Skeleton of a Cretaceous mammal from Madagascar reflects long-term insularity.

The fossil record of mammaliaforms (mammals and their closest relatives) of the Mesozoic era from the southern supercontinent Gondwana is far less extensive than that from its northern counterpart, Laurasia1,2. Among Mesozoic mammaliaforms, Gondwanatheria is one of the most poorly known clades, previously represented by only a single cranium and isolated jaws and teeth1-5. As a result, the anatomy, palaeobiology and phylogenetic relationships of gondwanatherians remain unclear. Here we report the discovery of an articulated and very well-preserved skeleton of a gondwanatherian of the latest age (72.1-66 million years ago) of the Cretaceous period from Madagascar that we assign to a new genus and species, Adalatherium hui. To our knowledge, the specimen is the most complete skeleton of a Gondwanan Mesozoic mammaliaform that has been found, and includes the only postcranial material and ascending ramus of the dentary known for any gondwanatherian. A phylogenetic analysis including the new taxon recovers Gondwanatheria as the sister group to Multituberculata. The skeleton, which represents one of the largest of the Gondwanan Mesozoic mammaliaforms, is particularly notable for exhibiting many unique features in combination with features that are convergent on those of therian mammals. This uniqueness is consistent with a lineage history for A. hui of isolation on Madagascar for more than 20 million years.

A new biomechanical model of the mammal jaw based on load path analysis.

The primary function of the tetrapod jaw is to transmit jaw muscle forces to bite points. The routes of force transfer in the jaw have never been studied, but can be quantified using load paths--the shortest, stiffest routes from regions of force application to support constraints. Here we use load path analysis to map force transfer from muscle attachments to bite point and jaw joint, and to evaluate how different configurations of trabecular and cortical bone affect load paths. We created three models of the mandible of the Virginia opossum, Didelphis virginiana, each with a cortical bone shell, but with different material properties for the internal spaces: a cortical-trabecular model, in which the interior space is modeled with bulk properties of trabecular bone; a cortical-hollow model, in which trabeculae and mandibular canal are modeled as hollow; and a solid-cortical model, in which the interior is modeled as cortical bone. The models were compared with published in vivo bite force and bone strain data, and the load paths calculated for each model. The cortical-trabecular model, which most closely approximates the actual morphology, was best validated by in vivo data. In all three models the load path was confined to cortical bone, although its route within the cortex varied depending on the material properties of the inner model. Our analysis shows that most of the force is transferred through the cortical, rather than trabecular bone, and highlights the potential of load path analysis for understanding form-function relationships in the skeleton.

Publisher Correction: Late-surviving stem mammal links the lowermost Cretaceous of North America and Gondwana.

The asterisked footnote to Extended Data Table 1 should state '*Including Thomasia and Haramiyavia'. This has been corrected online.

Late-surviving stem mammal links the lowermost Cretaceous of North America and Gondwana.

Haramiyida was a successful clade of mammaliaforms, spanning the Late Triassic period to at least the Late Jurassic period, but their fossils are scant outside Eurasia and Cretaceous records are controversial1-4. Here we report, to our knowledge, the first cranium of a large haramiyidan from the basal Cretaceous of North America. This cranium possesses an amalgam of stem mammaliaform plesiomorphies and crown mammalian apomorphies. Moreover, it shows dental traits that are diagnostic of isolated teeth of supposed multituberculate affinities from the Cretaceous of Morocco, which have been assigned to the enigmatic 'Hahnodontidae'. Exceptional preservation of this specimen also provides insights into the evolution of the ancestral mammalian brain. We demonstrate the haramiyidan affinities of Gondwanan hahnodontid teeth, removing them from multituberculates, and suggest that hahnodontid mammaliaforms had a much wider, possibly Pangaean distribution during the Jurassic-Cretaceous transition.

The First Southern Hemisphere Occurrence of the Extinct Cretaceous Sclerorhynchoid Sawfish Ptychotrygon (Chondrichthyes, Batoidea), With a Review of Ptychotrygon Taxonomy.

A new extinct sclerorhynchoid sawfish, Ptychotrygon ameghinorum sp. nov., is presented here based on abundant isolated teeth and some dermal denticles, which were recovered from the Mata Amarilla Formation, belonging to the lower Upper Cretaceous of the Santa Cruz Province in the Austral Basin of Patagonia, Argentina. This new species is the first Ptychotrygon occurrence in the southern hemisphere, which so far only has been reported from northern hemisphere deposits (Europe, North Africa, and North America). The presence of P. ameghinorum sp. nov. in these southern high-latitude deposits of Patagonia, Argentina, extends the geographic range of Ptychotrygon considerably southwards. This distribution pattern in the "middle" Cretaceous seems to correlate with the South Atlantic opening at the end of the Albian. The presence of lateral cephalic dermal denticles and the simultaneous absence of rostral denticles in the abundant fossil material support the view that Ptychotrygon did not develop such rostral structures. A reinvestigation of all known species assigned to Ptychotrygon reveals that P. ellae is a junior synonym of P. boothi, P. benningensis belongs to Texatrygon, P. rugosum belongs to Asflapristis, and P. clementsi represents an unidentifiable species (Ptychotrygon? sp.). The stratigraphic distribution demonstrates that Ptychotrygon might have originated in the Albian in south-western Europe and subsequently dispersed to obtain its widest distribution during the Cenomanian. In the Coniacian, a steep diversity decline is recognizable with a subsequent distribution shift from Europe to North America.

A derived dryolestid mammal indicates possible insular endemism in the Late Jurassic of Germany.

The Langenberg Quarry near Bad Harzburg has yielded the first Jurassic stem therian mammal of Germany, recovered from Kimmeridgian (Late Jurassic) near shore deposits of a palaeo-island within the Lower Saxony Basin of the European archipelago. The new stem therian is represented by one lower and three upper molars. Hercynodon germanicus gen. et sp. nov. is attributed to the Dryolestidae, a group of pretribosphenic crown mammals that was common in western Laurasia from the Middle Jurassic to the Early Cretaceous. The new taxon is characterised by small size, a reduced cusp pattern in the upper molars lacking a metacone, and enhancement of the shearing crests paracrista and metacrista. Phylogenetic analysis identified Hercynodon gen. nov. as sister taxon of Crusafontia from the Lower Cretaceous (Barremian) of Spain. Both taxa belong to an endemic European clade of dryolestids, including also Achyrodon and Phascolestes from the earliest Cretaceous (Berriasian) of England. Despite its greater geological age, Hercynodon gen. nov. is the most derived representative of that clade, indicated by the complete reduction of the metacone. The discrepancy between derived morphology and geological age may be explained by an increased rate of character evolution in insular isolation. Other insular phenomena have earlier been observed in vertebrates from the Langenberg Quarry, such as dwarfism in the small sauropod Europasaurus, and possible gigantism in the morganucodontan mammaliaform Storchodon and the pinheirodontid multituberculate mammal Teutonodon which grew unusually large.

First cranial remains of a gondwanatherian mammal reveal remarkable mosaicism.

Previously known only from isolated teeth and lower jaw fragments recovered from the Cretaceous and Palaeogene of the Southern Hemisphere, the Gondwanatheria constitute the most poorly known of all major mammaliaform radiations. Here we report the discovery of the first skull material of a gondwanatherian, a complete and well-preserved cranium from Upper Cretaceous strata in Madagascar that we assign to a new genus and species. Phylogenetic analysis strongly supports its placement within Gondwanatheria, which are recognized as monophyletic and closely related to multituberculates, an evolutionarily successful clade of Mesozoic mammals known almost exclusively from the Northern Hemisphere. The new taxon is the largest known mammaliaform from the Mesozoic of Gondwana. Its craniofacial anatomy reveals that it was herbivorous, large-eyed and agile, with well-developed high-frequency hearing and a keen sense of smell. The cranium exhibits a mosaic of primitive and derived features, the disparity of which is extreme and probably reflective of a long evolutionary history in geographic isolation.

Oldest known multituberculate stapes suggests an asymmetric bicrural pattern as ancestral for Multituberculata.

Middle ear ossicles (malleus, incus, stapes) are known for few multituberculate taxa, and three different stapedial morphotypes have been suggested: (i) slender, columelliform and microperforate, (ii) robust and rod-like, and (iii) bicrural. Reinvestigation of Upper Jurassic (Kimmeridgian) mammalian petrosals from the Guimarota coal mine in central Portugal (Western Europe) revealed an asymmetric bicrural stapes (ABS) in the paulchoffatiid Pseudobolodon oreas The middle ear ossicles displaced inside the osseous vestibule were detected by a µCT analysis. The Kimmeridgian age of the Guimarota stapes exceeds the stapes from the Early Cretaceous (Barremian) of Asia (about 122-124 Ma) by approximately 30 Myr, and is only slightly younger than the stapes of the recently described Oxfordian euharamiyidan Arboroharamiya allinhopsoni The Guimarota stapes indicates that the stapes of Lambdopsalis, described as columelliform and microperforate (small stapedial foramen), does not represent a general condition for multituberculates. The stapes of Pseudobolodon is bicrural, the anterior crus sits centrally on the oval footplate, and the stapedial head is simple and smaller than the footplate. We hypothesize that the ABS evolved from the symmetric bicrural stapes (SBS) of non-mammaliaform cynodonts. The ABS appears to be the ancestral morphotype of the mammalian SBS, and the mammalian columelliform imperforate stapes.

Comparative anatomy of neonates of the three major mammalian groups (monotremes, marsupials, placentals) and implications for the ancestral mammalian neonate morphotype.

The existing different modes of reproduction in monotremes, marsupials and placentals are the main source for our current understanding of the origin and evolution of the mammalian reproduction. The reproductive strategies and, in particular, the maturity states of the neonates differ remarkably between the three groups. Monotremes, for example, are the only extant mammals that lay eggs and incubate them for the last third of their embryonic development. In contrast, marsupials and placentals are viviparous and rely on intra-uterine development of the neonates via choriovitelline (mainly marsupials) and chorioallantoic (mainly placentals) placentae. The maturity of a newborn is closely linked to the parental care strategy once the neonate is born. The varying developmental degrees of neonates are the main focus of this study. Monotremes and marsupials produce highly altricial and nearly embryonic offspring. Placental mammals always give birth to more developed newborns with the widest range from altricial to precocial. The ability of a newborn to survive and grow in the environment it was born in depends highly on the degree of maturation of vital organs at the time of birth. Here, the anatomy of four neonates of the three major extant mammalian groups is compared. The basis for this study is histological and ultrastructural serial sections of a hatchling of Ornithorhynchus anatinus (Monotremata), and neonates of Monodelphis domestica (Marsupialia), Mesocricetus auratus (altricial Placentalia) and Macroscelides proboscideus (precocial Placentalia). Special attention was given to the developmental stages of the organs skin, lung, liver and kidney, which are considered crucial for the maintenance of vital functions. The state of the organs of newborn monotremes and marsupials are found to be able to support a minimum of vital functions outside the uterus. They are sufficient to survive, but without capacities for additional energetic challenges. The organs of the altricial placental neonate are further developed, able to support the maintenance of vital functions and short-term metabolic increase. The precocial placental newborn shows the most advanced state of organ development, to allow the maintenance of vital functions, stable thermoregulation and high energetic performance. The ancestral condition of a mammalian neonate is interpreted to be similar to the state of organ development found in the newborns of marsupials and monotremes. In comparison, the newborns of altricial and precocial placentals are derived from the ancestral state to a more mature developmental degree associated with advanced organ systems.

Function of pretribosphenic and tribosphenic mammalian molars inferred from 3D animation.

Appearance of the tribosphenic molar in the Late Jurassic (160 Ma) is a crucial innovation for food processing in mammalian evolution. This molar type is characterized by a protocone, a talonid basin and a two-phased chewing cycle, all of which are apomorphic. In this functional study on the teeth of Late Jurassic Dryolestes leiriensis and the living marsupial Monodelphis domestica, we demonstrate that pretribosphenic and tribosphenic molars show fundamental differences of food reduction strategies, representing a shift in dental function during the transition of tribosphenic mammals. By using the Occlusal Fingerprint Analyser (OFA), we simulated the chewing motions of the pretribosphenic Dryolestes that represents an evolutionary precursor condition to such tribosphenic mammals as Monodelphis. Animation of chewing path and detection of collisional contacts between virtual models of teeth suggests that Dryolestes differs from the classical two-phased chewing movement of tribosphenidans, due to the narrowing of the interdental space in cervical (crown-root transition) direction, the inclination angle of the hypoflexid groove, and the unicuspid talonid. The pretribosphenic chewing cycle is equivalent to phase I of the tribosphenic chewing cycle, but the former lacks phase II of the tribosphenic chewing. The new approach can analyze the chewing cycle of the jaw by using polygonal 3D models of tooth surfaces, in a way that is complementary to the electromyography and strain gauge studies of muscle function of living animals. The technique allows alignment and scaling of isolated fossil teeth and utilizes the wear facet orientation and striation of the teeth to reconstruct the chewing path of extinct mammals.

The origins of mammal growth patterns during the Jurassic mammalian radiation.

We use synchrotron x-ray tomography of annual growth increments in the dental cementum of mammaliaforms (stem and crown fossil mammals) from three faunas across the Jurassic to map the origin of patterns of mammalian growth patterns, which are intrinsically related to mammalian endothermy. Although all fossils studied exhibited slower growth rates, longer life spans, and delayed sexual maturity relative to comparably sized extant mammals, the earliest crown mammals developed significantly faster growth rates in early life that reduced at sexual maturity, compared to stem mammaliaforms. Estimation of basal metabolic rates (BMRs) suggests that some fossil crown mammals had BMRs approaching the lowest rates of extant mammals. We suggest that mammalian growth patterns first evolved during their mid-Jurassic adaptive radiation, although growth remained slower than in extant mammals.

Does age matter?-Efficiency of mechanical food break down in Tupaia belangeri at different ages.

The relationship of food comminution and individual age in Tupaia belangeri is investigated. It is hypothesized that with increasing age the performance of the molar dentition decreases due to progressive tooth wear. While this relationship is well-documented for herbivores, age-related test series are largely lacking for insectivorous mammals. 15 individuals of Tupaia belangeri were fed exclusively with mealworms, and their faeces were analyzed for the number and size of chitin particles. The exoskeleton of a mealworm is resistant to digestive fluids in the gastrointestinal tract, and the size of individual chitin particles indicates the effectiveness of mechanical comminution that occurs in the oral cavity during mastication. It is hypothesized that a more precise occlusion of the dentition results in smaller particle size. Although individuals of all ages (juvenile, adult, and senile) were able to effectively process mealworms with their dentition prior to digestion, a larger area of very large chitin particles (98% quantile of all particles in senile animals as compared to in the same quantile in adults) in the feces of senile animals was detected. Even though the particle size of indigestible material is irrelevant for the digestive process, these findings either document somatic senescence in the functionality of the teeth, or alternatively a change in chewing behaviour with age.

Fossil evidence on evolution of inner ear cochlea in Jurassic mammals.

The coiled cochlea is a key evolutionary innovation of modern therian mammals. We report that the Late Jurassic mammal Dryolestes, a relative to modern therians, has derived bony characteristics of therian-like innervation, but its uncoiled cochlear canal is less derived than the coiled cochlea of modern therians. This suggests a therian-like innervation evolved before the fully coiled cochlea in phylogeny. The embryogenesis of the cochlear nerve and ganglion in the inner ear of mice is now known to be patterned by neurogenic genes, which we hypothesize to have influenced the formation of the auditory nerve and its ganglion in Jurassic therian evolution, as shown by their osteological correlates in Dryolestes, and by the similar base-to-apex progression in morphogenesis of the ganglion in mice, and in transformation of its canal in phylogeny. The cochlear innervation in Dryolestes is the precursory condition in the curve-to-coil transformation of the cochlea in mammalian phylogeny. This provides the timing of the evolution, and where along the phylogeny the morphogenetic genes were co-opted into patterning the cochlear innervation, and the full coiling of the cochlea in modern therians.

The vertebrate middle and inner ear: A short overview.

The evolution of the various hearing adaptations is connected to major structural changes in nearly all groups of vertebrates. Besides hearing, the detection of acceleration and orientation in space are key functions of this mechanosensory system. The symposium "show me your ear - the inner and middle ear in vertebrates" held at the 11th International Congress of Vertebrate Morphology (ICVM) 2016 in Washington, DC (USA) intended to present current research addressing adaptation and evolution of the vertebrate otic region, auditory ossicles, vestibular system, and hearing physiology. The symposium aimed at an audience with interest in hearing research focusing on morphological, functional, and comparative studies. The presented talks and posters lead to the contributions of this virtual issue highlighting recent advances in the vertebrate balance and hearing system. This article serves as an introduction to the virtual issue contributions and intends to give a short overview of research papers focusing on vertebrate labyrinth and middle ear related structures in past and recent years.

Complementary approaches to tooth wear analysis in Tritylodontidae (Synapsida, Mammaliamorpha) reveal a generalist diet.

Stereoscopic microwear and 3D surface texture analyses on the cheek teeth of ten Upper Triassic to Lower Cretaceous tritylodontid (Mammaliamorpha) taxa of small/medium to large body size suggest that all were generalist feeders and none was a dietary specialist adapted to herbivory. There was no correspondence between body size and food choice. Stereomicroscopic microwear analysis revealed predominantly fine wear features with numerous small pits and less abundant fine scratches as principal components. Almost all analyzed facets bear some coarser microwear features, such as coarse scratches, large pits, puncture pits and gouges pointing to episodic feeding on harder food items or exogenous effects (contamination of food with soil grit and/or dust), or both. 3D surface texture analysis indicates predominantly fine features with large void volume, low peak densities, and various stages of roundness of the peaks. We interpret these features to indicate consumption of food items with low to moderate intrinsic abrasiveness and can exclude regular rooting, digging or caching behavior. Possible food items include plant vegetative parts, plant reproductive structures (seeds and seed-bearing organs), and invertebrates (i.e., insects). Although the tritylodontid tooth morphology and auto-occlusion suggest plants as the primary food resource, our results imply a wider dietary range including animal matter.

Inner ear labyrinth anatomy of monotremes and implications for mammalian inner ear evolution.

The monophyletic clade Monotremata branches early from the rest of the mammalian crown group in the Jurassic and members of this clade retain many ancestral mammalian traits. Thus, accurate and detailed anatomical descriptions of this group can offer unique insight into the early evolutionary history of Mammalia. In this study, we examine the inner ear anatomy of two extant monotremes, Ornithorhynchus anatinus and Tachyglossus aculeatus, with the primary goals of elucidating the ancestral mammalian ear morphology and resolving inconsistencies found within previous descriptive literature. We use histological serial sections and high-resolution microcomputed tomography (µCT) for correlating soft tissue features of the vestibule and cochlea to the osseous labyrinth endocast. We found that in both monotremes the scala tympani coils to a lesser degree than scala vestibuli and scala media, although all three scalae show an apical coil inside the osseous cochlear tube. The helicotrema (conduit between scala tympani and scala vestibuli) is in subapical position, and the cochlear and lagenar ganglia and their associated nerve fibers are not enclosed by bone. In comparison, in extant therian mammals (i.e., marsupials and placentals) the helicotrema is located at the apex of the osseous cochlear canal, the three scalae coil to the same degree and the cochlear ganglion is enclosed by the primary bony lamina. Whether the lagenar ganglion is lost in therian mammals or integrated into the cochlear ganglion is still debated. The presence of a sensory lagenar macula at the apex of the membranous cochlear duct, innervated by a separate lagenar nerve and ganglion is a plesiomorphic condition of amniotes that monotremes share. A separate osseous lagenar canaliculus for the lagenar nerve, and the coiling of the distended lagenar sac at the end of the cochlear duct are autapomorphies of monotremes. Based on our findings we hypothesize that the ancestral inner ear of stem mammaliaforms is characterized by a straight or slightly curved osseous cochlear canal, a lagenar macula, lagenar nerve fibers separated from a larger bundle of cochlear nerve fibers, the presence of an organ of Corti and an intra-otic cochlear ganglion suspended by membranous connective tissue. Among the major Mesozoic clades of crown mammals, cladotherians and gondwanatherians most likely acquired a fully functioning organ of Corti but lost the sensory lagenar macula, like extant therians. However, Mesozoic spalacotherioids, multituberculates and eutriconodonts likely retained the mammaliaform condition. J. Morphol. 278:236-263, 2017. © 2016 Wiley Periodicals,Inc.