A switch in jaw form-function coupling during the evolution of mammals.

The evolutionary shift from a single-element ear, multi-element jaw to a multi-element ear, single-element jaw during the transition to crown mammals marks one of the most dramatic structural transformations in vertebrates. Research on this transformation has focused on mammalian middle-ear evolution, but a mandible comprising only the dentary is equally emblematic of this evolutionary radiation. Here, we show that the remarkably diverse jaw shapes of crown mammals are coupled with surprisingly stereotyped jaw stiffness. This strength-based morphofunctional regime has a genetic basis and allowed mammalian jaws to effectively resist deformation as they radiated into highly disparate forms with markedly distinct diets. The main functional consequences for the mandible of decoupling hearing and mastication were a trade-off between higher jaw stiffness versus decreased mechanical efficiency and speed compared with non-mammals. This fundamental and consequential shift in jaw form-function underpins the ecological and taxonomic diversification of crown mammals. This article is part of the theme issue 'The mammalian skull: development, structure and function'.

The developing bird pelvis passes through ancestral dinosaurian conditions.

Living birds (Aves) have bodies substantially modified from the ancestral reptilian condition. The avian pelvis in particular experienced major changes during the transition from early archosaurs to living birds1,2. This stepwise transformation is well documented by an excellent fossil record2-4; however, the ontogenetic alterations that underly it are less well understood. We used embryological imaging techniques to examine the morphogenesis of avian pelvic tissues in three dimensions, allowing direct comparison with the fossil record. Many ancestral dinosaurian features2 (for example, a forward-facing pubis, short ilium and pubic 'boot') are transiently present in the early morphogenesis of birds and arrive at their typical 'avian' form after transitioning through a prenatal developmental sequence that mirrors the phylogenetic sequence of character acquisition. We demonstrate quantitatively that avian pelvic ontogeny parallels the non-avian dinosaur-to-bird transition and provide evidence for phenotypic covariance within the pelvis that is conserved across Archosauria. The presence of ancestral states in avian embryos may stem from this conserved covariant relationship. In sum, our data provide evidence that the avian pelvis, whose early development has been little studied5-7, evolved through terminal addition-a mechanism8-10 whereby new apomorphic states are added to the end of a developmental sequence, resulting in expression8,11 of ancestral character states earlier in that sequence. The phenotypic integration we detected suggests a previously unrecognized mechanism for terminal addition and hints that retention of ancestral states in development is common during evolutionary transitions.

Unveiling the third dimension in morphometry with automated quantitative volumetric computations.

As computed tomography and related technologies have become mainstream tools across a broad range of scientific applications, each new generation of instrumentation produces larger volumes of more-complex 3D data. Lagging behind are step-wise improvements in computational methods to rapidly analyze these new large, complex datasets. Here we describe novel computational methods to capture and quantify volumetric information, and to efficiently characterize and compare shape volumes. It is based on innovative theoretical and computational reformulation of volumetric computing. It consists of two theoretical constructs and their numerical implementation: the spherical wave decomposition (SWD), that provides fast, accurate automated characterization of shapes embedded within complex 3D datasets; and symplectomorphic registration with phase space regularization by entropy spectrum pathways (SYMREG), that is a non-linear volumetric registration method that allows homologous structures to be correctly warped to each other or a common template for comparison. Together, these constitute the Shape Analysis for Phenomics from Imaging Data (SAPID) method. We demonstrate its ability to automatically provide rapid quantitative segmentation and characterization of single unique datasets, and both inter-and intra-specific comparative analyses. We go beyond pairwise comparisons and analyze collections of samples from 3D data repositories, highlighting the magnified potential our method has when applied to data collections. We discuss the potential of SAPID in the broader context of generating normative morphologies required for meaningfully quantifying and comparing variations in complex 3D anatomical structures and systems.

The anatomy and palaeobiology of the early armoured dinosaur Scutellosaurus lawleri (Ornithischia: Thyreophora) from the Kayenta Formation (Lower Jurassic) of Arizona.

The armoured dinosaurs, Thyreophora, were a diverse clade of ornithischians known from the Early Jurassic to the end of the Cretaceous. During the Middle and Late Jurassic, the thyreophorans radiated to evolve large body size, quadrupedality, and complex chewing mechanisms, and members of the group include some of the most iconic dinosaurs, including the plated Stegosaurus and the club-tailed Ankylosaurus; however, the early stages of thyreophoran evolution are poorly understood due to a paucity of relatively complete remains from early diverging thyreophoran taxa. Scutellosaurus lawleri is generally reconstructed as the earliest-diverging thyreophoran and is known from over 70 specimens from the Lower Jurassic Kayenta Formation of Arizona, USA. Whereas Scutellosaurus lawleri is pivotal to our understanding of character-state changes at the base of Thyreophora that can shed light on the early evolution of the armoured dinosaurs, the taxon has received limited study. Herein, we provide a detailed account of the osteology of Scutellosaurus lawleri, figuring many elements for the first time. Scutellosaurus lawleri was the only definitive bipedal thyreophoran. Histological studies indicate that it grew slowly throughout its life, possessing lamellar-zonal tissue that was a consequence neither of its small size nor phylogenetic position, but may instead be autapomorphic, and supporting other studies that suggest thyreophorans had lower basal metabolic rates than other ornithischian dinosaurs. Faunal diversity of the Kayenta Formation in comparison with other well-known Early Jurassic-aged dinosaur-bearing formations indicates that there was considerable spatial and/or environmental variation in Early Jurassic dinosaur faunas.

An Evolutionary Microcircuit Approach to the Neural Basis of High Dimensional Sensory Processing in Olfaction.

Odor stimuli consist of thousands of possible molecules, each molecule with many different properties, each property a dimension of the stimulus. Processing these high dimensional stimuli would appear to require many stages in the brain to reach odor perception, yet, in mammals, after the sensory receptors this is accomplished through only two regions, the olfactory bulb and olfactory cortex. We take a first step toward a fundamental understanding by identifying the sequence of local operations carried out by microcircuits in the pathway. Parallel research provided strong evidence that processed odor information is spatial representations of odor molecules that constitute odor images in the olfactory bulb and odor objects in olfactory cortex. Paleontology provides a unique advantage with evolutionary insights providing evidence that the basic architecture of the olfactory pathway almost from the start ∼330 million years ago (mya) has included an overwhelming input from olfactory sensory neurons combined with a large olfactory bulb and olfactory cortex to process that input, driven by olfactory receptor gene duplications. We identify a sequence of over 20 microcircuits that are involved, and expand on results of research on several microcircuits that give the best insights thus far into the nature of the high dimensional processing.

Anatomy and systematics of the sauropodomorph Sarahsaurus aurifontanalis from the Early Jurassic Kayenta Formation.

Sarahsaurus aurifontanalis, from the Kayenta Formation of Arizona, is one of only three sauropodomorph dinosaurs known from the Early Jurassic of North America. It joins Anchisaurus polyzelus, from the older Portland Formation of the Hartford Basin, and Seitaad reussi, from the younger Navajo Sandstone of Utah, in representing the oldest North American sauropodomorphs. If it is true that sauropodomorphs were absent from North America during the Late Triassic, the relationship among these three dinosaurs offers a test of the mechanisms that drove recovery in North American biodiversity following the end-Triassic extinction event. Here we provide the first thorough description of Sarahsaurus aurifontanalis based on completed preparation and computed tomographic imaging of the holotype and referred specimens. With new anatomical data, our phylogenetic analysis supports the conclusion that Sarahsaurus aurifontanalis is nested within the primarily Gondwanan clade Massospondylidae, while agreeing with previous analyses that the three North American sauropodomorphs do not themselves form an exclusive clade. A revised diagnosis and more thorough understanding of the anatomy of Sarahsaurus aurifontanalis support the view that independent dispersal events were at least partly responsible for the recovery in North American vertebrate diversity following a major extinction event.

Jurassic stem-mammal perinates and the origin of mammalian reproduction and growth.

Transformations in morphology, physiology and behaviour along the mammalian stem lineage were accompanied by profound modifications to reproduction and growth, including the emergence of a reproductive strategy characterized by high maternal investment in a small number of offspring1,2 and heterochronic changes in early cranial development associated with the enlargement of the brain3. Because direct fossil evidence of these transitions is lacking, the timing and sequence of these modifications are unknown. Here we present what is, to our knowledge, the first fossil record of pre- or near-hatching young of any non-mammalian synapsid. A large clutch of well-preserved perinates of the tritylodontid Kayentatherium wellesi (Cynodontia, Mammaliamorpha) was found with a presumed maternal skeleton in Early Jurassic sediments of the Kayenta Formation. The single clutch comprises at least 38 individuals, well outside the range of litter sizes documented in extant mammals. This discovery confirms that production of high numbers of offspring represents the ancestral condition for amniotes, and also constrains the timing of a reduction in clutch size along the mammalian stem. Although tiny, the perinates have an overall skull shape that is similar to that of adults, with no allometric lengthening of the face during ontogeny. The only positive allometries are associated with the bones that support the masticatory musculature. Kayentatherium diverged just before a hypothesized pulse of brain expansion that reorganized cranial architecture at the base of Mammaliaformes4-6. The association of a high number of offspring and largely isometric cranial growth in Kayentatherium is consistent with a scenario in which encephalization-and attendant shifts in metabolism and development7,8-drove later changes to mammalian reproduction.

Nasolacrimal anatomy and haplorhine origins.

Computed tomography X-ray imaging of the internal face in well-preserved primate fossil crania permits reconstruction of the nature of their nasal anatomy, including some soft-tissue features. These features are diagnostic of the primate suborder Haplorhini, and allow reevaluation of the phylogenetic status of several purported early members of the group. Here we examine the nasolacrimal morphology of a broad sample of extant primates, as well as a number of Paleogene fossils. The extant sample confirms the distinctiveness of the two suborders. Of the fossils studied, only Shoshonius cooperi from the late-early Eocene exhibits evidence of a haplorhine nose. This suggests that the haplorhine oronasal complex may have evolved before the postorbital septum, and strengthens the claim that Shoshonius is a close relative of tarsiers and anthropoids. These results indicate that Omomyiformes is not a monophyletic group, and that few of its members possessed the derived oronasal morphology that characterizes crown haplorhines.

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.

Neocortical Lamination: Insights from Neuron Types and Evolutionary Precursors.

The neocortex is characterized by lamination of its neuron cell bodies in six layers, but there are few clues as to how this comes about and what is its function. Recent studies provide evidence that evolution from simple three-layer cortex may give insight into this problem. Three-layer cortex arose in the olfactory, hippocampal and dorsal cortex of the early amniote forebrain based on a cortical module of excitatory and inhibitory inputs to an intratelencephalic (IT) type of pyramidal neuron with feedback excitation and inhibition and related interneurons. We summarize recent evidence suggesting the hypothesis that the developmental program of three-layer olfactory cortex was co-opted to form six-layer mammalian neocortex, elaborating IT cortical units in layers 2-6 while adding layer 4 stellate cells, layer 5B pyramidal tract (PT) cells and layer 6 corticothalamic (CT) cells.

Open data and digital morphology.

Over the past two decades, the development of methods for visualizing and analysing specimens digitally, in three and even four dimensions, has transformed the study of living and fossil organisms. However, the initial promise that the widespread application of such methods would facilitate access to the underlying digital data has not been fully achieved. The underlying datasets for many published studies are not readily or freely available, introducing a barrier to verification and reproducibility, and the reuse of data. There is no current agreement or policy on the amount and type of data that should be made available alongside studies that use, and in some cases are wholly reliant on, digital morphology. Here, we propose a set of recommendations for minimum standards and additional best practice for three-dimensional digital data publication, and review the issues around data storage, management and accessibility.

A Dome-Headed Stem Archosaur Exemplifies Convergence among Dinosaurs and Their Distant Relatives.

Similarities in body plan evolution, such as wings in pterosaurs, birds, and bats or limblessness in snakes and amphisbaenians, can be recognized as classical examples of convergence among animals [1-3]. We introduce a new Triassic stem archosaur that is unexpectedly and remarkably convergent with the "dome-headed" pachycephalosaur dinosaurs that lived over 100 million years later. Surprisingly, numerous additional taxa in the same assemblage (the Otis Chalk assemblage from the Dockum Group of Texas) demonstrate the early acquisition of morphological novelties that were later convergently evolved by post-Triassic dinosaurs. As one of the most successful clades of terrestrial vertebrates, dinosaurs came to occupy an extensive morphospace throughout their diversification in the Mesozoic Era [4, 5], but their distant relatives were first to evolve many of those "dinosaurian" body plans in the Triassic Period [6-8]. Our analysis of convergence between archosauromorphs from the Triassic Period and post-Triassic archosaurs demonstrates the early and extensive exploration of morphospace captured in a single Late Triassic assemblage, and we hypothesize that many of the "novel" morphotypes interpreted to occur among archosaurs later in the Mesozoic already were in place during the initial Triassic archosauromorph, largely non-dinosaurian, radiation and only later convergently evolved in diverse dinosaurian lineages.

X-ray computed tomography datasets for forensic analysis of vertebrate fossils.

We describe X-ray computed tomography (CT) datasets from three specimens recovered from Early Cretaceous lakebeds of China that illustrate the forensic interpretation of CT imagery for paleontology. Fossil vertebrates from thinly bedded sediments often shatter upon discovery and are commonly repaired as amalgamated mosaics grouted to a solid backing slab of rock or plaster. Such methods are prone to inadvertent error and willful forgery, and once required potentially destructive methods to identify mistakes in reconstruction. CT is an efficient, nondestructive alternative that can disclose many clues about how a specimen was handled and repaired. These annotated datasets illustrate the power of CT in documenting specimen integrity and are intended as a reference in applying CT more broadly to evaluating the authenticity of comparable fossils.

Role of ortho-retronasal olfaction in mammalian cortical evolution.

Fossils of mammals and their extinct relatives among cynodonts give evidence of correlated transformations affecting olfaction as well as mastication, head movement, and ventilation, and suggest evolutionary coupling of these seemingly separate anatomical regions into a larger integrated system of ortho-retronasal olfaction. Evidence from paleontology and physiology suggests that ortho-retronasal olfaction played a critical role at three stages of mammalian cortical evolution: early mammalian brain development was driven in part by ortho-retronasal olfaction; the bauplan for neocortex had higher-level association functions derived from olfactory cortex; and human cortical evolution was enhanced by ortho-retronasal smell.

Cranial anatomy of the Duchesnean primate Rooneyia viejaensis: new insights from high resolution computed tomography.

Rooneyia viejaensis is a North American Eocene primate of uncertain phylogenetic affinities. Although the external cranial anatomy of Rooneyia is well studied, various authors have suggested that Rooneyia is a stem haplorhine, stem strepsirrhine, stem tarsiiform, or stem anthropoid. Here we describe the internal cranial anatomy of the Rooneyia holotype based on micro-computed tomography and discuss the phylogenetic implications of this anatomy. Precise measurements of the natural endocast filling the braincase of the Rooneyia holotype reveal that the genus had a relative brain size comparable to some living callitrichines and strepsirrhines. Rooneyia was thus probably more encephalized than any other known omomyiform, adapiform, or plesiadapiform. Relative olfactory bulb size in Rooneyia was most comparable to some living strepsirrhines and the stem anthropoid Parapithecus. The nasal fossa of Rooneyia resembled that of living strepsirrhines in retaining an obliquely oriented nasolacrimal canal, four ethmoturbinals, and an olfactory recess separated from the nasopharyngeal meatus by a transverse lamina. The ear region of Rooneyia is characterized by large and complete canals for both the stapedial and promontory branches of the internal carotid artery. Rooneyia also retains a patent parotic fissure and thus had an extrabullar origin of the stapedius muscle. In most of these respects, Rooneyia exhibits the condition that is presumed to be primitive for crown primates and lacks a number of key crown haplorhine synapomorphies (e.g., a dorso-ventrally oriented nasolacrimal canal, loss of the olfactory recess, loss of ethmoturbinals 3-4, loss or extreme reduction of the stapedial canal due to involution of the stapedial artery). These data are consistent with the hypothesis that Rooneyia is an advanced stem primate or a basal crown primate but are inconsistent with prior suggestions that Rooneyia is a crown haplorhine.

Functional implications of ubiquitous semicircular canal non-orthogonality in mammals.

The 'canonical model' of semicircular canal orientation in mammals assumes that 1) the three ipsilateral canals of an inner ear exist in orthogonal planes (i.e., orthogonality), 2) corresponding left and right canal pairs have equivalent angles (i.e., angle symmetry), and 3) contralateral synergistic canals occupy parallel planes (i.e., coplanarity). However, descriptions of vestibular anatomy that quantify semicircular canal orientation in single species often diverge substantially from this model. Data for primates further suggest that semicircular canal orthogonality varies predictably with the angular head velocities encountered in locomotion. These observations raise the possibility that orthogonality, symmetry, and coplanarity are misleading descriptors of semicircular canal orientation in mammals, and that deviations from these norms could have significant functional consequences. Here we critically assess the canonical model of semicircular canal orientation using high-resolution X-ray computed tomography scans of 39 mammal species. We find that substantial deviations from orthogonality, angle symmetry, and coplanarity are the rule for the mammals in our comparative sample. Furthermore, the degree to which the semicircular canals of a given species deviate from orthogonality is negatively correlated with estimated vestibular sensitivity. We conclude that the available comparative morphometric data do not support the canonical model and that its overemphasis as a heuristic generalization obscures a large amount of functionally relevant variation in semicircular canal orientation between species.

Evolutionary origins of the avian brain.

Features that were once considered exclusive to modern birds, such as feathers and a furcula, are now known to have first appeared in non-avian dinosaurs. However, relatively little is known of the early evolutionary history of the hyperinflated brain that distinguishes birds from other living reptiles and provides the important neurological capablities required by flight. Here we use high-resolution computed tomography to estimate and compare cranial volumes of extant birds, the early avialan Archaeopteryx lithographica, and a number of non-avian maniraptoran dinosaurs that are phylogenetically close to the origins of both Avialae and avian flight. Previous work established that avian cerebral expansion began early in theropod history and that the cranial cavity of Archaeopteryx was volumetrically intermediate between these early forms and modern birds. Our new data indicate that the relative size of the cranial cavity of Archaeopteryx is reflective of a more generalized maniraptoran volumetric signature and in several instances is actually smaller than that of other non-avian dinosaurs. Thus, bird-like encephalization indices evolved multiple times, supporting the conclusion that if Archaeopteryx had the neurological capabilities required of flight, so did at least some other non-avian maniraptorans. This is congruent with recent findings that avialans were not unique among maniraptorans in their ability to fly in some form.

Birds have paedomorphic dinosaur skulls.

The interplay of evolution and development has been at the heart of evolutionary theory for more than a century. Heterochrony­change in the timing or rate of developmental events­has been implicated in the evolution of major vertebrate lineages such as mammals, including humans. Birds are the most speciose land vertebrates, with more than 10,000 living species representing a bewildering array of ecologies. Their anatomy is radically different from that of other vertebrates. The unique bird skull houses two highly specialized systems: the sophisticated visual and neuromuscular coordination system allows flight coordination and exploitation of diverse visual landscapes, and the astonishing variations of the beak enable a wide range of avian lifestyles. Here we use a geometric morphometric approach integrating developmental, neontological and palaeontological data to show that the heterochronic process of paedomorphosis, by which descendants resemble the juveniles of their ancestors, is responsible for several major evolutionary transitions in the origin of birds. We analysed the variability of a series of landmarks on all known theropod dinosaur skull ontogenies as well as outgroups and birds. The first dimension of variability captured ontogeny, indicating a conserved ontogenetic trajectory. The second dimension accounted for phylogenetic change towards more bird-like dinosaurs. Basally branching eumaniraptorans and avialans clustered with embryos of other archosaurs, indicating paedomorphosis. Our results reveal at least four paedomorphic episodes in the history of birds combined with localized peramorphosis (development beyond the adult state of ancestors) in the beak. Paedomorphic enlargement of the eyes and associated brain regions parallels the enlargement of the nasal cavity and olfactory brain in mammals. This study can be a model for investigations of heterochrony in evolutionary transitions, illuminating the origin of adaptive features and inspiring studies of developmental mechanisms.

Fossil evidence on origin of the mammalian brain.

Many hypotheses have been postulated regarding the early evolution of the mammalian brain. Here, x-ray tomography of the Early Jurassic mammaliaforms Morganucodon and Hadrocodium sheds light on this history. We found that relative brain size expanded to mammalian levels, with enlarged olfactory bulbs, neocortex, olfactory (pyriform) cortex, and cerebellum, in two evolutionary pulses. The initial pulse was probably driven by increased resolution in olfaction and improvements in tactile sensitivity (from body hair) and neuromuscular coordination. A second pulse of olfactory enhancement then enlarged the brain to mammalian levels. The origin of crown Mammalia saw a third pulse of olfactory enhancement, with ossified ethmoid turbinals supporting an expansive olfactory epithelium in the nasal cavity, allowing full expression of a huge odorant receptor genome.