Developmental strategies underlying gigantism and miniaturization in non-avialan theropod dinosaurs.

In amniotes, the predominant developmental strategy underlying body size evolution is thought to be adjustments to the rate of growth rather than its duration. However, most theoretical and experimental studies supporting this axiom focus on pairwise comparisons and/or lack an explicit phylogenetic framework. We present the first large-scale phylogenetic comparative analysis examining developmental strategies underlying the evolution of body size, focusing on non-avialan theropod dinosaurs. We reconstruct ancestral states of growth rate and body mass in a taxonomically rich dataset, finding that contrary to expectations, changes in the rate and duration of growth played nearly equal roles in the evolution of the vast body size disparity present in non-avialan theropods-and perhaps that of amniotes in general.

Sauropodomorph evolution across the Triassic-Jurassic boundary: body size, locomotion, and their influence on morphological disparity.

Sauropodomorph dinosaurs were the dominant medium to large-sized herbivores of most Mesozoic continental ecosystems, being characterized by their long necks and reaching a size unparalleled by other terrestrial animals (> 60 tonnes). Our study of morphological disparity across the entire skeleton shows that during the Late Triassic the oldest known sauropodomorphs occupied a small region of morphospace, subsequently diversifying both taxonomically and ecologically, and shifting to a different and broader region of the morphospace. After the Triassic-Jurassic boundary event, there are no substancial changes in sauropodomorph morphospace occupation. Almost all Jurassic sauropodomorph clades stem from ghost lineages that cross the Triassic-Jurassic boundary, indicating that variations after the extinction were more related to changes of pre-existing lineages (massospondylids, non-gravisaurian sauropodiforms) rather than the emergence of distinct clades or body plans. Modifications in the locomotion (bipedal to quadrupedal) and the successive increase in body mass seem to be the main attributes driving sauropodomorph morphospace distribution during the Late Triassic and earliest Jurassic. The extinction of all non-sauropod sauropodomorphs by the Toarcian and the subsequent diversification of gravisaurian sauropods represent a second expansion of the sauropodomorph morphospace, representing the onset of the flourishing of these megaherbivores that subsequently dominated in Middle and Late Jurassic terrestrial assemblages.

The influence of juvenile dinosaurs on community structure and diversity.

Despite dominating biodiversity in the Mesozoic, dinosaurs were not speciose. Oviparity constrained even gigantic dinosaurs to less than 15 kg at birth; growth through multiple morphologies led to the consumption of different resources at each stage. Such disparity between neonates and adults could have influenced the structure and diversity of dinosaur communities. Here, we quantified this effect for 43 communities across 136 million years and seven continents. We found that megatheropods (more than 1000 kg) such as tyrannosaurs had specific effects on dinosaur community structure. Although herbivores spanned the body size range, communities with megatheropods lacked carnivores weighing 100 to 1000 kg. We demonstrate that juvenile megatheropods likely filled the mesocarnivore niche, resulting in reduced overall taxonomic diversity. The consistency of this pattern suggests that ontogenetic niche shift was an important factor in generating dinosaur community structure and diversity.

Development and evolution of the notarium in Pterosauria.

The notarium is the structure formed by fusion of the dorsal vertebrae which occurred independently in pterosaurs and birds. This ankylosis usually involves two to six elements and in many cases, also includes the last cervical vertebra. Fusion can occur in different degrees, uniting the vertebral centra, the neural spines, the transverse processes, the ventral processes, or a combination of these sites. A detailed assessment of the fusion process of pterosaur dorsal vertebrae is still lacking. Here we identify the fusion sequence of pterosaur notarial elements, demonstrating the order of ossification in vertebral bodies and neural spines based on fossils and extant birds. In both Pterosauria and Aves, the notarium generally develops in a antero-posterior direction, but the actual order of each fusion locus may present slight variations. Based on our data, we were able to identify seven developmental stages in the notarium formation, with broad implications for the prediction of ontogenetic stages for the Pterosauria. In addition, we report the occurrence of a notarium in Ardeadactylus longicollum (Kimmeridgian, Southern Germany), the oldest occurrence of this structure in pterosaurs.

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.

Variations of Mesozoic feathers: Insights from the morphogenesis of extant feather rachises.

The rachises of extant feathers, composed of dense cortex and spongy internal medulla, are flexible and light, yet stiff enough to withstand the load required for flight, among other functions. Incomplete knowledge of early feathers prevents a full understanding of how cylindrical rachises have evolved. Bizarre feathers with unusually wide and flattened rachises, known as "rachis-dominated feathers" (RDFs), have been observed in fossil nonavian and avian theropods. Newly discovered RDFs embedded in early Late Cretaceous Burmese ambers (about 99 million year ago) suggest the unusually wide and flattened rachises mainly consist of a dorsal cortex, lacking a medulla and a ventral cortex. Coupled with findings on extant feather morphogenesis, known fossil RDFs were categorized into three morphotypes based on their rachidial configurations. For each morphotype, potential developmental scenarios were depicted by referring to the rachidial development in chickens, and relative stiffness of each morphotype was estimated through functional simulations. The results suggest rachises of RDFs are developmentally equivalent to a variety of immature stages of cylindrical rachises. Similar rachidial morphotypes documented in extant penguins suggest that the RDFs are not unique to Mesozoic theropods, although they are likely to have evolved independently in extant penguins.

A new microraptorine theropod from the Jehol Biota and growth in early dromaeosaurids.

Fossils from the Jehol Group (Early Cretaceous, Liaoning Province, China) are integral to our understanding of Paraves, the clade of dinosaurs grouping dromaeosaurids, troodontids, and avialians, including living birds. However, many taxa are represented by specimens of unclear ontogenetic age. Without a more thorough understanding of ontogeny, evolutionary relationships and significance of character states within paravian dinosaurs may be obscured and our ability to infer their biology restricted. We describe a complete specimen of a new microraptorine dromaeosaur, Wulong bohaiensis gen. et sp. nov., from the geologically young Jiufotang Formation (Aptian) that helps solve this problem. Phylogenetic analysis recovers the specimen within a monophyletic Microraptorinae. Preserved in articulation on a single slab, the type specimen is small and exhibits osteological markers of immaturity identified in other archosaurs, such as bone texture and lack of fusion. To contextualize this signal, we histologically sampled the tibia, fibula, and humerus and compared them with new samples from the closely related and osteologically mature Sinornithosaurus. Histology shows both specimens to be young and still growing at death, indicating an age for the new dinosaur of about 1 year. The holotype possesses several feather types, including filamentous feathers, pennaceous primaries, and long rectrices, establishing that their growth preceded skeletal maturity and full adult size in some dromaeosaurids. Comparison of histology in the new taxon and Sinornithosaurus indicates that macroscopic signs of maturity developed after the first year, but before cessation of growth, demonstrating that nonhistological indicators of adulthood may be misleading when applied to dromaeosaurids. Anat Rec, 303:963-987, 2020. © 2020 American Association for Anatomy.

Birdlike growth and mixed-age flocks in avimimids (Theropoda, Oviraptorosauria).

Avimimids were unusual, birdlike oviraptorosaurs from the Late Cretaceous of Asia. Initially enigmatic, new information has ameliorated the understanding of their anatomy, phylogenetic position, and behaviour. A monodominant bonebed from the Nemegt Formation of Mongolia showed that some avimimids were gregarious, but the site is unusual in the apparent absence of juveniles. Here, a second monodominant avimimid bonebed is described from the Iren Dabasu Formation of northern China. Elements recovered include numerous vertebrae and portions of the forelimbs and hindlimbs, representing a minimum of six individuals. Histological sampling of two tibiotarsi from the bonebed reveals rapid growth early in ontogeny followed by unexpectedly early onset of fusion and limited subsequent growth. This indicates that avimimids grew rapidly to adult size, like most extant birds but contrasting other small theropod dinosaurs. The combination of adults and juveniles in the Iren Dabasu bonebed assemblage provides evidence of mixed-age flocking in avimimids and the onset of fusion in young individuals suggests that some of the individuals in the Nemegt Formation bonebed may have been juveniles. Regardless, these individuals were likely functionally analogous to adults, and this probably facilitated mixed-age flocking by reducing ontogenetic niche shift in avimimids.

Histological and developmental insights into the herbivorous dentition of tapinocephalid therapsids.

Tapinocephalids were one of the earliest therapsid clades to evolve herbivory. In acquiring derived tooth-to-tooth occlusion by means of an exaggerated heel and talon crown morphology, members of this family have long been considered herbivorous, yet little work has been done to describe their dentition. Given the early occurrence of this clade and their acquisition of a dentition with several derived features, tapinocephalids serve as an important clade in understanding adaptations to herbivory as well as macroevolutionary patterns of dental trait acquisition. Here we describe the histology of tapinocephalid jaws and incisors to assess adaptations to herbivory. Our results yield new dental characters for tapinocephalids including a peculiar enamel structure and reduced enamel deposition on the occlusal surface. These traits are convergent with other specialized herbivorous dentitions like those found in ornithischian dinosaurs and ungulates. Furthermore, these results demonstrate that while acquiring some specializations, tapinocephalids also retained plesiomorphic traits like alternate, continuous replacement. We interpret these findings as an example of how different combinations of traits can facilitate a derived and specialized dentition and then discuss their implications in the acquisition of a mammal-like dentition.

Comparing growth patterns of three species: Similarities and differences.

Quantitative studies of the growth of dinosaurs have made comparisons with modern animals possible. Therefore, it is meaningful to ask, if extinct dinosaurs grew faster than modern animals, e.g. birds (modern dinosaurs) and reptiles. However, past studies relied on only a few growth models. If these models were false, what about the conclusions? This paper fits growth data to a more comprehensive class of models, defined by the von Bertalanffy-Pütter (BP) differential equation. Applied to data about Tenontosaurus tilletti, Alligator mississippiensis and the Athens Canadian Random Bred strain of Gallus gallus domesticus the best fitting growth curves did barely differ, if they were rescaled for size and lifespan. A difference could be discerned, if time was rescaled for the age at the inception point (maximal growth) or if the percentual growth was compared.

Trends in embryonic and ontogenetic growth metabolisms in nonavian dinosaurs and extant birds, mammals, and crocodylians with implications for dinosaur egg incubation.

The embryonic metabolism of the saurischian dinosaur Troodon formosus and the ornithischian dinosaurs Protoceratops andrewsi and Hypacrosaurus stebingeri have been determined by using a mass growth model based on conservation of energy and found to be very similar. Embryonic and ontogenetic growth metabolisms are also evaluated for extant altricial birds, precocial birds, mammals, and crocodylians to examine for trends in the different groups of animals and to provide a context for interpreting our results for nonavian dinosaurs. This analysis reveals that the embryonic metabolisms of these nonavian dinosaurs were closer to the range observed in extant crocodylians than extant birds. The embryonic metabolisms of nonavian dinosaurs were in the range observed for extant mammals of similar masses. The measured embryonic metabolic rates for these three nonavian dinosaurs are then used to calculate the incubation times for eggs of 22 nonavian dinosaurs from both Saurischia and Ornithischia. The calculated incubation times vary from about 50 days for Archaeopteryx lithographica to about 150 days for Alamosaurus sanjuanensis.

Osteohistology of the silesaurid Sacisaurus agudoensis from southern Brazil (Late Triassic) and implications for growth in early dinosaurs.

The non-dinosaurian dinosauriform silesaurids are the closest relatives of crown-group dinosaurs and are thus, important for understanding the origins of that group. Here, we describe the limb bone histology of the Late Triassic silesaurid Sacisaurus agudoensis from the Candelária Sequence of the Santa Maria Supersequence, Rio Grande do Sul state, Brazil. The sampled bones comprise eight femora and one fibula from different individuals. The microscopic analysis of all elements reveals uninterrupted fibrolamellar bone tissue indicating rapid growth. A transition to slower growing peripheral parallel-fibered bone tissue in some individuals indicates a decrease in growth rate, suggesting ontogenetic variation within the sample. The osteohistology of Sacisaurus agudoensis is similar to that of other silesaurids and supports previous hypotheses that rapid growth was attained early in the dinosauromorph lineage. However, silesaurids lack the complex vascular arrangements seen in saurischian dinosaurs. Instead, they exhibit predominantly longitudinally-oriented primary osteons with few or no anastomoses, similar to those of some small early ornithischian dinosaurs. This simpler vascular pattern is common to all silesaurids studied to date and indicates relatively slower growth rates compared to most Dinosauria.

Description of Tooth Ontogeny and Replacement Patterns in a Juvenile Tarbosaurus bataar (Dinosauria: Theropoda) Using CT-Scan Data.

Teeth are continually replaced in most of non-mammalian gnathostomes to maintain their functional dentitions. To clarify the tooth replacement patterns in tyrannosaurid theropod dinosaurs, we examined well-preserved dentitions (both premaxillae, left maxilla, partial right maxilla, and both dentaries) of a juvenile Tarbosaurus bataar (MPC-D 107/7) using X-ray computed tomographic (CT) imaging. Three-dimensional (3D) rendering of the dentitions and staging of replacement teeth allowed quantitative analyses of the tooth ontogeny and replacement patterns in this specimen. These strategies were validated by comparing the results between MPC-D 107/7 and extant crocodilians, which are taxa that have previously been studied using non-CT methods. 3D-rendered dentitions of MPC-D 107/7 showed alternate replacement patterns between odd- and even-numbered alveoli. Such patterns were discontinuous at the premaxilla-maxilla junctions, suggesting the division of replacement patterns between the two dentitions possessing morpho-functionally different features. The replacement process in the odd-numbered alveoli of the left maxilla sequentially proceeded from distal alveoli. Meanwhile, in the both dentaries, there were simple alternate patterns in which functional teeth would be simultaneously shed out in every second alveoli. Such a simple alternation had never been reported in the adult tyrannosaurid dentaries. Under this pattern, the half of functional teeth in a single dentition would be shed at the same time, which may hamper foraging functions. We conclude that the simple alternate patterns found in the dentary dentitions of MPC-D 107/7 represent transient condition in juvenile tyrannosaurids, suggesting ontogenetic changes in tooth replacement patterns in the tyrannosaurid dentary. Anat Rec, 302:1210-1225, 2019. © 2018 Wiley Periodicals, Inc.

Ontogeny and taxonomy of the hadrosaur (Dinosauria, Ornithopoda) remains from Basturs Poble bonebed (late early Maastrichtian, Tremp Syncline, Spain).

The lower Maastrichtian site of Basturs Poble (southern Pyrenees, Spain) is the first hadrosaur bonebed reported from Europe. It is an accumulation of disarticulated lambeosaurine skeletal elements, possibly belonging to Pararhabdodon isonensis. The sample shows high intraspecific morphological variability among many skeletal elements, suggesting the need for caution in choosing characters for phylogenetic analyses. Juvenile to adult individuals are represented in the sample, while hatchling remains are absent. Bone histology reveals that juveniles are over-represented and that the youngest individuals represented by tibia specimens were two years old. Adult individuals, with tibiae 550-600 mm long, were 14-15 years old when they died. However, individual variation in tibia length at skeletal maturity occurs within the sample, so individual maturity cannot be assumed on the basis of bone size alone. The Basturs Poble bonebed occurs within the upper part of the C31r magnetochron. Thus, lambeosaurine hadrosaurids were already present and abundant in the Ibero-Armorica Island at the end of the early Maastrichtian and P. isonensis spans the upper part of the lower Maastrichtian to the upper part of the upper Maastrichtian (upper part of C31r-lower part of C29r).

Developmental patterns and variation among early theropods.

Understanding ontogenetic patterns is important in vertebrate paleontology because the assessed skeletal maturity of an individual often has implications for paleobiogeography, species synonymy, paleobiology, and body size evolution of major clades. Further, for many groups the only means of confidently determining ontogenetic status of an organism is through the destructive process of histological sampling. Although the ontogenetic patterns of Late Jurassic and Cretaceous dinosaurs are better understood, knowledge of the ontogeny of the earliest dinosaurs is relatively poor because most species-level growth series known from these groups are small (usually, maximum of n ~ 5) and incomplete. To investigate the morphological changes that occur during ontogeny in early dinosaurs, I used ontogenetic sequence analysis (OSA) to reconstruct developmental sequences of morphological changes in the postcranial ontogeny of the early theropods Coelophysis bauri and Megapnosaurus rhodesiensis, both of which are known from large sample sizes (n = 174 and 182, respectively). I found a large amount of sequence polymorphism (i.e. intraspecific variation in developmental patterns) in both taxa, and especially in C. bauri, which possesses this variation in every element analyzed. Megapnosaurus rhodesiensis is similar, but it possesses no variation in the sequence of development of ontogenetic characters in the tibia and tarsus. Despite the large amount of variation in development, many characters occur consistently earlier or later in ontogeny and could therefore be important morphological features for assessing the relative maturity of other early theropods. Additionally, there is a phylogenetic signal to the order in which homologous characters appear in ontogeny, with homologous characters appearing earlier or later in developmental sequences of early theropods and the close relatives of dinosaurs, silesaurids. Many of these morphological features are important characters for the reconstruction of archosaurian phylogeny (e.g. trochanteric shelf). Because these features vary in presence or appearance with ontogeny, these characters should be used with caution when undertaking phylogenetic analyses in these groups, since a specimen may possess certain character states owing to ontogenetic stage, not evolutionary relationships.

The skull roof tracks the brain during the evolution and development of reptiles including birds.

Major transformations in brain size and proportions, such as the enlargement of the brain during the evolution of birds, are accompanied by profound modifications to the skull roof. However, the hypothesis of concerted evolution of shape between brain and skull roof over major phylogenetic transitions, and in particular of an ontogenetic relationship between specific regions of the brain and the skull roof, has never been formally tested. We performed 3D morphometric analyses to examine the deep history of brain and skull-roof morphology in Reptilia, focusing on changes during the well-documented transition from early reptiles through archosauromorphs, including nonavian dinosaurs, to birds. Non-avialan taxa cluster tightly together in morphospace, whereas Archaeopteryx and crown birds occupy a separate region. There is a one-to-one correspondence between the forebrain and frontal bone and the midbrain and parietal bone. Furthermore, the position of the forebrain-midbrain boundary correlates significantly with the position of the frontoparietal suture across the phylogenetic breadth of Reptilia and during the ontogeny of individual taxa. Conservation of position and identity in the skull roof is apparent, and there is no support for previous hypotheses that the avian parietal is a transformed postparietal. The correlation and apparent developmental link between regions of the brain and bony skull elements are likely to be ancestral to Tetrapoda and may be fundamental to all of Osteichthyes, coeval with the origin of the dermatocranium.

The Origin and Evolutionary Consequences of Skeletal Traits Shaped by Embryonic Muscular Activity, from Basal Theropods to Modern Birds.

Embryonic muscular activity (EMA) is involved in the development of several distinctive traits of birds. Modern avian diversity and the fossil record of the dinosaur-bird transition allow special insight into their evolution. Traits shaped by EMA result from mechanical forces acting at post-morphogenetic stages, such that genes often play a very indirect role. Their origin seldom suggests direct selection for the trait, but a side-effect of other changes such as musculo-skeletal rearrangements, heterochrony in skeletal maturation, or increased incubation temperature (which increases EMA). EMA-shaped traits like sesamoids may be inconstant, highly conserved, or even disappear and then reappear in evolution. Some sesamoids may become increasingly influenced in evolution by genetic-molecular mechanisms (genetic assimilation). There is also ample evidence of evolutionary transitions from sesamoids to bony eminences at tendon insertion sites, and vice-versa. This can be explained by newfound similarities in the earliest development of both kinds of structures, which suggest these transitions are likely triggered by EMA. Other traits that require EMA for their formation will not necessarily undergo genetic assimilation, but still be conserved over tens and hundreds of millions of years, allowing evolutionary reduction and loss of other skeletal elements. Upon their origin, EMA-shaped traits may not be directly genetic, nor immediately adaptive. Nevertheless, EMA can play a key role in evolutionary innovation, and have consequences for the subsequent direction of evolutionary change. Its role may be more important and ubiquitous than currently suspected.

Novel insight into the origin of the growth dynamics of sauropod dinosaurs.

Sauropod dinosaurs include the largest terrestrial animals and are considered to have uninterrupted rapid rates of growth, which differs from their more basal relatives, which have a slower cyclical growth. Here we examine the bone microstructure of several sauropodomorph dinosaurs, including basal taxa, as well as the more derived sauropods. Although our results agree that the plesiomorphic condition for Sauropodomorpha is cyclical growth dynamics, we found that the hypothesized dichotomy between the growth patterns of basal and more derived sauropodomorphs is not supported. Here, we show that sauropod-like growth dynamics of uninterrupted rapid growth also occurred in some basal sauropodomorphs, and that some basal sauropods retained the plesiomorphic cyclical growth patterns. Among the sauropodomorpha it appears that the basal taxa exploited different growth strategies, but the more derived Eusauropoda successfully utilized rapid, uninterrupted growth strategies.

Dinosaurs, Chameleons, Humans, and Evo-Devo Path: Linking Étienne Geoffroy's Teratology, Waddington's Homeorhesis, Alberch's Logic of "Monsters," and Goldschmidt Hopeful "Monsters".

Since the rise of evo-devo (evolutionary developmental biology) in the 1980s, few authors have attempted to combine the increasing knowledge obtained from the study of model organisms and human medicine with data from comparative anatomy and evolutionary biology in order to investigate the links between development, pathology, and macroevolution. Fortunately, this situation is slowly changing, with a renewed interest in evolutionary developmental pathology (evo-devo-path) in the past decades, as evidenced by the idea to publish this special, and very timely, issue on "Developmental Evolution in Biomedical Research." As all of us have recently been involved, independently, in works related in some way or another with evolution and developmental anomalies, we decided to join our different perspectives and backgrounds in the present contribution for this special issue. Specifically, we provide a brief historical account on the study of the links between evolution, development, and pathologies, followed by a review of the recent work done by each of us, and then by a general discussion on the broader developmental and macroevolutionary implications of our studies and works recently done by other authors. Our primary aims are to highlight the strength of studying developmental anomalies within an evolutionary framework to understand morphological diversity and disease by connecting the recent work done by us and others with the research done and broader ideas proposed by authors such as Étienne Geoffroy Saint-Hilaire, Waddington, Goldschmidt, Gould, and Per Alberch, among many others to pave the way for further and much needed work regarding abnormal development and macroevolution.

Medullary bone in fossils: function, evolution and significance in growth curve reconstructions of extinct vertebrates.

Medullary bone (MB) is a special endosteal tissue forming in the bones of female birds during egg laying to serve as a labile calcium reservoir for building the hard eggshell. Therefore, the presence of MB reported in multiple nonavian dinosaurs is currently considered as evidence that those specimens were sexually mature females in their reproductive period. This interpretation has led to further inferences on species-specific growth strategies and related life-history aspects of these extinct vertebrates. However, a few studies questioned the reproductive significance of fossil MB by either regarding the tissue pathological or attributing alternative functions to it. This study reviews the general inferences on extinct vertebrates and discusses the primary role, distribution, regulation and adaptive significance of avian MB to point out important but largely overlooked uncertainties and inconsistencies in this matter. Emerging discordancy is demonstrated when the presence of MB vs. trade-off between growth and reproduction is used for interpreting dinosaurian growth curves. Synthesis of these data suggests that fossil MB was related to high calcium turnover rates but not exclusively to egg laying. Furthermore, revised application of Allosaurus growth data by modelling individual-based growth curves implies a much higher intraspecific variability in growth strategies, including timing of sexual maturation, than usually acknowledged. New hypotheses raised here to resolve these incongruences also propose new directions of research on the origin and functional evolution of this curious bone tissue.