The middle and inner ears of the Palaeogene golden mole Namachloris: A comparison with extant species

Many living species of golden moles (Chrysochloridae) have greatly enlarged middle ear ossicles, believed to be used in the detection of ground vibrations through inertial bone conduction. Other unusual features of chrysochlorids include internally coupled middle ear cavities and the loss of the tensor tympani muscle. Our understanding of the evolutionary history of these characteristics has been limited by the paucity of fossil evidence. In this article, we describe for the first time the exquisitely preserved middle and inner ears of Namachloris arenatans from the Palaeogene of Namibia, visualised using computed tomography, as well as ossicles attributed to this species. We compare the auditory region of this fossil golden mole, which evidently did not possess a hypertrophied malleus, to those of three extant species with similarly sized ear ossicles, Amblysomus hottentotus, Calcochloris obtusirostris, and Huetia leucorhinus. The auditory region of Namachloris shares many common features with the living species, including a pneumatized, trabeculated basicranium and lateral skull wall, arteries and nerves of the middle ear contained in bony tubes, a highly coiled cochlea, a secondary crus commune, and no identifiable canaliculus cochleae for the perilymphatic duct. However, Namachloris differs from extant golden moles in the apparent absence of a basicranial intercommunication between the right and left ears, the possession of a tensor tympani muscle and aspects of ossicular morphology. One Namachloris skull showed what may be pneumatization of some of the dorsal cranial bones, extending right around the brain. Although the ossicles are small in absolute terms, one of the Huetia leucorhinus specimens had a more prominent malleus head than the other. This potentially represents a previously unrecognised subspecific difference.     

Proliferation of vertebrate inner ear supporting cells

Using two S phase markers, we determined the cell‐cycle behavior of inner ear supporting cells from two species, the chicken and the oscar. The results indicate that chicken utricular supporting cells divide once and do not return to the cell cycle for at least 7 days. In contrast, supporting cell progeny in the oscar saccule return to S phase after 5 days. While both the chicken utricle and oscar saccule show ongoing supporting cell proliferation, these data indicate that there may be a dedicated recycling population of supporting cells in the oscar saccule but not in the chicken utricle that is responsible for hair cell production. An expulsion of proliferative cell progeny in the chicken utricle after 7 days may be a driving force for proliferation, as well as an explanation for why hair cell numbers do not increase in the chicken utricle with age. This was not seen in the oscar saccule, possibly explaining how this end organ increases in size throughout the adult life of the animal. The absence of S phase cell expulsion, however, does not rule out the role of cell death in the oscar saccule. © 1999 John Wiley & Sons, Inc. J Neurobiol 39: 527–535, 1999     

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.     

Petrosal and inner ear anatomy and allometry amongst specimens referred to Litopterna (Placentalia)

New isolated petrosals from the Itaboraí beds of Brazil (late Palaeocene or early Eocene) are here described and referred to the early diverging litoptern Miguelsoria parayirunhor, based on phylogenetic, size, and abundance arguments. Both the external and internal anatomy of these specimens were investigated, which for the first time document many details of the auditory region of a Palaeogene litoptern. Our cladistic analysis, which included our new observations, failed to recover a monophyletic Litopterna but did not exclude it. A constrained analysis for the monophyly of this order showed that several features such as a (sub)quadrangular and anteroposteriorly elongated tensor tympani fossa and a large notch in the vicinity of the external opening of the cochlear canaliculus may constitute synapomorphies for Litopterna. The evolution of several other auditory characters amongst Litopterna is discussed and the relative dimensions of the inner ear and surrounding petrosal in the group were also investigated. This allowed detection of negative allometry of the bony labyrinth within the petrosal, which was confirmed by measurements and regression analysis across a larger sample of placental mammals. This scaling effect probably has an important influence on several characters of the bony labyrinth and petrosal, amongst which are the length of the vestibular aqueduct and cochlear canaliculus. It demonstrates that many aspects of the morphological variation of the bony labyrinth need to be thoroughly investigated before being incorporated into phylogenetic analyses. © 2015 The Linnean Society of London     

The ear ossicles and the evolution of the primate ear: A biomechanical approach

From a morphometric viewpoint the variability of human and other primate ear ossicles appears to be suitable for the study of taxonomic and phylogenetic distinction among Primates. It may also be of interest to determine whether they are useful to show differences in the perception of sound from the environment and from conspecifics. The energy transmitted through the ossicles is mantained by the action of different leverages. These modify the action of the ossicles from relatively wide, low energy, movements of the hammer to the smaller, high energy, movements of the stirrup. It seems that the pongid type of ossicle leverage combination saves more energy, possibly with a certain loss of subtle information, but this may be more useful in the wild than decoding voice modulation. The human type leverage, being less demultiplied, may produce a major loss of energy but, perhaps, a more precise conservation of sound information useful for speech communication.     

Morphological variation among the inner ears of extinct and extant baleen whales (Cetacea: Mysticeti)

Living mysticetes (baleen whales) and odontocetes (toothed whales) differ significantly in auditory function in that toothed whales are sensitive to high‐frequency and ultrasonic sound vibrations and mysticetes to low‐frequency and infrasonic noises. Our knowledge of the evolution and phylogeny of cetaceans, and mysticetes in particular, is at a point at which we can explore morphological and physiological changes within the baleen whale inner ear. Traditional comparative anatomy and landmark‐based 3D‐geometric morphometric analyses were performed to investigate the anatomical diversity of the inner ears of extinct and extant mysticetes in comparison with other cetaceans. Principal component analyses (PCAs) show that the cochlear morphospace of odontocetes is tangential to that of mysticetes, but odontocetes are completely separated from mysticetes when semicircular canal landmarks are combined with the cochlear data. The cochlea of the archaeocete Zygorhiza kochii and early diverging extinct mysticetes plot within the morphospace of crown mysticetes, suggesting that mysticetes possess ancestral cochlear morphology and physiology. The PCA results indicate variation among mysticete species, although no major patterns are recovered to suggest separate hearing or locomotor regimes. Phylogenetic signal was detected for several clades, including crown Cetacea and crown Mysticeti, with the most clades expressing phylogenetic signal in the semicircular canal dataset. Brownian motion could not be excluded as an explanation for the signal, except for analyses combining cochlea and semicircular canal datasets for Balaenopteridae. J. Morphol. 277:1599–1615, 2016. © 2016 Wiley Periodicals, Inc.     

Bony labyrinth morphometry reveals hidden diversity in lungless salamanders (Family Plethodontidae): Structural correlates of ecology,development, and vision in the inner ear

Lungless salamanders (Family Plethodontidae) form a highly speciose group that has undergone spectacular adaptive radiation to colonize a multitude of habitats. Substantial morphological variation in the otic region coupled with great ecological diversity within this clade make plethodontids an excellent model for exploring the ecomorphology of the amphibian ear. We examined the influence of habitat, development, and vision on inner ear morphology in 52 plethodontid species. We collected traditional and 3D geometric morphometric measurements to characterize variation in size and shape of the otic endocast and peripheral structures of the salamander ear. Phylogenetic comparative analyses demonstrate structural convergence in the inner ear across ecologically similar species. Species that dwell in spatially complex microhabitats exhibit robust, highly curved semicircular canals suggesting enhanced vestibular sense, whereas species with reduced visual systems demonstrate reduced canal curvature indicative of relaxed selection on the vestibulo‐ocular reflex. Cave specialists show parallel enlargement of auditory‐associated structures. The morphological correlates of ecology among diverse species reveal underlying evidence of habitat specialization in the inner ear and suggest that there exists physiological variation in the function of the salamander ear even in the apparent absence of selective pressures on the auditory system to support acoustic behavior.     

Evolutionary analysis of the middle and inner ear of Late Jurassic multituberculates

We describe three previously unreported specimens of petrosal bones of paulchoffatiid multituberculate mammals, collected from strata of Late Jurassic age in the Guimarota lignite mine of Leiria, west-central Portugal. The new fossils allow correction, supplementation, and confirmation of anatomical details, thus refining knowledge of general adaptation in the ear region among Jurassic multituberculates. Virtually all observed characters in the paulchoffatiid otic region are primitive relative to homologous features seen among Late Cretaceous and younger representatives of the Multituberculata; we recognize few unique otic specializations in paulchoffatiids that would preclude ancestry to later multituberculates. The plesiomorphic nature of paulchoffatiid ear regions provides no evidence in support of the hypothesis of a special, sister-group relationship between multituberculates and Late Cretaceous/Cenozoic marsupials plus placentals. Used in isolation, objective evidence derived from paulchoffatiid ear regions is consistent with interpretation of multituberculate divergence from other mammals predating the stem to living monotremes and postdating the stem to extinct morganucodontids. More broadly based comparative studies among Mesozoic mammals, however, suggest that independent acquisition of similarly advanced mammalian features was a pervasive theme among evolutionary histories of early mammals, probably including multituberculates. Although the phylogenetic position of multituberculates relative to other mammalian groups has yet to be unequivocally resolved, we suggest that a very early divergence of the group remains a distinct possibility.     

The braincase and middle ear region of Dendrerpeton acadianum (Tetrapoda: Temnospondyli)

Dendrerpeton acadianum from the Westphalian A (Upper Carboniferous) of Joggins, Nova Scotia, is a phylogenetically and chronologically early temnospondyl. Its external cranial anatomy has been used previously to suggest the presence of a tympanic membrane, and thus of an ear adapted to the perception of airborne sound. However, supporting evidence provided by stapedial and braincase morphology has so far been lacking. The braincase and middle ear region have remained almost wholly unknown. CT scanning and 3-D computer reconstruction of BMNH R.436 have been used to shed light on these important areas. Both stapes prove to be present in the specimen; the right stapes is distorted, but the left stapes lies inside the cranial cavity and is perfectly preserved. The latter resembles the stapes of the relatively few other temnospondyls in which the bone has been described and is most similar to that of Doleserpeton . The morphology and orientation of the stapes provide strong evidence for the presence of an ear adapted to the perception of airborne sound, with similarities to the extant anuran condition. The reconstructed braincase shows a high degree of similarity to that of other adequately known temnospondyls. This gives supporting evidence that D. acadianum is correctly placed in the temnospondyl phylogeny and thus demonstrates one of the earliest hearing systems adapted to the perception of airborne sound that can be homologized with the extant anuran condition.  © 2005 The Trustees of the Natural History Museum, Zoological Journal of the Linnean Society , 2005, 143 , 577−597.     

Extracellular nucleotide signaling in the inner ear

Extracellular nucleotides, particularly adenosine 5′-triphosphate (ATP), act as signaling molecules in the inner ear. Roles as neurotransmitters, neuromodulators, and as autocrine or paracrine humoral factors are evident. The diversity of the signaling pathways for nucleotides, which include a variety of ATP-gated ion channels (assembled from different subtypes of P2X-receptor subunit) and also different subtypes of G protein-coupled nucleotide receptors (P2Y receptors) supports a major physiological role for ATP in the regulation of hearing and balance. Almost invariably both P2X and P2Y receptor expression is apparent in the complex tissue structures associated with the inner-ear labyrinth. However P2X-receptor expression, commonly associated with fast neurotransmission, is apparent not only with the cochlear and vestibular primary afferent neurons, but also appears to mediate humoral signaling via ATP-gated ion channel localization to the endolymphatic surface of the cochlear sensory epithelium (organ of Corti). This is the site of the sound-transduction process and recent data, including both electrophysiological, imaging, and immunocytochemistry, has shown that the ATP-gated ion channels are colocalized here with the mechano-electrical transduction channels of the cochlear hair cells. In contrast to this direct action of extracellular ATP on the sound-transduction process, an indirect effect is apparent via P2Y-receptor expression, prevalent on the marginal cells of the stria vascularis, a tissue that generates the standing ionic and electrical gradients across the cochlear partition. The site of generation of these gradients, including the dark-cell epithelium of the vestibular labyrinth, may be under autocrine or paracrine regulation mediated by P2Y receptors sensitive to both purines (ATP) and pyrimidines such as UTP. There is also emerging evidence that the nucleoside adenosine, formed as a breakdown product of ATP by the action of ectonucleotidases and acting via P1 receptors, is also physiologically significant in the inner ear. P1-receptor expression (including A₁, A₂, and A₃ subtypes) appear to have roles associated with stress, acting alongside P2Y receptors to enhance cochlear blood flow and to protect against the action of free radicals and to modulate the activity of membrane conductances. Given the positioning of a diverse range of purinergic-signaling pathways within the inner ear, elevations of nucleotides and nucleosides are clearly positioned to affect hearing and balance. Recent data clearly supports endogenous ATP- and adenosine-mediated changes in sensory transduction via a regulation of the electrochemical gradients in the cochlea, alterations in the active and passive mechanical properties of the cells of the sensory epithelium, effects on primary afferent neurons, and control of the blood supply. The field now awaits conclusive evidence linking a physiologically-induced modulation of extracellular nucleotide and nucleoside levels to altered inner ear function.     

A comparison of the external morphology of the membranous inner ear in elasmobranchs

Studies on the elasmobranch inner ear have focused predominantly on a small group of sharks, particularly, carcharhinids. As a result, subsequent studies in other species have subdivided species into two main groups: those typical and those atypical of carcharhinid sharks. This study proposes a different set of inner‐ear morphology groupings to those previously suggested. The inner ears from 17 species of elasmobranchs (representing both sharks and rays) are examined in this study and based on morphometric data some groups include both rays and sharks. Four groups are now proposed based predominantly on the shape and dimensions of the membranous otoconial organs, and characteristics of the semicircular canals. Evident morphological differences between the ear types belonging to the new groups include the membranes of the semicircular canals being bound to the otoconial organs in some species, while only being connected via the canal ducts in others, as well as clear variation present in saccular organ size. Previous studies examining variation in the inner ear have attributed differences to either phylogeny or functional significance. Results from this study suggest that neither phylogeny nor feeding strategy solely accounts for the morphological diversity present in the external morphology of the elasmobranch inner ear. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

The periotic of Moeritherium (Mammalia, Proboscidea): homology or homoplasy in the ear region of Tethytheria McKenna, 1975?

The periotic of Moeritherium is described for the first time. A number of potentially autapomorphic features are identified; however, in common with living elephants and seacows the moerithere periotic is shown to lack the fenestra cochleae and aqueductus cochleae typical of therian mammals. Instead, it possesses a secondarily undivided perilymphatic foramen, a feature considered to be a synapomorphy uniting Proboscidea and Sirenia within the Tethytheria. The supposedly more derived fossil proboscidean, Mimidotherium , along with the primitive fossil sirenian Prorastomus , possess the typical therian pattern of openings to the pars cochlearis of the periotic. It is therefore unclear whether the condition in Recent tethytheres is homologous or independently derived. It is argued that the presence in Moeritherium of a suite of periotic characters more derived than those in Mimidotherium undermines the primitive status of moeritheres relative to numidotheres and all other Proboscidea, and therefore weakens the hypothesis of a secondary reversal to a more primitive auditory region in Numidotheriurn. The biological role of auditory specializations in Recent tethytheres is shown to have been very different, and it is argued that this functional disparity extends to the most primitive members of each order. Demonstrable homoplasy in structure and lack of functional congruence in basal members of both Sirenia and Proboscidea are deemed to be indicative of an independent acquisition of similar structures in the ear region of Recent tethytheres.     

Sexual dimorphism of the bony labyrinth: A new age‐independent method

Currently in physical anthropology there is a need for reliable methods of sex estimation for immature individuals and highly fragmented remains. This study develops a sex estimation technique from discriminant function analysis of the bony labyrinth as it matures before puberty and can survive taphonomic conditions that would destroy most other skeletal material. The bony labyrinth contains the organs of hearing and balance. For this reason biologists and paleoanthropologists have undertaken research in this area to understand evolutionary changes in locomotion. Prior studies have found clear differences between species, but within‐species variation has not been satisfactorily investigated. 3D segmentations of the left and right labyrinths of 94 individuals from a Cretan collection were generated and measured. Mean measurements of height, width, size, and shape indices were analyzed for sexual dimorphism, bilateral asymmetry, and measurement error. Significant sexual dimorphism was detected for several measurements. For sex estimation, the single best variable was the radius of curvature of the posterior semicircular canal, which achieved 76% accuracy. Two multivariate functions increased accuracy to 84%. Although these equations are less accurate than equations for complete long bones and crania, they appear to be as accurate as or better than other techniques for sexing immature individuals and temporal bones. Am J Phys Anthropol 151:290–301, 2013. © 2013 Wiley Periodicals, Inc.     

The homeobox gene Emx2 underlies middle ear and inner ear defects in the deaf mouse mutant pardon

The semi-dominantly inherited mouse mutation pardon (Pdo) was isolated due to the lack of a Preyer reflex (ear flick) in response to sound from a large-scale N-ethyl-N-nitrosourea (ENU) mutagenesis programme. Dissection of the middle ear revealed malformations in all three ossicles, rendering the ossicular chain incomplete. Hair cell counts in the apical turn of the organ of Corti revealed a significant 22.7% increase in the number of outer hair cells. Raised compound action potential thresholds in Pdo/+ mutants suggested a combined sensorineural/conductive hearing loss. We show that a missense mutation in the homeobox gene Emx2 is responsible for these defects, identifying a new function for this gene in the development of specific structures in the ear.     

Remarks on the inner ear of elasmobranchs and its interpretation from skeletal labyrinth morphology.

The structure and function of the craniate inner ear is reviewed, with 33 apomorphic characters of the membranous labyrinth and associated structures identified in craniates, gnathostomes, and elasmobranchs. Elasmobranchs are capable of low-frequency semi-directional phonoreception, even in the absence of any pressure-to-displacement transducer such as ear ossicles. The endolymphatic (parietal) fossa, semicircular canals, and crista (macula) neglecta are all adapted toward phonoreception. Some (but not all) of the morphological features associated with phonoreception can be inferred from the elasmobranch skeletal labyrinth. Endocranial spaces such as the skeletal labyrinth also provide suites of morphological characters that may be incorporated into phylogenetic analyses, irrespective of how closely these spaces reflect underlying soft anatomy. The skeletal labyrinths of Squalus and Notorynchus are compared using silicone endocasts and high-resolution CT-scanning. The latter procedure offers several advantages over other techniques; it is more informative, nondestructive, preserves relationships of surrounding structures, and it can be applied both to modern and fossil material.     

A potential link between lateral semicircular canal orientation,head posture,and dietary habits in extant rhinos (Perissodactyla,Rhinocerotidae)

Extant rhinoceroses share the characteristic nasal horn, although the number and size of horns varies among the five species. Although all species are herbivores, their dietary preferences, occipital shapes, and common head postures vary. Traditionally, to predict the “usual” head posture (the most used head posture of animals during normal unstressed activities, i.e., standing) of rhinos, the occipital shape was used. While a backward inclined occiput implies a downward hanging head (often found in grazers), a forward inclined occiput is related to the horizontal head posture in browsing rhinos. In this study, the lateral semicircular canal (LSC) of the bony labyrinth was virtually reconstructed from µCT‐images in order to investigate a possible link between LSC orientation and head posture in extant rhinoceroses. The usual head posture was formerly reconstructed for several non‐rhinoceros taxa with the assumption that the LSC of the inner ear is held horizontal (parallel to the ground) during normal activity of the living animal. The current analysis of the LSC orientation resulted in a downward inclined usual head posture for the grazing white rhinoceros and a nearly horizontal head posture in the browsing Javan rhinoceros. The other three browsing or mixed feeding species show subhorizontal (closer to horizontal than a downgrade inclination) head postures. The results show that anatomical and behavioral aspects, like occipital shape, presence and size of horns/tusk‐like lower incisors, as well as feeding and feeding height preferences influence the usual head posture. Because quantitative behavioral data are lacking for the usual head postures of the extant rhinos, the here described relationship between the LSC orientation and the resulting head posture linked to feeding preferences gives new insights. The results show, that the inner ear provides additional information to interpret usual head postures linked to feeding preferences that can easily be adapted to fossil rhinoceroses.