EARLIEST KNOWN CARNIVORAN AUDITORY BULLA AND SUPPORT FOR A RECENT ORIGIN OF CROWN-GROUP CARNIVORA (EUTHERIA, MAMMALIA)

Abstract:  An ossified auditory bulla of a basal carnivoran is described for the first time. Although broken, the bulla of Viverravus acutus (Viverravidae, Carnivora) appears to have enclosed the middle ear and to have been composed exclusively of an ectotympanic bone. The structure of the bulla and other basicranial features support the hypothesis that viverravids lie phylogenetically outside crown-group Carnivora and that the last common ancestor of living carnivorans may have existed as recently as 42 million years ago, not 60–70 million years ago as suggested by some authors.     

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.     

New basicrania of Paleocene-Eocene Ignacius: re-evaluation of the Plesiadapiform-Dermopteran link

Plesiadapiformes has long been considered to be an archaic group of Primates. Discovery of a paromomyid plesiadapiform skull and independent analysis of referred postcrania have led investigators to conclude that Plesiadapiformes shares a closer relationship to extant flying lemurs (Dermoptera) than to Primates (= Euprimates of Hoffstetter [1977] Bull Mem Soc Anthropol Paris Ser 13 4:327-346). Despite challenges to this interpretation, the plesiadapiform-dermopteran relationship has gained currency in recent years. Here we show that newly discovered crania of Ignacius graybullianus, preserving previously undocumented portions of the ear, are more similar to primates than to dermopterans. New specimens confirm that paromomyids lacked the petrosal bulla of primates. However, these new specimens also demonstrate that paromomyids likely had: 1) a small promontorial branch of the internal carotid artery; 2) a lateral route for the internal carotid nerves crossing the promontorium; and 3) a ring-like ectotympanic with an annular bridge. This pattern is similar to primitive primates and fundamentally different from dermopterans, which have: 1) no internal carotid artery; 2) internal carotid nerves that take a more medial route; and 3) no annular bridge. Recognition of some primate-like traits, documented here by new evidence, indicates that Paromomyidae is likely to be more closely related to other Paleogene Plesiadapiformes and Eocene Primates than to extant Dermoptera. In view of these findings, a link between paromomyids and extant dermopterans ("Eudermoptera") is not convincingly supported by a single characteristic of the basicranium.     

New notharctine (primates,adapiformes) skull from the Uintan (middle Eocene) of San Diego County,California

A new genus and species of notharctine primate, Hesperolemur actius, is described from Uintan (middle Eocene) aged rocks of San Diego County, California. Hesperolemur differs from all previously described adapiforms in having the anterior third of the ectotympanic anulus fused to the internal lateral wall of the auditory bulla. In this feature Hesperolemur superficially resembles extant cheirogaleids. Hesperolemur also differs from previously known adapiforms in lacking bony canals that transmit the internal carotid artery through the tympanic cavity. Hesperolemur, like the later occurring North American cercamoniine Mahgarita stevensi, appears to have lacked a stapedial artery. Evidence from newly discovered skulls of Notharctus and Smilodectes, along with Hesperolemur, Mahgarita, and Adapis, indicates that the tympanic arterial circulatory pattern of these adapiforms is characterized by stapedial arteries that are smaller than promontory arteries, a feature shared with extant tarsiers and anthropoids and one of the characteristics often used to support the existence of a haplorhine-strepsirhine dichotomy among extant primates. The existence of such a dichotomy among Eocene primates is not supported by any compelling evidence. Hesperolemur is the latest occurring notharctine primate known from North America and is the only notharctine represented among a relatively diverse primate fauna from southern California. The coastal lowlands of southern California presumably served as a refuge area for primates during the middle and later Eocene as climates deteriorated in the continental interior. Hesperolemur probably was an immigrant taxon that entered California from either the northern (Wyoming/Utah) or southern (New Mexico) western interior during the middle Eocene © 1995 Wiley-Liss, Inc.     

Unlocking the ring: Occurrence and development of the uninterrupted intrabullar septum in Canidae

The maned wolf, Chrysocyon brachyurus, and some of the earliest canids are known for the peculiar ring-like shape of their intrabullar septum (an incomplete bony partition in the auditory bulla). In attempt to understand the origin of this character state, the auditory bullae in adult and juvenile dried skulls of 28 species of living Caninae were examined with a special emphasis on the occurrence of a ring-like (uninterrupted) septum. In addition to C. brachyurus, this morphology was invariably found in the bush dog, Speothos venaticus, what makes the presence of the uninterrupted septum the first osteological synapomorphy supporting the Chrysocyon–Speothos clade recently revealed by molecular systematics.The canine juvenile morphologies indicate that the intrabullar septum is ring-like at its early developmental stage. As ontogeny progresses, the septum resorbs differentially, depending on taxon, to become horseshoe- or crescent-like. By this transformation of the initially ring-like septum, Caninae seem to ontogenetically parallel a trend found in the phylogeny of Hesperocyoninae, an extinct canid group. The reverse recapitulation occurs, however, in the evolution of Caninae themselves, with their most-derived members having a least-resorbed septum. This implies that the ontogenetic criterion cannot be used for inference of the polarity of septal character states within the Caninae. The evolution of the canine intrabullar septum could have involved a series of heterochronies towards increasingly paedomorphic states in several lineages of the tribe Canini.New data were also obtained on the bone composition of the canid intrabullar septum. While the dorsal septum is entotympanic, the ventral one is in fact ectotympanic in adult Caninae. This compound structure results from penetration of the ventral entotympanic sinus into the ectotympanic.     

Cranial anatomy of the Paleocene plesiadapiform Carpolestes simpsoni (Mammalia, Primates) using ultra high-resolution X-ray computed tomography, and the relationships of plesiadapiforms to Euprimates

Central to issues surrounding the origin of euprimates, affinities of Paleocene Carpolestidae have been controversial. Carpolestids have been classified as plesiadapoid primates, tarsiiform euprimates, dermopterans, or the sister taxon of euprimates to the exclusion of other plesiadapiforms, based exclusively on dental or postcranial data. Newly discovered crania of Carpolestes simpsoni from the latest Paleocene of the Clarks Fork Basin, Wyoming, are the first described for the family Carpolestidae. The two best preserved skulls were studied using ultra high-resolution X-ray computed tomography. Comparison of these specimens to those of other stem primates (Plesiadapiformes) demonstrates that the diversity of cranial morphology in this group is greater than previously thought. Carpolestes differs from euprimates and is similar to other plesiadapiforms (Ignacius and Plesiadapis) in lacking a postorbital bar and having a relatively long rostrum. Carpolestes is similar to fossil euprimates and Plesiadapis in having a bullar morphology consistent with a petrosal origin, and differs from Ignacius, in which the bulla is composed of the entotympanic. Carpolestes differs from primitive euprimates and all other known plesiadapiforms in possessing a two-chambered auditory bulla, similar to that of modern Tarsius. However, Carpolestes had an internal carotid artery (ICA) that took a transpromontorial route from a posteromedially positioned posterior carotid foramen (pcf), unlike Tarsius, in which this artery takes a perbullar route from an anterolaterally positioned pcf. Carpolestes has clear grooves on the promontorium for both the promontorial and stapedial arteries, indicating that it had an unreduced internal carotid circulation, similar to that of early euprimates. Carpolestes differs from primitive euprimates and some specimens of Ignacius in not having bony tubes surrounding the branches of the ICA. Cladistic analysis of cranial data fails to support a close relationship of Carpolestidae to either tarsiiform euprimates or extant Dermoptera, but suggests a close relationship between Carpolestidae, Plesiadapidae, and Euprimates.     

Ontogeny,auditory structures,and primate evolution

The anatomy of the auditory region, particularly the carotid circulatory patterns and ectotympanic-petrosal relationships, has played a prominent role in primate systematics and phylogenetic reconstructions. Ontogenetic stages of petrosal-ectotympanic relationship are presented for certain strepsirhines. It is suggested that the “ectotympanic tube” or “ossified annulus membrane” found in early Tertiary primates is not necessarily an homologous structure to the true ectotympanic tube seen in haplorhines, and thus cannot be considered a shared, derived feature linking known Paleogene primates from Europe or North America to tarsioid and/or anthropoid ancestry. No fossil primate yet discovered makes a convincing ancestor for the earliest known anthropoids from the Oligocene of Africa. This is probably due to the fact that it still lies undiscovered in the Paleogene of Africa.     

Skull of Catopithecus browni,an early tertiary catarrhine

Fossil crania from quarry L-41, Fayum, Egypt, representing Catopithecus browni, a primate similar in size to callitrichids but with a catarrhine dental formula, provide the geologically earliest record of an anthropoidean skull. Catopithecus had postorbital closure developed to the stage seen in extant anthropoideans, with direct contact between zygomatic plate and maxillary tuber, isolating an anterior orbital fissure from the inferior orbital fissure. The auditory region also resembles that of later anthropoideans: The posterior carotid foramen is placed adjacent to the jugular fossa; a large promontory canal crosses the promontorium; and the annular ectotympanic is fused ventrally to the bulla. The incisors and canines show an assemblage of features found only among modern anthropoideans and adapoids. The face is characterized by a relatively deep maxilla, broad ascending wing of the premaxilla, and long nasal bones, yielding a moderate muzzle similar to that of Aegyptopithecus. The small braincase bears an anteriorly broad frontal trigon and a posteriorly developed sagittal crest. The mandibular symphysis is unfused even in mature adults. The encephalization quotient (EQ) probably falls within the range of Eocene prosimians, much lower than the EQs of Neogene anthropoideans. © 1996 Wiley-Liss, Inc.     

The entotympanic of Equus caballus (Perissodactyla,Mammalia)

In the majority of extant placental mammals the bulla tympanica is composed of two skeletal elements, the entotympanic and the ectotympanic. Former studies revealed that the presence of an entotympanic in the bulla tympanica of extant Perissodactyla is restricted to Rhinocerotidae. The existence of the entotympanic in Tapiridae and Equidae remained speculative. Here we present the first evidence of an entotympanic, strictly speaking rostral entotympanic, in the domestic horse, Equus caballus. The enchondrally ossified entotympanic can be easily separated from the desmal ectotympanic by its greater thickness and by its cancellous bone texture in a late fetal stage. Both elements are separated by a suture that is in the process of coalescence. The complete fusion of the two elements and the unification of bone texture are almost accomplished at birth but the entotympanic and ectotympanic assume the same thickness obviously not until early postnatal development. Based on modern phylogenetic hypotheses we can conclude that the common ancestor of Perissodactyla must have possessed a well-developed entotympanic, probably only evident in their fetal life. This must be considered as a plesiomorphic character state of this order, because the entotympanic is a neomorphic apomorphy of placental mammals. However, the prenatal fusion of the entotympanic and the ectotympanic is an apomorphy of Equus caballus and possibly of the Equidae as a whole.     

Intraspecific morphological variation of the middle ear in the European badger,Meles meles (Carnivora: Mustelidae)

Many studies have been conducted about the information contained in the anatomy of the mammalian middle ear. Most of these only use a few specimens. Thus we aim to provide a quantitative analysis of the intraspecific and interspecific variations of the middle ear, focusing on the auditory bulla. For that purpose, we focused on the mustelids, as a quite generalist taxon and, more specifically, on the European badger, Meles meles. Our study includes two types of statistical methods. We first compared the mean of a subjectively chosen measure between individuals of the same species and between individuals of different species. We then used a multidimensional scaling procedure to cluster individuals according to different measures. We conclude that the middle ear varies effectively less intraspecifically than interspecifically. However, we think that the few anatomical parameters to measure in the auditory bulla involve using more specimens or focusing on geometric morphometrics in studies focusing on middle ear.     

A clupeomorph fish from the Gault (Lower Cretaceous)

A primitive clupeomorph fish, Spratticepsgaultinus gen. et sp. nov., is described on the basis of incomplete braincases from the Gault (Albian) of Folkestone, Kent. This is the earliest clupeomorph in which any details of cranial structure are known. Spratticeps is more primitive than living clupeomorphs in having no recessus lateralis, auditory fenestra, pterotic bulla or sinus temporalis, and in having a heavily ornamented, entire skull roof, with the sensory canals bone enclosed and the post-temporal fossa roofed. The fish is too primitive to be placed in either suborder of Clupeomorpha, and is left incertae sedis. The primary characters of the Clupeomorpha are discussed.     

New discoveries on the middle ear anatomy of Ignacius graybullianus (Paromomyidae,Primates) from ultra high resolution X-ray computed tomography

A skull of Ignacius graybullianus (USNM 421608) was studied using ultra high resolution X-ray computed tomography (uhrCT). The anatomy of the middle ear in this specimen was previously studied through partial removal of the auditory bulla on one side. The data now available allow for examination of the others unprepared ear, which is more completely preserved, as well as adding to the information available about the previously studied ear. Analysis of the relationships between the bones making up the auditory bulla confirms previous assertions that it is formed from the entotympanic, and not from the petrosal, basioccipital, or basisphenoid. Contrary to previous reconstructions of the middle ear anatomy in all known plesiadapiforms, this specimen exhibits a bony canal for the promontorial artery and/or internal carotid nerves running across the lateral extreme of the promontorium. The identification of this structure is confirmed by the clear presence of a lumen, and its origination at a posterior carotid foramen (pcf) in a position that corresponds to that identified in previous studies of the paromomyid basicranium (Am. J. Phys. Anthropol., 36 (1972) 59, Am. J. Phys. Anthropol., 89 (1992) 477). Remnants of this canal are present bilaterally in USNM 421608, which additionally supports its identification. The presence of bony canals for branches of the internal carotid artery and the internal carotid nerves is a feature seen in scandentians and euprimates that is missing in dermopterans. The unusual lateral route followed by the internal carotid nerves is a primitive euprimate feature missing in all other archontans. As such, this evidence is consistent with a close euprimate-paromomyid relationship, and the inclusion of the latter in the order Primates. The discovery of this feature in paromomyids after almost 30 years of study of the ear region of this family acts as a cautionary note to the interpretation of the middle ear in damaged specimens.     

Overview of Sensory Systems of <Emphasis Type="Italic">Tarsius</Emphasis>

Tarsiers form the sister taxon to anthropoid primates, and their brains possess a mix of primitive and specialized features. We describe architectonically distinct subdivisions of the somatosensory, auditory, and visual systems for tarsiers, as well as nocturnal New World owl monkeys (Aotus) and strepsirhine galagos (Otolemur) for comparison. In general, the dorsal column nuclei, the ventroposterior nucleus, and primary somatosensory cortex are somewhat less distinctly differentiated in tarsiers, suggesting that the somatosensory system is less specialized for somatosensory processing. Although the inferior colliculus and the medial geniculate complex of the auditory system are architectonically similar across the 3 primates, the primary auditory cortex of tarsiers is more distinct, suggesting a greater role in auditory cortical processing. In the visual system, the differentiation of the superior colliculus is similar in all 3 primates, whereas the laminar pattern in the lateral geniculate nucleus and the subdivisions of the inferior pulvinar in tarsiers resemble those of anthropoid primates rather than strepsirhines, in agreement with the evidence that tarsiers form the sister clade for anthropoids. In addition, primary visual cortex has more distinct sublayers in tarsiers than other primates, attesting to its importance in this visual predator. Overall, tarsiers have well developed visual and auditory systems, and a less well developed somatosensory system, suggesting an enhanced reliance on the visual and auditory senses, rather than somatosensory sense.     

A requirement for Fgfr2 in middle ear development

The skeletal structure of the mammalian middle ear, which is composed of three endochondral ossicles suspended within a membranous air‐filled capsule, plays a critical role in conducting sound. Gene mutations that alter skeletal development in the middle ear result in auditory impairment. Mutations in fibroblast growth factor receptor 2 (FGFR2), an important regulator of endochondral and intramembranous bone formation, cause a spectrum of congenital skeletal disorders featuring conductive hearing loss. Although the middle ear malformations in multiple FGFR2 gain‐of‐function disorders are clinically characterized, those in the FGFR2 loss‐of‐function disorder lacrimo‐auriculo‐dento‐digital (LADD) syndrome are relatively undescribed. To better understand conductive hearing loss in LADD, we examined the middle ear skeleton of mice with conditional loss of Fgfr2. We find that decreased auditory function in Fgfr2 mutant mice correlates with hypoplasia of the auditory bulla and ectopic bone growth at sites of tendon/ligament attachment. We show that ectopic bone associated with the intra‐articular ligaments of the incudomalleal joint is derived from Scx‐expressing cells and preceded by decreased expression of the joint progenitor marker Gdf5. Together, these results identify a role for Fgfr2 in development of the middle ear skeletal tissues and suggest potential causes for conductive hearing loss in LADD syndrome.     

Partitions in the carnivoran auditory bulla: their formation and significance for systematics

The common notion that the septa in the carnivoran auditory bulla are formed by the growth of bone edges inwards the bullar cavity is a mistaken assumption based on the data of the late 19th century. Intrabullar partitions are in fact a result of the differential resorption of the bulla internal surface during the growth of the external surface. A septum develops at the boundary between local, relatively independent, ‘inflations’ of the bulla wall. This explanation, given by Van Kampen in 1905 for the case of the Canidae and some Mustelidae, can be applied to the whole order, including the aeluroid families with their ‘bilaminar’ septum bullae. Such an approach seems to solve the problem of homology of the intrabullar septa throughout the Carnivora, a question which has long been confused because of insufficient knowledge of septum morphogenesis. The partitions can really be considered as indicators of independent attempts to increase the size of a middle‐ear cavity among the infraorders. This conclusion follows immediately from the difference between major carnivoran taxa in the arrangement of separate inflations on the bulla wall, which can be considered as additional sinuses enlarging the hypotympanic space. It is precisely this difference that conditions the relative contribution of several bones (mainly of the ectotympanic and caudal entotympanic) to the intrabullar septa. Thus, the initial topographies of the above sinuses – whichever subsequent bone modelling of septa occurs – represent unique patterns useful in the higher‐level systematics of the Carnivora.     

Rudabánya: A late miocene subtropical swamp deposit with evidence of the origin of the African apes and humans

Rudabánya, a rich late Miocene fossil site in northern central Hungary, has yielded an abundant record of fossil primates, including the primitive catarrhine Anapithecus and the early great ape Dryopithecus. While the affinities of Anapithecus are not clear, Dryopithecus is clearly a great ape sharing numerous characteristics of its dental, cranial and postcranial anatomy with living great apes. Like all Miocene hominids (great apes and humans), Dryopithecus is more primitive in a number of ways than any living hominid, which is probably related to the passage of time since the divergence of the various lineages of living hominids, allowing for similar refinements in morphology and adaptation to take place independently. On the other hand, Dryopithecus (and Ouranopithecus) share derived characters with hominines (African apes and humans), and Sivapithecus (and Ankarapithecus) share derived characters with orangutans, thus dating the split between pongines and hominines to a time before the evolution of these fossil great apes. Pongines and hominines follow similar fates in the late Miocene, the pongines moving south into Southeast Asia from southern or eastern Asia and the hominines moving south into East Africa from the Mediterranean region, between 6 to 9 Ma.     

New faces of Aegyptopithecus from the Oligocene of Egypt

Three recently discovered faces of Aegyptopithecus zeuxis from the Oligocene Jebel Qatrani Formation of Egypt provide new information about the shape and variation of the facial cranium, the earliest preserved for a presumed forerunner of apes and humans. Although varying considerably in details of shape and proportion, the new finds and a skull found in 1966 all appear to be of males, a conclusion based in part on the development of temporal and sagittal crests and on the large size of upper canines or their sockets (female canines are much smaller). The snouts of the three new faces all are shorter and broader than that of the earlier found skull as reconstructed. As in most later species of Anthropoidea, variation between these specimens is high.Aegyptopithecus helps define the nature of the oldest Anthropoidea and generally most resembles later-occurring apes. Many features, both derived and shared primitive, link Aegyptopithecus, the large Miocene great apes of the Proconsul group, and modern great apes. That these shared features and proportions are not direct allometric consequences of body size is indicated by Aegyptopithecus' resemblance to the large apes and its many distinctions from similar-sized Hylobates.In Aegyptopithecus brain volume scales smaller than in later catarrhines relative to facial size, the ectotympanic tube is less developed and the premaxilla is more primitive than in later higher primates. In closure of orbits and conformation of forehead, face and dentition, Aegyptopithecus closely resembles higher primates and not prosimians. Taken together, its overall cranial and dental anatomy constitutes one of the most important connecting links in primate evolutionary history.     

Hoc alterum auditus organi ossiculum est: Ear Ossicles in Physical Anthropology

In spite of the importance of auditory ossicles in anthropological studies, very little attention has been paid to these bones, which are only rarely recovered in archaeological excavations and in osteological collections. In this paper, we attempt to review some studies that started in the 1960 from when we first collected and prepared ossicles from the early Egyptian osteological collection of Giovanni Marro in Turin (Italy). We attempt to delineate the potential of ear bones in the study of man. In a few cases, archaeological ossicles were discussed in connection with some forms of pathology. Other studies examined the phylogeny of primates based on auditory ossicles. The function of the ossicles is to transmit sound waves to the cochlear endolymph. The energy transmitted through the ossicles is conserved by the action of two levers, which convert the relatively wide and low-energy movements of the hammer into smaller high-energy movements of the stirrup. It is a matter of argument whether the different proportions of the ossicles may imply variations in auditory perception in primates, including man. While the hammer of modern humans and that of the great apes show similar absolute sizes, nevertheless, the ape manubrium is appreciably greater than that of man. This difference, combined with stirrup proportions, causes a strong “low-gear” effect in apes and, as a consequence, probably a different auditory acuity. Although only a few fossil Neanderthal auditory ossicles are known, it may be, nevertheless, of interest studying the ossicles from the viewpoint of vibration transfer impedance function. The methodology may also be appropriate to study the few Australopithecine ossicles that are known. It is a matter of question whether the ossicles may have a meaning in distinguishing human populations; nevertheless, at least a case of clear distinction between human population has been achieved as in the case of Antinoe Roman–Egyptians.