Evolution of the middle ear apparatus in Talpid moles

The middle ear structures of eight species of mole in the family Talpidae (Mammalia: Eulipotyphla) were studied under light and electron microscopy. Neurotrichus, Parascalops, and Condylura have a simple middle ear cavity with a loose ectotympanic bone, ossicles of a "microtype" morphology, and they retain a small tensor tympani muscle. These characteristics are ancestral for talpid moles. Talpa, Scalopus, Scapanus, and Parascaptor species, on the other hand, have a looser articulation between malleus and ectotympanic bone and a reduced or absent orbicular apophysis. These species lack a tensor tympani muscle, possess complete bullae, and extensions of the middle ear cavity pneumatize the surrounding basicranial bones. The two middle ear cavities communicate in Talpa, Scapanus, and Parascaptor species. Parascaptor has a hypertrophied malleus, a feature shared with Scaptochirus but not found in any other talpid genus. Differences in middle ear morphology within members of the Talpidae are correlated with lifestyle. The species with middle ears closer to the ancestral type spend more time above ground, where they will be exposed to high-frequency sound: their middle ears appear suited for transmission of high frequencies. The species with derived middle ear morphologies are more exclusively subterranean. Some of the derived features of their middle ears potentially improve low-frequency hearing, while others may reduce the transmission of bone-conducted noise. By contrast, the unusual middle ear apparatus of Parascaptor, which exhibits striking similarities to that of golden moles, probably augments seismic sensitivity by inertial bone conduction.     

Resolving the evolution of the mammalian middle ear using Bayesian inference

Background

The minute, finely-tuned ear ossicles of mammals arose through a spectacular evolutionary transformation from their origins as a load-bearing jaw joint. This involved detachment from the postdentary trough of the mandible, and final separation from the dentary through resorption of Meckel’s cartilage. Recent parsimony analyses of modern and fossil mammals imply up to seven independent postdentary trough losses or even reversals, which is unexpected given the complexity of these transformations. Here we employ the first model-based, probabilistic analysis of the evolution of the definitive mammalian middle ear, supported by virtual 3D erosion simulations to assess for potential fossil preservation artifacts.

Results

Our results support a simple, biologically plausible scenario without reversals. The middle ear bones detach from the postdentary trough only twice among mammals, once each in the ancestors of therians and monotremes. Disappearance of Meckel’s cartilage occurred independently in numerous lineages from the Late Jurassic to the Late Cretaceous. This final separation is recapitulated during early development of extant mammals, while the earlier-occurring disappearance of a postdentary trough is not.

Conclusions

Our results therefore suggest a developmentally congruent and directional two-step scenario, in which the parallel uncoupling of the auditory and feeding systems in northern and southern hemisphere mammals underpinned further specialization in both lineages. Until ~168 Ma, all known mammals retained attached middle ear bones, yet all groups that diversified from ~163 Ma onwards had lost the postdentary trough, emphasizing the adaptive significance of this transformation.

     

Probable diphyletic formation of the mammalian middle ear: Monotremata and Theria

The first steps in the formation of the middle ear of the mammalian type, with the tympanum and three auditory ossicles, have only been passed by higher cynodonts. They have an incipient malleus, which developed from the anterior process of the articulare rather than the retroarticular process, which is rudimentary in cynodonts. The tympanic bone is formed of the anterior projections of the angulare. In some gorgonopians, the retroarticular process is elongated and curved anteriorly, resembling the malleus of mammals; however, this is only convergent similarity.     

Ear ossicle morphology of the Jurassic euharamiyidan Arboroharamiya and evolution of mammalian middle ear

The middle ear bones of Mesozoic mammals are rarely preserved as fossils and the morphology of these ossicles in the earliest mammals remains poorly known. Here, we report the stapes and incus of the euharamiyidan Arboroharamiya from the lower Upper Jurassic (～160 Ma) of northern China, which represent the earliest known mammalian middle ear ossicles. Both bones are miniscule in relation to those in non‐mammalian cynodonts. The skull length/stapedial footplate diameter ratio is estimated as 51.74 and the stapes length as the percentage of the skull length is 4%; both numbers fall into the stapes size ranges of mammals. The stapes is “rod‐like” and has a large stapedial foramen. It is unique among mammaliaforms in having a distinct posterior process that is interpreted as for insertion of the stapedius muscle and homologized to the ossified proximal (stapedial) end of the interhyal, on which the stapedius muscle attached. The incus differs from the quadrate of non‐mammalian cynodonts such as morganucodontids in having small size and a slim short process. Along with lack of the postdentary trough and Meckelian groove on the medial surface of the dentary, the ossicles suggest development of the definitive mammalian middle ear (DMME) in Arboroharamiya. Among various higher‐level phylogenetic hypotheses of mammals, the one we preferred places “haramiyidans” within Mammalia. Given this phylogeny, development of the DMME took place once in the allotherian clade containing euharamiyidans and multituberculates, probably independent to those of monotremes and therians. Thus, the DMME has evolved at least three times independently in mammals. Alternative hypothesis that placed “haramiyidans” outside of Mammalia would require independent acquisition of the DMME in multituberculates and euharamiyidans as well as parallel evolution of numerous derived similarities in the dentition, occlusion pattern, mandibles, cranium, and postcranium between the two groups and between “haramiyidans” and other mammals. J. Morphol. 279:441–457, 2018. © 2016 Wiley Periodicals, Inc.     

Occurrence and distribution of calcitonin gene-related peptide in the mammalian respiratory tract and middle ear

Summary Nerve fibres displaying immunoreactivity to calcitonin gene-related peptide (CGRP) are abundantly distributed in the respiratory tract of man, dog, cat, guineapig, rat and mouse. Numerous fine, beaded CGRP fibres were seen in the middle ear mucosa, and a moderate supply was found in the ear drum. In the nasal mucosa and in the wall of the Eustachian tube CGRP fibres occurred around blood vessels, arteries in particular. A conspiciously rich supply of CGRP fibres was seen beneath and within the epithelium. In addition, a few fibres were seen in smooth muscle bundles and close to sero-mucous glands. In the tracheo-bronchial wall CGRP fibres were distributed beneath and within the epithelium, in vascular and non-vascular smooth muscle and sometimes close to small glands. A few CGRP-immunoreactive endocrine-like cells were, in addition, distributed in the tracheal epithelium of cat, rat and mouse. The trigeminal, spinal and nodose ganglia, studied in rats and guinea-pigs, harboured numerous CGRP-immunoreactive nerve cell bodies. The cervical sympathetic ganglia were devoid of immunoreactive neuronal perikarya. Surgical and chemical (6-hydroxydopamine treatment) sympathectomy did not affect the number and distribution of CGRP fibres. The distribution of CGRP fibres in the respiratory tract suggests that CGRP may take part in sensory transmission. In addition, CGRP may affect the regulation of local blood flow, smooth muscle tone and glandular secretion.     

Mammalian development does not recapitulate suspected key transformations in the evolutionary detachment of the mammalian middle ear

The ectotympanic, malleus and incus of the developing mammalian middle ear (ME) are initially attached to the dentary via Meckel''s cartilage, betraying their origins from the primary jaw joint of land vertebrates. This recapitulation has prompted mostly unquantified suggestions that several suspected—but similarly unquantified—key evolutionary transformations leading to the mammalian ME are recapitulated in development, through negative allometry and posterior/medial displacement of ME bones relative to the jaw joint. Here we show, using µCT reconstructions, that neither allometric nor topological change is quantifiable in the pre-detachment ME development of six marsupials and two monotremes. Also, differential ME positioning in the two monotreme species is not recapitulated. This challenges the developmental prerequisites of widely cited evolutionary scenarios of definitive mammalian middle ear (DMME) evolution, highlighting the requirement for further fossil evidence to test these hypotheses. Possible association between rear molar eruption, full ME ossification and ME detachment in marsupials suggests functional divergence between dentary and ME as a trigger for developmental, and possibly also evolutionary, ME detachment. The stable positioning of the dentary and ME supports suggestions that a ‘partial mammalian middle ear’ as found in many mammaliaforms—probably with a cartilaginous Meckel''s cartilage—represents the only developmentally plausible evolutionary DMME precursor.     

Isolation of Streptobacillus moniliformis from the middle ear of rats.

Streptobacillus moniliformis was isolated from the middle ear of 9 of 16 rats used for otological studies. Examination of rat sera for the presence of anti-Streptobacillus moniliformis antibodies using an ELISA technique resulted in 15 seropositive animals. The source of the S. moniliformis infection was not determined.     

Variations in the middle ear of the Mammalia

The comparative morphology of mammalian middle ear structures has been studied by examining the histological sections of the ears of 144 specimens of mammals which had been collected, with a few exceptions, in two expeditions to the Caribbean area. Fifty-four species of six orders of mammals were represented. Sixteen structural features or relationships were specifically studied and the bearing of taxonomic groupings on the variability was analysed.
A taxonometric analysis using these middle ear features indicated that Microdipodops may lie nearer to Dipodomys than to Perognathus.
A table presenting the detailed results has been deposited with the British Museum (Natural History).     

Operations on the middle ear and mastoid

From 1953 to 1957, inclusive, 373 patients were operated on for chronic mastoid disease at the Mayo Clinic. Mainly because of the extensive use of magnifying glasses and microscopes, through these years, closer attention has been given to the preservation or improvement of hearing by meticulous procedures on the structures of the middle ear and the use of skin grafts. It is stressed, however, that it is extremely important to eradicate the underlying disease. Illustrative cases to represent different types of procedures are presented. The author recommends closer attention to the condition of the round window in the future.     

The mechanism of the middle ear: Part II. The drum

The ear drum is considered to be a thin circular membrane with radial and circular fibers, whose center is pulled inwards by the handle of the hammer. It is shown that such a membrane is equivalent to a rigid piston connected by a lever to the handle of the hammer, and subjected to elastic forces. The stability of the equivalent system is great, and the flexibility of the lever is very small. The lever is such that small pressures in the auditory canal are transformed into larger forces on the hammer. The leverage ratio increases with the tension of the tensor tympani and decreases with the number of circular fibers.     

The middle ear in the ontogenesis of mammals

The middle ear in mammals is characterized by structural variations and a broad spectrum of adaptive transformations related to peculiarities of species ecology, but it preserves the general basic principle of structure in most mammals. In species remote from a phylogenetic point of view but close in ecologic specialization, features of parallelism are observed concerning the development of separate elements of auditory ossicles as well as the way of their interconnection and attachment to the tympanum. Along the way to the adaptation to the water lifestyle in semi-aquatic and aquatic species, new additional structures, not intrinsic to initial terrestrial forms, have been formed. The use of ecological and morphological approaches to research the peripheral division of the auditory system of mammals with different ecological specialization in the ontogenesis permitted us to reveal that peculiarities of its structure in different groups of mammals are preconditioned by the animals’ adaptation to specific acoustic properties of their environment. Morphological and functional adaptations of the peripheral auditory system aimed at optimizing auditory sensitivity in the environments differing in physical properties are of great importance in evolution. Adaptive specific features in the structure of the middle ear in aquatic species appear at early stages of development in spite of intrauterine growth without the direct influence of environmental conditions.     

The ossified Meckel's cartilage and internal groove in Mesozoic mammaliaforms: implications to origin of the definitive mammalian middle ear

The ossified Meckel's cartilage is described in detail from three adult individuals of two triconodont mammals, Repenomamus and Gobiconodon , which have been discovered in the Lower Cretaceous of Liaoning, China. A possible ossified Meckel's cartilage has also been recognized in the Early Cretaceous symmetrodont Zhangheotherium from Liaoning. The rod-like ossified Meckel's cartilage in Repenomamus bridges the dentary and the ear region of the cranium. Its shape and position are similar to those of Meckel's cartilage in prenatal and in some postnatal extant mammals. The ossified Meckel's cartilage may have functioned as an attachment site for the medial pterygoid muscle. These specimens provide direct evidence for the function of the internal groove which is commonly present in the dentary of early mammals and their relatives. The evidence weakens the hypothesis of multiple origins for the definitive mammalian middle ear. It supports the assumption that a persistent or ossified Meckel's cartilage has been present in adults of the common ancestor of mammals. The new evidence of Repenomamus does not support the model in which brain expansion and negative allometry of the auditory chain are primarily responsible for the detachment of ear ossicles in mammalian ontogeny and evolution. An alternative hypothesis is proposed which does not require brain expansion as the initial factor for the detachment of ear ossicles during mammalian evolution. © 2003 The Linnean Society of London. Zoological Journal of the Linnean Society , 2003, 138 , 431–448.