Irina Ruf

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.

High morphological variation of vestibular system accompanies slow and infrequent locomotion in three-toed sloths.

The semicircular canals (SCs), part of the vestibular apparatus of the inner ear, are directly involved in the detection of angular motion of the head for maintaining balance, and exhibit adaptive patterns for locomotor behaviour. Consequently, they are generally believed to show low levels of intraspecific morphological variation, but few studies have investigated this assumption. On the basis of high-resolution computed tomography, we present here, to our knowledge, the first comprehensive study of the pattern of variation of the inner ear with a focus on Xenarthra. Our study demonstrates that extant three-toed sloths show a high level of morphological variation of the bony labyrinth of the inner ear. Especially, the variation in shape, relative size and angles of their SCs greatly differ from those of other, faster-moving taxa within Xenarthra and Placentalia in general. The unique pattern of variation in three-toed sloths suggests that a release of selection and/or constraints on their organ of balance is associated with the observed wide range of phenotypes. This release is coincident with their slow and infrequent locomotion and may be related, among other possible factors, to a reduced functional demand for a precise sensitivity to movement.

Petrosal anatomy and inner ear structures of the Late Jurassic Henkelotherium (Mammalia, Cladotheria, Dryolestoidea): insight into the early evolution of the ear region in cladotherian mammals

The petrosal anatomy and inner ear structure of Jurassic cladotherian mammals represent the ancestral morphological conditions (groundplan) from which modern therian mammals (marsupials and placentals) have evolved. We present the reconstruction of the petrosal and inner ear features of the Late Jurassic dryolestoid mammal Henkelotherium guimarotae from high‐resolution computed tomography and three‐dimensional imaging analysis. This study of Henkelotherium revealed a combination of derived and primitive features, including: cladotherian apomorphies, such as the promontorial sulcus for the internal carotid artery and reduced lateral trough; trechnotherian characters, such as an enclosed cochlear canaliculus for the perilymphatic duct, post‐promontorial tympanic sinus and caudal tympanic process; in addition to plesiomorphic mammalian features, such as the cavum supracochleare and prootic canal. The inner ear of Henkelotherium shows a division between the utricle and saccule, a cochlear canal coiled through at least 270°, a distinctive primary bony lamina for the basilar membrane, and a secondary bony lamina. The development of the primary and secondary bony laminae in the cochlear canal is suggested here to be correlated with the concurrent coiling of the bony canal and membranous duct of the inner ear cochlea, apomorphies of the more inclusive cladotherian clade that also represent the ancestral morphotype of modern therian mammals. Because these features are crucial for high‐frequency hearing in extant therian mammals, their early appearance in Late Jurassic cladotherians suggests a more ancient origination for high‐frequency hearing in mammalian history than previously thought.

Digital reconstruction of the otic region and inner ear of the non-mammalian cynodont brasilitherium riograndensis (late triassic, brazil) and its relevance to the evolution of the mammalian ear

The external anatomy of the petrosal, the bony labyrinth of the inner ear, and the stapes of Brasilitherium riograndensis (specimen UFRGS-PV-1043-T) were investigated by digital 3D reconstructions based on μCT scan images. Brasilitherium is the most basal taxon bearing a distinct promontorium, although less inflated than that of Morganucodon and still lacking a flat medial facet. A bony wall formed by the petrosal separates the cochlear canal and the vestibule from the brain cavity, with an internal acoustic meatus bearing distinct foramina for the facial nerve (VII) and vestibulocochlear nerve (VIII). The semicircular canals are irregular in shape, the anterior canal being the largest and the lateral one the smallest. Brasilitherium has an elongated but straight cochlear canal. The stapes resembles the morphology of derived non-mammaliaform cynodonts, such as Probainognathus and Pachygenelus, and differs from Thrinaxodon. By the allometric relationship of the cochlear canal and the estimated body mass, Brasilitherium can be grouped with Yunnanodon and Morganucodon in a regression line, which is below the line of mammals and above the line of non-avian reptiles. Brasilitherium fits in a sequence of gradual elongation of the cochlear canal associated with the enhancement in the capacity to hear higher frequencies. Among the constraints that might have triggered these transformations in small, insectivorous, and possibly nocturnal Mesozoic cynodont taxa is the improvement of detecting acoustically active insects.

Reinvestigation of the basicranium of Haldanodon exspectatus (Mammaliaformes, Docodonta)

ABSTRACT The docodont Haldanodon exspectatus, a mammaliaform from the Late Jurassic of Portugal, is a crucial taxon for studying higher-level relationships of mammaliaforms and their morphological evolution. Based on high-resolution computed tomography scanning of three specimens of Haldanodon, we developed a new reconstruction of the basicranium including the petrosal and the inner ear. Our study confirms that Haldanodon and other basal mammaliaforms, such as Morganucodon and Sinoconodon, are similar in the main characteristics of their external anatomy of the petrosal. However, Haldanodon shows several derived features that support a phylogenetic position of docodonts more derived than Morganucodon and Sinoconodon: (1) elongated and curved cochlear canal (nearly 180°), (2) single lateral flange foramen of petrosal, (3) absence of anterior paroccipital process, and (4) squamosal constriction. The bony labyrinth reveals a secondary crus commune, which is regarded to be a plesiomorphic feature of the mammaliaform groundplan. The cochlear canal shows an apical inflation connected to a distinct sulcus and a separate notch in the internal acoustic meatus, supporting the existence of a lagenar nerve and macula as in monotremes. Haldanodon is unique among Mesozoic mammaliaforms in having a hypertrophied paroccipital region that is excavated into large tympanic pneumatic recesses, which are connected with the extensive porous and probably also pneumatic internal structures of the surrounding bones. The curved cochlear canal and the pneumatized middle ear region support the hypothesis that Haldanodon had more effective low-frequency hearing as an adaptation to a fossorial mode of life.

The inner ear of Megatherium and the evolution of the vestibular system in sloths.

Extant tree sloths are uniquely slow mammals with a very specialized suspensory behavior. To improve our understanding of their peculiar evolution, we investigated the inner ear morphology of one of the largest and most popular fossil ground sloths, Megatherium americanum. We first address the predicted agility of this animal from the scaling of its semicircular canals (SC) relative to body mass, based on recent work that provided evidence that the size of the SC in mammals correlates with body mass and levels of agility. Our analyses predict intermediate levels of agility for Megatherium, contrasting with the extreme slowness of extant sloths. Secondly, we focus on the morphology of the SC at the inner ear scale and investigate the shape and proportions of these structures in Megatherium and in a large diversity of extant xenarthrans represented in our database. Our morphometric analyses demonstrate that the giant ground sloth clearly departs from the SC morphology of both extant sloth genera (Choloepus, Bradypus) and is in some aspects closer to that of armadillos and anteaters. Given the close phylogenetic relationships of Megatherium with the extant genus Choloepus, these results are evidence of substantial homoplasy of the SC anatomy in sloths. This homoplasy most likely corresponds to an outstanding convergent evolution between extant suspensory sloth genera.

Nasal anatomy of the non-mammaliaform cynodont Brasilitherium riograndensis (Eucynodontia, Therapsida) reveals new insight into mammalian evolution.

The mammalian nasal cavity is characterized by a unique anatomy with complex internal features. The evolution of turbinals was correlated with endothermic and macrosmatic adaptations in therapsids and in early mammals, which is still apparent in their twofold function (warming and moistening of air, olfaction). Fossil evidence for the transformation from the nonmammalian to the mammalian nasal cavity pattern has been poor and inadequate. Ossification of the cartilaginous nasal capsule and turbinals seems to be a feature that occurred only very late in synapsid evolution but delicate ethmoidal bones are rarely preserved. Here we provide the first µCT investigation of the nasal cavity of the advanced non‐mammaliaform cynodont Brasilitherium riograndensis from the Late Triassic of Southern Brazil, a member of the sister‐group of mammaliaforms, in order to elucidate a critical anatomical transition in early mammalian evolution. Brasilitherium riograndensis already had at least partially ossified turbinals as remnants of the nasoturbinal and the first ethmoturbinal are preserved. The posterior nasal septum is partly ossified and contributes to a mesethmoid. The nasal cavity is posteriorly expanded and forms a distinctive pars posterior (ethmoidal recess) that is ventrally separated from the nasopharyngeal duct by a distinct lamina terminalis. Thus, our observations clearly demonstrate that principal features of the mammalian nasal cavity were already present in the sister‐group of mammaliaforms. Anat Rec, 297:2018–2030, 2014.

Evolution of the mammalian middle ear: a historical review.

Here we present a brief, historical review of research into the mammalian middle ear structures. Most of their essential homologies were established by embryologists, notably including Reichert, during the 19th century. The evolutionary dimension was confirmed by finds of fossil synapsids, mainly from the Karroo of South Africa. In 1913, Ernst Gaupp was the first to present a synthesis of the available embryological and paleontological data, but a number of morphological details remained to be solved, such as the origin of the tympanic membrane. Gaupp favoured an independent origin of the eardrum in anurans, sauropsids, and mammals; we support most of his ideas. The present review emphasizes the problem of how the mammalian middle ear structures that developed at the angle of the lower jaw were transferred to the basicranium; the ontogenesis of extant marsupials provides important information on this question.

Bony labyrinth morphometry indicates locomotor adaptations in the squirrel-related clade (Rodentia, Mammalia)

The semicircular canals (SCs) of the inner ear detect angular acceleration and are located in the bony labyrinth of the petrosal bone. Based on high-resolution computed tomography, we created a size-independent database of the bony labyrinth of 50 mammalian species especially rodents of the squirrel-related clade comprising taxa with fossorial, arboreal and gliding adaptations. Our sampling also includes gliding marsupials, actively flying bats, the arboreal tree shrew and subterranean species. The morphometric anatomy of the SCs was correlated to the locomotion mode. Even if the phylogenetic signal cannot entirely be excluded, the main significance for functional morphological studies has been found in the diameter of the SCs, whereas the radius of curvature is of minor interest. Additionally, we found clear differences in the bias angle of the canals between subterranean and gliding taxa, but also between sciurids and glirids. The sensitivity of the inner ear correlates with the locomotion mode, with a higher sensitivity of the SCs in fossorial species than in flying taxa. We conclude that the inner ear of flying and gliding mammals is less sensitive due to the large information flow into this sense organ during locomotion.

Study of a digital cranial endocast of the non-mammaliaform cynodont Brasilitherium riograndensis (Later Triassic, Brazil) and its relevance to the evolution of the mammalian brain

A digital cranial endocast of the specimen UFRGS-PV-1043-T, Brasilitherium riograndensis, was obtained from high-resolution computed tomography (μCT) scan images. This taxon is a small cynodont from the Late Triassic of Brazil, and has been used as the sister-group of the mammaliaforms in cladistic analyses. The digital endocast of UFRGS-PV-1043-T is mostly complete, allowing the description and collection of accurate linear and volumetric measurements, which were taken and compared with other non-mammaliaform cynodonts. Impressions of vessels were observed in the inner walls of the braincase. Despite the lack of a cribiform plate and the presence of a wide orbital vacuity, the endocast of Brasilitherium shows olfactory bulb casts that are relatively larger than in other non-mammaliaform cynodonts, suggesting a pattern of gradual increase in size and improvement of the olfactory sense for these structures toward the mammalian condition. The cerebral hemispheres are elongated and clearly divided by a median sulcus. The parafloccular casts are well defined, and their position corresponds to the maximum width of the endocast. In the ventral view, a large hypophyseal cast and a wide opening for the cavum epiptericum are evident. The encephalization quotient (EQ) calculated for Brasilitherium is greater than the range of EQs reported for most non-mammaliaform cynodonts (although it may be similar to that of some taxa, according to the equation used to estimate their body masses), but it is smaller than that of the mammaliaforms and mammals. A slighter increase in the brain size of Brasilitherium compared with other non-mammaliaform cynodonts was observed, along with a more significant increase in the size of the olfactory bulbs. This study supports the proposition of an early evolution of the mammalian brain associated with selective pressures for better sensorial acuity, especially regarding improved olfaction, which began with small Triassic mammaliamorphs.KurzfassungMittels μCT-Daten wurde ein virtueller Gehirnausguss von Brasilitherium riograndensis (UFRGS-PV-1043-T) erstellt. Bei diesem Taxon handelt es sich um einen kleinen Cynodontier aus der späten Trias von Brasilien, der in cladistischen Analysen die Schwestergruppe der Mammaliaformes repräsentiert. Der fast vollständige virtuelle Gehirnausguss von UFRGS-PV-1043-T ermöglicht die Beschreibung sowie genaueste lineare und volumetrische Messungen im Vergleich mit anderen nicht-mammaliaformen Cynodontier. Am inneren Schädeldach befinden sich einige Abdrücke von Blutgefässen. Obwohl eine Lamina cribrosa fehlt und die Augenhöhlen sehr groß sind, weist der virtuelle Ausguss von Brasilitherium relativ größere Bulbi olfactorii auf als bei anderen nicht-mammaliaformen Cynodontiern. Somit lässt sich eine graduelle Größenzunahme sowie Verbesserung des Riechsinns hin zu einem säugerähnlichen Zustand beobachten. Die Großhirnhälften sind verlängert und deutlich durch einen medianen Sulcus voneinander getrennt. Die Paraflocculusausgüsse sind deutlich ausgeprägt und ihre Lage korrespondiert mit der maximalen Breite des gesamten Gehirnausgusses. In ventraler Ansicht ist ein prominenter Ausguss der Hypophyse sowie eine große Öffnung in das Cavum epiptericum zu erkennen. Der für Brasilitherium berechnete Enzephalisationsquotient (EQ) ist größer als die Spannbreite der EQs der meisten anderen nicht-mammaliaformen Cynodontier. Aufgrund der Schätzung des Körpergewichts von Brasilitherium könnte dessen EQ jedoch dem bestimmter Taxa durchaus entsprechen; er ist jedoch sicherlich geringer als bei Mammaliaformes und Mammalia. Brasilitherium zeigt eine geringere Größenzunahme des Gehirns im Vergleich zu anderen nicht-mammaliaformen Cynodontiern, mit wesentlich deutlicherer Größenzunahme der Bulbi olfactorii. Diese Studie unterstützt die Annahme einer frühen Evolution des Säugergehirns assoziiert mit der Selektion erhöhter sensorischer Schärfe, insbesondere der Verbesserung der Riechleistung, die bereits bei triassischen kleinen Mammaliamorpha auftritt.