Evolutionary Paths to Mammalian Cochleae

Manley, Geoffrey A.

doi:10.1007/s10162-012-0349-9

Cited by 69 publications

(64 citation statements)

References 72 publications

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“…In the inner ear of vertebrates, the five vestibular end organs devoted to equilibration (utricle, saccule, and three semicircular canals) have remained fairly constant during evolution, whereas the auditory organ has undergone substantial changes that ultimately led to the emergence of the mammalian cochlea containing the electromotile outer hair cells (3,18) (Fig. 1 A and E).…”

Section: Differential Distribution Of Spectrin βV In Amphibian and Mamentioning

confidence: 99%

“…The cochlear outer hair cells are unique to mammals, but the existence of somatic electromotility in nonmammalian species has been a matter of debate (2,3,13). Indeed, it has been suggested that a prestin-dependent amplification mechanism also exists in the chicken auditory short hair cells, which could be correlated with the presence of prestin in the plasma membrane of their apical circumference (12).…”

Section: And Ref 30)mentioning

confidence: 99%

“…unconventional spectrins | inner ear | F-actin cytoskeleton | cortical lattice | phylogenetics T he response of the mammalian auditory organ (cochlea) to acoustic stimuli in an extended frequency range (including high frequencies) has remarkable properties including very high sensitivity and exquisitely sharp tuning (1)(2)(3). These properties are the consequence of an evolutionary process that involved major morphological and functional changes.…”

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Spectrin βV adaptive mutations and changes in subcellular location correlate with emergence of hair cell electromotility in mammalians

Cortese

Papal

Pisciottano

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The remarkable hearing capacities of mammals arise from various evolutionary innovations. These include the cochlear outer hair cells and their singular feature, somatic electromotility, i.e., the ability of their cylindrical cell body to shorten and elongate upon cell depolarization and hyperpolarization, respectively. To shed light on the processes underlying the emergence of electromotility, we focused on the βV giant spectrin, a major component of the outer hair cells' cortical cytoskeleton. We identified strong signatures of adaptive evolution at multiple sites along the spectrin-βV amino acid sequence in the lineage leading to mammals, together with substantial differences in the subcellular location of this protein between the frog and the mouse inner ear hair cells. In frog hair cells, spectrin βV was invariably detected near the apical junctional complex and above the cuticular plate, a dense F-actin meshwork located underneath the apical plasma membrane. In the mouse, the protein had a broad punctate cytoplasmic distribution in the vestibular hair cells, whereas it was detected in the entire lateral wall of cochlear outer hair cells and had an intermediary distribution (both cytoplasmic and cortical, but restricted to the cell apical region) in cochlear inner hair cells. Our results support a scenario where the singular organization of the outer hair cells' cortical cytoskeleton may have emerged from molecular networks initially involved in membrane trafficking, which were present near the apical junctional complex in the hair cells of mammalian ancestors and would have subsequently expanded to the entire lateral wall in outer hair cells.unconventional spectrins | inner ear | F-actin cytoskeleton | cortical lattice | phylogenetics T he response of the mammalian auditory organ (cochlea) to acoustic stimuli in an extended frequency range (including high frequencies) has remarkable properties including very high sensitivity and exquisitely sharp tuning (1-3). These properties are the consequence of an evolutionary process that involved major morphological and functional changes. One of them is the emergence, in the cochlea, of the outer hair cells, a unique type of specialized sensory cells that display somatic electromotility, i.e., they undergo periodic length changes in response to the oscillation of their membrane potential evoked by the sound wave (they shorten upon depolarization and elongate upon hyperpolarization) (SI Appendix, Fig. S1 A-C). This process has endowed the mammalian auditory organ with a singular mechanism of spectral analysis of the acoustic stimulus through frequencyselective mechanical amplification (1-3), whereas spectral analysis in other vertebrates (fish, amphibians, reptiles, and birds) primarily relies on electrical tuning of the hair cells (4, 5).An intriguing question is how the emergence of somatic electromotility is related with the evolution of individual proteins involved in this process. The electromotility of outer hair cells critically depends on the presence, in th...

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Section: Differential Distribution Of Spectrin βV In Amphibian and Mamentioning

confidence: 99%

Section: And Ref 30)mentioning

confidence: 99%

mentioning

confidence: 99%

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Spectrin βV adaptive mutations and changes in subcellular location correlate with emergence of hair cell electromotility in mammalians

Cortese

Papal

Pisciottano

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Evolution of the auditory system has seen a major reinterpretation in the last 20 years or so [Clack, 1997;Carr and Soares, 2002;Manley, 2012;Nothwang, 2016]. It is now agreed that the auditory endorgans (amphibian papilla, basilar papilla or organ of Corti) of the different groups of land vertebrates diverged during a long period of independent evolution.…”

Section: Introductionmentioning

confidence: 99%

Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear

et al. 2018

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The ear of extant vertebrates reflects multiple independent evolutionary trajectories. Examples include the middle ear or the unique specializations of the mammalian cochlea. Another striking difference between vertebrate inner ears concerns the differences in the magnitude of the endolymphatic potential. This differs both between the vestibular and auditory part of the inner ear as well as between the auditory periphery in different vertebrates. Here we provide a comparison of the cellular and molecular mechanisms in different endorgans across vertebrates. We begin with the lateral line and vestibular systems, as they likely represent plesiomorphic conditions, then review the situation in different vertebrate auditory endorgans. All three systems harbor hair cells bathed in a high (K⁺) environment. Superficial lateral line neuromasts are bathed in an electrogenically maintained high (K⁺) microenvironment provided by the complex gelatinous cupula. This is associated with a positive endocupular potential. Whether this is a special or a universal feature of lateral line and possibly vestibular cupulae remains to be discovered. The vestibular system represents a closed system with an endolymph that is characterized by an enhanced (K⁺) relative to the perilymph. Yet only in land vertebrates does (K⁺) exceed (Na⁺). The endolymphatic potential ranges from +1 to +11 mV, albeit we note intriguing reports of substantially higher potentials of up to +70 mV in the cupula of ampullae of the semicircular canals. Similarly, in the auditory system, a high (K⁺) is observed. However, in contrast to the vestibular system, the positive endolymphatic potential varies more substantially between vertebrates, ranging from near zero mV to approximately +100 mV. The tissues generating endolymph in the inner ear show considerable differences in cell types and location. So-called dark cells and the possibly homologous ionocytes in fish appear to be the common elements, but there is always at least one additional cell type present. To inspire research in this field, we propose a classification for these cell types and discuss potential evolutionary relationships. Their molecular repertoire is largely unknown and provides further fertile ground for future investigation. Finally, we propose that the ultimate selective pressure for an increased endolymphatic potential, as observed in mammals and to a lesser extent in birds, is specifically to maintain the AC component of the hair-cell receptor potential at high frequencies. In summary, we identify intriguing questions for future directions of research into the molecular and cellular basis of the endolymph in the different compartments of the inner ear. The answers will provide important insights into evolutionary and developmental processes in a sensory organ essential to many species, including humans.

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“…While there are several characteristics in the postcranial skeleton unique to mammals, such as differentiation of the vertebral series, the shoulder girdle and the limb muscles to permit parasagittal gait and agile locomotion (Bramble & Jenkins, 1989), many distinctive osteological features are focussed in the cranial skeleton. For example, (i) a mediolaterally expanded braincase to accommodate an enlarged brain, (ii) fusion of the palatal processes of the premaxilla and maxilla to form a secondary bony palate separating the oral and nasal cavities, (iii) a unique middle and inner ear morphology capable of high-frequency sound detection, (iv) formation of a single bony housing (petrosal) for the inner ear, (v) an expanded, single bone (dentary) forming the lower jaw, (vi) a novel craniomandibular jaw joint formed by the squamosal and dentary, and (vii) a heterodont dentition differentiated into functional groups with a single (diphyodont) replacement phase between deciduous and permanent teeth (Kielan-Jaworowska, Cifelli & Luo, 2004;Kemp, 2005;Rowe, Macrini & Luo, 2011;Manley, 2012). The sequence of hard-tissue character transformations leading to the development of these characters is remarkably well documented in the fossil record, representing the evolution of a suite of correlated structural innovations rooted in modifications of the feeding and auditory systems (Allin & Hopson, 1992;Sidor & Hopson, 1998;Kemp, 2005;Luo, 2011).…”

Section: Introductionmentioning

confidence: 99%

Morphological evolution of the mammalian jaw adductor complex

et al. 2016

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The evolution of the mammalian jaw during the transition from non-mammalian synapsids to crown mammals is a key event in vertebrate history and characterised by the gradual reduction of its individual bones into a single element and the concomitant transformation of the jaw joint and its incorporation into the middle ear complex. This osteological transformation is accompanied by a rearrangement and modification of the jaw adductor musculature, which is thought to have allowed the evolution of a more-efficient masticatory system in comparison to the plesiomorphic synapsid condition. While osteological characters relating to this transition are well documented in the fossil record, the exact arrangement and modifications of the individual adductor muscles during the cynodont-mammaliaform transition have been debated for nearly a century.We review the existing knowledge about the musculoskeletal evolution of the mammalian jaw adductor complex and evaluate previous hypotheses in the light of recently documented fossils that represent new specimens of existing species, which are of central importance to the mammalian origins debate. By employing computed tomography (CT) and digital reconstruction techniques to create three-dimensional models of the jaw adductor musculature in a number of representative non-mammalian cynodonts and mammaliaforms, we provide an updated perspective on mammalian jaw muscle evolution.As an emerging consensus, current evidence suggests that the mammal-like division of the jaw adductor musculature (into deep and superficial components of the m. masseter, the m. temporalis and the m. pterygoideus) was completed in Eucynodontia. The arrangement of the jaw adductor musculature in a mammalian fashion, with the m. pterygoideus group inserting on the dentary was completed in basal Mammaliaformes as suggested by the muscle reconstruction of Morganucodon oehleri. Consequently, transformation of the jaw adductor musculature from the ancestral ('reptilian') to the mammalian condition must have preceded the emergence of Mammalia and the full formation of the mammalian jaw joint. This suggests that the modification of the jaw adductor system played a pivotal role in the functional morphology and biomechanical stability of the jaw joint.

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Evolutionary Paths to Mammalian Cochleae

Cited by 69 publications

References 72 publications

Spectrin βV adaptive mutations and changes in subcellular location correlate with emergence of hair cell electromotility in mammalians

Spectrin βV adaptive mutations and changes in subcellular location correlate with emergence of hair cell electromotility in mammalians

Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear

Morphological evolution of the mammalian jaw adductor complex

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