previous claims, based on two-dimensional fossils, that they correspond to an extinct morphotype and it cautions about the common practice of extrapolating developmental aspects (and mechanical attributes) of modern feathers to those of stem birds (and their dinosaurian outgroups) because the latter need not to have developed through identical pathways.

New Bohaiornis-like bird from the Early Cretaceous of China: enantiornithine interrelationships and flight performance.

During the last decade, several Bohaiornis-like enantiornithine species-and numerous specimens-have been recognized from the celebrated Jehol Biota of northwestern China. In this paper, we describe the anatomy of another "bohaiornithid" species from the 125 million-year-old Yixian Formation of Liaoning Province, China. The new taxon differs from previously recognized "bohaiornithids" on a number of characters from the forelimb and shoulder girdle. We also provide a new phylogenetic framework for enantiornithine birds, which questions the monophyly of the previously recognized bohaiornithid clade and highlights ongoing challenges for resolving enantiornithine interrelationships. Additionally, we offer the first assessment of the flight properties of Bohaiornis-like enantiornithines. Our results indicate that while "bohaiornithids" were morphologically suited for flying through continuous flapping, they would have been unable to sustain prolonged flights. Such findings expand the flight strategies previously known for enantiornithines and other early birds.

A New Enantiornithine Bird with Unusual Pedal Proportions Found in Amber.

Recent discoveries of vertebrate remains trapped in middle Cretaceous amber from northern Myanmar [1, 2] have provided insights into the morphology of soft-tissue structures in extinct animals [3-7], in particular, into the evolution and paleobiology of early birds [4, 8, 9]. So far, five bird specimens have been described from Burmese amber: two isolated wings, an isolated foot with wing fragment, and two partial skeletons [4, 8-10]. Most of these specimens contain the remains of juvenile enantiornithine birds [4]. Here, we describe a new specimen of enantiornithine bird in amber, collected at the Angbamo locality in the Hukawng Valley. The new specimen includes a partial right hindlimb and remiges from an adult or subadult bird. Its foot, of which the third digit is much longer than the second and fourth digits, is distinct from those of all other currently recognized Mesozoic and extant birds. Based on the autapomorphic foot morphology, we erect a new taxon, Elektorornis chenguangi gen. et sp. nov. We suggest that the elongated third digit was employed in a unique foraging strategy, highlighting the bizarre morphospace in which early birds operated.

A fully feathered enantiornithine foot and wing fragment preserved in mid-Cretaceous Burmese amber.

Over the last three years, Burmese amber (~99 Ma, from Myanmar) has provided a series of immature enantiornithine skeletal remains preserved in varying developmental stages and degrees of completeness. These specimens have improved our knowledge based on compression fossils in Cretaceous sedimentary rocks, adding details of three-dimensional structure and soft tissues that are rarely preserved elsewhere. Here we describe a remarkably well-preserved foot, accompanied by part of the wing plumage. These body parts were likely dismembered, entering the resin due to predatory or scavenging behaviour by a larger animal. The new specimen preserves contour feathers on the pedal phalanges together with enigmatic scutellae scale filament (SSF) feathers on the foot, providing direct analogies to the plumage patterns observed in modern birds, and those cultivated through developmental manipulation studies. Ultimately, this connection may allow researchers to observe how filamentous dinosaur 'protofeathers' developed-testing theories using evolutionary holdovers in modern birds.

Avian tail ontogeny, pygostyle formation, and interpretation of juvenile Mesozoic specimens.

The avian tail played a critical role in the evolutionary transition from long- to short-tailed birds, yet its ontogeny in extant birds has largely been ignored. This deficit has hampered efforts to effectively identify intermediate species during the Mesozoic transition to short tails. Here we show that fusion of distal vertebrae into the pygostyle structure does not occur in extant birds until near skeletal maturity, and mineralization of vertebral processes also occurs long after hatching. Evidence for post-hatching pygostyle formation is also demonstrated in two Cretaceous specimens, a juvenile enantiornithine and a subadult basal ornithuromorph. These findings call for reinterpretations of Zhongornis haoae, a Cretaceous bird hypothesized to be an intermediate in the long- to short-tailed bird transition, and of the recently discovered coelurosaur tail embedded in amber. Zhongornis, as a juvenile, may not yet have formed a pygostyle, and the amber-embedded tail specimen is reinterpreted as possibly avian. Analyses of relative pygostyle lengths in extant and Cretaceous birds suggests the number of vertebrae incorporated into the pygostyle has varied considerably, further complicating the interpretation of potential transitional species. In addition, this analysis of avian tail development reveals the generation and loss of intervertebral discs in the pygostyle, vertebral bodies derived from different kinds of cartilage, and alternative modes of caudal vertebral process morphogenesis in birds. These findings demonstrate that avian tail ontogeny is a crucial parameter specifically for the interpretation of Mesozoic specimens, and generally for insights into vertebrae formation.

A diminutive perinate European Enantiornithes reveals an asynchronous ossification pattern in early birds.

Fossils of juvenile Mesozoic birds provide insight into the early evolution of avian development, however such fossils are rare. The analysis of the ossification sequence in these early-branching birds has the potential to address important questions about their comparative developmental biology and to help understand their morphological evolution and ecological differentiation. Here we report on an early juvenile enantiornithine specimen from the Early Cretaceous of Europe, which sheds new light on the osteogenesis in this most species-rich clade of Mesozoic birds. Consisting of a nearly complete skeleton, it is amongst the smallest known Mesozoic avian fossils representing post-hatching stages of development. Comparisons between this new specimen and other known early juvenile enantiornithines support a clade-wide asynchronous pattern of osteogenesis in the sternum and the vertebral column, and strongly indicate that the hatchlings of these phylogenetically basal birds varied greatly in size and tempo of skeletal maturation.