The Middle Ear pp 7-30

Part of the Springer Handbook of Auditory Research book series (SHAR)

The Evolution and Development of Middle Ears in Land Vertebrates

Chapter

Abstract

New fossil evidence and supporting data from embryological studies have helped to consolidate interpretations of the structures that assemble the middle ear apparatus of different lineages of land vertebrates. The middle ears of modern land vertebrate groups evolved independently of one another during the Triassic era of the Mesozoic. Thus, two dogmata have fallen: (1) The tympanic middle ear is not a monophyletic development, i.e., the eardrum-bearing middle ears of modern land vertebrates are not descended from one common ancestral type. (2) The mammalian middle ear did not emerge by the addition of two more ossicles to an existing, one-ossicle middle ear because mammalian ancestors, like all other vertebrate lineages of late Permian–early Triassic times, lacked a tympanic middle ear. Whereas most lineages evolved a single-ossicle system, mammals developed a three-ossicle system. This difference is due to mammals simultaneously evolving a secondary jaw joint, a process that freed up small bones at the rear of the jaw that became incorporated into the middle ear. Functionally, there are only small differences between the resulting two types of middle ear. Because all middle ear systems were constructed from preexisting components of the skull that subserved other functions, there are striking similarities in the embryological origins and the developmental pathways of all land vertebrate middle ears and homologous, ancestral jaw components.

Keywords

Embryology of middle ear Middle ear development Middle ear evolution Three-ossicle Tympanic 

References

  1. Aitkin, L. M., & Johnstone, B. M. (1972). Middle-ear function in a monotreme: The echidna (Tachyglossus aculeatus). Journal of Experimental Zoology, 180, 245–250.PubMedCrossRefGoogle Scholar
  2. Allin, E. F. (1986). The auditory apparatus of advanced mammal-like reptiles and early mammals. In H. Hotton, P. D. MacLean, J. J. Roth, & E. C. Roth (Eds.), The ecology and biology of mammal-like reptiles (pp. 283–294). Washington, DC: Smithsonian Institution Press.Google Scholar
  3. Allin, E. F., & Hopson, J. A. (1992). Evolution of the auditory system in Synapsida (“Mammal-like reptiles” and primitive mammals) as seen in the fossil record. In D. B. Webster, R. R. Fay, & A. N. Popper (Eds.), The evolutionary biology of hearing (pp. 587–614). New York: Springer-Verlag.CrossRefGoogle Scholar
  4. Bennett, A. F., & Ruben, J. A. (1986). The metabolic and thermoregulatory status of therapods. In H. Hotton, P. D. MacLean, J. J. Roth, & E. C. Roth (Eds.), The ecology and biology of mammal-like reptiles (pp. 207–218). Washington, DC: Smithsonian Institution Press.Google Scholar
  5. Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L., & Purvis, A. (2007). The delayed rise of present-day mammals. Nature, 446, 507–512.PubMedCrossRefGoogle Scholar
  6. Brazeau, M. D., & Ahlberg, P. E. (2006). Tetrapod-like middle ear architecture in a Devonian fish. Nature, 439, 318–321.PubMedCrossRefGoogle Scholar
  7. Carroll, R.L. (1988) Vertebrate paleontology and evolution. New York: Freeman.Google Scholar
  8. Chapman, S. C. (2011). Can you hear me now? Understanding vertebrate middle ear development. Frontiers of Bioscience, 16, 1675–1692.CrossRefGoogle Scholar
  9. Chin, K., Kurian, R., & Saunders, J. C. (1997). Maturation of tympanic membrane layers and collagen in the embryonic and post-hatch chick (Gallus domesticus). Journal of Morphology, 233, 257–266.PubMedCrossRefGoogle Scholar
  10. Christensen-Dalsgaard, J. (2010). Vertebrate pressure-gradient receivers. Hearing Research, 273, 37–45.PubMedCrossRefGoogle Scholar
  11. Christensen-Dalsgaard, J., & Manley, G. A. (2008). Acoustical coupling of lizard eardrums. Journal of the Association for Research in Otolaryngology, 9, 407–416.PubMedCentralPubMedCrossRefGoogle Scholar
  12. Clack, J. A. (2002). Patterns and processes in the early evolution of the tetrapod ear. Journal of Neurobiology, 53, 251–264.PubMedCrossRefGoogle Scholar
  13. Clack, J. A. (2009). The fin to limb transition: New data, interpretations, and hypotheses from paleontology and developmental biology. Annual Review of Earth and Planetary Sciences, 37, 163–179.CrossRefGoogle Scholar
  14. Clack, J. A., & Allin, E. (2004). The evolution of single- and multiple-ossicle ears in fishes and tetrapods. In G. A. Manley, A. N. Popper, & R. R. Fay (Eds.), Evolution of the vertebrate auditory system (pp. 128–163). New York: Springer.CrossRefGoogle Scholar
  15. Clack, J. A., Ahlberg, P. E., Finney, S. M., Dominguez Alonso, P., Robinson, J., & Ketcham, R. A. (2003). A uniquely specialised ear in a very early tetrapod. Nature, 425, 65–69.PubMedCrossRefGoogle Scholar
  16. Coates, M. I., & Clack, J. A. (1990). Polydactyly in the earliest known tetrapod limbs. Nature, 347, 66–69.CrossRefGoogle Scholar
  17. Coleman, M. N., & Boyer, D. M. (2012). Inner ear evolution in primates through the Cenozoic: Implications for the evolution of hearing. The Anatomical Record, DOI 10.1002/ar.22422.
  18. Depew, M. J., Lufkin, T., & Rubenstein, J. L. R. (2002). Specification of jaw subdivisions by Dlx genes. Science, 298, 381–385.PubMedCrossRefGoogle Scholar
  19. Evans, A. R., Jones, D., Boyer, A. G., Brown, J. H., Costa, D. P., Morgan Ernest, S. K., Fitzgerald, E,. M. G.,, Fortelius, M., Gittleman, J. L., Hamilton, M. J., Harding, L. E., Lintulaakso, K., Lyons, S.K., Okie, J. G., Saarinen, J. J., Siblyo, R. M., Smith, F. A., Stephens, P. R., Theodor, J. M., & Uhen, M. D.. (2012) The maximal rate of mammal evolution. Proceedings of the National Academy of Sciences of the USA,doi/10.1073/pnas.1120774109.
  20. Feng, A. S., Narins, P. M., Xu, C. H., Lin, W. Y., Yu, Z. L., Qiu, Q., Xu, Z. M., Shen, J. X. (2006). Ultrasonic communication in frogs. Nature, 440, 333–336.PubMedCrossRefGoogle Scholar
  21. Gates, G. R., Saunders, J., & Bock, G. R. (1974). Peripheral auditory function in the platypus, Ornithorhynchus anatinus. Journal of the Acoustical Society of America, 56, 152–156.PubMedCrossRefGoogle Scholar
  22. Gaupp, E. (1912). Die Reichertsche Theorie. Archives of Anatomy and Physiology Supplement, 1–416.Google Scholar
  23. Gendron-Maguire, M., Mallo, M., Zhang, M., & Gridley, T. (1993). Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell, 75, 1317–1331.PubMedCrossRefGoogle Scholar
  24. Grammatopoulos, G. A., Bell, E., Toole, L., Lumsden, A., & Tucker, A. S. (2000). Homeotic transformation of branchial arch identity after Hoxa2 overexpression. Development, 127, 5355–5365.PubMedGoogle Scholar
  25. Graybeal, A., Rosowski, J. J., Ketten, D. R., & Crompton, A. W. (1989). Inner-ear structure in Morganucodon, an early Jurassic mammal. Zoological Journal of the Linnean Society, 96, 107–117.CrossRefGoogle Scholar
  26. Hall, B. K., & Miyake, T. (1995). Divide, accumulate, differentiate: Cell condensation in skeletal development revisited. International Journal of Developmental Biology, 39, 881–893.PubMedGoogle Scholar
  27. Heffner, R. S., Koay, G., & Heffner, H. E. (2001). Audiograms of five species of rodents: Implications for the evolution of hearing and the perception of pitch. Hearing Research, 157, 138–152.PubMedCrossRefGoogle Scholar
  28. Hemilä, S., Nummela, S., & Reuter, T. (1995). What middle ear parameters tell about impedance matching and high frequency hearing. Hearing Research, 85, 31–44.PubMedCrossRefGoogle Scholar
  29. Hotton, N. (1959). The pelycosaur tympanum and early evolution of the middle ear. Evolution, 13, 99–121.CrossRefGoogle Scholar
  30. Hurum, J. H. (1998). The inner ear of two late Cretaceous multituberculate mammals, and its implications for multituberculate hearing. Journal of Mammalian Evolution, 5, 65–93.CrossRefGoogle Scholar
  31. Jaskoll, T., & Maderson, P. (1978). A histological study of the development of the avian middle ear and tympanum. Anatomical Record, 190, 177–200.PubMedCrossRefGoogle Scholar
  32. Kemp, T. S. (2007). Acoustic transformer function of the postdentary bones and quadrate of a nonmammalian cynodont. Journal of Vertebrate Paleontology, 27, 431–441.CrossRefGoogle Scholar
  33. Koentges, G., & Lumsden, A. (1996). Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development, 122, 3229–3242.Google Scholar
  34. Koentges, G., & Matsuoka, T. (2002). Evolution: Jaws of the fates. Science, 298, 371–373.PubMedCrossRefGoogle Scholar
  35. Ladich, F., & Popper, A. N. (2004). Parallel evolution in fish hearing organs. In G. A. Manley, A. N. Popper, & R. R. Fay (Eds.), Evolution of the vertebrate auditory system. (pp. 95–127). New York: Springer.CrossRefGoogle Scholar
  36. Lucas, S. G., & Luo, Z. (1993). Adelobasileus from the upper Triassic of west Texas: The oldest mammal. Journal of Vertebrate Paleontology, 13, 309–334.CrossRefGoogle Scholar
  37. Luo, Z.-X. (2007). Transformation and diversification in early mammal evolution. Nature, 450, 1011–1019.PubMedCrossRefGoogle Scholar
  38. Luo, Z.-X. (2011). Developmental patterns in Mesozoic evolution of mammal ears. Annual Review of Ecology and Evolution Systematics, 42, 355–380.CrossRefGoogle Scholar
  39. Luo, Z., & Ketten, D. R. (1991). CT scanning and computerized reconstructions of the inner ear of multituberculate mammals. Journal of Vertebrate Paleontology, 11, 220–228.CrossRefGoogle Scholar
  40. Luo, Z-X., Crompton, A. W., & Sun, A. L. (2001). A new mammaliaform from the early Jurassic and evolution of mammalian characteristics. Science, 292, 1535–1540.PubMedCrossRefGoogle Scholar
  41. Luo, Z-X., Rif, I., Schultz, J. A., & Martin, T. (2010). Fossil evidence on evolution of inner ear cochlea in Jurassic mammals. Proceedings of the Royal Society B: Biological Sciences, 278, 28–34.PubMedCentralPubMedCrossRefGoogle Scholar
  42. Maier, W. (1990). Phylogeny and ontogeny of mammalian middle ear structures. Netherlands Journal of Zoology, 40, 55–74.CrossRefGoogle Scholar
  43. Mallo, M. (2001). Formation of the middle ear: Recent progress on the developmental and molecular mechanisms. Developmental Biology, 231, 410–419.PubMedCrossRefGoogle Scholar
  44. Mallo, M., Schrewe, H., Martin, J. F., Olson, E. N., & Ohnemus, S. (2000). Assembling a functional tympanic membrane: Signals from the external acoustic meatus coordinate development of the malleal manubrium. Development, 127, 4127–4136.PubMedGoogle Scholar
  45. Manley, G. A. (1972) Frequency response of the middle ear of geckos. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 81, 251–258.CrossRefGoogle Scholar
  46. Manley, G. A. (1973). A review of some current concepts of the functional evolution of the ear in terrestrial vertebrates. Evolution, 26, 608–621.CrossRefGoogle Scholar
  47. Manley, G. A. (2000). Cochlear mechanisms from a phylogenetic viewpoint. Proceedings of the National Academy of Sciences of the USA, 97, 11736–11743.PubMedCentralPubMedCrossRefGoogle Scholar
  48. Manley, G. A. (2010). An evolutionary perspective on middle ears. Hearing Research, 263, 3–8.PubMedCrossRefGoogle Scholar
  49. Manley, G. A. (2011). Vertebrate hearing: Origin, evolution and functions. In F. G. Barth, H.-D. Klein, & P. Giampieri-Deutsch (Eds.), Sensory perception: Mind and matter (pp. 23–40). Vienna, New York: Springer.Google Scholar
  50. Manley, G.A. (2012) Evolutionary paths to mammalian cochleae. JARO 13, 733–743.Google Scholar
  51. Manley, G. A., & Johnstone, B. M. (1974). Middle-ear function in the guinea pig. Journal of the Acoustical Society of America, 56, 571–576.PubMedCrossRefGoogle Scholar
  52. Manley, G. A., & Köppl, C. (1998). Phylogenetic development of the cochlea and its innervation. Current Opinion in Neurobiology, 8, 468–474.PubMedCrossRefGoogle Scholar
  53. Manley, G. A., & Clack, J. A. (2004). An outline of the evolution of vertebrate hearing organs. In G. A. Manley, A. N. Popper, & R. R. Fay (Eds.), Evolution of the vertebrate auditory system (pp. 1–26). New York: Springer.CrossRefGoogle Scholar
  54. Manley, G. A., & Kraus, J. E. M. (2010). Exceptional high-frequency hearing and matched vocalizations in Australian pygopod geckos. Journal of Experimental Biology, 213, 1876–1885.PubMedCrossRefGoogle Scholar
  55. Martin, T., & Luo, Z-X. (2005). Homoplasy in the mammalian ear. Science, 307, 861–862.CrossRefGoogle Scholar
  56. Masterton, B., Heffner, H., & Ravizza, R. (1969). The evolution of mammalian hearing. Journal of the Acoustical Society of America, 45, 966–985.PubMedCrossRefGoogle Scholar
  57. Meng, J., Wang, Y., & Li, C. (2011). Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont. Nature, 472, 181–185.PubMedCrossRefGoogle Scholar
  58. Müller, J., & Tsuji, L. A. (2007). Impedance-matching hearing in paleozoic reptiles: Evidence of advanced sensory perception at an early stage of amniote evolution. PLoS ONE, 2, e889.PubMedCentralPubMedCrossRefGoogle Scholar
  59. Noden, D. M. (1991). Cell movements and control of patterned tissue assembly during craniofacial development. Journal of Craniofacial Genetics and Developmental Biology, 11, 192–213.PubMedGoogle Scholar
  60. Novacek, M. J. (1977). Aspects of the problem of variation, origin and evolution of the eutherian auditory bulla. Mammal Reviews, 7, 131–149.CrossRefGoogle Scholar
  61. Obrist, M. K., Fenton, M. B., Eger, J. L., & Schlegel, P. A. (1993). What ears do for bats: A comparative study of pinna sound pressure transformation in Chiroptera. Journal of Experimental Biology, 180, 119–152.PubMedGoogle Scholar
  62. O’Gorman, S. (2005). Second branchial arch lineages of the middle ear of wild-type and Hoxa2 mutant mice. Developmental Dynamics, 234, 124–131.PubMedCrossRefGoogle Scholar
  63. Plant, M. R., MacDonald, M. E., Grad, L. I., Ritchie, S. J., & Richman, J. M. (2000). Locally released retinoic acid repatterns the first branchial arch cartilages in vivo. Developmental Biology, 222, 12–26.PubMedCrossRefGoogle Scholar
  64. Puria, S., & Steele, C. R. (2008) Mechano-acoustical transformations. In R. R. Hoy, G. M. Shepherd, A. I. Basbaum, A. Kaneko, & G. Westheimer (Eds.), The senses: A comprehensive reference (pp. 165–201). Amsterdam: Elsevier.CrossRefGoogle Scholar
  65. Qiu, M., Bulfone, A., Martinez, S., Meneses, J. J., Shimamura, K., Pedersen, R. A., & Rubenstein, J. L. (1995). Null mutation of Dlx-2 results in abnormal morphogenesis of proximal first and second branchial arch derivatives and abnormal differentiation in the forebrain. Genes and Development, 9, 2523–2538.PubMedCrossRefGoogle Scholar
  66. Reichert, K. B. (1837). Über die Visceralbogen der Wirbelthiere im Allgemeinen und deren Metamorphosen bei den Vögeln und Säugethieren. Archiv der Anatomie, Physiologie und Wissenschaftliche Medizin, 1837, 120–220.Google Scholar
  67. Rich, T. H., Hopson, J. A., Musser, A. M., Flannery, T. F., & Vickers-Rich, P. (2005). Independent origins of middle ear bones in monotremes and therians. Science, 307, 910–914.PubMedCrossRefGoogle Scholar
  68. Rijli, F. M., Mark, M., Lakkaraju, S., Dierich, A., Dollé, P., & Chambon, P. (1993). A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell, 75, 1333–1349.PubMedCrossRefGoogle Scholar
  69. Rosowski, J. J. (1992). Hearing in transitional mammals: Predictions from the middle ear anatomy and hearing capabilities of extant mammals. In D. B. Webster, R. R. Fay, & A. N. Popper (Eds.), The evolutionary biology of hearing (pp. 615–632). New York: Springer.CrossRefGoogle Scholar
  70. Rosowski, J. J. (1994). Outer and middle ears. In R. R. Fay & A. N. Popper (Eds.), Comparative hearing: Mammals (pp. 172–247). New York: Springer.CrossRefGoogle Scholar
  71. Rosowski, J. J., & Graybeal, A. (1991). What did Morganucodon hear? Zoological Journal of the Linnean Society, 101, 131–168.CrossRefGoogle Scholar
  72. Rowe, T. (1996). Coevolution of the mammalian middle ear and neocortex. Science, 273, 651–654.PubMedCrossRefGoogle Scholar
  73. Rowe, T. B., Macrini, T. E., & Luo, Z-X. (2011). Fossil evidence on origin of the mammalian brain. Science, 332, 955–957.PubMedCrossRefGoogle Scholar
  74. Ruf, I., Luo, Z-X., Wible, J. R., & 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. Journal of Anatomy, 214, 679–693.PubMedCentralPubMedCrossRefGoogle Scholar
  75. Ruggero, M. A., & Temchin, A. N. (2002). The roles of the external, middle, and inner ears in determining the bandwidth of hearing. Proceedings of the National Academy of Sciences of the USA, 99, 13206–13210.PubMedCentralPubMedCrossRefGoogle Scholar
  76. Schilling, T. F., Prince, V., & Ingham, P.W. (2001). Plasticity in zebrafish hox expression in the hindbrain and cranial neural crest. Developmental Biology, 231, 201–216.PubMedCrossRefGoogle Scholar
  77. Schneider, R. A., & Helms, J. A. (2003). The cellular and molecular origins of beak morphology. Science, 299, 565–568.PubMedCrossRefGoogle Scholar
  78. Shigetani, Y., Sugahara, F., Kawakami, Y., Murakami, Y., Hirano, S., & Kuratani, S. (2002). Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution. Science, 296, 1316–1319.PubMedCrossRefGoogle Scholar
  79. Sienknecht, U. J., & Fekete, D. M. (2008). Comprehensive Wnt-related gene expression during cochlear duct development in chicken. Journal of Comparative Neurology, 510, 378–395.PubMedCentralPubMedCrossRefGoogle Scholar
  80. Smotherman, M., & Narins, P. (2004). Evolution of the amphibian ear. In G. A. Manley, A. N. Popper, & Fay, R. R. (Eds.), Evolution of the vertebrate auditory system. (pp. 164–199). New York: Springer.CrossRefGoogle Scholar
  81. Takechi, M., & Kuratani, S. (2010). History of studies on mammalian middle ear evolution: A comparative morphological and developmental biology perspective. Journal of Experimental Zoology B: Molecular and Developmental Evolution, 314B, 417–433.CrossRefGoogle Scholar
  82. Taylor, G. D. (1969). Evolution of the ear. Laryngoscope, 79, 638–651.PubMedCrossRefGoogle Scholar
  83. Trainor, P., & Krumlauf, R. (2000). Plasticity in mouse neural crest cells reveals a new patterning role for cranial mesoderm. Nature Cell Biology, 2, 96–102.PubMedCrossRefGoogle Scholar
  84. Wang, Y., Hu Y., Meng J., & Li, C. (2001). An ossified Meckel’s cartilage in two cretaceous mammals and origin of the mammalian middle ear. Science, 294, 357–361.PubMedCrossRefGoogle Scholar
  85. Xu, P. X., Adams, J., Peters, H., Brown, M. C., Heaney, S., & Maas, R. (1999). Eya1–deficient mice lack ears and kidneys and show abnormal apoptosis of organ primordia. Nature Genetics, 23, 113–117.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Cochlear and Auditory Brainstem Physiology, IBU, Faculty VCarl von Ossietzky University OldenburgOldenburgGermany

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