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The Foundations of High-Frequency Hearing in Early Mammals

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Abstract

It has become common in the paleontological literature to assume that the presence of secondary bony laminae in the cochleae of early mammals indicates that these species were able to perceive high sound frequencies (>20 kHz). This review examines the validity of this idea in the context of comparative physiological data from extant amniotes and surveys a number of unique features of mammalian cochleae that correlate with high-frequency hearing. As it is difficult to imagine how all of these features could have arisen simultaneously, high-frequency hearing probably had a more gradual origin. This suggests that the presence or absence of secondary laminae should be interpreted with greater caution.

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References

  • Aitkin LM, Gates GR, Kenyon CE (1979) Some peripheral auditory characteristics of the marsupial brush-tailed possum, Trichosurus vulpecula. J Exp Zool 209:317–322

    Article  Google Scholar 

  • Arch VS, Grafe TU, Narins PM (2008) Ultrasonic signalling by a Bornean frog. Biol Lett 4:19–22

    Article  PubMed  Google Scholar 

  • Beurg M, Nam J-H, Crawford A, Fettiplace R (2008) The actions of calcium on hair bundle mechanics in mammalian cochlear hair cells. Biophys J 94:2639–2653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beurg M, Tan X, Fettiplace R (2013) A prestin motor in chicken auditory hair cells: active force generation in a nonmammalian species. Neuron 79:1–13

    Article  Google Scholar 

  • Bosher K, Warren RL (1978) Very low calcium content of cochlear endolymph, an extracellular fluid. Nature 273:377–378

    Article  CAS  PubMed  Google Scholar 

  • Coleman MN, Boyer DM (2012) Inner ear evolution in primates through the Cenozoic: implications for the evolution of hearing. Anat Rec 295:615–631

    Article  Google Scholar 

  • Corns LF, Johnson SL, Kros CJ, Marcotti W (2014) Calcium entry into stereocilia drives adaptation of the mechanoelectrical transducer current of mammalian cochlear hair cells. Proc Natl Acad Sci USA 111:14918–14923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dallos P (2008) Cochlear amplification, outer hair cells and prestin. Curr Opin Neurobiol 18:370–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies KTJ, Maryanto I, Rossiter SJ (2013) Evolutionary origins of ultrasonic hearing and laryngeal echolocation in bats inferred from morphological analyses of the inner ear. Frontiers Zool 10:2

    Article  Google Scholar 

  • Echteler SM, Fay RR, Popper AN (1994) Structure of the mammalian cochlea. In: Fay RR, Popper AN (eds) Comparative Hearing: Mammals. Springer, New York, pp 134–171

  • Ekdale EG (2013) Comparative anatomy of the bony labyrinth (inner ear) of placental mammals. PLoS One 8(6): e66624. doi:10.1371/journal.pone.0066624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ekdale EG (2016) Form and function of the mammalian inner ear. J Anat 228:324–337

    Article  PubMed  Google Scholar 

  • Fernandez C, Schmidt RS (1963) The opposum ear and evolution of the coiled cochlea. J Comp Neurol 121:151–159

    Article  CAS  PubMed  Google Scholar 

  • Fettiplace R, Crawford A C (1978) The coding of sound pressure and frequency in cochlear hair cells of the terrapin. Proc Roy Soc Lond B 203:209–218

    Article  CAS  Google Scholar 

  • Fettiplace R, Fuchs PA (1999) Mechanisms of hair cell tuning. Annu Rev Physiol 61:809–34

    Article  CAS  PubMed  Google Scholar 

  • Franchini LF, Elgoyhen AB (2006) Adaptive evolution in mammalian proteins involved in cochlear outer hair cell electromotility. Mol Phylogenet Evol 41:622–635

    Article  CAS  PubMed  Google Scholar 

  • Gans C, Wever EG (1976) The ear and hearing in Sphenodon punctatus. Proc Natl Acad Sci USA 73:4244–4246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gates GR, Saunders JC, Bock GR, Aitkin LM, Elliot MA (1974) Peripheral auditory function in the platypus, Ornithorhynchus anatinus. J Acoust Soc Amer 56: 152–156

    Article  CAS  Google Scholar 

  • Goodyear JG, Richardson GP (2002) Extracellular matrices associated with the apical surfaces of sensory epithelia in the inner ear: molecular and structural diversity. J Neurobiol 52: 212–227

    Article  Google Scholar 

  • Heffner RS, Heffner HE (1982) Hearing in the elephant (Elephas maximus): absolute sensitivity, frequency discrimination and sound localization. J Comp Physiol Psychol 96:926–944

    Article  CAS  PubMed  Google Scholar 

  • Heffner RS, Koay G, Heffner HE (2001) Audiograms of five species of rodents: implications for the evolution of hearing and the perception of pitch. Hear Res 157:138–152

    Article  CAS  PubMed  Google Scholar 

  • Hoffman S, O’Connor PM, Kirk EC, Wible JR, Krause DW (2014) Endocranial and inner ear morphology of Vintana sertichi (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar. J Vertebr Paleontol 34(6):110–136

    Article  Google Scholar 

  • Hudspeth AJ (2008) Making an effort to listen: mechanical amplification in the ear. Neuron 59:530–545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirk EC, Hoffmann S, Kemp AD, Krause DW, O'Connor PM (2014) Sensory anatomy and sensory ecology of Vintana sertichi (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar. J Vertebr Paleontol 36:203–222.

    Article  Google Scholar 

  • Köppl C (1997) Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. J Neurosci 17:3312–3321

    Article  PubMed  Google Scholar 

  • Köppl C, Manley GA (1992) Functional consequences of morphological trends in the evolution of lizard hearing organs. In: Fay RR, Popper AN, Webster DB (eds) The Evolutionary Biology of Hearing. Springer-Verlag, Heidelberg, pp 489–509

    Chapter  Google Scholar 

  • Kronester-Frei A (1979) The effect of changes in endolymphatic ion concentrations on the tectorial membrane. Hear Res 1:81–94

    Article  CAS  PubMed  Google Scholar 

  • Ladhams A, Pickles JO (1996) Morphology of the monotreme organ of Corti and macula lagena. J Comp Neurol 366:335–347

    Article  CAS  PubMed  Google Scholar 

  • LeMasurier M, Gillespie PG (2005) Hair-cell mechanotransduction and cochlear amplification. Neuron 48:403–415

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Li G-H, Huang J-F, Murphy RW, Shi P (2012) Hearing aid for vertebrates via multiple episodic adaptive events on prestin genes. Mol Biol Evol 29:2187–2198

    Article  CAS  PubMed  Google Scholar 

  • Luo Z, Ketten DR (1991) CT scanning and computerized reconstructions of the inner ear of multituberculate mammals. J Vertebr Paleontol 11:220–228

    Article  Google Scholar 

  • Luo Z-X, Ruf I, Martin T (2012) The petrosal and inner ear of the Late Jurassic cladotherian mammal Dryolestes leiriensis and implications for ear evolution in therian mammals. Zool J Linn Soc 166:433–463

    Article  Google Scholar 

  • Luo Z-X, Ruf I, Schultz JA, Martin T (2011) Fossil evidence on evolution of inner ear cochlea in Jurassic mammals. Proc Roy Soc B 278:28–34

    Article  Google Scholar 

  • Manley GA (1970) Comparative studies of auditory physiology in reptiles. Z vergl Physiol 67:363–382

    Article  Google Scholar 

  • Manley GA (1990) Peripheral Hearing Mechanisms in Reptiles and Birds. Springer-Verlag, Heidelberg

    Book  Google Scholar 

  • Manley GA (2000) Cochlear mechanisms from a phylogenetic viewpoint. Proc Natl Acad Sci USA 97:11736–11743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manley GA (2010) An evolutionary perspective on middle ears. Hear Res 263:3–8

    Article  PubMed  Google Scholar 

  • Manley GA (2012) Evolutionary paths to mammalian cochleae. JARO 13:733–743

    Article  PubMed  PubMed Central  Google Scholar 

  • Manley GA (2016) Comparative auditory neuroscience: understanding the evolution and function of ears. JARO. doi:10.1007/s10162-016-0579-3

    PubMed  PubMed Central  Google Scholar 

  • Manley GA, Irvine DRF, Johnstone BM (1972) Frequency response of the bat tympanic membrane. Nature 237:112–113

    Article  Google Scholar 

  • Manley GA, Johnstone BM (1974) Middle-ear function in the guinea pig. J Acoust Soc Am 56:571–576

    Article  CAS  PubMed  Google Scholar 

  • Manley GA, Kirk D, Köppl C, Yates GK (2001) In-vivo evidence for a cochlear amplifier in the hair-cell bundle of lizards. Proc Natl Acad Sci USA 98:2826–2831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manley GA, Köppl C (1998) Phylogenetic development of the cochlea and its innervation. Curr Opin Neurobiol 8:468–474

    Article  CAS  PubMed  Google Scholar 

  • Manley GA, Ladher R (2008) Phylogeny and evolution of ciliated mechano-receptor cells. In: Hoy RR, Shepherd GM, Basbaum AI, Kaneko A, Westheimer G (eds) The Senses: A Comprehensive Reference. Amsterdam, Elsevier, pp 1–34

  • Manley GA, Sienknecht U, Köppl C (2004) Calcium modulates the frequency and amplitude of spontaneous otoacoustic emissions in the bobtail skink. J Neurophysiol. 92:2685–2693

    Article  CAS  PubMed  Google Scholar 

  • Martin P, Hudspeth AJ (1999) Active hair-bundle movements can amplify a hair cell’s response to oscillatory mechanical stimuli. Proc Natl Acad Sci USA 96:14306–14311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meaud J, Grosh K (2011) Coupling active hair bundle mechanics, fast adaptation, and somatic motility in a cochlear model. Biophys J 100:2576–2585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng J, Fox RC (1995) Therian petrosals from the Oldman and Milk River formations (Late Cretaceous), Alberta, Canada. J Vertebr Paleontol 15:122–130

  • Miller MR (1980) The reptilian cochlear duct. In: Popper AN, Fay RR (eds) Comparative Studies of Hearing in Vertebrates. Springer-Verlag, New York, pp 169–204

    Chapter  Google Scholar 

  • Miller MR (1992) The evolutionary implications of the structural variations in the auditory papilla of lizards. In: Fay RR, Popper AN, Webster DB (eds) The Evolutionary Biology of Hearing. Springer-Verlag, Heidelberg, pp 463–487

    Chapter  Google Scholar 

  • Mills DM, Shepherd RK (2001) Distortion product otoacoustic emission and auditory brainstem responses in the echidna (Tachyglossus aculeatus). JARO 2:130–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller M, Hoidis S, Smolders JWT (2010) A physiological frequency-position map of the chinchilla cochlea. Hear Res 268:184–193

    Article  PubMed  Google Scholar 

  • Nowotny M, Gummer AW (2011) Vibration responses of the organ of Corti and the tectorial membrane to electrical stimulation. J Acoust Soc Am 130:3852–3872

    Article  PubMed  Google Scholar 

  • Payan P, Borelli G, Priouzeau F, De Pontual H, Boeuf G, Mayer-Gostan N (2002) Otolith growth in trout Oncorhynchus mykiss: supply of Ca2 and Sr2 to the saccular endolymph. J Exp Biol 205:2687–2695

    CAS  PubMed  Google Scholar 

  • Peng AW, Effertz T, Ricci AJ (2013) Adaptation of mammalian auditory hair cell mechanotransduction is independent of calcium entry. Neuron 80:960–972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pye A (1966) The structure of the cochlea in Chiroptera. I. Microchiroptera, Emballonuroidea and Rhinolophoidea. J Morphol 118:495–510

    Article  CAS  PubMed  Google Scholar 

  • Pye A (1979) The structure of the cochlea in some mammals. J Zool Lond 187:39–53

    Article  Google Scholar 

  • Ramanathan K, Michael TH, Jiang G-J, Hiel H, Fuchs PA (1999) A molecular mechanism for electrical tuning of cochlear hair cells. Science 283:215–217

    Article  CAS  PubMed  Google Scholar 

  • Rossiter SJ, Zhang S, Liu Y (2011) Prestin and high frequency hearing in mammals. Comm Integr Biol 4:236–239

    Article  CAS  Google Scholar 

  • Ruf I, Luo Z-X, Wible JR, Martin T (2009) Petrosal anatomy and inner ear structures of the Late Jurassic Henkelotherium (Mammalia, Cladotheria, Dryolestoidea): insight into the early evolution of the ear region in cladotherian mammals. J Anat 214:679–693

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruggero MA, Temchin AN (2002) The roles of the external, middle, and inner ears in determining the bandwidth of hearing. Proc Natl Acad Sci USA 99:13206–13210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salt AN, Inamura N, Thalmann R, Vora A (1989) Calcium gradients in inner ear endolymph. Am J Otolaryngol 10:371–375

    Article  CAS  PubMed  Google Scholar 

  • Santos-Sacchi J (1992) On the frequency limit and phase of outer hair cell motility: effects of the membrane filter. J Neurosci 12:1906–1916

    Article  CAS  PubMed  Google Scholar 

  • Sauer G, Richter C-P, Klinke R (1999) Sodium, potassium and calcium concentrations measured in pigeon perilymph and endolymph. Hear Res 129:1–6

    Article  CAS  PubMed  Google Scholar 

  • Schultz JA, Zeller U, Luo Z-X (2016) Inner ear labyrinth of monotremes and implications for mammalian inner ear evolution. J Morphol doi:10.1002/jmor.20632

    PubMed  Google Scholar 

  • Shen B, Avila-Flores R, Liu Y, Rossiter SJ, Zhang S (2012) Prestin shows divergent evolution between constant frequency echolocating bats. J Mol Evol 73:109–115

    Article  Google Scholar 

  • Sterkers O, Ferrary E, Amiel C (1988) Production of inner ear fluids. Physiol Rev 68:1083–1128

    Article  CAS  PubMed  Google Scholar 

  • Tan X, Pecka JL, Tang J, Lovas S, Beisel KW, He DZZ (2012) A motif of eleven amino acids is a structural adaptation that facilitates motor capability of eutherian prestin. J Cell Sci 125:1–9

    Article  Google Scholar 

  • Tan X, Pecka JL, Tang J, Okoruwa OE, Zhang Q, Beisel KW, He DZZ (2011) From zebrafish to mammal: functional evolution of prestin, the motor protein of cochlear outer hair cells. J Neurophysiol 105:36–44

    Article  PubMed  Google Scholar 

  • van Dijk P, Manley GA (2009) The effect of ear canal pressure on spontaneous otoacoustic emissions: comparison between human and lizard ears. In: Cooper NP, Kemp DT (eds) Concepts and Challenges in the Biophysics of Hearing. World Scientific, Singapore, pp 196–202

    Chapter  Google Scholar 

  • Weiss TF, Rose C (1988) A comparison of synchronization filters in different auditory receptor organs. Hear Res 33:175–180

    Article  CAS  PubMed  Google Scholar 

  • Wever EG (1978) The Reptile Ear. Princeton University Press, Princeton

    Google Scholar 

  • Wu Y-C, Art JJ, Goodman MB, Fettiplace R (1995) A kinetic description of the calcium-activated potassium channel and its application to electrical tuning of hair cells. Prog Biophys Mol Biol 63:131–158

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Thanks to Ulrike Sienknecht and Christine Köppl for very useful comments on an earlier version, and to Zhe-Xi Luo and an anonymous reviewer for important suggestions to improve the manuscript.

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Correspondence to Geoffrey A. Manley.

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Manley, G.A. The Foundations of High-Frequency Hearing in Early Mammals. J Mammal Evol 25, 155–163 (2018). https://doi.org/10.1007/s10914-016-9379-0

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