Advertisement

Evolution of the Middle and Inner Ears of Mammaliaforms: The Approach to Mammals

  • Zhe-Xi Luo
  • Julia A. Schultz
  • Eric G. EkdaleEmail author
Chapter
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 59)

Abstract

Transformations of ear structures in the evolution of early mammals can be studied with the fossils of mammaliaforms. The middle ear is fully attached to the mandibles in mammaliaforms; however, in Mesozoic eutriconodont and spalacotherioid mammals, it is only connected to the mandible by an ossified Meckel’s cartilage, with the ectotympanic and malleus already displaced from the mandible. Recent morphogenetic studies have shown that the developmental potential for ossification of Meckel’s element is conserved in extant mammals. New fossils further revealed that this pattern actually evolved in mammaliaform phylogeny and that disconnection of the ear from the mandible occurred independently in monotremes, in therians, and in multituberculate mammals. The inner ear of mammaliaforms is derived in having a single petrosal bone enclosing the entire inner ear and a promontorium for an elongate cochlear canal. Mammaliaforms and most Mesozoic mammals had ancestral features of a simple cochlear canal with a single cochlear nerve foramen but no interior bony laminae nor did they have a bony canal for the cochlear ganglion. The sieve-like foramina for cochlear nerve fibers to enter the cochlear canal evolved independently three times in Mesozoic mammals. Cochlear canal curvature is homoplastic among mammaliaform groups, and a curvature beyond 270° only evolved in cladotherians, accompanied by Rosenthal’s canal for the cochlear ganglion. The homoplasies of ear structures in early mammalian evolution, although seemingly complex, are consistent with the new understanding of a labile morphogenesis of mammalian ears under a complex developmental genetic network.

Keywords

Cochlear canal Cochlear innervation Development Evolutionary homoplasies Inner ear Meckel’s cartilage Mesozoic mammaliaforms Middle ear 

Notes

Compliance with Ethics Requirements

Zhe-Xi Luo, Julia A. Schultz, and Eric G. Ekdale have declared that they have no conflicts of interest for this publication.

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. Alexander, G. (1904). Entwicklung und Bau des inneren Gehörorganes von Echidna aculeata. Denkschriften der Medizinisch–Naturwissenschaftlichen Gesellschaft Jena, 6(2), 1–118.Google Scholar
  3. Allin, E. F. (1975). Evolution of the mammalian middle ear. Journal of Morphology, 147, 403–438.PubMedCrossRefGoogle Scholar
  4. 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
  5. Anthwal, N., Joshi, L., & Tucker, A. S. (2013). Evolution of the mammalian middle ear and jaw: Adaptations and novel structures. Journal of Anatomy, 222, 147–160. doi: 10.1111/j.1469–7580.2012.01526.x PubMedCrossRefGoogle Scholar
  6. Appler, J. M., & Goodrich, L. V. (2011). Connecting the ear to the brain: Molecular mechanisms of auditory circuit assembly. Progress in Neurobiology, 93, 488–508. doi: 10.1016/j.pneurobio.2011.01.004 PubMedPubMedCentralCrossRefGoogle Scholar
  7. Archer, M., Flannery, T. F., Ritchie, A., & Molnar, R. (1985). First Mesozoic mammal from Australia—an Early Cretaceous monotreme. Nature, 318, 363–366.CrossRefGoogle Scholar
  8. Bi, S., Wang, Y.-Q., Guan, J., Sheng, X., & Meng, J. (2014). Three new Jurassic euharamiyidan species reinforce early divergence of mammals. Nature, 514, 579–584. doi: 10.1038/nature13718 Google Scholar
  9. Bok, J., Chang, W., & Wu, D. K. (2007). Patterning and morphogenesis of the vertebrate inner ear. International Journal of Developmental Biology, 51, 521–533. doi: 10.1387/ijdb.072381jb PubMedCrossRefGoogle Scholar
  10. Bonaparte, J. F., Martinelli, A. G., & Schultz, C. L. (2005). New information on Brazilodon and Brasilitherium (Cynodontia, Progainognathia) from the Late Triassic of Southern Brazil. Revista Brasileira de Paleontologia, 8, 25–46.CrossRefGoogle Scholar
  11. Brink, A. S. (1963). Two cynodonts from the Ntawere Formation in the Luangwa Valley of Northern Rhodesia. Palaeontologica Africana, 8, 77–96.Google Scholar
  12. Clack, J. A., & Allin, E. F. (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 Science+Business Media.CrossRefGoogle Scholar
  13. Close, R. A., Friedman, M., Lloyd, G. T., & Benson, R. B. J. (2015). Evidence for a Mid-Jurassic adaptive radiation in Mammals. Current Biology, 25, 2137–2142. doi: 10.1016/j.cub.2015.06.047 PubMedCrossRefGoogle Scholar
  14. Crompton, A. W., & Luo, Z.-X. (1993). Relationships of the Liassic mammals Sinoconodon, Morganucodon, and Dinnetherium. In F. S. Szalay, M. J. Novacek, & M. C. McKenna (Eds.), Mammal phylogeny: Mesozoic differentiation, multituberculates, monotremes, early therians, and marsupials, vol. 1 (pp. 30–44). New York: Springer-Verlag.CrossRefGoogle Scholar
  15. Doran, A. H. G. (1879). Morphology of the mammalian ossicula auditus. Transactions of the Linnean Society, 1, 271–498.Google Scholar
  16. Durrant, J. D., & Lovrinic, J. H. (1995). Bases of hearing science, 3rd ed. Baltimore: Williams and Wilkins.Google Scholar
  17. Echteler, S. M., Fay, R. R., & Popper, A. N. (1994). Structure of the mammalian cochlea. In R. R. Fay & A. N. Popper (Eds.), Comparative hearing: Mammals (pp. 134–171). New York: Springer-Verlag.CrossRefGoogle Scholar
  18. Ekdale, E. G. (2013). Comparative anatomy of the bony labyrinth (inner ear) of placental mammals. PLoS ONE 8(6), e66624. doi: 10.1371/journal.pone.0066624 PubMedPubMedCentralCrossRefGoogle Scholar
  19. Ekdale, E. G., & Rowe, T. (2011). Morphology and variation within the bony labyrinth of zhelestids (Mammalia, Eutheria) and other therian mammals. Journal of Vertebrate Paleontology, 31, 658–675. doi: 10.1080/02724634.2011.557284 CrossRefGoogle Scholar
  20. Fernandez, V., Abdala, F., Carlson, K. J., Cook, D. C., et al. (2013). Synchrotron reveals Early Triassic odd couple: Injured amphibian and aestivating therapsid share burrow. PLoS ONE, doi: 10.1371/journal.pone.0064978.Google Scholar
  21. Fleischer, G. (1973). Studien am Skelett des Gehörorgans der Säugetiere, einschließlich des Menschen. Säugetierkundliche Mitteilungen, 21, 131–239.Google Scholar
  22. Fleischer, G. (1976). Hearing in extinct cetaceans as determined by cochlear structure. Journal of Palaeontology, 50, 133–152.Google Scholar
  23. Fourie, S. (1974). The cranial morphology of Thrinaxodon liorhinus Seeley. Annals of the South African Museum, 65, 337–400.Google Scholar
  24. Fox, R. C., & Meng, J. (1997). An X-radiographic and SEM study of the osseous inner ear of multituberculates and monotremes (Mammalia): Implications for mammalian phylogeny and evolution of hearing. Zoological Journal of the Linnean Society, 121, 249–291.CrossRefGoogle Scholar
  25. Fritzsch, B., Pan, N., Jahn, I., & Elliott, K. L. (2015). Inner ear development: Building a spiral ganglion and an organ of Corti out of unspecified ectoderm. Cell and Tissue Research, 361, 7–24. doi: 10.1007/s00441–014–2031–5 PubMedCrossRefGoogle Scholar
  26. Fröbisch, J., & Reisz, R. R. (2009). The Late Permian herbivore Suminia and the early evolution of arboreality in terrestrial vertebrate ecosystems. Proceedings of the Royal Society of London B: Biological Sciences, 276, 3611–3618. doi: 10.1098/rspb.2009.0911 CrossRefGoogle Scholar
  27. Gill, P. G., Purnell, M. A., Crumpton, N., Robson Brown, K., et al. (2014). Dietary specializations and diversity in feeding ecology of the earliest stem mammals. Nature, 512, 303–306. doi: 10.1038/nature13622 PubMedCrossRefGoogle Scholar
  28. Gow, C. E. (1986). A new skull of Megazostrodon (Mammalia: Triconodonta) from the Elliot Formation (Lower Jurassic) of southern Africa. Palaeontologia Africana, 26, 13–23.Google Scholar
  29. Harada, Y., & Ishizeki, K. (1998). Evidence for transformation of chondrocytes and site-specific resorption during the degradation of Meckel’s cartilage. Anatomy and Embryology, 197, 439–450.PubMedCrossRefGoogle Scholar
  30. Heffner, H. E., & Heffner, R. S. (2014). The behavioral study of mammalian hearing. In A. N. Popper & R. R. Fay (Eds.), Perspectives on auditory research (pp. 269–285). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  31. Hoffmann, S., O’Connor, P. M., Kirk, E. C., Wible, J. R., & Krause, D. W. (2014). Endocranial and inner ear morphology of Vintana sertichi (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar. Journal of Vertebrate Paleontology, 34(supplement 1), 110–137. doi: 10.1080/02724634.2014.956878 CrossRefGoogle Scholar
  32. Hopson, J. A., & Kitching, J. W. (2001). A probainognathian cynodont from South Africa and the phylogeny of non-mammalian cynodonts. Bulletin of the Museum of Comparative Zoology, 156, 5–35.Google Scholar
  33. Hurum, J. H. (1998). The inner ear of two Late Cretaceous multituberculate mammals, and its implications for multituberculate hearing. Journal of Mammalian Evolution, 5, 65–94.CrossRefGoogle Scholar
  34. Ji, Q., Luo, Z.-X., Yuan, C.-X., & Tabrum, A. R. (2006). A swimming mammaliaform from the Middle Jurassic and ecomorphological diversification of early mammals. Science, 311, 1123–1127. doi: 10.1126/science.1123026 PubMedCrossRefGoogle Scholar
  35. Ji, Q., Luo, Z.-X., Zhang, X.-L., Yuan, C.-X., & Xu, L. (2009). Evolutionary development of the middle ear in Mesozoic therian mammals. Science, 326, 278–231. doi: 10.1126/science.1178501 PubMedCrossRefGoogle Scholar
  36. Jørgensen, J. M., & Locket, N. A. (1995). The inner ear of the echidna Tachyglossus aculeatus: The vestibular sensory organs. Proceedings of the Royal Society of London B: Biological Sciences, 260, 183–189.CrossRefGoogle Scholar
  37. Kemp, T. S. (2005). The origin and evolution of mammals. Oxford: Oxford University Press.Google Scholar
  38. Kemp, T. S. (2007). Acoustic transformer function of the postdentary bones and quadrate of a non-mammalian cynodont. Journal of Vertebrate Paleontology, 27, 431–441. doi: 10.1671/0272–4634(2007)27[431:ATFOTP]2.0.CO;2 CrossRefGoogle Scholar
  39. Kermack, K. A., & Mussett, F. (1983). The ear in mammal-like reptiles and early mammals. Acta Palaeontologica Polonica, 28, 147–158.Google Scholar
  40. Kermack, K. A., Mussett, F., & Rigney, H. W. (1973). The lower jaw of Morganucodon. Zoological Journal of the Linnean Society, 53, 87–175.CrossRefGoogle Scholar
  41. Kermack, K. A., Mussett., F., & Rigney, H. W. (1981). The skull of Morganucodon. Zoological Journal of the Linnean Society, 71, 1–158.CrossRefGoogle Scholar
  42. Kielan-Jaworowska, Z., Cifelli, R. L., & Luo, Z.-X. (2004). Mammals from the age of dinosaurs: Origins, evolution, and structure. New York: Columbia University Press.CrossRefGoogle Scholar
  43. Kirk, E. C., Hoffmann, S., Kemp, A. D., Krause, D. W., & O’Connor, P. M. (2014). Sensory anatomy and sensory ecology of Vintana sertichi (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar. Journal of Vertebrate Paleontology, 34 (supplement 1), 203–222. doi: 10.1080/02724634.2014.963232 CrossRefGoogle Scholar
  44. Krause, D. W., Hoffmann, S., Wible, J. R., Kirk, E. C., et al. (2014). First cranial remains of a gondwanatherian mammal reveal remarkable mosaicism. Nature, 515, 512–517. doi: 10.1038/nature13922 PubMedCrossRefGoogle Scholar
  45. Laaß, M. (2014). Bone conduction hearing and seismic sensitivity of the Late Permian anomodont Kawingasaurus fossilis. Journal of Morphology, 276, 121–143. doi: 10.1002/jmor.20325 PubMedCrossRefGoogle Scholar
  46. Laaß, M. (2015) The origins of the cochlear and impedance matching hearing in synapsids. Acta Palaeontologica Polonica. doi: 10.4202/app.00140.2014.Google Scholar
  47. Ladevèze, S., de Muizon, C., Colbert, M., & Smith, T. (2010). 3D computational imaging of the petrosal of a new multituberculate mammal from the Late Cretaceous of China and its paleobiologic inferences. Comptes Rendus Palevol, 9, 319–330. doi: 10.1016/j.crpv.2010.07.008 CrossRefGoogle Scholar
  48. Ladhams, A., & Pickles, J. O. (1996). Morphology of the monotreme organ of Corti and macula lagena. Journal of Comparative Neurology, 366, 335–347.PubMedCrossRefGoogle Scholar
  49. Li, C.-K., Wang, Y.-Q., Hu, Y.-M., & Meng, J. (2003). A new species of Gobiconodon (Triconodonta, Mammalia) and its implication for age of Jehol Biota. Chinese Science Bulletin (English Edition), 48, 1129–1134.Google Scholar
  50. Li, J.-L, Wang, Y., Wang, Y.-Q., & Li, C.-K. (2001). A new family of primitive mammals from the Mesozoic of western Liaoning, China. Chinese Science Bulletin (English Edition), 46, 782–785.CrossRefGoogle Scholar
  51. Lillegraven, J. A., & Krusat, G. (1991). Cranio-mandibular anatomy of Haldanodon exspectatus (Docodonta; Mammalia) from the Late Jurassic of Portugal and its implications to the evolution of mammalian characters. Contributions to Geology, University of Wyoming, 28, 39–138.Google Scholar
  52. Liu, J., & Olsen, P. (2010). The phylogenetic relationships of Eucynodontia (Amniota: Synapsida). Journal of Mammalian Evolution, 17, 151–176. doi: 10.1007/s10914–010–9136–8 CrossRefGoogle Scholar
  53. Luo, Z.-X. (1994). Sister taxon relationships of mammals and the transformations of the diagnostic mammalian characters. In N. C. Fraser & H.-D. Sues (Eds.), In the shadow of dinosaurs—Early Mesozoic tetrapods (pp. 98–128). Cambridge (UK): Cambridge University Press.Google Scholar
  54. Luo, Z.-X. (2001). Inner ear and its bony housing in tritylodonts and implications for evolution of mammalian ear. Bulletin of the Museum of Comparative Zoology, 156, 81–97.Google Scholar
  55. Luo, Z.-X. (2007). Transformation and diversification in the early mammalian evolution. Nature, 450, 1011–1019. doi: 10.1038/nature06277 PubMedCrossRefGoogle Scholar
  56. Luo, Z.-X. (2011). Developmental patterns in Mesozoic evolution of mammal ears. Annual Review of Ecology, Evolution and Systematics, 42, 355–380. doi: 10.1146/annurev–ecolsys–032511–142302 CrossRefGoogle Scholar
  57. Luo, Z.-X., & Crompton, A. W. (1994). Transformations of the quadrate (incus) through the transition from non–mammalian cynodonts to mammals. Journal of Vertebrate Paleontology, 14, 341–374.CrossRefGoogle Scholar
  58. Luo, Z.-X., Crompton, A. W., & Lucas, S. G. (1995). Evolutionary origins of the mammalian promontorium and cochlea. Journal of Vertebrate Paleontology, 15, 113–121.CrossRefGoogle Scholar
  59. Luo, Z.-X., Crompton, A. W., & Sun, A. L. (2001). A new mammaliaform from the Early Jurassic of China and evolution of mammalian characteristics. Science, 292, 1535–1540.PubMedCrossRefGoogle Scholar
  60. Luo, Z.-X., Kielan-Jaworowska, Z., & Cifelli, R. L. (2002). In quest for a phylogeny of Mesozoic mammals. Acta Palaeontologica Polonica, 47, 1–78.Google Scholar
  61. Luo, Z.-X., Chen, P.-J., Li, G., & Chen, M. (2007). A new eutriconodont mammal and evolutionary development of early mammals. Nature, 446, 288–293. doi: 10.1038/nature05627 Google Scholar
  62. Luo, Z.-X., Ruf, I., Schultz, J. A, & Martin, T. (2011). Fossil evidence on evolution of inner ear cochlea in Jurassic mammals. Proceedings of Royal Society of London B: Biological Sciences, 278, 28–34. doi: 10.1073/pnas.1519387112 CrossRefGoogle Scholar
  63. Luo, Z.-X., Ruf, I., & Martin, T. (2012). The petrosal and inner ear of the Late Jurassic cladotherian mammal Dryolestes leiriensis and implications for evolution of the ear in therian mammals. Zoological Journal of the Linnean Society, 166, 433–463. doi: 10.1111/j.1096–3642.2012.00852.x CrossRefGoogle Scholar
  64. Luo, Z.-X., Gatesy, S. M., Jenkins, F. A., & Amaral, A. A. (2015a). Mandibular and dental characteristics of Late Triassic mammaliaform Haramiyavia and their ramifications for basal mammal evolution. Proceedings of National Academy of Sciences of the USA, 112, E7101–E7109. doi: 10.1073/pnas.1519387112 Google Scholar
  65. Luo, Z.-X., Meng, Q.-J., Ji, Q., Liu, D., Zhang, Y.-G., & Neander, A. I. (2015b). Evolutionary development in basal mammaliaforms as revealed by a docodontan. Science, 347, 760–764. doi: 10.1126/science.1260880 PubMedCrossRefGoogle Scholar
  66. Maier, W., & van den Heever, J. (2002). Middle ear structures in Permian Glanosuchus sp. (Therocephalia, Therapsida), based on thin sections. Mitteilungen aus dem Museum für Naturkunde in Berlin (Geowissenschaften Eihe), 5, 309–318.Google Scholar
  67. Maier, W., & Ruf, I. (2016). Evolution of the mammalian middle ear: A historical review. Journal of Anatomy, 228, 270–283. doi: 10.1111/joa.12379 PubMedCrossRefGoogle Scholar
  68. Manley, G. A. (2010). An evolutionary perspective on middle ears. Hearing Research, 263, 3–8. doi: 10.1016/j.heares.2009.09.004 PubMedCrossRefGoogle Scholar
  69. Manley, G. A. (2012). Evolutionary paths to mammalian cochleae. Journal of Association of Research on Otolaryngology, 13, 733–743. doi: 10.1007/s10162–012–349–9 CrossRefGoogle Scholar
  70. Manley, G. A., & Clack, J. A. (2004). An outline of 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 Science+Business Media.CrossRefGoogle Scholar
  71. Martin, T., Marugán–Lobón, J., Vullo, R., Martín–Abad, H., Luo, Z.-X., & Buscalioni, A. D. (2015). A Cretaceous eutriconodont and integument evolution in early mammals. Nature, 526, 380–384. doi: 10.1038/nature14905 PubMedCrossRefGoogle Scholar
  72. Mason, M. J., & Narins, P. M. (2001). Seismic signal use by fossorial mammals. American Zoologist, 41(5), 1171–1184.Google Scholar
  73. Meng, J. (1992) The stapes of Lambdopsalis bulla (Multituberculata) and transformational analyses on some stapedial features in Mammaliaformes. Journal of Vertebrate Paleontology, 12, 459–471.CrossRefGoogle Scholar
  74. Meng, J., & Fox, R. C. (1995). Osseous inner ear structures and hearing in early marsupials and placentals. Zoological Journal of the Linnean Society, 115, 47-71.CrossRefGoogle Scholar
  75. Meng, J., Hu, Y.-M., Wang, Y.-Q., & Li, C.-K. (2003). The ossified Meckel’s cartilage and internal groove in Mesozoic mammaliaforms: Implications to origin of the definitive mammalian middle ear. Zoological Journal of the Linnean Society, 138, 431–448.Google Scholar
  76. Meng, J., Wang, Y.-Q., & Li, C. (2011). Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont. Nature, 472, 181–185. doi: 10.1038/nature09921 PubMedCrossRefGoogle Scholar
  77. Meng, Q.-J., Ji, Q., Zhang, Y.-G., Liu, D., et al. (2015). An arboreal docodont from the Jurassic and mammaliaform ecological diversification. Science, 347, 764–768. doi: 10.1126/science.1260879 Google Scholar
  78. Miao, D. (1988). Skull morphology of Lambdopsalis bulla (Mammalia, Multituberculata). Contributions in Geology, University of Wyoming, Special Papers, 4, 1–104.Google Scholar
  79. Novacek, M. J., & Wyss, A. (1986) Origin and transformation of the mammalian stapes. Contributions to Geology, University of Wyoming, Special Papers, 3, 35–53.Google Scholar
  80. O’Gorman, S. (2005). Second branchial arch lineages of the middle ear of wild‐type and Hoxa2 mutant mice. Developmental Dynamics, 234(1), 124–131. doi: 10.1002/dvdy.20402 PubMedCrossRefGoogle Scholar
  81. O’Meara, R. N., & Thompson, R. S. (2014). Were there Miocene meridolestidans? Assessing the phylogenetic placement of Necrolestes paragonenesis and the presence of a 40 million year meridiolestidan ghost lineage. Journal of Mammalian Evolution, 21, 271–284. doi: 10.1007/s10914–013–9252–3 CrossRefGoogle Scholar
  82. Phillips, M. J., Bennett, T. H., & Lee, M. S. Y. (2009). Molecules, morphology, and ecology indicate a recent, amphibious ancestry for echidnas. Proceedings of the National Academy of Sciences of the USA, 106, 17089–17094. doi: 10.1073/pnas.0904649106 PubMedPubMedCentralCrossRefGoogle Scholar
  83. Pye, A. (1970). The structure of the cochlea in Chiroptera—a selection of Microchiroptera from Africa. Journal of Zoology (London), 162, 335–343.CrossRefGoogle Scholar
  84. Quiroga, J. C. (1979). The inner ear of two cynodonts (Repitlia–Therapsida) and some comments on the evolution of the inner ear from pelycosaurs to mammals. Gegenbauers Morphologishces Jahrbuch, 125, 178–190.Google Scholar
  85. Rich, T. H., Vickers-Rich, P., Trusler, P., Flannery, T. F., et al. (2001). Monotreme nature of the Australian Early Cretaceous mammal Teinolophos trusleri. Acta Palaeontologica Polonica, 46, 113–118.Google Scholar
  86. Rich, T. H., Hopson, J. A., Musser, A. M., Flannery, T. F., & Vickers, P. (2005). Independent origins of middle ear bones in monotremes and therians. Science, 307, 910–914. doi: 10.1126/science.1105717 PubMedCrossRefGoogle Scholar
  87. Rodrigues, G. P., Ruf, I., & Schultz, C. L. (2013). 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. Journal of Mammalian Evolution, 20, 291–307. doi: 10.1007/s10914–012–9221–2 CrossRefGoogle Scholar
  88. 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. 615–631). New York: Springer-Verlag.CrossRefGoogle Scholar
  89. Rougier, G. W., & Wible, J. R. (2006). Major changes in the mammalian ear region and basicranium. In M. T. Carrano, T. J. Gaudin, R. W. Blob, & J. R. Wible (Eds.), Amniote paleobiology: Perspectives on the evolution of mammals, birds, and reptiles (pp. 269–311). Chicago: University of Chicago Press.Google Scholar
  90. Rougier, G. W., Wible, J. R., & Hopson, J. A. (1996). Basicranial anatomy of Priacodon fruitaensis (Triconodontidae, Mammalia) from the Late Jurassic of Colorado, and a reappraisal of mammaliaforms interrelationships. American Museum Novitates, 3183, 1–38.Google Scholar
  91. Rougier, G. W., Forasiepi, A. M., & Martinelli, A. G. (2005). Comments on “Independent origins of the middle ear bones in monotremes and therians” (II). Science, 309, 1492E.CrossRefGoogle Scholar
  92. Rougier, G. W., Martinelli, A. G., Forasiepi, A. M., & Novacek, M. J. (2007). New Jurassic mammals from Patagonia, Argentina: A reappraisal of australosphenidan morphology and interrelationship. American Museum Novitates, 3566, 1–54. doi: 10.1206/0003–0082(2007)3580[1:FJTFSA]2.0.CO;2 CrossRefGoogle Scholar
  93. Rowe, T. (1988). Definition, diagnosis, and origin of Mammalia. Journal of Vertebrate Paleontology, 8, 241–264.CrossRefGoogle Scholar
  94. Rowe, T. B. (1993). Phylogenetic systematics and the early history of mammals. In F. S. Szalay, M. J. Novacek, & M. C. McKenna (Eds.), Mammal phylogeny: Mesozoic differentiation, multituberculates, monotremes, early therians, and marsupials (pp. 129–145). New York: Springer-Verlag.CrossRefGoogle Scholar
  95. Rowe, T., Carlson, W., & Bottorff, W. (1995). Thrinaxodon – Digital Atlas of the skull. Austin (TX): University of Texas Press.Google Scholar
  96. Rowe, T. B., Rich, T. H., Vickers–Rich, P., Woodburne, M. O., & Springer, M. (2008). The oldest platypus and its bearing on divergence timing of the platypus and echidna clades. Proceedings of the National Academy of Sciences of the USA, 105, 1238–1342. doi: 10.1073/pnas.0706385105 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Ruf, I., Luo, Z.-X., Wible, J. R., & Martin, T. (2009). Petrosal anatomy and inner ear structure of the Late Jurassic mammal Henkelotherium and the ear region characters of basal therian mammals. Journal of Anatomy, 214, 679–693. doi: 10.1111/j.1469–7580.2009.01059.x
  98. Ruf, I., Luo, Z.-X., & Martin, T. (2013). Re–investigation of the basicranium of Haldanodon exspectatus (Docodonta, Mammaliaformes). Journal of Vertebrate Paleontology, 33, 382–400. doi: 10.1080/02724634.2013.722575 CrossRefGoogle Scholar
  99. Schmelzle, T. M. R., Nummela, S., & Sanchez–Villagra, M. R. (2005). Phylogenetic transformations of the ear ossicles in marsupial mammals, with special reference to diprotodontians: A character analysis. Annals of the Carnegie Museum, 74, 189–200.CrossRefGoogle Scholar
  100. Sidor, C. A. (2001). Simplification as a trend in synapsid cranial evolution. Evolution, 55, 1419–1442.PubMedCrossRefGoogle Scholar
  101. Sues, H.-D. (1986). The skull and dentition of two tritylodontid synapsids from the Lower Jurassic of western North America. Bulletin of the Museum of Comparative Zoology, 151, 217–268.Google Scholar
  102. Takechi, M., & Kuratani, S. (2010). History of studies on mammalian middle ear evolution: A comparative morphological and developmental biology perspective. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 314B, 417–433. doi: 10.1002/jez.b.21347 CrossRefGoogle Scholar
  103. Tumarkin, A. (1968). Evolution of the auditory conducting apparatus in terrestrial vertebrates. In A. S. de Reuck & J. Knight (Eds.), Cib foundation symposium on hearing mechanisms in vertebrates (pp. 18–37). London: Churchill.Google Scholar
  104. Vater, M., & Kössl, M. (2011). Comparative aspects of cochlear functional organization in mammals. Hearing Research, 273, 89–99. doi: 10.1016/j.heares.2010.05.018 PubMedCrossRefGoogle Scholar
  105. Walsh, S. A., Luo, Z.-X., & Barrett, P. M. (2013). Modern imaging techniques as a window to prehistoric auditory worlds. In C. Köppel, G. A. Manley, A. N. Popper, & R. R. Fay (Eds.), Insights from comparative hearing research. (pp. 227–261). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  106. Wang, Y., Zheng, Y., Chen, D., & Chen, Y.-P. (2013). Enhanced BMP signaling prevents degeneration and leads to endochondral ossification of Meckel’s cartilage in mice. Developmental Biology, 381, 301–311. doi: 10.1016/j.ydbio.2013.07.016 PubMedPubMedCentralCrossRefGoogle Scholar
  107. Weston, J. K. (1939). Notes on comparative anatomy of the ganglion cells associated with the vertebrate inner ear sensory areas. Journal of Anatomy, 73, 263–288.PubMedPubMedCentralGoogle Scholar
  108. Wever, E. G. (1978). The reptile ear. Princeton: Princeton University Press.Google Scholar
  109. Wible, J. R., & Hopson, J. A. (1993). Basicranial evidence for early mammal phylogeny. In F. S. Szalay, M. J. Novacek, & M. C. McKenna (Eds.), Mammal phylogeny: Mesozoic differentiation, multituberculates, monotremes, early therians, and marsupials (pp. 45–62). New York: Springer-Verlag.CrossRefGoogle Scholar
  110. Williams, P. L., Williams, R., Dyson, M., & Bannister, L. H. (1989). Gray’s Anatomy, 37th ed. New York: Churchill Livingstone.Google Scholar
  111. Witmer, L. M. (1995). The Extant Phylogenetic Bracket and the importance of reconstructing soft tissues in fossils. In J. Thomason (Ed.), Functional morphology in vertebrate paleontology (pp. 19–33). Cambridge (UK): Cambridge University Press.Google Scholar
  112. Zeller, U. (1989). Die Enwicklung und Morphologie des Schädels von Ornithorhynchus anatinus (Mammalia: Prototheria: Monotremata). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, 545, 1–188.Google Scholar
  113. Zhou, C.-F., Wu, S., Martin, T., & Luo, Z.-X. (2013). A Jurassic mammaliaform and the earliest mammalian evolutionary adaptations. Nature, 500, 163–167. doi: 10.1038/nature12429 Google Scholar

Copyright information

© Springer International Publishing AG 2016

Authors and Affiliations

  • Zhe-Xi Luo
    • 1
  • Julia A. Schultz
    • 1
  • Eric G. Ekdale
    • 2
    • 3
    Email author
  1. 1.Department of Organismal Biology and AnatomyThe University of ChicagoChicagoUSA
  2. 2.Department of BiologySan Diego State UniversitySan DiegoUSA
  3. 3.Department of PaleontologySan Diego Natural History MuseumSan DiegoUSA

Personalised recommendations