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The early formation of the skull in extant and Paleozoic amphibians
Published online by Cambridge University Press: 08 April 2016
Abstract
Understanding of evolutionary changes in the vertebrate skull is greatly influenced by the knowledge of ontogeny. Extant amphibians are an outstanding example in this field, because their life cycles are complex and have been intensively studied. At the same time, fossil material of Paleozoic amphibians has become available that sheds light on the ontogeny of a long-extinct clade, prompting comparison with recent forms. In this paper, the formation of the skull of a Paleozoic amphibian (the branchiosaurid temnospondyl Apateon) is analyzed in comparison with that of an extant salamander (the hynobiid Ranodon). Both temporal patterns (sequence of ossification) and spatial patterns (morphological changes) are described. The general results are that (1) the sequence of ossification is similar in many aspects, and (2) most dermal bones share fundamental similarities in morphogenesis, although sometimes the morphological result in adults may differ conspicuously.
The comparison reveals that the parasphenoid, premaxillae, maxillae, frontals, parietals, squamosals, and prefrontals are strikingly similar in their mode of growth. In particular, the appearance of the earliest primordia and the subsequent stages of morphological transformation are almost identical. The development of the pterygoids and nasals is different in the earliest stages, but the ontogenetic trajectories converge in later stages. In Ranodon and other transforming urodeles, the pterygoids and vomers experience extensive resorption during metamorphic climax, whereas in branchiosaurids the morphology of this region remains stable throughout ontogeny.
In the sequence of cranial ossifications, the early appearance of the premaxilla and tooth-bearing elements of the palate characterize both genera, but the maxilla forms much later in Ranodon. The ectopterygoid, absent in all salamanders, is the last palatal element to appear in branchiosaurids. In the skull roof, the parietals, frontals, and squamosals are the first bones to form in both groups. Conversely, the circumorbital elements and tabular are among the last ossifications in branchiosaurids, and the prefrontal and lacrimal (the only circumorbital bones present in salamanders) form within the same interval in urodele ontogeny. The septomaxilla is the last dermal element to ossify in both groups. Comparison with caecilians and anurans indicates that salamanders are much more similar to Paleozoic branchiosaurids than to other extant lissamphibians. A major difference between salamanders and branchiosaurids is that the morphology of the latter is much less affected by developmental perturbations, such as larval specializations and metamorphosis.
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Literature Cited
Aoyama, F. 1930. Die Entwicklungsgeschichte des Kopfskeletts des Cryptobranchus japonicus. Zeitschrift für Anatomie und Entwicklungsgeschichte 93:106–181.Google Scholar
Bolt, J. R. 1977. Dissorophoid relationships and ontogeny, and the origin of the Lissamphibia. Journal of Paleontology 51:235–249.Google Scholar
Bolt, J. R. 1979. Amphibamus grandiceps as a juvenile dissorophid: evidence and implications. Pp. 529–563in Nitecki, M. H., ed. Mazon Creek fossils. Academic Press, London.Google Scholar
Bolt, J. R., and Lombard, R. E. 1985. Evolution of the amphibian tympanic ear and the origin of frogs. Biological Journal of the Linnean Society 24:83–99.Google Scholar
Boulenger, G. A. 1882. Catalogue of the Batrachia Gradientia S. caudata and Batrachia apoda in the collection of the British Museum, 2d ed.British Museum (Natural History), London.Google Scholar
Boy, J. A. 1972. Die Branchiosaurier (Amphibia) des saarpfälzischen Rotliegenden (Unter-Perm; SW-Deutschland. Abhandlungen des Hessischen Landesamts für Bodenforschung 65:1–137.Google Scholar
Boy, J. A. 1974. Die Larven der rhachitomen Amphibien (Amphibia: Temnospondyli; Karbon–Trias). Paläontologische Zeitschrift 48:236–268.Google Scholar
Boy, J. A. 1987. Studien über die Branchiosauridae (Amphibia: Temnospondyli; Ober-Karbon–Unter-Perm). Systematische Übersicht. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 174:75–104.Google Scholar
Boy, J. A. 1988. Über einige Vertreter der Eryopoidea (Amphibia: Temnospondyli) aus dem europäischen Rotliegend (? höchstes Karbon–Perm). 1. Sclerocephalus. Paläontologische Zeitschrift 62:107–132.Google Scholar
Boy, J. A. 1995. Über die Micromelerpetontidae (Amphibia: Temnospondyli). 1. Morphologie und Paläoökologie des Micromelerpeton credneri (Unter-Perm; SW-Deutschland). Paläontologische Zeitschrift 69:429–457.Google Scholar
Boy, J. A., and Sues, H.-D. 2000. Brachiosaurs: larvae, metamorphosis, and heterochrony in temnospondyls and seymouriomorphs. Pp. 1150–1197in Heatwole, H. and Carroll, R. L., eds. Amphibian biology, Vol. 4. Paleontology. Beatty, Chipping Norton, England.Google Scholar
Caldwell, M. 1994. Developmental constraints and limb evolution in Permian and extant lepidosauromorph diapsids. Journal of Vertebrate Paleontology 14:459–471.Google Scholar
Carroll, R. L. 1997. Patterns and processes in vertebrate evolution. Cambridge Palaeobiology Series 2. Cambridge University Press, Cambridge.Google Scholar
Carroll, R. L., Kuntz, A., and Albright, K. 1999. Vertebral development and amphibian evolution. Evolution and Development 1:36–48.Google Scholar
Clemen, G., and Greven, H. 1974. Morphologische Untersuchungen an der Mundhöhle von Urodelen. I. Die Gaumenzähne von Salamandra salamandra (L.) (Salamandridae: Amphibia). Forma et Functio 7:249–280.Google Scholar
Clemen, G., and Greven, H. 1977. Morphologische Untersuchungen an der Mundhöhle von Urodelen. III. Die Munddachbezahnung von Ambystoma mexicanum Cope (Ambystomatidae: Amphibia). Zoologisches Jahrbuch Abteilung Anatomie und Ontogenie der Tiere 98:95–136.Google Scholar
Coates, M. I. 1991. New palaeontological contributions to limb ontogeny and phylogeny. Pp. 325–337in Hinchliffe, J. R., Hurle, J. M., and Summerbell, D., eds. Developmental patterning of the vertebrate limb. Plenum, New York.Google Scholar
Coates, M. I. 1995. Fish fins or tetrapod limbs—a simple twist of fate? Current Biology 5:844–848.Google Scholar
Credner, H. 1882. Die Stegocephalen (Labyrinthodonten) aus dem Rothliegenden des Plauenschen Grundes bei Dresden. 3. Theil. Zeitschrift der Deutschen Geologischen Gesellschaft 34:213–237.Google Scholar
DeBeer, G. R. 1937. The development of the vertebrate skull. University of Chicago Press, Chicago.Google Scholar
DeVilliers, C. G. S. 1936. Some aspects of the amphibian suspensorium, with special reference to the paraquadrate and quadratomaxillary. Anatomischer Anzeiger 81:225–304.Google Scholar
Dilkes, D. 1991. Reinterpretation of a larval dissorophoid amphibian from the Lower Permian of Texas. Canadian Journal of Earth Science 28:1488–1492.Google Scholar
Drüner, L. 1901. Studien zur Anatomie des Zungenbein-, Kiemenbogen- und Kehlkopfmuskels der Urodelen. 1. Theil. Zoologische Jahrbücher, Abteilung Anatomie 15:435–622.Google Scholar
Dunn, E. R. 1923. The salamanders of the family Hynobiidae. Proceedings of the New England Zoological Club 7:55–59.CrossRefGoogle Scholar
Erdmann, K. 1933. Zur Entwicklung des knöchernen Skeletts von Triton und Rana unter besonderer Berücksichtigung der Zeitfolge der Ossifikationen. Zeitschrift für Anatomie und Entwicklungsgeschichte 101:566–651.Google Scholar
Fritsch, A. 1876. Über die Fauna der Gaskohle des Pilsner und Rakonitzer Beckens. Sitzungsberichte der Königlich Böhmischen Gesellschaft der Wissenschaften Prag 1875:70–79.Google Scholar
Gaudry, M. A. 1875. Sur la découverte de batraciens dans le terrain primaire. Bulletin de la Société Géologique de France 3:299–306.Google Scholar
Greven, H., and Clemen, G. 1976. Morphologische Untersuchungen an der Mundhöhle von Urodelen. II. Die Gaumenzahnfelder des Hydromantes italicus Dunn (Plethodontidae: Amphibia). Zoologische Beiträge 22:489–506.Google Scholar
Greven, H., and Clemen, G. 1985. Metamorphose-bedingte Veränderungen der Zähne und zahntragenden Knochen im Munddach von Salamandra salamandra (L.) (Amphibia: Urodela). Verhandlungen der Deutschen Zoologischen Gesellschaft 78:162.Google Scholar
Hanken, J. 1984. Miniaturization and its effects on cranial morphology in plethodontid salamanders, genus Thorius (Amphibia: Plethodontidae). I. Osteological variation. Biological Journal of the Linnean Society 23:55–75.Google Scholar
Hanken, J. 1999. Larvae in amphibian development and evolution. Pp. 61–108in Hall, B. K. and Wake, M. H., eds. The origin and evolution of larval forms. Academic Press, New York.Google Scholar
Hanken, J., and Hall, B. K. 1988. Skull development during anuran metamorphosis. I. Early development of the first three bones to form—the exoccipital, the parasphenoid, and the frontoparietal. Journal of Morphology 195:247–256.Google Scholar
Hertwig, O. 1874. Über das Zahnsystem der Amphibien und seine Bedeutung für die Genese des Skelets der Mundhöhle: eine vergleichend anatomische, entwicklungsgeschichtliche Untersuchung. Archiv für Mikroskopische Anatomie 11(Suppl.):1–208.Google Scholar
Keller, R. 1946. Morphogenetische Untersuchungen am Skelett von Siredon mexicanus Shaw mit besonderer Berücksichtigung des Ossifikationsmodus beim neotenen Axolotl. Revue Suisse de Zoologie 53:329–426.Google Scholar
Kessler, K. F. 1866. Einige Bemerkungen über die Verwandlung der Schwanzlosen Batrachier. St. Petersburger Naturforschende Gesellschaft 11:99–108.Google Scholar
Kingsbury, B. G., and Reed, H. D. 1909. The columella auris in Amphibia. Journal of Morphology 20:549–628.Google Scholar
Klembara, J. 1997. The cranial anatomy of Discosauriscus Kuhn, a seymouriamorph tetrapod from the Lower Permian of the Boscovice Furrow (Czech Republic). Philosophical Transactions of the Royal Society of London B 352:257–302.Google Scholar
Lapage, E. O. 1928. The septomaxillary. I. In the amphibia Urodela. Journal of Morphology 45:441–471.Google Scholar
Larsen, J. H. Jr. 1963. The cranial osteology of neotenic and transformed salamanders and its bearing on interfamilial relationships. Ph.D. dissertation. University of Washington, Seattle.Google Scholar
Laurin, M., and Reisz, R. 1997. A new perspective on tetrapod phylogeny. Pp. 9–59in Sumida, S. S. and Martin, K., eds. Amniote origins: completing the transition to land. Academic Press, London.Google Scholar
Lebedkina, N. S. 1960. Razvite parasfenoida khvostatykh amfibij. Doklady Akademiya Nauk SSSR 131:1476–1479.Google Scholar
Lebedkina, N. S. 1964. Razvite pokrovnykh kostej osnovaniya čerepa khvostatykh amfibij sem. Hynobiidae. Trudy Zoologičeskogo Instituta Akademiya Nauk SSSR 33:75–172.Google Scholar
Lebedkina, N. S. 1968a. Razvite kostej kryshi čerepa khvostatykh amfibij. Trudy Zoologičeskogo Instituta Akademiya Nauk SSSR 46:86–124.Google Scholar
Lebedkina, N. S. 1968b. The development of the skull bones in urodeles. Pp. 317–329in Ørvig, T., ed. Current problems of lower vertebrate phylogeny (Nobel Symposium No. 4). Almqvist and Wiksell, Stockholm.Google Scholar
Lebedkina, N. S. 1979. Evolyuziya čerepa amfibij. K problem'e morfologičeskoj integrazij. Nauka, Moscow.Google Scholar
Medvedeva, I. M. 1959. Slesno-nosovoj protok i ego svyas s pokrovnymi kostyami lachrymale i septomaxillare u Ranodon sibiricus. Doklady Akademiya Nauk SSSR 128:425–428.Google Scholar
Meyer, H. von. 1848. Apateon pedestris aus der Steinkohlenformation von Münsterappel. Palaeontographica 1:153.Google Scholar
Milner, A. R. 1982. Small temnospondyls from the Middle Pennsylvanian of Illinois. Palaeontology 25:635–664.Google Scholar
Milner, A. R. 1988. The relationships and origin of living amphibians. In Benton, M. J., ed. Phylogeny and classification of the tetrapods, Vol. 1. Amphibians, reptiles, birds. Systematics Association Special Volume 35A:59–102. Clarendon, Oxford.Google Scholar
Milner, A. R. 1993. The Paleozoic relatives of lissamphibians. Herpetological Monographs 7:8–27.Google Scholar
Noble, G. K. 1927. The value of life history data in the study of the evolution of the Amphibia. Annals of the New York Academy of Sciences 30:31–128.Google Scholar
Papendieck, H. I. C. M. 1954. Contributions to the cranial morphology of Ambystoma macrodactylum. Annals of the University of Stellenbosch 30:151–177.Google Scholar
Parker, W. K. 1879. On the morphology of the skull in the Amphibia Urodela. Transactions of the Linnean Society of London 2:165–212.Google Scholar
Reig, O. 1964. El problema del origen monofilético o polifilético de los anfibios, con consideraciones sobre las relaciones entre Anuros, Urodelos y Apodos. Ameghiniana 3:191–211.Google Scholar
Reilly, S. M. 1986. Ontogeny of cranial ossification in the eastern newt, Notophthalmus viridescens (Caudata: Salamandridae), and its relationship to metamorphosis and neoteny. Journal of Morphology 188:315–326.Google Scholar
Reilly, S. M., and Altig, R. 1996. Cranial ontogeny in Siren intermedia (Caudata: Sirenidae): paedomorphic, metamorphic, and novel patterns of heterochrony. Copeia 1996:29–41.Google Scholar
Reiss, J. 1996. Palatal metamorphosis in basal caecilians (Amphibia: Gymnophiona) as evidence for lissamphibian monophyly. Journal of Herpetology 30:27–39.Google Scholar
Romer, A. S. 1947. Review of the Labyrinthodontia. Bulletin of the Museum of Comparative Zoology at Harvard College 99:1–368.Google Scholar
Rose, C. S., and Reiss, J. O. 1993. Metamorphosis of the vertebrate skull: ontogenetic patterns and developmental mechanisms. Pp. 289–346in Hanken, J. and Hall, B. K., eds. The skull, Vol. 1. University of Chicago Press, Chicago.Google Scholar
Schmalhausen, I. I. 1968. The origin of terrestrial vertebrates. Academic Press, London.Google Scholar
Schoch, R. R. 1992. Comparative ontogeny of early Permian branchiosaurid amphibians. Developmental stages. Palaeontographica, Abteilung A 222:43–83.Google Scholar
Schoch, R. R. 1995. Heterochrony and the evolution of the amphibian head. Pp. 107–124in McNamara, K., ed. Evolutionary change and heterochrony. Wiley, Chichester, England.Google Scholar
Schoch, R. R. 1998. Homology of cranial bones in urodeles: the significance of developmental data for fossil basal tetrapods. Neues Jahrbuch für Geologie und Paläontologie, Monatshefte 1998:1–25.Google Scholar
Schoch, R. R. 1999. Studies on braincases of early tetrapods: Structure, homology, and phylogeny. 2. Kamacops acervalis and other advanced temnospondyls. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 213:289–299.Google Scholar
Schoch, R. R. 2000. The stapes of Mastodonsaurus giganteus (Jaeger, 1828)—structure, articulation, ontogeny, and functional implications. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 215:177–200.Google Scholar
Schoch, R. R. 2001. Can metamorphosis be recognised in Paleozoic amphibians? Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 220:335–367.Google Scholar
Schoch, R. R. 2002. The neurocranium of the stereospondyl Mastodonsaurus giganteus. Palaeontology 45.Google Scholar
Schoch, R. R.In press. Early larval ontogeny of the Permo-Carboniferous temnospondyl Sclerocephalus. Palaeontology.Google Scholar
Schoch, R. R., and Milner, A. R. 2000. Stereospondyli. Pp. 1–203in Wellnhofer, P., ed. Handbuch der Paläoherpetologie, Vol. 3B. Pfeil, Munich.Google Scholar
Schultze, H.-P. 1984. Juvenile specimens of Eusthenopteron foordi Whiteaves, 1881 (osteolepiform rhipidistian, Pisces) from the Late Devonian of Miguasha, Quebec, Canada. Journal of Vertebrate Paleontology 4:1–16.Google Scholar
Stadtmüller, F. 1924. Studien am Urodelenschädel. I. Zur Entwicklungsgeschichte des Kopfskeletts der Salamandra maculosa. Zeitschrift für Anatomie und Entwicklungsgeschichte 75:149–225.Google Scholar
Stadtmüller, F. 1936. Kranium und Visceralskelett der Stegocephalen und Amphibien. Pp. 501–698in Bolk, L., Göppert, E., Kallius, E., and Lubosch, W., eds. Handbuch der vergleichenden Anatomie der Wirbeltiere. Urban and Schwarzenberg, Berlin.Google Scholar
Steen, M. C. 1938. On the fossil Amphibia from the gas coal of Nýřany and other deposits in Czechoslovakia. Proceedings of the Zoological Society London 108:205–283.Google Scholar
Strauch, A. 1870. Revision der Salamandriden-Gattungen nebst Beschreibung einiger neuer oder weniger bekannten Arten dieser Familie. Mémoires de l'Academie Imperiale de Sciences de St.-Pétersbourg, VIIe série, 16:78–109.Google Scholar
Trueb, L. 1985. A summary of osteocranial development in anurans with notes on the sequence of cranial ossification in Rhinophrynus dorsalis (Anura: Pipoidea: Rhinophrynidae). South African Journal of Science 81:181–185.Google Scholar
Trueb, L. 1993. Patterns of cranial diversity among the Lissamphibia. Pp. 255–343in Hanken, J. and Hall, B. K., eds. The skull, Vol. 1. University of Chicago Press, Chicago.Google Scholar
Trueb, L., and Cloutier, R. 1991. A phylogenetic investigation of the inter- and intrarelationships of the Lissamphibia (Amphibia: Temnospondyli). Pp. 223–313in Schultze, H.-P. and Trueb, L., eds. Origins of the higher groups of tetrapods: controversy and consensus. Cornell University Press, Ithaca, N.Y.Google Scholar
Wake, D. B. 1996. Introduction. Pp. xvii–xxvin Sanderson, M. J. and Hufford, L., eds. Homoplasy: the recurrence of similarity in evolution. Academic Press, London.Google Scholar
Wake, D. B., and Hanken, J. 1996. Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? International Journal of Developmental Biology 40:859–869.Google Scholar
Wake, D. B., and Larson, A. 1987. Multidimensional analysis of an evolving lineage. Science 238:42–48.Google Scholar
Wake, M. H., and Hanken, J. 1982. Development of the skull of Dermophis mexicanus (Amphibia: Gymnophiona), with comments of skull kinesis and amphibian relationships. Journal of Morphology 173:203–223.Google Scholar
Wake, T. A., Wake, D. B., and Wake, M. H. 1983. The ossification sequence of Aneides lugubris, with comments on heterochrony. Journal of Herpetology 17:10–22.Google Scholar
Watson, D. M. S. 1940. The origin of frogs. Transactions of the Royal Society of Edinburgh 60:195–231.Google Scholar
Wellstead, C. F. 1991. Taxonomic revision of the Lysorophia, Permo-Carboniferous lepospondyl amphibians. Bulletin of the American Museum of Natural History 209:1–90.Google Scholar
Werneburg, R. 1988. Die Stegocephalen (Amphibia) der Goldlauterer Schichten (Unterrotliegendes, Perm) des Thüringer Waldes, Teil III. Apateon dracyiensis (Boy), Branchierpeton reinholdi n. sp. und andere. Veröffentlichungen des Naturkundemuseums Erfurt 1988:80–96.Google Scholar
Werneburg, R. 1989. Labyrinthodontier (Amphibia) aus dem Oberkarbon und Unterperm Mitteleuropas: Systematik, Phylogenie und Stratigraphie. Freiberger Forschungshefte C 436:7–57.Google Scholar
Wiedersheim, R. 1877. Das Kopfskelet der Urodelen. Morphologisches Jahrbuch 2:352–548.Google Scholar
Wilder, I. W. 1925. The morphology of amphibian metamorphosis. Smith College, Northampton, Mass.Google Scholar
Wintrebert, R. 1922. La chronologie des processus de métmorphose effectues a la voute palatine des Salamandridae. Comptes Rendus de la Société Biologique 87:863–865.Google Scholar
Worthington, R. D., and Wake, D. B. 1971. Larval morphology and ontogeny of the ambystomatid salamander, Rhyacotriton olympicus. American Midland Naturalist 85:349–365.Google Scholar