Postmaturation Skull Development in Xenopus laevis (Anura, Pipidae): Late-Appearing Bones and Their Bearing on the Pipid Ancestral Morphology

Sergei V. Smirnov

Abstract


Cranial morphology was examined in 2-1/N12-year-old of Xenopus laevis. Cranial development was shown to continue after sexual maturation, and in older animals, elements that are commonly admitted as being absent in X. laevis (and in pipids) make their appearance. Among these are the palatine, the preorbital process of the maxillary, and the lateral alae of the parasphenoid. Vomers, which are usually azygous in Xenopus, become paired in old specimens. Two additional dermal ossifications previously recorded only in some casque-headed hylids (Trueb, 1970), were revealed in the skull of the 9- and 12-year-old X. laevis frogs. These bones, which lie on the premaxillary symphasis and dorsal to the septum nasi, are proposed to be homologous with the postrostrals of crossopterygians. Xenopus is proved to be a neotenic frog in which morphological underdevelopment results from the incomplete realization of its morphogenetic program caused by the retardation of somatic development. Prolongation of somatic development occurring in old animals permits the animal’s morphogenetic program to be realized more completely, and features normally lacking in Xenopus but characteristic of its presumed ancestor may make their appearance.

Keywords


pipids; neoteny; skull development

Full Text:

PDF

References


Bernasconi A. F. (1951), «Über den Ossifikationsmodus bei Xenopus laevis Daud,» Mem. Soc. Helvet. Sci. Nat., 79, 191 – 252.

Bolt J. R. and Lombard R. E. (1985), «Evolution of the amphibian tympanic ear and the origin of frogs,» Biol. J. Linn. Soc., 24, 83 – 99.

Bowler J. K. (1977), «Longevity of reptiles and amphibians in North American collections,» Herpetol. Circ., 6, 1 – 32.

Bridges C. D. B., Hollyfield J. G., Withovsky P., and Gallin E. (1977), «The visual pigment and vitamin A of Xenopus laevis embryos, larvae, and adults,» Exp. Eye, 24, 7 – 13.

Cannatella D. C. and Trueb L. (1988), «Evolution of pipoid frogs: intergeneric relationships of the aquatic frog family Pipidae (Anura),» Zool. J. Linn. Soc., 94, 1 – 38.

de Villiers C. G. S. (1930), «On the cranial characters of the South African Brevicipitid, Phrynomerus bifasciatus,» Quart. J. Micr. Sci., 73, 667 – 705.

de Villiers C. G. S. (1934), «Some points in the anatomy of Microbatrachella capensis Hewitt and their bearing upon the question of phylogenetic neoteny,» South Afr. J. Sci., 21, 406 – 414.

Deuchar E. M. (1975), Xenopus: the South African Clawed Frog, Wiley, New York.

Duellman W. E. and Trueb L. (1986), Biology of Amphibians, McGraw-Hill, New York.

Estes R. and Reig O. A. (1973), «The early fossil record of frogs. A review of the evidence,» in: J. L. Vial (ed.), Evolutionary Biology of the Anurans, Univ. Missouri Press, Columbia, pp. 11 — 63.

Etkin W. E. (1968), «Hormonal control of amphibian metamorphosis,» in: W. E. Etkin and L. I. Gilbert (eds.), Metamorphosis. A Problem in Developmental Biology, Appleton – Century – Crofts, New York, pp. 313 – 348.

Gilchrist J. D. F. and von Bonde C. (1919), Dissection of the Platanna and the Frog, Univ. Cape Town.

Gould S. J. (1977), Ontogeny and Phylogeny, Harvard Univ. Press, Cambridge.

Grande L. and Bemis W. E. (1991), «Osteology and phylogenetic relationships of fossil and recent paddlefishes (Polyodontidae) with comments on the interrelationships of Acipenseriformes,» J. Vert. Paleontol., 11 (Suppl.), 1 – 121.

Greven H. (1989), «Teeth of extant amphibia: morphology and some implications,» in: H. Splechtna and H. Hilgers (eds.). Trends in Vertebrate Morphology, Gustav Fisher Verlag, Stuttgart – New York, pp. 451 – 455.

Griffiths L. (1963), «The phytogeny of the Salientia,» Biol. Rev., 38, 241 – 292.

Hanken J. (1984), «Miniaturization and its effects on cranial morphology in plethodontid salamanders, genus Thorius (Amphibia: Plethodontidae). I. Osteological variation,» Biol. J. Linn. Soc., 23, 55 – 75.

Kluge A. G. (1981), «The life history, social organization, and parental behavior of Hyla rosenbergi Boulenger, a nest-building gladiator frog,» Misc. Publ. Mus. Zool. Univ. Michigan, 160, 1 – 170.

Lebedkina N. S. (1979), The Evolution of the Amphibian Skull, Nauka, Moscow [in Russian].

Lynch J. D. (1973), «The transition from archaic to advanced frogs,» in: J. L. Vial (ed.). The Evolutionary Biology of the Anurans, Univ. Missouri Press, Columbia, pp. 133 – 182.

Maclean N. and Jurd R. D. (1971), «Electrophoretic analysis of the haemoglobins of Ambystoma mexicanum,» Comp. Biochem. Physiol., 40(B), 751 – 755.

Maree W. A. (1945), «Contribution to the cranial morphology of the European anuran Alytes obstetricans (Laurenti),» Ann. Univ. Stellenbosch, 23(A), 43 – 65.

Millard N. (1949), «The development of the venous system of Xenopus laevis,» Trans. Roy. Soc. South Afr., 32, 55 – 99.

Moulton J. M., Jurand A., and Fox H. (1968), «A cytological study of Mauther’s cells in Xenopus laevis and Rana temporaria during metamorphosis,» J. Embryol. Exp. Morphol., 19, 4l5 – 431.

Nevo E. (1968), «Pipid frogs from the early Cretaceous of Israel and pipid evolution,» Bull. Mus. Comp. Zool. Harvard Univ., 136, 225 – 318.

Noble G. K. (1931), The Biology of the Amphibia, McGraw-Hill, New York.

Paterson N. F. (1939), «The head of Xenopus laevis,» Quart. J. Micr. Sci., 81, 161 – 234.

Paterson N. F. (1955), «The skull of the toad, Hemipipa carvalhoi Mir.-Rib. with remarks on other Pipidae,» Proc. Zool. Soc. (Lond.), 125, 223 – 252.

Reig O. A. (1958), «Proposiciones para una nueva macrosistematica de los anuros. Nota preliminar,» Physis., 2B, 109 – 118.

Roček Z. (1990), «Ethmoidal endocranial structures in primitive tetrapods: their bearing on the search for anuran ancestry,» Zool. J. Linn. Soc., 99, 389 – 407.

Ryke P. A. J. (1953), «The ontogenetic development of the somatic musculature of the trunk of the aglossal anuran, Xenopus laevis (Daudin),» Acta Zool. (Stockh.), 34, 1 – 70.

Sedra S. N. and Michael M. I. (1957), «The development of the skull, visceral arches, larynx and visceral muscles of the South African clawed toad, Xenopus laevis (Daudin) during the process of metamorphosis (from stage 55 to stage 66),» Verh. Kon. Ned. Ahad. Wetensch. Afd. Natuurk., 51, 1 – 80.

Shishkin M. N. (1973), The Morphology of the Early Amphibia and Some Problems of the Lower Tetrapod Evolution, Nauka, Moscow [in Russian].

Smirnov S. V. (1989), «Postmetamorphic skull development in Bombina orientalis (Amphibia, Discoglossidae), with comments on neoteny,» Zool. Anz., 223, 91 – 99.

Smirnov S. V. (1990), «Evidence of neoteny: a paedomorphic morphology and retarded development in Bombina orientalis (Anura, Discoglossidae),» Zool. Anz., 225, 324 – 332.

Steen M. C. (1938), «On the fossil Amphibia from the Gas Coal of Nyrany and other deposits in Czechoslovakia,» Proc. Zool. Soc. (Lond.) B, 108, 205 – 283.

Tihen J. A. (1965), «Evolutionary trends in frogs,» Am. Zoologist, 5, 309 – 318.

Trueb L. (1970), «Evolutionary relationships of casque-headed tree frogs with co-ossified skulls (family Hylidae),» Univ. Kansas Publ. Mus. Nat. Hist., 18, 547 – 716.

Trueb L. and Cloutier R. (1991), «A phylogenetic investigation of the inter- and intrarelationships of the Lissamphibia (Amphibia: Temnospondyli),» in: H-P. Schultze and L. Trueb (eds.), Origins of the Higher Groups of Tetrapods: Controversy and Consensus, Cornell Univ. Press, New York, pp. 175 – 193.

Trueb L. and Hanken J. (1992), «Skeletal development in Xenopus laevis (Anura: Pipidae),» J. Morphol., 214, 1 – 41.

Chugunova T. Ya. (1981), «Interfrontalia in Bombina orientalis (Blgr.) and Bombina bombina (L.),» in: L. J. Borkin (ed.), Herpetological Investigations in Siberia and the Far East, Izd. Zool. Inst. Acad. Nauk SSSR, Leningrad, pp. 117 – 121 [in Russian].

Wagler J. G. (1830), Naturliches System der Amphibien, mit Vorangehender Classification der Saugethiere und Vogel, Stuttgart und Tübingen, Münich.

Wagner D. S. (1934), «On the cranial characters of Leiopelma hochstetteri,» Anat. Anz., 79, 65 – 77.

Wake D. B. (1980), «Evidence of heterochronic evolution: a nasal bone in the Olympic salamander, Rhyacotriton olympicus,» J. Herpetol., 14, 292 – 295.

Watson D. M. S. (1926), «Croonian lecture — the evolution and origin of Amphibia,» Phil. Trans. Royal. Soc. (Lond.) B., 214, 189 – 257.

Westoll T. S. (1943), «The origin of the tetrapods,» Biol. Rev., 18, 78 – 98.

Will U., Luhede G., and Corner P. (1985), «The area octavo-lateralis in Xenopus laevis. I. The primary afferent projection,» Cell Tissue Res., 239, 147 – 161.




DOI: https://doi.org/10.30906/1026-2296-1994-1-1-21-29

Refbacks

  • There are currently no refbacks.


You can subscribe to the print or electronic version of the journal on the site of EastView Company. If you have any questions, please write to the email sales@ivis.ru