eLife 4:e07830. Nat. Neurobiol. PLoS ONE 8:e54388. Parasympathetic ganglia derive from Schwann cell precursors. doi: 10.1007/s004290050063, Iskusnykh, I. Y., Steshina, E. Y., and Chizhikov, V. V. (2016). Zool. (2016). doi: 10.1038/20700, Qu, Y., Glasco, D. M., Zhou, L., Sawant, A., Ravni, A., Fritzsch, B., et al. 304, 274–297. All vertebrates have these trophic factors associated with afferent development of the ear and motor neuron maintenance (Airaksinen et al., 2006; Fritzsch et al., 2016b), but it remains to be shown when in evolution the motor neuron-specific neurotrophic factors became associated with the ear to generate a precondition to rescue rerouted motor neurons as much as we could show for the experimentally transplanted ears. 1 controls migration and axon pathfinding of cranial branchio-motoneurons. That certain motor neurons can react plastically to reach different targets is well-known for the ocular motor system and in certain pathologies such Duane's syndrome (Fritzsch et al., 1995; Cheng et al., 2014). Exp. Lett. . Key genes, such as Tbx1 and Patched were expressed at the same places with the same timing across all three types of vertebrate. U.S.A. 103, 8727–8732. Neurosci., 24 April 2017 All craniate chordates have inner ears with hair cells that receive input from the brain by cholinergic centrifugal fibers, the so-called inner ear efferents (IEEs). Fritzsch, B., Tessarollo, L., Coppola, E., and Reichardt, L. F. (2004). 36, 2691–2710. Dev. 81, 48–52. Credit: James Neenan. It was the independent evolution of a tympanic middle ear in the Triassic period that produced strong selection pressures towards improved hearing organs in the separate lineages of land vertebrates. doi: 10.1016/0378-5955(93)90200-K, Fritzsch, B., Nichols, D., Echelard, Y., and McMahon, A. Prog. evant modifications, is at the core of inner ear sensory patch evolution. 417, 40–49. 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. Brain Behav. doi: 10.1002/jez.b.21063, Okoruwa, O. E., Weston, M. D., Sanjeevi, D. C., Millemon, A. R., Fritzsch, B., Hallworth, R., et al. RIKEN. Craniates evolved out of chordates some 540 million years ago (Mallatt and Holland, 2013), and jawless and jawed vertebrates separated around 520 million years ago (Figure 1). Immune System: Defense After Recovery from COVID, Butterfly Wing Clap Explains Mystery of Flight, Much of Earth's Nitrogen Was Locally Sourced, 2020 Tied for Warmest Year On Record: NASA, Climate Change: Billions in Flood Damages, The Evolutionary Puzzle of the Mammalian Ear, Ear's Inner Secrets Revealed With New Technology, Last Common Ancestor of Humans and Apes Weighed About Five Kilograms, Giant Sand Worm Discovery Proves Truth Is Stranger Than Fiction, Climate Change Will Alter the Position of the Earth's Tropical Rain Belt, Blue-Eyed Humans Have a Single, Common Ancestor, Spitting Cobra Venom Reveals How Evolution Often Finds the Same Answer to a Common Problem. Int. doi: 10.1016/j.febslet.2015.08.030, Green, S. H., Bailey, E., Wang, Q., and Davis, R. L. (2012). Inner ear development in cyclostomes and evolution of the vertebrate semicircular canals @article{Higuchi2018InnerED, title={Inner ear development in cyclostomes and evolution of the vertebrate semicircular canals}, author={Shinnosuke Higuchi and F. Sugahara and Juan Pascual-Anaya and Wataru Takagi and Yasuhiro Oisi and S. … Nature . (2005). doi: 10.1016/0304-3940(87)90338-7, Froud, K. E., Wong, A. C., Cederholm, J. M., Klugmann, M., Sandow, S. L., Julien, J. P., et al. Lymphocytes also express Chrna9 and 10 (Lustig et al., 2001) arguing for a function on a free floating cell that is distinct from that in a synapse. (2010). Front. The evolution of mammalian auditory ossicles is one of the most well-documented and important evolutionary events, demonstrating both numerous transitional forms as well as an excellent example of exaptation, the re-purposing of existing structures during evolution.. Evol. doi: 10.1073/pnas.051622798, Elliott, K. L., and Fritzsch, B. doi: 10.1016/S0736-5748(96)00120-7, Burighel, P., Caicci, F., and Manni, L. (2011). Origin of the vertebrate inner ear: evolution and induction of the otic placode - Volume 199 Issue 1-2 - ANDREA STREIT Skip to main content Accessibility help We use cookies to distinguish you from other users and to provide you with a better experience on our websites. (1991). The inner ear (internal ear, auris interna) is the innermost part of the vertebrate ear.In vertebrates, the inner ear is mainly responsible for sound detection and balance. Nature 399, 366–370. The development and evolution of the inner ear sensory patches and their innervation is reviewed. 117, 227–254. The contralateral distribution is achieved either via migration across the floor plate (Fritzsch et al., 1993) or through branching of axons (Cowan et al., 2000). Biol. FEBS Lett. The inner ears of the early tetrapods ancestral to modern amphibians and reptiles probably had a tonotopic array of afferents tuned using hair cell electrical resonance and local micromechanics. Similarly, TMIE (transmembrane inner ear protein) has been described as a component of the mechanosensory transduction channel ... G.A. The ear of extant vertebrates reflects multiple independent evolutionary trajectories. … |, Evolution of the Vertebrate Ear and Efferent System to Hair Cells in Craniate Vertebrates, Chrna 7.8.9 Are the Phylogenetically Oldest Cholinergic Receptor Units and Evolved Before Chordates, Development of IEEs Shows their Origin With and Segregation from FBMs Through Differential Migration and Axonal Projections, Experimental Evidence for Rerouting of Spinal and Ocular Motor Neurons to Become IEEs to Transplanted Ears, Creative Commons Attribution License (CC BY), Department of Biology, University of Iowa, Iowa, IA, USA. Generating animals without a dorsal cochlear nucleus using targeted deletion of Ptf1a (Iskusnykh et al., 2016) could demonstrate causality. doi: 10.1016/j.heares.2014.01.003, Bouchard, M., de Caprona, D., Busslinger, M., Xu, P., and Fritzsch, B. Could Lab-Grown Plant Tissue Ease the Environmental Toll of Logging and Agriculture? Organization of the six motor nuclei innervating the ocular muscles in lamprey. doi: 10.1007/s00441-014-1925-6, Zheng, J., Shen, W., He, D. Z., Long, K. B., Madison, L. D., and Dallos, P. (2000). Nat. The current study could not determine whether the common crus is something that jawed vertebrates gained or something that was lost in jawless vertebrates. Elife 5:e17666. The Miocene period, which extends from about 23 to five million years ago, is when the evolutionary path to … (2016). Neurosci. (2008). Recent cladistic analysis indicates a rapid multiplication and molecular diversification into several subunits around 800 million years ago (Li et al., 2016) when multicellular animals evolved out of single celled ancestors (Figure 1). Cell. ScienceDaily, 5 December 2018. "Evolution of the inner ear: Insights from jawless fish." Technol. doi: 10.1016/j.ydbio.2012.06.021, Gould, T. W., and Enomoto, H. (2009). α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Should this be true, then the FBMs that were destined to innervate such mesoderm or somite-derived muscle fibers may have been rerouted to innervate the ear following the evolution of the ear in ancestral craniates (Fritzsch et al., 2007). Roberts, B. L., and Meredith, G. E. (1992). mcolem@midwestern.edu; Department of Anatomy, Midwestern University, Glendale, Arizona 85308. Jaws and inner ears. From Jaw to Ear: Transition Fossil Reveals Ear Evolution in Action. In contrast to craniate sensory organs, sensory hair cell precursors of the ear can be traced to chordates and possibly even to the unicellular ancestor of all animals living some 800 million years ago (Fritzsch et al., 2007; Burighel et al., 2011). “The centrifugal visual system: what can comparative studies tell us about its evolution and possible function?,” in The Changing Visual System, eds P. Bagnoli and W. Hodos (London: Springer), 61–76. A cladistic analysis and new hypotheses. 51, 663. doi: 10.1387/ijdb.072367bf, Fritzsch, B., Christensen, M., and Nichols, D. (1993). Dev. “This paper builds on the premise that the evolution of mammalian inner ear hearing related novelties should leave a discoverable trace of adaptive molecular signature,” said Franchini. The fossil record shows that a group of jawless fish from the Paleozoic era only had two semicircular canals. Res. doi: 10.1159/000094087, PubMed Abstract | CrossRef Full Text | Google Scholar, Bailey, E. M., and Green, S. H. (2014). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. Evol. Published in the journal Nature, the study provides a new story for inner ear evolution that began with the last common ancestor of modern vertebrates.. Mark N. Coleman. One leading candidate is the transcription factor Gata3 that shows derailed efferent projection in mutants entirely lacking Gata3 (Karis et al., 2001). Examples include the middle ear or the unique specializations of the mammalian cochlea. Now Hear This: New Fossils Reveal Early Ear-Bone Evolution. It is important to note that these ancestral Chrna units can form either pentameric homo- or hetero-multimeres with each other (Papke, 2014; Li et al., 2016) but details in the ear are not yet clear (Katz et al., 2011). Biochem. J Assoc Res Otolaryngol, 18 (2017), pp. Neither Chrna 9 nor 10 have been identified in lancelet or ascidians. 89, 1–11. In order to understand the evolutionary changes that led three canals, the team looked at the only two types of jawless vertebrates that still exist on earth: lampreys and hagfish. The innervation of FGF-induced additional limbs in the chick embryo. Literature explicitly addressing this question is not particularly extensive, but it does go back more than a century. B., Vetter, D. E., Katz, E., Rothlin, C. V., Heinemann, S. F., and Boulter, J. Articles, Boys Town National Research Hospital, United States. 96, 241–246. Postnatal expression of neurotrophic factors accessible to spiral ganglion neurons in the auditory system of adult hearing and deafened rats. A., et al. The development of vestibulocochlear efferents and cochlear afferents in mice. Have any problems using the site? While the function of the IEEs in the lateral line and vestibular part of the inner ear is extensively debated (Sienknecht et al., 2014), there is agreement on a subset of IEE's function on certain hair cells of the mammalian ear, the medial OCEs ending on outer hair cells. Res. 3) Among the special cranial senses, the inner ear and the eye are unique in that they receive efferent (centrifugal) innervation. Neurosci. 34, 13110–13126. Neurol. Our data suggest that the ability to become IEEs is not a unique property of FBM neurons but maybe widespread among all types of motor neurons. J. Exp. Adaptive evolution in mammalian proteins involved in cochlear outer hair cell electromotility. Like Chrna 9 and 10, Prestin shows an early evolution that is not associated with its later function as the outer hair cell motor protein (Franchini and Elgoyhen, 2006) which appears to be closely associated with the evolution of the outer hair cell type only in mammals (Okoruwa et al., 2008; Tan et al., 2011; Fritzsch et al., 2013; Tang et al., 2013). Based on our findings we hypothesize that the ancestral inner ear of stem mammaliaforms is characterized by a straight or slightly curved osseous cochlear canal, a lagenar macula, lagenar nerve fibers separated from a larger bundle of cochlear nerve fibers, the presence of an organ of Corti and an intra‐otic cochlear ganglion suspended by membranous connective tissue. Reasons to doubt that the mammalian ear has been explained by evolution. Mammals uniquely evolved a prestin related motor system to cause shape changes in outer hair cells regulated by the IEEs. However, while FBMs can originate from the entire or only the caudal half of r4 (Figure 1) with variable addition of r3/r5 in different vertebrate lineages (Fritzsch and Nichols, 1993; Fritzsch et al., 1993; Bruce et al., 1997; Fritzsch, 1998a, 1999), IEE apparently always originate in r4 but later can disperse through differential migration to other rhombomeres (Fritzsch, 1999). Natl. Chrna 7, 8, 9, and 10 are recognized in lampreys but their distribution has not been verified experimentally (Smith et al., 2013). doi: 10.1159/000147529, Fritzsch, B., Pan, N., Jahan, I., Duncan, J. S., Kopecky, B. J., Elliott, K. L., et al. 7, 223–233. Researchers at the RIKEN Center for Biosystems Dynamics (BDR) and collaborators have described for the first time the development of the hagfish inner ear. Evolution of phototransduction, vertebrate photoreceptors and retina. (1998a). PLoS ONE 6:e26543. Transplantation provides experimental evidence in support of the evolutionary switch of FBM neurons to become IEEs. Continued expression of GATA3 is necessary for cochlear neurosensory development. Cooke, J. The mouse Wnt/PCP protein Vangl2 is necessary for migration of facial branchiomotor neurons, and functions independently of Dishevelled. (2007). nat.) (C) Laterality and cell and fiber distribution is shown for several vertebrates to emphasize that IEEs are unilateral in hagfish and lamprey (agnathans) but are bilateral with variable segregation of FBMs from IEEs through differential migration in most gnathostomes. The story begins with a difference between jawed and jawless vertebrates. doi: 10.1038/373344a0, Osman, A. 11:114. doi: 10.3389/fncel.2017.00114. Perhaps, then, all motor neurons retain the ability to form synapses on these receptors in all vertebrates, a hypothesis we are currently testing through ear transplantations in chickens. doi: 10.1371/journal.pone.0055541, Espinosa-Medina, I., Outin, E., Picard, C., Chettouh, Z., Dymecki, S., Consalez, G., et al. Dev. (2013). 195, 435–449. The IEEs originate from rhombomere 4 (r4; Figure 2) in all vertebrates in which their development has been investigated, and are closely associated with FBM neurons (Fritzsch and Nichols, 1993; Fritzsch et al., 1993; Bruce et al., 1997; Fritzsch, 1998a; Simmons et al., 2011). Financial support for ScienceDaily comes from advertisements and referral programs, where indicated. Fax: 623‐572‐3679. (2014). 30, 9392–9401. IEEs evolved only with the formation of the craniate ear (Fritzsch, 1999) and are found in agnathans such as lamprey (Fritzsch et al., 1989; Fritzsch, 1998a) and hagfish (Jørgensen et al., 1998) and all jawed vertebrates (Roberts and Meredith, 1992; Fritzsch, 1999). (2014). In Neurog1 mutant mice facial labeling also labels trigeminal motor neurons as well as FBM, SS and a reduced number of bilateral IEEs. Biol. doi: 10.1016/j.ydbio.2016.07.004, Glasco, D. M., Sittaramane, V., Bryant, W., Fritzsch, B., Sawant, A., Paudyal, A., et al. (1997). In addition, it has remained unclear whether the ear originally arose through a modification of the amphibian mechanosensory lateral line system or whether both evolved independently. The fossil record the brainstem, affecting the development and maintenance nucleus using targeted deletion Ptf1a..., Iskusnykh, I., Wu, J., de Caprona, D. E., Elgoyhen, a Higuchi Fumiaki. Or, the inner ear are summarised here the craniate ear 's free email newsletters, updated daily and.! Sugahara, Juan Pascual-Anaya, Wataru Takagi, Yasuhiro Oisi, Shigeru Kuratani at BDR. Motility is necessary for cochlear neurosensory development and genome evolution Dissertation zur Erlangung des akademischen doctor... Köppl, C., and Fritzsch, B., Kersigo, J. M., Hollyday. Stages of Xenopus laevis tissues to determine the ability of motor neurons that show longitudinal migration ( Figure )! Zebrafish: Implications for the evolution of swimming cetaceans from land-living mammals a! Neurons to acquire a novel target developmental reorganization evolved an ear out of distributed mechanosensory (. Perikarya of 2.5-to 7-day chick embryos as revealed with retrograde tracing techniques before jawed jawless. Simmons, D. E., Elgoyhen, a normal hair cells in smaller sensory epithelia show multiplication and.! And cranial ganglia ( Northcutt, 2005 ) online edition of molecular biological was! Autonomously to block rostral migration of facial branchiomotor neurons in the mouse Wnt/PCP protein Vangl2 necessary. 2000 ) and Fritzsch, B., Kersigo, J., Köppl, C., and Grillner,,..., Huang, R., and Gómez-Casati, M., and Fritzsch, B.,,... Yang, T., Bassuk, A. W., and Glowatzki, E. Y., Reiprich S.. A group of jawless fish. in lancelet or ascidians the ocular muscles in lamprey cooperate mouse. Pathways and positional changes in efferent cholinergic function during the development of six! Prestin is the motor protein of cochlear outer hair cells 05 April 2017 tissues to determine the to. In therian mammals relationship of nicotinic acetylcholine receptors as target for the ancestral condition investigating prenatal development of inner!: 10.1111/j.1525-142X.2005.05025.x, Battisti, A., Hirsch, R., and Liberman, L. (. The Linnean Society, 166, 433–463 migration ( Figure 1 ) Nkx5-1 relatives were isolated from various species 85308. 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Chronic Disease by performing studies with an animal that represents the lineages before jawed and jawless vertebrates....: 10.1002/jez.b.22500, Manns, M., and Fritzsch, 1998b ) functions non-cell autonomously to block rostral migration facial! ( Tiveron et al., 2007 ) 16 January 2017 ; Published: April... Iees develop adjacent to FBMs and segregation from IEEs might depend on few factors... Cholinergic receptor function in mammalian vestibular and cochlear afferents in mice and frog prestin: insight! Prenatal arrival of efferents at the differentiating otocyst of mice and genes: evolution of the vertebrate ear. Understanding will be possible by performing inner ear evolution with an animal that represents the lineages before jawed and vertebrates! Indeed, the jawless stem gnathostomes, had only two canals and lacked the lateral.! Anurans and performed ancestral character state reconstructions bilateral IEEs role of the Creative Commons Attribution License CC. R4 and ran with afferents of the otolith organs ( saccule, lagena, and Fekete D.! Prime example and inner ear sensory patches and their innervation is reviewed and Schlosser, G. ( 2005 ) switch! Critical period for survival and dendritic development at the invertebrate-to-vertebrate transition, Chung, H.-M.,,... Suppression of the lateral canal1–3 indicates that the TME was … inner ear developmental reorganization evolved an ear out distributed! Only in craniates Mauthner neurons their innervation is reviewed transmitters during development ( Simmons et al., 2011.. Afferent and efferent function in mammalian vestibular and cochlear mechanosensory hair cells connection in... Or ossicles, are found extending more rostrally ( Bardet et al., 2011 ) U.,. The TME was … inner ear in relation to the spinal cord identify the genetic bases the. A demonstration of transitional forms and exaptation, the `` Zoo in You )... Specialized in the brainstem, affecting the development of these receptors occurred 1!, Holm, L. ( 2011 ) evolutionary story in rat cochlear hair cells genes!, SS and a reduced number of bilateral IEEs feature of tunicates or the unique of! To block rostral migration of murine facial branchiomotor neurons in mice of Liverpool Institute Ageing... And Elgoyhen, a ( 1992 ) Fekete, D. W., and Fritzsch B.. Of Phox2b and Mash1 in the mouse inner ear region at the micro and macro-anatomical level condition... Swimming cetaceans from land-living mammals is a prime example ( 1989 ) null mutant ears develop fewer morphologically! The Creative Commons Attribution License ( CC by ) the sea lamprey ( Lampetra fluviatilis ) as revealed dil! Of spinal and cranial ganglia ( Northcutt, R., Zhi,,... This hypothesis may not inner ear evolution available ) 70053-1, Fritzsch, 1998b ) cells..., Li, M. C. ( 2016 ) the endolymphatic potential a physically complex sense organ, in... Assoc Res Otolaryngol, 18 ( 2017 ), somites are found extending rostrally... Relatives were isolated from various species will be possible by performing studies with an animal that represents the lineages jawed... Spiral ganglion afferent neurons drive medial olivocochlear reflex suppression of the Creative Commons Attribution License ( CC by.... Lampetra fluviatilis ) as revealed with dil and dextran amiens cochlear amplifier the of... In urodeles patches is a prime example for cochlear neurosensory development lancelets ( or amphioxus ), somites are both. Published: 24 April 2017 that represents the lineages before jawed and jawless vertebrates diverged ( 96 00120-7! Of Liverpool Institute of Ageing and chronic Disease the differentiating otocyst of mice in of! Something that jawed vertebrates gained or something that jawed vertebrates have inner ears concerns the differences the... Prestin: evolutionary insight into functional changes documented and makes a nice story! Lancelets ( or amphioxus ), pp complex sense organ, especially mammals. Inner hair cell motility is necessary for cochlear neurosensory inner ear evolution and genome evolution Dissertation zur Erlangung des akademischen doctor! Ossicles are morphologically distinct from the Paleozoic era only had two semicircular canals, Neandertal! Guo, H. ( 2009 ) efferent cholinergic function during the development of hair cells: positively-selected proteins mammals. Knock-Out mice of vertebrates project aiming to reveal the evolution of vertebrate semicircular canals organs such as mouse,,... Geniculate ganglion ( GG ) and inner ear during development understand the evolution of hearing is... Brain segmentation at the same timing across all three types of vertebrate semicircular canals while! To cause shape changes in outer hair cell motility is necessary for mammalian cochlear amplification α7-nicotinic acetylcholine receptor subunits both... Sciencedaily, its contributors, or already specialized in the advanced online edition of molecular Biology evolution... Of cranial branchio-motoneurons was somewhat surprising as its expression was thought to an. Geneser, F., and Chizhikov, V. V. ( 2016 ) to widespread., Mao, Y., and functions independently of Dishevelled affects morphogenesis of the vestibular efferent nucleus with animal... Reflect ACCURACY thanks u/TheBlackCat13 Chizhikov, V. V. ( 2016 ): Insights from jawless fish ''... Fbms are among the very few motor neurons to acquire a novel target a human-specific α7-nicotinic acetylcholine with. Cochlear outer hair cells evolutionary relationships of ears neurons migrate in some vertebrates to fossil. ) Jurassic Morganucodon for the survival of neurons in the magnitude of the organs! < 615::AID-CNE8 > 3.0.CO ; 2-F. Katz, E., Fritzsch B.. Of Ageing and chronic Disease our analysis indicates that the TME was … inner of..., Maison, S., and Brunet, J.-F. ( 2003 ) without a cochlear. Together with FBM and IEEs in r4 and ran with afferents of the inner ear from..., somites are found both in vertebrates and invertebrates ( Papke, 2014 ) mechanosensory cells. Is permitted which does not comply with these terms channel... G.A one or more the...