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The inner ear of gymnophione amphibians and its nerve supply: A comparative study of regressive events in a complex sensory system (Amphibia, Gymnophiona)

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Summary

The inner ears of representatives of all six gymnophionan families, as well as an ontogenetic series of one species, were studied in order to understand the origin and changes of the amphibian and basilar papillae. The amphibian papilla is in close proximity to the papilla neglecta in some adult gymnophionans. During ontogeny, both epithelia are adherent before they are separated by the formation of the utriculosaccular foramen. The nerve fibers to both epithelia run together, and both epithelia show a comparable variation in size and position among amphibians (amphibian papilla) and among vertebrates (papilla neglecta). Based on these arguments we propose that the amphibian papilla is a translocation of a part of the papilla neglecta specific to amphibians. Present in all primitive gymnophionans, the basilar papilla is lost in all derived gymnophionans. In contrast to anurans, but similar to some urodeles, amniotes, and Latimeria, the basilar papilla rests partly on a basilar membrane. Because of similarities in structure, topology, and innervation, the basilar papilla is suggested to be homologous in Latimeria and tetrapods. The structural differences of most amphibian basilar papillae, compared to those of amniotes and Latimeria, may be due to the different course of the periotic system and the formation of a basilar papillar recess rather than to a separate evolution of this epithelium. In addition to loss of the basilar papilla, some derived gymnophionans have lost the lagena, presumably independently, and the amphibian papilla is extremely reduced in the only genus without a stapes (Scolecomorphus). The papilla neglecta is, for unknown functional reasons, relatively large in aquatic gymnophionans, whereas it is almost lost in some thoroughly terrestrial gymnophionans. The regressive changes in the inner ear are not reflected in obvious changes in the pattern of eighth nerve projection. However, there is a rearrangement of cell masses in the rhombencephalic alar plate of derived gymnophionans, which may be related to the partial or complete loss of lateral line afferents. We propose that the presence of a basilar papilla is a synapomorphy of tetrapods and Latimeria, that the translocation of the papilla neglecta is related to the unique course of the amphibian periotic canal, and that regressive changes in the inner ear are related to the primitive absence of a tympanic ear.

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References

  • Alexander G (1904) Entwicklung und Bau des inneren Gehörorgans von Echidna ac. Denkschr Med Naturwiss Ges Jena 6:1–160

    Google Scholar 

  • Alfs B, Schneider H (1973) Vergleichend-anatomische Untersuchungen am Labyrinth zentraleuropäischer Froschlurch-Arten (Anura). Z Morphol Tiere 76:129–143

    Google Scholar 

  • Baird IL (1974) Anatomical features of the inner ear in submammalian vertebrates. In: Keidel WD, Neff WD (eds) Handbook of sensory physiology, vol. V/1. Springer, Berlin Heidelberg New York, pp 159–212

    Google Scholar 

  • Brand DJ (1956) On the cranial morphology of Scolecomorphus uluguruensis (Barbour and Loveridge). Ann Univ Stellenbosch 32:1–25

    Google Scholar 

  • Billo R, Wake MH (1987) Tentacle development in Dermophis mexicanus (Amphibia, Gymnophiona) with an hypothesis of tentacle origin. J Morphol 192:101–111

    Google Scholar 

  • Corwin JT (1981) Postembryonic production and aging of inner ear hair cells in sharks. J Comp Neurol 201:541–554

    Google Scholar 

  • Corwin JT (1985) Perpetual production of hair cells and maturational changes in hair cell ultrastructure accompany postembryonic growth in an amphibian ear. Proc Natl Acad Sci USA 82:3911–3915

    Google Scholar 

  • de Burlet HM (1928) Über die Papilla neglecta. Anat Anz 66:199–209

    Google Scholar 

  • de Burlet HM (1929) Zur vergleichenden Anatomie der Labyrinth-innervation. J Comp Neurol 47:155–169

    Google Scholar 

  • de Burlet HM (1934) Vergleichende Anatomie des statoakustischen Organs. a) Die innere Ohrsphäre; b) Die mittlere Ohrsphäre. In: Bolk L, Göppert E, Kallius E, Lubosch W (eds) Handbuch der Vergleichenden Anatomie der Wirbeltiere, vol 2. Urban & Schwarzenberg, Berlin

    Google Scholar 

  • De Villiers CGS (1938) A comparison of some cranial features of the East African gymnophiones Boulengerula boulengeruli, Tornier and Scolecomorphus uluguruensis, Boulenger. Anat Anz 86:1–26

    Google Scholar 

  • Duellman WE, Trueb L (1986) Biology of amphibians. McGraw-Hill, New York, pp 670

    Google Scholar 

  • Filipski GT, Wilson MVH (1984) Sudan Black B as a nerve stain for whole cleared fishes. Copeia 1:204–208

    Google Scholar 

  • Fleissig J (1908) Die Entwicklung des Geckolabyrinths. Anat Hefte 37:1–116

    Google Scholar 

  • Fritzsch B (1981) The pattern of lateral line afferents in urodeles. Cell Tissue Res 218:581–594

    Google Scholar 

  • Fritzsch B (1987) The inner ear of the coelacanth fish Latimeria has tetrapod affinities. Nature 327:153–154

    Google Scholar 

  • Fritzsch B (1988a) Phylogenetic and ontogenetic origin of the dorsolateral auditory nucleus of anurans. In: Fritzsch B, Ryan M, Wilczynski W, Hetherington TH, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 561–585

    Google Scholar 

  • Fritzsch B (1988b) The inner ear projections of larval and adult urodeles. Brain Behav Evol 31:325–348

    Google Scholar 

  • Fritzsch B, Wake MH (1986) A note on the distribution of ampullary organs in gymnophiones. J Herpetol 20:90–93

    Google Scholar 

  • Fritzsch B, Nikundiwe AM, Will U (1984) Projection patterns of lateral line afferents in anurans. A comparative study using transganglionic transport of HRP. J Comp Neurol 229:451–469

    Google Scholar 

  • Fritzsch B, Crapon de Caprona M-D, Himstedt W (1985a) Visual projections in larval Ichthyophis kohtaoensis (Amphibia: Gymnophiona). Dev Brain Res 23:201–210

    Google Scholar 

  • Fritzsch B, Wahnschaffe U, Crapon de Caprona M-D, Himstedt W (1985b) Anatomical evidence for electroreception in larval Ichthyophis kohtaoensis. Naturwissenschaften 72:102–104

    Google Scholar 

  • Fritzsch B, Wahnschaffe U, Bartsch U (1988) Metamorphic changes in the octavolateralis system of amphibians. In: Fritzsch B, Ryan M, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 359–376

    Google Scholar 

  • Harrison HS (1902) On the perilymphatic spaces of the amphibian ear. Int Monatsschr Anat Physiol 19:221–261

    Google Scholar 

  • Hasse C (1868) Das Gehörorgan der Frösche. Z Wiss Zool 18:1–120

    Google Scholar 

  • Hetherington TE (1988) Metamorphic changes in the middle ear. In: Fritzsch B, Ryan M, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 339–357

    Google Scholar 

  • Hudspeth AJ (1983) The hair cells of the inner ear. Sci Am 248:42–52

    Google Scholar 

  • Jaslow AP, Hetherington TE, Lombard RE (1988) Structure and function of the amphibian middle ear. In: Fritzsch B, Ryan M, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 69–91

    Google Scholar 

  • Jörgensen JM (1981) On a possible hair cell turn-over in the inner ear of the caecilian Ichthyophis glutinosus (Amphibia: Gymnophiona). Acta Zool 62:171–186

    Google Scholar 

  • Lewis ER, Leverenz EL, Bialek W (1985) The vertebrate inner ear. CRC Press, Boca Raton, p. 256

    Google Scholar 

  • Lewis ER, Lombard RE (1988) The amphibian inner ear. In: Fritzsch B, Ryan M, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 93–123

    Google Scholar 

  • Lombard RE (1977) Comparative morphology of the inner ear in salamanders (Caudata: Amphibia). Contrib Vert Evol 2:1–143

    Google Scholar 

  • Lombard RE, Bolt JR (1979) Evolution of the tetrapod ear: an analysis and reinterpretation. Biol J Linn Soc 11:19–76

    Google Scholar 

  • Lombard RE, Bolt JR (1988) Evolution of the stapes in paleozoic tetrapods. In: Fritzsch B, Ryan M, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 37–67

    Google Scholar 

  • McCormick CA, Braford MR (1987) Central connections of the octavo-lateralis system: evolutionary considerations. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals, Springer, Berlin Heidelberg New York, pp 733–756

    Google Scholar 

  • Millot J, Anthony J (1965) Anatomie de Latimeria chalumnae. Tome II. Paris, CNRS, p 125

    Google Scholar 

  • Northcutt RG (1984) Evolution of the vertebrate central nervous system: patterns and processes. Am Zool 24:701–716

    Google Scholar 

  • Northcutt RG (1986) Electroreception in nonteleost bony fishes. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 257–287

    Google Scholar 

  • Okajima K (1911) Die Entwicklung des Gehörorgans von Hynobius. Anat Hefte 45:1–80

    Google Scholar 

  • Popper AN (1978) A scanning electron microscopic study of the otolithic organs in the bichir (Polypterus bichir) and shovel nose sturgeon (Scaphyrhinchus platorhynchus). J Comp Neurol 181:117–128

    Google Scholar 

  • Proebsting G (1924) Zellenzahl und Zellengröße im Labyrinthorgan der Tritonen, nebst anderen damit zusammenhängenden Fragen. Zool Jahrb Abt Allg Zool Physiol Tiere 41:425–488

    Google Scholar 

  • Purves D, Lichtman JW (1985) Principles of neuronal development. Sinauer, Sunderland, p 287

    Google Scholar 

  • Remane A (1956) Die Grundlagen des natürlichen Systems, der vergleichenden Anatomie und der Phylogenetik. Koeltz, Koenigstein, pp 364

    Google Scholar 

  • Retzius G (1881a) Das Gehörorgan der Wirbeltiere. I. Das Gehörorgan der Fische und Amphibien. Samson und Wallin, Stockholm, p 286

    Google Scholar 

  • Retzius G (1881b) Das membranöse Gehörorgan von Polypterus bichir Geoffr. und Calomoichthys calabricus J A Smith. Biol Unters 4:61–66

    Google Scholar 

  • Retzius G (1884) Das Gehörorgan der Wirbeltiere: II. Das Gehörorgan der Amnioten. Samson und Wallin, Stockholm, pp 345

    Google Scholar 

  • Roth G, Wake DB (1985) The structure of the brainstem and cervical spinal cord in lungless salamanders (Family Plethodontidae) and its relation to feeding. J Comp Neurol 241:99–110

    Google Scholar 

  • Sarasin P, Sarasin F (1888) Zur Entwicklungsgeschichte und Anatomie der ceylonesischen Blindwühle Ichthyophis glutinosus. Das Gehörorgan. Ergebnisse Naturwiss Forsch auf Ceylon, Bd 2. Kreidels Verlag, Wiesbaden, pp 207–222

    Google Scholar 

  • Sarasin P, Sarasin F (1892) Über das Gehörorgan der Caeciliiden. Anat Anz 7:812–815

    Google Scholar 

  • Starck D (1979) Die vergleichende Anatomie der Wirbeltiere. Springer, Berlin Heidelberg New York, p 274

    Google Scholar 

  • van Bergijk WA (1967) Evolution of the sense of hearing in vertebrates. Am Zool 6:371–377

    Google Scholar 

  • Wake MH (1980) Fetal tooth development and adult replacement in Dermophis mexicanus (Amphibia: Gymnophiona): fields versus clones. J Morphol 166:203–216

    Google Scholar 

  • Wake MH (1982) Diversity within a framework of constraints. In: Mossakowski D, Roth G (eds) Environmental adaptation and evolution. Fischer, Stuttgart, pp 87–106

    Google Scholar 

  • Wake MH (1985) The comparative morphology and evolution of the eyes of caecilians (Amphibia, Gymnophiona). Zoomorphology 105:277–295

    Google Scholar 

  • Wake MH (1986) A perspective on the systematics and morphology of the Gymnophiona (Amphibia). Mem Soc Zool Fr 43:21–38

    Google Scholar 

  • Wake MH, Hanken J (1982) The development of the skull of Dermophis mexicanus (Amphibia: Gymnophiona), with comments on scull kinesis and amphibian relationships. J Morphol 173:203–223

    Google Scholar 

  • Wegener NT, Jörgensen JM (1982) Hair cell polarization in the inner ear of a caecilian. Ichthyophis glutinosus (Amphibia: Gymnophiona). Acta Zool 63:1–6

    Google Scholar 

  • Werner G (1960) Das Labyrinth der Wirbeltiere. Fischer, Jena, p 309

    Google Scholar 

  • Wever EG (1974) The evolution of vertebrate hearing. In: Keidel WD, Neff WD (eds) Handbook of sensory physiology, vol V/1: Auditory system. Springer, Berlin Heidelberg New York, pp 423–454

    Google Scholar 

  • Wever EG (1978) The reptilian ear. Princeton University Press, New Jersey, p 806

    Google Scholar 

  • Wever EG (1985) The amphibian ear. Princeton University Press, New Jersey, p 405

    Google Scholar 

  • White JS, Baird IL (1982) Comparative morphological features of the caecilian inner ear with comments on the evolution of amphibian auditory structures. Scann Electron Microbiol 3:1301–1312

    Google Scholar 

  • Will U, Fritzsch B (1988) The octavus nerve of amphibians: Patterns of afferents and efferents. In: Fritzsch B, Ryan M, Wilczynski W, Hetherington T, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 159–183

    Google Scholar 

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  1. Faculty of Biology, University of Bielefeld, D-4800, Bielefeld 1, Federal Republic of Germany

    B. Fritzsch

  2. Department of Zoology and Museum of Vertebrate Zoology, University of California, 94720, Berkeley, CA, USA

    M. H. Wake

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  1. B. Fritzsch
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Fritzsch, B., Wake, M.H. The inner ear of gymnophione amphibians and its nerve supply: A comparative study of regressive events in a complex sensory system (Amphibia, Gymnophiona). Zoomorphology 108, 201–217 (1988). https://doi.org/10.1007/BF00312221

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