Julia A. Schultz

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.

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.

Jaw movement in fossil mammals: analysis, description and visualization

A terminology for and visualizations of different mammalian mastication paths are provided, resulting from orientation of attritional and abrasional facets and striation on fossil (and extant) teeth. The occlusal motion of the left lower jaw is considered, and a moderate wear stage (IDAS 3) is used as standard. In contrast to conventional terminologies, the proposed nomenclature differentiates between the inclination and the direction of the lower jaw movement as projected onto a horizontal plane for each phase of the power stroke. The proposed mastication compass attempts to combine three aspects of the power stroke: (1) the number of phases, (2) the occlusal direction, and (3) the inclination of each phase. Descriptions and visualizations are given for several taxa in order to demonstrate its general applicability. The proposed new terminology and the mastication compass simplify comparisons of different modes of mastication in different mammalian taxa.KurzfassungFür den Mastikationsweg fossiler (und rezenter) Bezahnungen der Mammalia wurde eine neue Terminologie und bildliche Darstellung entwickelt, die sich auf die Ausrichtung von Attritions- und Abrasionsfacetten sowie der Striationen auf der Zahnoberfläche stützt. Dabei wird die Bewegung des unteren linken Unterkieferastes in einem mittleren Abkaustadium (IDAS 3) standardmäßig dargestellt. Im Gegensatz zu den bisherigen Beschreibungen, unterscheidet das vorliegende System für jede Phase des Kauzyklus zwischen Richtung und Steigungswinkel in Bezug auf die Sagittalebene bzw. die horizontale Bezugsebene. Der vorgeschlagene Mastkations-Kompass vereinigt dabei die drei hauptsächlichen Aspekte des “power stroke” während der Mastikationsbewegung: (1) die Anzahl der Kauphasen, (2) die Richtung und (3) den Inklinationswinkel jeder einzelnen Phase. Zur Demonstration der vielseitigen Anwendbarkeit des Mastikations-Kompasses, wird dieser beispielhaft für verschiedenste Taxa dargestellt. Er ermöglicht den Vergleich der Mastikationsbewegungen innerhalb unterschiedlicher Säugetiergruppen.

Occlusal Pattern in Paulchoffatiid Multituberculates and the Evolution of Cusp Morphology in Mammaliamorphs with Rodent-like Dentitions

Multituberculates developed a very complex masticatory apparatus during their long evolutionary history from the Jurassic to the Paleogene. Besides their rodent-like elongated incisors and diastemata, Cenozoic cimolodont Multituberculata display masticatory movements involving two distinct cycles in the mastication. An orthal slicing-crushing cycle associated with an enlarged lower fourth premolar precedes a palinal grinding cycle linked to upper molars with three longitudinal rows of cusps. With their plesiomorphic lower premolars and upper molars, the Late Jurassic/Early Cretaceous multituberculate family Paulchoffatiidae can provide the key for the understanding of the origin of the complex mastication of the Cimolodonta. Using for the first time propagation phase contrast Synchrotron X-Ray microtomography to perform both microwear and topographic analyses in order to characterize the mastication of Paulchoffatiidae, we digitized dental material from the Late Jurassic of the Guimarota Coal Mine (Leiria, Portugal) at the European Synchrotron Facility (Grenoble, France). Mastication in Paulchoffatiidae is characterized by a palinal grinding cycle. In contrast to Cimolodonta, no evidence of an orthal slicing-crushing cycle has been observed: the lower premolars mainly have a grinding function like the molars as they do exhibit buccal attrition facets bearing longitudinal striations. Nevertheless, the slightly oblique striations observed on the mesial part of the paulchoffatiid lower premolars possibly presage the orthal phase of the Cimolodonta. Our topographic analysis indicates that a strong relationship between individual cusp shape and direction of chewing is emphasized in rodents and rodent-like Mammaliamorpha such as Cimolodonta and Tritylodonta. Surprisingly, this relationship is not evident in Paulchoffatiidae. This unexpected result can be explained by the non-involvement in the attrition of many premolar cusps in Paulchoffatiidae, as indicated by our microwear analysis. The stronger the attrition, the more the direction of the masticatory movements influences the cusp morphology in Mammaliamorpha.

Tooth Morphology in Fossil and Extant Lagomorpha (Mammalia) Reflects Different Mastication Patterns

The functional interpretation of the cheek teeth and the mastication cycle of Lagomorpha are deduced from various aspects of tooth morphology of fossil and extant species. Mastication is composed of an almost orthal shearing and transverse grinding in a lingual direction. Shearing blades are not only indicated by facets but as well by thickened enamel. A primary shearing blade (PSB) inherited from stem lagomorphs occurs in all examined species. It can be correlated with facets 1 and 5 (sensu Crompton 1971) and occurs in very few mammals; it is conspicuously absent in the sister-taxon Rodentia. A secondary shearing blade (SSB) occurs in derived Ochotonidae and two basal Leporidae (Romerolagus and Pronolagus) as a convergent pattern. In fossil ochotonids from Europe, the “lagicone structure” is gradually reduced in favor of the SSB. Thus, ochotonids strengthen the shearing ability, whereas most leporids favor the grinding function realized by the partial crenulation of the enamel band of the re-entrant folds. For the mastication cycle, the distinct phases were recognized, related to phase I of the tribosphenic model. The first movement (phase Ia) is directed almost orthally, the second (phase Ib) lingually. Only in Lepus europaeus was an additional phase detected, which might correspond to phase II.

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.

Evolution of the Middle and Inner Ears of Mammaliaforms: The Approach to Mammals

Transformations of ear structures in the evolution of early mammals can be studied with the fossils of mammaliaforms. The middle ear is fully attached to the mandibles in mammaliaforms; however, in Mesozoic eutriconodont and spalacotherioid mammals, it is only connected to the mandible by an ossified Meckel’s cartilage, with the ectotympanic and malleus already displaced from the mandible. Recent morphogenetic studies have shown that the developmental potential for ossification of Meckel’s element is conserved in extant mammals. New fossils further revealed that this pattern actually evolved in mammaliaform phylogeny and that disconnection of the ear from the mandible occurred independently in monotremes, in therians, and in multituberculate mammals. The inner ear of mammaliaforms is derived in having a single petrosal bone enclosing the entire inner ear and a promontorium for an elongate cochlear canal. Mammaliaforms and most Mesozoic mammals had ancestral features of a simple cochlear canal with a single cochlear nerve foramen but no interior bony laminae nor did they have a bony canal for the cochlear ganglion. The sieve-like foramina for cochlear nerve fibers to enter the cochlear canal evolved independently three times in Mesozoic mammals. Cochlear canal curvature is homoplastic among mammaliaform groups, and a curvature beyond 270° only evolved in cladotherians, accompanied by Rosenthal’s canal for the cochlear ganglion. The homoplasies of ear structures in early mammalian evolution, although seemingly complex, are consistent with the new understanding of a labile morphogenesis of mammalian ears under a complex developmental genetic network.

Virtopsy of the controlled decomposition of a dormouse Eliomys quercinus as a tool to analyse the taphonomy of Heterohyus nanus from Messel (Eocene, Germany)

Fossil vertebrate skeletons from subaquatic sediments display a melange of decomposition processes, compaction and diagenesis, which have to be discriminated for a detailed taphonomic analysis. The sequence of decomposition and disarticulation of skeletal elements is controlled intrinsically by the different resistances of soft tissues to decay, as well as extrinsically by temperature and oxygen availability. Water pressure has a significant influence on the extent of bloating caused by gases of putrefaction. Bloated carcasses float at the surface, or can refloat from the bottom of the water body (depending on the water pressure), where they can be moved by currents or wind. During the last decade, forensic radiographic examinations by computed tomography (CT; Virtopsy) have evolved into a new approach for actuopalaeontological experiments, which allow a continuous insight into the decay process. In order to elucidate the taphonomy of the apatemyid mammal Heterohyus, we investigated the controlled decay of a dormouse (Eliomys quercinus) carcass in detail, using high-resolution micro-CT. Taphonomic study of a fossil specimen of a Heterohyus nanus from Messel revealed that decomposition came to a premature halt, as indicated by the disarticulation sequence of the skeletal elements, which stopped after a while. Little information is available about internal decay processes affecting the coherence of the skeletal system. The results of the actualistic study were compared with the state of disarticulation of the fossil apatomyid. The combination of different indicators of the decomposition process, the lack of skeletal disintegration in Heterohyus and palaeo-environmental data lead to the assumption that Heterohyus went through an adipocere forming phase before embedding.

Dental Function and Diet of Vintana Sertichi (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar

ABSTRACT—The nearly complete and well-preserved cranium of Vintana sertichi provides an opportunity to investigate its dietary adaptations. We used a combination of comparative morphological and biomechanical analyses to reveal the direction of its power stroke during mastication, reconstruct the positions and relative sizes of its muscles of mastication, and predict its capacity to produce bite forces during incision and molariform occlusion. The orientation of dental wear striations on the upper molariform teeth of Vintana, in combination with the orientation of the enamel islets and synclines and the position of leading and trailing edges, demonstrates that the power stroke was primarily palinal (distally directed), with a significant buccally directed component that is absent in multituberculates, haramiyidans, and other gondwanatherians. The large palinal component of jaw movement was corroborated by biomechanical analyses of the moments generated by the primary jaw adductors around the dentary-squamosal joint axis. Similar analyses also confirmed the previously documented proal (mesially directed) power stroke of the extant rodent Myocastor. Finite element analyses predict that Vintana was capable of producing bite forces that were more than twice as high as the similarly sized Myocastor. Vintana was almost certainly an herbivore, as claimed previously for other sudamericid gondwanatherians. Its size and capacity to generate high bite forces at both the incisors and the molariform teeth suggest that it was a mixed feeder whose diet may have included relatively large, hard food items such as roots, seeds, twigs, or nut-like fruits.

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.