The inner ear of <Emphasis Type="Italic">Protungulatum</Emphasis> (Pan-Euungulata,Mammalia)

We present new anatomical details about the bony labyrinth of Protungulatum based on micro CT-scan investigation of an isolated petrosal bone retrieved at the Puercan locality of Bug Creek Anthills and referred to Protungulatum sp. The exceptional state of preservation of the specimen allowed us to reconstruct the very fine details of the inside of the petrosal bone, including the bony labyrinth, the innervation of the vestibule and the innervation and vasculature of the cochlea. Estimation of the auditory capability of Protungulatum based on cochlear morphology indicate that Protungulatum was specialized for high-frequency hearing, with estimated low frequency limits above 1 KHz. Comparisons with Late Cretaceous non-placental eutherians and with early Tertiary pan-euungulates indicate that the bony labyrinth of Protungulatum is closer in general morphology to Mesozoic forms (low coiling and low aspect ratio of the cochlea, posterior orientation of the common crus, dorsal outpocketing of the cochlear fossula), and shares only a few characters with pan-euungulate and euungulate taxa. Interestingly, the bony labyrinth of Protungulatum also shares some morphological features with South American notoungulates and litopterns recently described from Itaboraí, Brazil. These new observations provide new morphological features of potential phylogenetic interest.     

The petrosal and inner ear of the Late Jurassic cladotherian mammal Dryolestes leiriensis and implications for ear evolution in therian mammals

Dryolestes leiriensis is a Late Jurassic fossil mammal of the dryolestoid superfamily in the cladotherian clade that includes the extant marsupials and placentals. We used high resolution micro‐computed tomography (µCT) scanning and digital reconstruction of the virtual endocast of the inner ear to show that its cochlear canal is coiled through 270°, and has a cribriform plate with the spiral cochlear nerve foramina between the internal acoustic meatus and the cochlear bony labyrinth. The cochlear canal has the primary bony lamina for the basilar membrane with a partially formed (or partially preserved) canal for the cochlear spiral ganglion. These structures, in their fully developed condition, form the modiolus (the bony spiral structure) of the fully coiled cochlea in extant marsupial and placental mammals. The CT data show that the secondary bony lamina is present, although less developed than in another dryolestoid Henkelotherium and in the prototribosphenidan Vincelestes. The presence of the primary bony lamina with spiral ganglion canal suggests a dense and finely distributed cochlear nerve innervation of the hair cells for improved resolution of sound frequencies. The primary, and very probably also the secondary, bony laminae are correlated with a more rigid support for the basilar membrane and a narrower width of this membrane, both of which are key soft‐tissue characteristics for more sensitive hearing for higher frequency sound. All these cochlear features originated prior to the full coiling of the therian mammal cochlea beyond one full turn, suggesting that the adaptation to hearing a wider range of sound frequencies, especially higher frequencies with refined resolution, has an ancient evolutionary origin no later than the Late Jurassic in therian evolution. The petrosal of Dryolestes has added several features that are not preserved in the petrosal of Henkelotherium. The petrosal characters of dryolestoid mammals are essentially the same as those of Vincelestes, helping to corroborate the synapomorphies of the cladotherian clade in neural, vascular, and other petrosal characteristics. The petrosal characteristics of Dryolestes and Henkelotherium together represent the ancestral morphotype of the cladotherian clade (Dryolestoidea + Vincelestes + extant Theria) from which the extant therian mammals evolved their ear region characteristics. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166 , 433–463.     

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.     

Inner-ear structure in Morganucodon, an early Jurassic mammal

The shapes and dimensions of the cochlear cavities from four petrosals of the genus Morganucoden obtained through sectioning and reconstruction. Morganucodon dates from the early Jurassic and represents many of the earliest known mammal specimens. Each Morganucodon petrosal fossil was embedded in Araldite and shaved with an ultramicrotome to expose the internal structure. Line drawings of the exposed cross-sections were digitized and used to produce three-dimensional reconstructions. The reconstructed Monganucodon cochlear cavities differ from extant mammalian cochleas in several respects: they are uncoiled, shorter in length, and lack the bony lamina which supports the basilar membrane. These three features ar characteristic of extant Aves and Reptilia.     

Homoplasy in the ear region of Tethytheria and the systematic position of Embrithopoda (Mammalia,Afrotheria)

The ear region of mammals has long been considered as morphologically very conservative and accordingly, phylogenetically useful. In this study, the anatomy of the petrosal and bony labyrinth (osseous inner ear) of Numidotherium (Proboscidea) and Arsinoitherium (Embrithopoda) are investigated and compared in order to assess the evolution of ear region characters in proboscideans and embrithopods. Using a cladistic analysis across Paenungulata based on ear region characters only, we found that Arsinoitherium is surprisingly best placed as a crown proboscideans to the exclusion of Numidotherium and Phosphatherium, which results in the paraphyly of proboscidean. The clade Proboscidea is actually well supported by dental and post-cranial characters, and we propose that this result underlines the great amount of morphological convergences in the ear region of Embrithopoda and Proboscidea, possibly due to convergent evolution of capabilities toward infrasonic hearing.     

The petrosal bone and bony labyrinth of early to middle Miocene European deer (Mammalia,Cervidae) reveal their phylogeny

Deer (Cervidae) have a long evolutionary history dating back to the Early Miocene, around 19 million years ago. The best known fossils to document this history belong to European taxa, which all bear cranial appendages more or less similar to today's deer antlers. Despite the good fossil record, relationships of the earliest stem deer and earliest crown deer are much debated. This hampers precise calibration against the independent evidence of the fossil record in molecular clock analyses. While much has been written on the Early and Middle Miocene deer, only two phylogenetic analyses have been performed on these taxa to date mostly based on cranial appendage characters. Because the petrosal bone and bony labyrinth have been shown to be relevant for phylogeny in ruminants, we describe for the first time these elements for four iconic early cervids from Europe (Procervulus dichotomus, Heteroprox larteti, Dicrocerus elegans and Euprox furcatus) and include them in a phylogenetic analysis based on the ear region exclusively. The analysis recovered E. furcatus in a sister position to the living red deer (Cervus elaphus). Further, it placed D. elegans in a sister position to Euprox + Cervus and a clade Procervulinae that includes P. dichotomus and H. larteti, in sister position to all other deer. The inclusion of E. furcatus in crown Cervidae, which was previously suggested based on antler morphology, cannot be ruled out here but needs a more comprehensive comparison to other crown deer to be confirmed. J. Morphol. 277:1329–1338, 2016. © 2016 Wiley Periodicals, Inc.     

The petrosal and bony labyrinth of Diplobune minor,an enigmatic Artiodactyla from the Oligocene of Western Europe

Anoplotheriinae are Paleogene European artiodactyls that present a unique postcranial morphology with a tridactyl autopodium and uncommon limb orientation. This peculiar morphology led to various hypotheses regarding anoplotheriine locomotion from semiaquatic to partly arboreal or partly bipedal. The petrosal bone, housing the organs of balance, and hearing, offers complementary information to postcranial morphology on the ecology of this uncommon artiodactyl. Here, we investigate the middle ear and bony labyrinth of the small anoplotheriine Diplobune minor based on four specimens from the Early Oligocene locality of Itardies (Quercy, France). A macroscopic study coupled with a μCT scan investigation of the petrosal anatomy provides novel information on the bony labyrinth, stapes, and innervation and vasculature of the inner ear of this enigmatic taxon. The petrosal of D. minor exhibits a mosaic of plesiomorphic characters and peculiar features that shed new light into the anatomy of this poorly studied taxon of an obscure taxonomic clade. We can confidently reject that D. minor was a semiaquatic species based on the petrosal morphology: presence of a large mastoid process and nonpachyostotic tegmen tympani do not support underwater hearing. On the other hand, the average semicircular canal radius points to a slow or medium slow agility for D. minor , and fully rejects it was a fast moving animal, which is congruent with its postcranial anatomy.     

The first French tragulid skull (Mammalia,Ruminantia, Tragulidae) and associated tragulid remains from the Middle Miocene of Contres (Loir-et-Cher,France)

The Faluns Auger quarry (Contres, France) is famous for its Langhian mammal fauna (MN5) and tragulid remains have been identified as Dorcatherium sp. New excavations provided a fragmented skull of a tragulid, dental remains, and a metapodium which we describe here. Based on morphological and morphometrical characters, these specimens are attributed to Dorcatherium crassum. CT-scans provide insight in the petrosal bone and bony labyrinth. We prove intra-population variability of the p4 and intra-specific variability of the bony labyrinth. Nevertheless, we can demonstrate that the bony labyrinth is useful for systematics. Thus, we confirm the presence of D. crassum in the Pontlevoy–Thenay and Savigné-sur-Lathan Faluns Basins as reported already prior to our study. Yet, we cannot confirm evidence for Dorcatherium naui. D. naui specimens reported from these basins may belong to another species. D. naui should be absent from the Faluns before MN7, such as in the rest of Europe.     

Petrosal and Bony Labyrinth Morphology Supports Paraphyly of Elephantulus Within Macroscelididae (Mammalia,Afrotheria)

Interest in the phylogeny of Macroscelididae (sengis or elephant shrews) has been prompted by molecular studies indicating that Elephantulus rozeti is best placed as the sister group of Petrodromus tetradactylus (this clade being in turn the sister taxon to Macroscelides proboscideus) than among other species of the genus Elephantulus. Until now, no discrete morphological characters have been proposed to support the grouping of E. rozeti, Petrodromus, and Macroscelides into this single so-called ‘Panelephantulus’ clade. Here, we employed μCT scanning in order to investigate the petrosal and bony labyrinth (bony capsule of the inner ear) morphology of most species of extant Macroscelididae. We performed a cladistic analysis on ear traits and found that despite some convergences (e.g., concerning the bony arterial canals in Macroscelides and Rhynchocyon) the middle and inner ear morphology furnishes significant support for the ‘Panelephantulus’ clade. In our analysis, this clade is unambigously supported by the presence of a fully ossified stapediofacial tube. Two additional characters (the presence of a bony septum at the mouth of the fenestra cochleae dividing the D3 sinus into two distinct cavities and the absence of an accessory lateral pneumatic fossa) could also support ‘Panelephantulus.’ These newly discovered morphological characters support the molecular phylogenies published and highlight the importance of coding hitherto difficult to sample morphologies within cladistic analyses using micro-CT techniques. Taxonomic implications are briefly discussed.     

Cranial anatomy of Ignacius graybullianus and the affinities of the Plesiadapiformes

A nearly complete cranium of Ignacius graybullianus provides increased understanding of the cranial anatomy of Plesiadapiformes. In nearly all details of cranial anatomy, Ignacius differs markedly from primates. USNM 421608 exhibits a long tapering snout, small widely spaced orbits, and a complete lack of postorbital process or bar. Large olfactory bulbs are inferred from the wide interorbital space. The marked flare of the zygomatic arches suggests that Ignacius possessed large and powerful temporal muscles. The basicranial region is particularly well preserved and reveals a distinct suture between the petrosal bone and an entotympanic bulla. This suture is visible on both the left and right sides of the skull and dispels the hypothesis that Ignacius and, by inference, other Plesiadapiformes share the primate synapomorphy of a petrosal bulla. To test the phylogenetic position of Ignacius, cranial characters were identified and scored for Ignacius, Plesiadapis, Cynocephalus, and a number of primates, bats, and scandentians. Two erinaceomorph insectivores were also included to allow the assessment of archontan monophyly. These characters were incorporated into a maximum-parsimony analysis to determine the phylogenetic position of Plesiadapiformes. There are several important phylogenetic conclusions that can be inferred from this analysis: 1) Ignacius and Plesiadapis make up a monophyletic clade; 2) Plesiadapiformes may be the sister group of Dermoptera; 3) Scandentia, not Plesiadapiformes, is the sister group of Primates; and 4) Primates, plesiadapiforms, bats, colugos, and scandentians may not form a monophyletic clade Archonta. Consequently, the taxon Archonta is in need of review. © 1992 Wiley-Liss, Inc.     

The Ear Region of the Pen-tailed Treeshrew, Ptilocercus lowii Gray, 1848 (Placentalia, Scandentia, Ptilocercidae)

The ear region of the pen-tailed treeshrew, Ptilocercus lowii Gray, 1848 (Scandentia, Ptilocercidae), is described and illustrated in detail based on five museum specimens from the National Museum of Natural History, two with the auditory bulla removed exposing the intratympanic surfaces. Soft tissues (arteries, veins, nerves, and muscles) are reconstructed onto the adult skulls based on published reports of these elements in a fetal P. lowii. Comparisons are made with four specimens of the common treeshrew, the tupaiid Tupaia glis (Diard, 1820), from the Carnegie Museum of Natural History, including one with the auditory bulla removed. The mammalian ear region widely is regarded to be a rich source of characters for phylogenetic analysis. This study supports this view by identifying numerous features that are shared between the two treeshrews as well as numerous features that distinguish them. Several features used in the past to distinguish tupaiid treeshrews from primates are found to differ between P. lowii and T. glis: the composition of the bony tubes for the internal carotid artery and the composition of the intrabullar septa and spaces. Despite the compositional differences, it seems likely that the bony carotid tubes and intrabullar septa and spaces shared by P. lowii and T. glis occurred in their common ancestor. Evaluating the utility of these and other ear region features awaits future phylogenetic analysis of treeshrews and related Euarchontoglires.     

Bony labyrinth morphology in early neopterygian fishes (Actinopterygii: Neopterygii)

Endocasts of the osseous labyrinth have the potential to yield information about both phylogenetic relationships and ecology. Although bony labyrinth morphology is well documented in many groups of fossil vertebrates, little is known for early Neopterygii, the major fish radiation containing living teleosts, gars and the bowfin. Here, we reconstruct endocasts of the bony labyrinth and associated structures for a sample of Mesozoic neopterygian fishes using high‐resolution computed tomography. Our sample includes taxa unambiguously assigned to either the teleost (Dorsetichthys, “Pholidophorus,” Elopoides) and holostean (“Aspidorynchus,” “Caturus,” Heterolepidotus) total‐groups, as well as examples of less certain phylogenetic position (an unnamed parasemionotid and Dapedium). Our models provide a test of anatomical interpretations for forms where bony labyrinths were reconstructed based on destructive tomography (“Caturus”) or inspection of the lateral wall of the cranial chamber (Dorsetichthys), and deliver the first detailed insights on inner ear morphology in the remaining taxa. With respect to relationships, traits apparent in the bony labyrinth and associated structures broadly support past phylogenetic hypotheses concerning taxa agreed to have reasonably secure systematic placements. Inner ear morphology supports placement of Dapedium with holosteans rather than teleosts, while preserved structure in the unnamed parasemionotid is generalized to the degree that it provides no evidence of close affinity with either of the crown neopterygian lineages. This study provides proof‐of‐concept for the systematic utility of the inner ear in neopterygians that, in combination with similar findings for earlier‐diverging actinopterygian lineages, points to the substantial potential of this anatomical system for addressing the longstanding questions in the relationships of fossil ray‐finned fishes to one another and living groups. J. Morphol. 279:426–440, 2018. © 2016 Wiley Periodicals, Inc.     

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.     

Phylogenetic Affinities Among the Extant Malagasy Lemurs (Lemuriformes) Based on Morphology and Behavior

The difficulty in achieving a consensus on the phylogenetic relationships of lemuriform primates has been due largely to the lack of a lemur fossil record and to the lack of an appropriate outgroup that would facilitate polarization of character states. Recent findings allow us to polarize some of the bony characters, but to a large extent this problem still remains. In the past, phylogenetic analyses have focused on specialized character sets such as dentition or basicranial traits, or they have employed differential weighting schemes to a more variable set of characters. In the analysis presented here, I combined all relevant characters available in the literature into one data set but restricted my selection to those traits having discontinuous states and for which no contradictory coding schemes were published. I reduced the assumptions in this analysis by removing most external weighting and ordering effects on these data sets. The available data from the literature were supplemented with data from my own observations at the Duke University Primate Center. Data were collected for 25 characters and 20 taxa and were submitted to a cladistic analysis. Some important findings from this study include support for (1) a sister-group relationship between Lepilemur and the Indridae, (2) a sister-group relationship between the Lemuridae (except Varecia) and the Indridae/Lepilemur clade, (3) a monophyletic genus Eulemur, and (4) the exclusion of Varecia from the Lemuridae.     

Evidence of early evolution of Australidelphia (Metatheria,Mammalia) in South America: phylogenetic relationships of the metatherians from the Late Palaeocene of Itaboraí (Brazil) based on teeth and petrosal bones

New metatherian petrosal bones from the mid to Late Palaeocene of Itaboraí, belonging to three morphotypes (VI, VII, and VII), are formally described and compared to fossil and extant taxa known by their auditory region. An attempt at assigning petrosal types to tooth‐based taxa from Itaboraí was made by combining parsimony and morphometric methods. The first large scale phylogenetic analysis of the Itaboraían metatherians, involving basicranial and dental characters in a larger number of taxa, is provided here and is at the basis of a systematic revision of the metatherians from Itaboraí. The combination of morphometric and cladistic analyses helps in understanding the affinities between the petrosals and the tooth‐based taxa. The metatherians from Itaboraí were taxonomically diverse, belonging to each of the most important radiations in marsupial evolutionary history (Didelphimorphia, Paucituberculata, Eometatheria). The inclusion of Palaeocene taxa in the crown group Marsupialia and above all in the Eometatheria radiation points to an early emergence of these clades in South America and corroborates the main molecular hypotheses. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159 , 746–784.     

Cranial morphology of the early tertiary Phenacolemur and its bearing on primate phylogeny

An early Eocene skull of the paromomyid Phenacolemur, a plesiadapoid primate, is described with particular emphasis on the ear region. The auditory bulla is composed of the petrosal and of a large ectotympanic plate which is outside of the bulla. The preserved morphology of the middle ear is distinctly more primitive than that of the older Plesiadapis. It cannot be determined with certainty whether Phenacolemur had the carotid circulation enclosed in bony tubes or not. The auditory bulla of early primates and relevant living ones is discussed and it is suggested that an extrabullar ectotympanic, as seen in all non-lemuriform fossil and extant primates, was probably the primitive ordinal condition, rather than the intrabullar ring-like ectotympanic in the Lemuriformes. Aspects of the carotid circulation are discussed as they pertain to the relationship of early Tertiary primates, living Tarsiiformes, Lemuriformes and Lorisiformes.     

Morphological Evidence for the Phylogeny of Cetacea

A cladistic analysis of 54 extant and extinct cetacean taxa scored for 304 morphological characters supports a monophyletic Odontoceti, Mysticeti, Autoceta, and Cetacea. Forcing a sister-group relationship between Mysticeti and Physeteridae, as suggested by some, but not all, molecular studies, requires an additional 72 steps. In agreement with recent molecular studies, morphological data divide extant mysticetes into two clades: Balaenopteroidea (Eschrichtiidae + Balaenopteridae) and Balaenoidea (Balaenidae + Neobalaenidae). Cetotheriopsinae is removed from Cetotheriidae, elevated to Family Cetotheriopsidae, and placed within the Superfamily Eomysticetoidea. All extant mysticetes and all cetotheriids are placed in a new Parvorder Balaenomorpha, which is diagnosed by many morphological characters, including fusion of the anterior and posterior processes of petrosal to ectotympanic bulla, pronounced median keel on palate, and absence of ventral margin of sigmoid process of bulla. Many of the clades within Odontoceti in the most parsimonious trees of this study are at odds with recent phylogenetic analyses. For example, Platanistidae is not closely related to the extinct odontocete families Squalodontidae and Squalodelphinidae. Instead, it is more closely related to extant river-dwelling odontocetes (i.e., Lipotes, Inia), suggesting a single dispersal of odontocetes into freshwater habitats. We found several characters to support Physeteroidea (Physeteridae + Ziphiidae), a taxon considered paraphyletic by several molecular and some morphological analyses. Lack of agreement on the phylogeny within Odontoceti indicates that additional analyses, which include molecular and anatomical data as well as extant and extinct taxa, are needed.     

The Bony Labyrinth in Diprotodontian Marsupial Mammals: Diversity in Extant and Extinct Forms and Relationships with Size and Phylogeny

The shape of the bony labyrinth of the inner ear was quantified using geometric morphometrics in a sample of 16 species of living marsupial diprotodontians, the extinct Diprotodon and Thylacoleo, and four outgroups. X-ray micro-computed tomography (μCT) and conventional computed tomography (CT) were used to acquire 3D data. The analyses of 22 landmarks revealed a strong body-mass related allometric pattern. A discriminant analysis on allometry-free labyrinthine shape served to evaluate the phylogenetic signal portion of the labyrinth for Macropodiformes, Phalangeroidea, Petauroidea, and Vombatiformes. The inner shape of Thylacoleo is consistent with its phylogenetic placement as a vombatiform.