Abstract
This chapter presents the history of discoveries in hair cell evolution, mechanosensory organ evolution (vestibular ears, lateral line, and paratympanic organ) and evolution of the auditory system and relates them to the molecular basis of their development and evolution. The mechanosensory hair cell, once recognized as a unique vertebrate cell peculiar to the mechanosensory organs of the inner ear and lateral line, can now be developmentally and molecularly linked to nonmechanosensory cells in vertebrates (the electroreceptive “hair cells” of many aquatic vertebrates) and other outgroups (various ciliated cells of diploblasts and triploblasts that share gene expression similarities. This progress in understanding the evolution of the vertebrate mechanosensory cell is put into the context of understanding the evolution of mechanosensory organs. Progress in this area hinges on molecular comparisons of eye and ear development and indicates that both organ types may share a “deep molecular homology” of a super regulator, the Pax genes. Evolutionary transformation of gravistatic sensors into sound pressure receivers happened multiple times in aquatic vertebrates but the transformation of the tetrapod system differs in many structural and molecular aspects from that in bony fish. The current state of our understanding of the molecular basis of this transition is reviewed and put into the historical context of ideas around this subject and their changes over time.
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References
Arendt, D. (2003). Evolution of eyes and photoreceptor cell types. International Journal of Developmental Biology, 47(7–8), 563–571.
Bouchard, M., Busslinger, M., Xu, P., De Caprona, D., & Fritzsch, B. (2010). PAX2 and PAX8 cooperate in mouse inner ear morphogenesis and innervation. BMC Developmental Biology, 10, 89.
Braun, C. B., & Northcutt, R. G. (1997). The lateral line system of hagfishes (Craniata: Myxinoidea). Acta Zoologica, 3, 247–268.
Darwin, C. (1859). On the origin of species by means of natural selection or the preservation of favoured races in the struggle for life. London: Murray.
de Burlet, H. M. (1934). Vergleichende Anatomie des statoakustischen Organs. a) Die innere Ohrsphäre. In L. Bolk, E. Göppert, E. Kallius & W. Lubosch (Eds.), Handbuch der Vergleichenden Anatomie der Wirbeltiere (Vol. 2, pp. 1293–1432). Berlin: Urban and Schwarzenberg.
Duncan, J. S., & Fritzsch, B. (2012). Evolution of sound & balance perception: Innovations that aggregate single hair cells into the ear and transform a gravistatic sensor into the organ of Corti. Journal of Anatomy, 295, 1760–1774.
Fritzsch, B. (1981). The pattern of lateral-line afferents in urodeles: A horseradish-peroxidase study. Cell and Tissue Research, 218(3), 581–594.
Fritzsch, B. (1991). Ontogenetic clues to the phylogeny of the visual system. In P. Bagnoli & W. Hodos (Eds.), The changing visual system (pp. 33–49). London: Plenum Press.
Fritzsch, B. (1992). The water-to-land transition: Evolution of the tetrapod basilar papilla, middle ear and auditory nuclei. In D. B. Webster, R. R. Fay, & A. N. Popper (Eds.), The evolutionary biology of hearing (pp. 351–375). New York: Springer-Verlag.
Fritzsch, B. (1999). Hearing in two worlds: Theoretical and realistic adaptive changes of the aquatic and terrestrial ear for sound reception. In R. R. Fay & A. N. Popper (Eds.), Comparative hearing: Fish and amphibians. (pp. 15–42). New York: Springer-Verlag.
Fritzsch, B., & Wahnschaffe, U. (1983). The electroreceptive ampullary organs of urodeles. Cell and Tissue Research, 229(3), 483–503.
Fritzsch, B., & Wake, M. H. (1988). The inner ear of gymnophione amphibians and its nerve supply: A comparative study of regressive events in a complex sensory system. Zoomorphology, 108, 210–217.
Fritzsch, B., & Glover, J. C. (2007). Evolution of the deuterostome central nervous system: An intercalation of developmental patterning processes with cellular specification processes. In J. H. Kaas (Ed.), Evolution of nervous systems (Vol. 2, pp. 1–24). Oxford: Academic Press.
Fritzsch, B., Eberl, D. F., & Beisel, K. W. (2010). The role of bHLH genes in ear development and evolution: Revisiting a 10-year-old hypothesis. Cell and Molecular Life Sciences, 67(18), 3089–3099.
Fritzsch, B., Pan, N., Jahan, I., Duncan, J. S., Kopecky, B. J., Elliott, K. L., Kersigo, J., & Yang, T. (2013). Evolution and development of the tetrapod auditory system: An organ of Corti-centric perspective. Evolution & Development, 15, 63–79.
Gehring, W. J. (2011). Chance and necessity in eye evolution. Genome Biology and Evolution, 3, 1053–1066.
Grocott, T., Tambalo, M., & Streit, A. (2012). The peripheral sensory nervous system in the vertebrate head: A gene regulatory perspective. Developmental Biology, 370(1), 3–23.
Grothe, B., Carr, E. C., Casseday, J. H., Fritzsch, B., & Köppl, C. (2004). The evolution of central pathways and their neural processing patterns. In G. A. Manley, A. N. Popper, & R. R. Fay (Eds.), Evolution of the vertebrate auditory system. (pp. 289–359). New York: Springer Science+Business Media.
Jahan, I., Pan, N., Kersigo, J., Calisto, L. E., Morris, K. A., Kopecky, B., Duncan, J. S., Beisel, K. W., & Fritzsch, B. (2012). Expression of Neurog1 instead of Atoh1 can partially rescue organ of Corti cell survival. PLoS One, 7(1), e30853.
Jørgensen, J. M. (1989). Evolution of octavolateralis sensory cells. In S. Coombs, P. Goerner, & H. Muenz (Eds.), The mechanosensory lateral line: Neurobiology and evolution (pp. 99–115.). New York: Springer Verlag.
Ladich, F., & Popper, A. N. (2004). Parallel evolution of 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 Science+Business Media.
Lamb, T. D. (2013). Evolution of phototransduction, vertebrate photoreceptors and retina. Progress in Retinal and Eye Research, 36, 52–119.
Lewis, E. R., & Fay, R. R. (2004). Environmental variables and the fundamental nature of hearing. In G. A. Manley, A. N. Popper, & R. R. Fay (Eds.), Evolution of the vertebrate auditory system (pp. 27–54). New York: Springer Science+Business Media.
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.
Markl, H. (1974). The perception of gravity and of angular acceleration in invertebrates. In H. H. Kornhuber (Ed.), Handbook of sensory physiology (Vol. VI/1: Vestibular system, pp. 17–74). Berlin: Springer-Verlag.
Munz, H., Claas, B., & Fritzsch, B. (1982). Electrophysiological evidence of electroreception in the axolotl Siredon mexicanum. Neuroscience Letters, 28(1), 107–111.
O’Neill, P., Mak, S.-S., Fritzsch, B., Ladher, R. K., & Baker, C. V. H. (2012). The amniote paratympanic organ develops from a previously undiscovered sensory placode. Nature Communications, 3, 1041.
Pan, N., Kopecky, B., Jahan, I., & Fritzsch, B. (2012). Understanding the evolution and development of neurosensory transcription factors of the ear to enhance therapeutic translation. Cell and Tissue Research, 349, 415–432.
Reichert, C. (1837). Ueber die Visceralbogen der Wierbelthiere im allgemeinen und deren Metamorphose bei den Saeugethieren und Voegeln. Acta Anatomica & Physiologica, 120–222.
Retzius, G. (1881). Das Gehörorgan der Wirbeltiere (Vol. I. ). Stockholm: Valin.
Senthilan, P. R., Piepenbrock, D., Ovezmyradov, G., Nadrowski, B., Bechstedt, S., Pauls, S., Winkler, M., Mobius, W., Howard, J., & Gopfert, M. C. (2012). Drosophila auditory organ genes and genetic hearing defects. Cell, 150(5), 1042–1054.
Shubin, N., Tabin, C., & Carroll, S. (2009). Deep homology and the origins of evolutionary novelty. Nature, 457(7231), 818–823.
Simmons, D., Duncan, J., Crapon de Caprona, D., & Fritzsch, B. (2011). Development of the inner ear efferent system. In D. K. Ryugo, R. R. Fay, & A. N. Popper (Eds.), Auditory and vestibular efferents (pp. 187–216.). New York: Springer Science+Business Media.
Wagner, A. (2011). The origins of evolutionary innovations. Oxford: Oxford University Press.
Acknowledgments
This work has been supported by grants from National Aeronautics and Space Administration, National Institutes of Health, the German Science Foundation, and funds from Office of the Vice Provost for Research of the University of Iowa.
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Fritzsch, B., de Caprona, MD.C. (2014). Evolving Mechanosensory Hair Cells to Hearing Organs by Altering Genes and Their Expression: The Molecular and Cellular Basis of Inner Ear and Auditory Organ Evolution and Development. In: Popper, A., Fay, R. (eds) Perspectives on Auditory Research. Springer Handbook of Auditory Research, vol 50. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-9102-6_10
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