Extant Therians Research Articles

Inner ear morphology of Adalatherium hui (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar

ABSTRACT The cochlear canal of Adalatherium hui, from the Late Cretaceous of Madagascar, exhibits a combination of features previously unknown among mammaliaforms. The cochlear canal of Adalatherium is short and ‘C’-shaped (curved through at least 210°). A presumptive lagenar nerve canal extends from the apex of the cochlea to the internal acoustic meatus. In conjunction with an apical expansion of the cochlear canal, this morphology suggests that Adalatherium retained a lagenar macula. Adalatherium is derived among mammaliaforms in possessing primary and secondary osseous laminae, a cribriform plate, and a distinct cochlear ganglion canal. Strikingly, Adalatherium shows a single-layered primary osseous lamina that lacks internal, radially oriented canaliculi for auditory nerve fibers. In this respect, the primary lamina of Adalatherium is structurally different from the double-layered primary lamina containing habenulae perforatae of extant therians. Furthermore, Adalatherium resembles the gondwanatherian Vintana in possessing a secondary canal running parallel to the cochlear ganglion canal. Although its exact role and homology are uncertain, the morphology of this secondary canal and its tributary canaliculi is most consistent with a vascular function. The inner ear of Adalatherium augments a growing list of characters (or character combinations) in which gondwanatherians are not only different from the inferred plesiomorphic condition for mammaliaforms but also distinct from the derived characters of therians. Collectively, the new morphological and phylogenetic data support homoplastic transformation of such structures as the cribriform plate and primary osseous lamina in mammals and independent loss of the lagenar macula within gondwanatherians.

Molar occlusion and jaw roll in early crown mammals

Triconodontidae are considered the first carnivorous crown mammals. A virtual reconstruction of the masticatory cycle in the Late Jurassic Priacodon showed that triconodontid dental function is characterized by precise cutting on elongated crests. The combination of traits linked to both carnivorous diets (e.g. fore-aft cutting edges) and insectivorous diets (transverse crests and lobes) suggests a varied faunivorous diet appropriate to the small body size of most triconodontids. Total length of molar shear decreased with wear, suggesting a dietary shift during ontogeny. Embrasure occlusion is confirmed for P. fruitaensis as indicated by premolar positioning, facet orientation, and collision areas. Embrasure occlusion is considered a general feature of all Eutriconodonta, whereas the previously assumed Morganucodon-like pattern is limited to few early mammaliaforms. Unlike modern carnivores, significant roll of around 10° of the active hemimandible occurred during the power stroke. Roll was likely passive in Triconodontidae in contrast to active roll described for extant therians. The triconodontid molar series was highly uniform and adapted to a precise fit, with self-sharpening lower molar cusps. Whereas the uniformity ensured good cutting capabilities, it likely put the dentition under greater constraints, conserving the highly stereotyped nature of triconodontid molars for 60–85 Ma.

Petrosal morphology and cochlear function in Mesozoic stem therians.

Here we describe the bony anatomy of the inner ear and surrounding structures seen in three plesiomorphic crown mammalian petrosal specimens. Our study sample includes the triconodont Priacodon fruitaensis from the Upper Jurassic of North America, and two isolated stem therian petrosal specimens colloquially known as the Höövör petrosals, recovered from Aptian-Albian sediments in Mongolia. The second Höövör petrosal is here described at length for the first time. All three of these petrosals and a comparative sample of extant mammalian taxa have been imaged using micro-CT, allowing for detailed anatomical descriptions of the osteological correlates of functionally significant neurovascular features, especially along the abneural wall of the cochlear canal. The high resolution imaging provided here clarifies several hypotheses regarding the mosaic evolution of features of the cochlear endocast in early mammals. In particular, these images demonstrate that the membranous cochlear duct adhered to the bony cochlear canal abneurally to a secondary bony lamina before the appearance of an opposing primary bony lamina or tractus foraminosus. Additionally, while corroborating the general trend of reduction of venous sinuses and plexuses within the pars cochlearis seen in crownward mammaliaforms generally, the Höövör petrosals show the localized enlargement of a portion of the intrapetrosal venous plexus. This new vascular feature is here interpreted as the bony accommodation for the vein of cochlear aqueduct, a structure that is solely, or predominantly, responsible for the venous drainage of the cochlear apparatus in extant therians. Given that our fossil stem therian inner ear specimens appear to have very limited high-frequency capabilities, the development of these modern vascular features of the cochlear endocast suggest that neither the initiation or enlargement of the stria vascularis (a unique mammalian organ) was originally associated with the capacity for high-frequency hearing or precise sound-source localization.

The postcranial anatomy of Brasilodon quadrangularis and the acquisition of mammaliaform traits among non-mammaliaform cynodonts.

Brasilodon quadrangularis (Cynodontia, Probainognathia) is an iconic non-mammaliaform cynodont from the Late Triassic of Brazil (Riograndia Assemblage Zone, Candelária Sequence), being considered as the sister taxon of Mammaliaformes. Although its phylogenetic position is very important, several aspects of its postcranial anatomy remain unclear or unstudied. Here, we present a detailed description of the postcranial elements referred to Brasilodon, including previously mentioned specimens and new ones, which add relevant information about its postcranial morphology and provide a new insight into the anatomical transition between advanced non-mammaliaform cynodonts and early mammaliaforms. Functional and ecological implications are also investigated, based on the postcranial morphology and muscular reconstructions. The postcranium of Brasilodon differs from most non-mammaliaform cynodonts and presents similarities with tritylodontids, early mammaliaforms and extant therians, such as a ventrally oriented scapular glenoid facet, a distinct and ossified greater humeral tubercle, lack of ectepicondylar foramen, olecranon process, hemispherical humeral and femoral heads and a prominent intertrochanteric crest. The humeral torsion, the length of the deltopectoral crest, the large bicipital groove and the well-developed lesser tubercle, indicate that the forelimb of Brasilodon was hold in a semi-sprawling position, with well-developed adductor muscles to maintain the body off the ground. The short femoral neck and the strong medial projection of the femoral head indicate the femur was held in a more erect posture than in basal non-mammaliaform cynodonts. The anterodorsally projected iliac blade with reduced postacetabular process, reduction of the anterior part of the pubis, medially located lesser trochanter indicate a basically mammalian pattern of pelvic musculature, able to swing the femur in a nearly parasagittal plane.

Postcranial Skeleton of Henkelotherium guimarotae (Cladotheria, Mammalia) and Locomotor Adaptation

X-ray computed tomography of the cladotherian Henkelotherium guimarotae from the Kimmeridgian Guimarota coal mine (Portugal) adds new information on its postcranial skeleton. Contrary to earlier description, the humerus of Henkelotherium shows a plesiomorphic cladotherian condition similar to that seen in Dryolestes leiriensis in having individual radial and ulnar condyles on the anterior aspect of the distal joint, whereas the posterior aspect appears to be trochlear. The scapula is also more plesiomorphic than previously assumed in having a laterally flared crest on the inferior margin. In this regard, it is similar to the scapula of spalacotherioid “symmetrodontans” such as Zhangheotherium but more derived than the latter, in having a larger supraspinous fossa. The hind limb is similar to that of small extant therians, which is interpreted to be assocated with an upright limb posture. The previously proposed hypothesis of an arboreal lifestyle for Henkelotherium is corroborated by a number of skeletal features such as large humeral entepicondyles, prominent digital flexor tubercles, elongated and slender tail vertebrae, as well as a high pedal phalangeal index of 153%.

Inner Ear Morphology of Basal‐Most Mammaliaform Morganucodon

Extant therians are unique in their ability to hear at higher and at greater ranges of frequencies than most other vertebrates. This ability has been associated with changes in inner ear morphology, including elongation of the cochlear canal following loss of the lagena maculae, coiling of the cochlear canal, and stabilization of the hearing membrane through bony laminae. Presence and absence of these features is variable across Mesozoic mammaliaforms. To gain insights into the evolution of the inner ear and hearing in mammaliaforms, we document inner ear morphology in the basal‐most mammaliaform Morganucodon in unprecedented detail. We μCT scanned 30 petrosals of Morganucodon from several Jurassic fissure fillings in the UK. Surface reconstructions of the inner ears demonstrate that the cochlear canal gently varies in curvature and length (1.64–1.80 mm, measured from the posterior aspect of the cochlear foramen to the apex). All specimens show a distinct expansion of the apex of the cochlear canal suggesting the presence of a lagenar macula. Interestingly, the size of the apical expansion varies within our sample. None of the specimens preserve complete ossified laminae, but a shallow groove is visible on the ventrolateral surface of the cochlear canal endocasts, extending from the base of the canal (between the perilymphatic foramen and the fenestra vestibule) anteriorly towards the apex. We identify this groove as the attachment for the basilar membrane (termed here “base of secondary lamina”), as seen in extant monotremes. If the base of the secondary lamina is indeed reflective of basilar membrane length in Morganucodon then this could represents the first accurate reconstruction of the length of the basilar membrane in a fossil mammaliaform that retains a lagena. The base of the secondary lamina ends shortly before the apex of the canal and ranges between 1.17 and 1.45 mm. It moderately correlates (R2=0.58) with total cochlear canal length in our sample. Most intriguingly, the bony wall of the promontorium contains a network of canals that surrounds the cochlea, previously described as the circumpromontorium plexus. The plexus enters the cochlear canal next to the base of the secondary lamina and extends along the laminas full length. This strongly suggests that the blood supply to the cochlea might have been substantially different in Morganucodon compared to extant therians where blood vessel enter the cochlea through the cochlear foramen along with the cochlear nerve.This abstract is from the Experimental Biology 2018 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Origin of the Lateral Wall of the Mammalian Skull: Fossils, Monotremes and Therians Revisited

To interpret the fundamental differences in the structure and origin of the braincase sidewalls of monotremes, multituberculates, and therians, we examined MicroCT scans of a mammaliaform, Morganucodon; two non-mammalian cynodonts, Massetognathus and Probainognathus; a stem therian, Vincelestes; a juvenile and adult monotreme, Ornithorhynchus; and two marsupials, Monodelphis and Didelphis. The skull of Morganucodon resembles the pattern predicted for an early mammal: the descending flanges of the frontal and parietal cover the lateral surface of the orbitosphenoid and the palatine forms most of the medial wall of the orbit. In monotremes, the lateral region of the chondrocranium ossifies to form a long presphenoid/orbitosphenoid complex. During the transition from early mammals to extant mammals the height of the alisphenoid decreased drastically, the anterior lamina extended anteriorly to form part of the sidewall while the lateral surface of the orbitosphenoid was exposed by the dorsal withdrawal of the frontal and parietal. By contrast, in multituberculates and therians the lateral edges of the frontals extended further ventrally and the orbitosphenoid was reduced to a smaller orbital exposure below the frontals. In multituberculates the alisphenoid decreased in height, replaced by an anterior extension of the anterior lamina. The palatine withdrew from the orbital wall, replaced by a dorsally directed expansion of the maxilla. Extant therians have lost the anterior lamina. The inferior edges of the frontal followed the further ventral migration of the orbitosphenoid. The alisphenoid and parietal form most of the braincase sidewall.

Meckel’s cartilage breakdown offers clues to mammalian middle ear evolution

A key transformation in mammalian ear evolution was incorporation of the primary jaw joint of premammalian synapsids into the definitive mammalian middle ear of living mammals. This evolutionary transition occurred in two-steps, starting with a partial or "transitional" mammalian middle ear in which the ectotympanic and malleus were still connected to the mandible by an ossified Meckel's Cartilage (MC), as observed in many Mesozoic mammals. This was followed by MC breakdown, freeing the ectotympanic and the malleus from the mandible and creating the definitive mammalian middle ear. Here we report novel findings on the role of chondroclasts in MC breakdown, shedding light on how therian mammals lost MC connecting the ear to the jaw. Genetic or pharmacological loss of clast cells in mice and opossums leads to persistence of embryonic MC beyond juvenile stages, with MC ossification in mutant mice. The persistent MC causes a distinctive postnatal groove on the mouse dentary. This morphology phenocopies the ossified MC and Meckelian groove observed in Mesozoic mammals. Clast cell recruitment to MC is not observed in reptiles, where MC persists as a cartilaginous structure. We hypothesize that ossification of MC is an ancestral feature of mammaliaforms, and that a shift in the timing of clast cell recruitment to MC prior to its ossification is a key developmental mechanism for the evolution of the definitive mammalian middle ear in extant therians.

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.

Comparative Myology and Evolution of Marsupials and Other Vertebrates, With Notes on Complexity, Bauplan, and "Scala Naturae".

Opossums are frequent subjects of developmental studies because marsupials share developmental features not seen in placentals and because Didelphimorpha is the sister-group of other extant Marsupialia. But is the adult marsupial muscular system markedly different from that of placentals or is it, like the skeletal system, very similar? We provide, for the first time, a brief description of all head and limb muscles of Didelphis virginiana based on our dissections and using a unifying nomenclature by integrating the data gathered in our long-term project on the development, homologies, and evolution of the muscles of all major vertebrate taxa. Our data indicate that there were many more muscle synapomorphic changes from the last common ancestor (LCA) of amniotes to the mammalian LCA (63) and from this LCA to the LCA of extant therians (48) than from this latter LCA to the LCA of extant placentals (10 or 11). Importantly, Didelphis is anatomically more plesiomorphic (only 14 changes from LCA of extant therians) than are rats (37 changes) and humans (63 changes), but its musculature is more complex (193 muscles) than that of humans (only 180 muscles). Of the 194 muscles of Didelphis, 172 (89%) are present in rats, meaning that their adult muscle anatomy is indeed very similar. This similarity supports the existence of a common, easy recognizable therian Bauplan, but one that is caused by developmental constraints and by evolutionary change driven by the needs of the embryos/neonates, rather than by a "goal" toward a specific adult plan/"archetype," as the name Bauplan suggests. Anat Rec, 299:1224-1255, 2016. © 2016 Wiley Periodicals, Inc.

Sensory Anatomy and Sensory Ecology of Vintana Sertichi (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar

ABSTRACT—Living mammals are distinguished from other extant tetrapods by adaptations for improved senses of hearing, touch, and smell. These adaptations, and concomitant reductions in visual anatomy, evolved during the Mesozoic in the mammalian and therian stem lineages. Here, we present a comparative study of the sensory anatomy of the Late Cretaceous gondwanatherian mammaliaform Vintana sertichi in order to draw inferences regarding its sensory abilities and sensory ecology. Our analyses demonstrate that Vintana has relatively large orbits that may have accommodated large eyes. Vintana also possessed cochlear primary and secondary osseous laminae and a cochlear canal that was relatively longer than in non-mammaliaform cynodonts but shorter than in extant therians. These features suggest that Vintana had some capacity for high-frequency hearing (i.e., >20 kHz), but that its cochlea may have encoded a more limited range of frequencies than the cochleas of most extant therians. The semicircular canals of Vintana have large radii of curvature and are nearly orthogonal, suggesting high sensitivity to angular head accelerations. These vestibular features may have evolved in order to stabilize large eyes during rapid and/or agile locomotion. Combined with evidence for large olfactory bulbs and a large trigeminal endocast, these data reveal that Vintana possessed a unique suite of sensory adaptations that distinguish it from other Mesozoic mammaliaforms. If these inferences are correct, then Vintana was probably a large-eyed and agile species, with a keen sense of smell and better high-frequency hearing than most other Mesozoic mammaliaforms.SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVP

Endocranial and Inner Ear Morphology of Vintana Sertichi (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar

ABSTRACTWe present the first digital reconstruction of the endocranial cavity and endosseous labyrinth of the Late Cretaceous gondwanatherian mammal Vintana sertichi from the Maevarano Formation of Madagascar. The Malagasy specimen is exceptionally well preserved and represents the only described cranium known for Gondwanatheria, an enigmatic clade from the Late Cretaceous and Paleogene of Gondwana. The endocranial cast of Vintana is relatively small for an animal of its estimated body mass. Its encephalization quotient is 0.28–0.56 for a range of body mass estimates, which is similar to that of basal mammaliaforms. The olfactory bulbs are very large, occupying over 14% of the endocranial volume. The cerebral hemispheres are only slightly expanded, more similar to the condition in Morganucodon than to that in multituberculates and monotremes. Unlike the condition in other Mesozoic mammaliaforms, the endocast is greatly flexed at the circular fissure. The osseous labyrinth displays a mixture of derived and primitive features. The cochlear canal is only slightly curved and short compared with that of extant therians. The ratio between total cochlear canal length and maximum cranial length is smaller than in basal mammaliaforms and approximates that of non-mammaliaform cynodonts. By contrast, the presence of both primary and secondary osseous laminae, the tractus foraminosus, and Rosenthal's canal represent derived characteristics of the mammalian inner ear typical of cladotherians. A modern innervation of the cochlea has either evolved independently in Vintana and cladotherians or was already present in the last common ancestor of both clades.SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVP

Metabolic profile of the perivertebral muscles in small therian mammals: implications for the evolution of the mammalian trunk musculature

In order to gain a better understanding of the ancestral properties of the perivertebral muscles of mammals, this study investigated the fiber type composition of these muscles in six small, extant therians (two metatherians and four eutherians) similar in body shape to early mammals. Despite a few species-specific differences, the investigated species were very similar in their overall distribution of fiber types indicating similar functional demands on the back muscles in mammals of this body size and shape. Deep and short, mono- or multisegmental muscles (i.e., mm. interspinales, intermammillares, rotatores et intertransversarii) consistently showed the highest percentage of slow, oxidative fibers implying a function as local stabilizers of the vertebral column. Superficial and large, polysegmental muscles (i.e., mm. multifidus, sacrospinalis, iliopsoas et psoas minor) were predominantly composed of fast, glycolytic fibers suggesting they function to both globally stabilize and mobilize the spine during rapid non-locomotor and locomotor activities. Some muscles contained striking accumulations of oxidative fibers in specific regions (mm. longissimus et quadratus lumborum). These regions are hypothesized to function independently from the rest of the muscle belly and may be comparable in their functionality to regionalized limb muscles. The deep, central oxidative region in the m. longissimus lumborum appears to be a general feature of mammals and likely serves a proprioceptive function to control the postural equilibrium of the pelvic girdle and lumbar spine. The potential functions of the m. quadratus lumborum during ventilation and ventral stabilization of the vertebral column are discussed. Because representatives of the stem lineage of mammals were comparable in their body proportions and probably also locomotor parameters to the species investigated here, I suggest that the described fiber type distribution is representative of the ancestral condition in mammals. The origin of mammals was associated with a substantial enlargement of the epaxial muscles and the addition of subvertebral muscle mass. Because this novel muscle mass is mainly composed of fast, glycolytic fibers in extant species, it is plausible that these changes were associated with the evolution of increased sagittal mobility in the posterior trunk region in the therapsid ancestors of mammals. The caudally increasing role of sagittal bending in body propulsion is consistent with the overall increase in the percentage of glycolytic fibers in the cranio-caudal direction. The evolution of mammals was also associated with a loss of ribs in the posterior region of the trunk. This loss of ribs is thought to have decreased the stability of the posterior trunk, which may explain the observed greater oxidative capacity of the caudal local stabilizers. The increased need for postural feedback in the more mobile lumbar region may also explain the evolution of the proprioceptive system in the m. longissimus lumborum. Furthermore, the anatomical subdivision of the transversospinal muscle into several smaller muscle entities is suggested to facilitate their functional specialization.

Dual origin of tribosphenic mammals.

Marsupials, placentals and their close therian relatives possess complex (tribosphenic) molars that are capable of versatile occlusal functions. This functional complex is widely thought to be a key to the early diversification and evolutionary success of extant therians and their close relatives (tribosphenidans). Long thought to have arisen on northern continents, tribosphenic mammals have recently been reported from southern landmasses. The great age and advanced morphology of these new mammals has led to the alternative suggestion of a Gondwanan origin for the group. Implicit in both biogeographic hypotheses is the assumption that tribosphenic molars evolved only once in mammalian evolutionary history. Phylogenetic and morphometric analyses including these newly discovered taxa suggest a different interpretation: that mammals with tribosphenic molars are not monophyletic. Tribosphenic molars evolved independently in two ancient (holotherian) mammalian groups with different geographic distributions during the Jurassic/Early Cretaceous: an australosphenidan clade endemic to Gondwanan landmasses, survived by extant monotremes; and a boreosphenidan clade of Laurasian continents, including extant marsupials, placentals and their relatives.