Developmental Pattern and Morphology of Salamandrella keyserlingii Limbs (Amphibia, Hynobiidae) Including Some Evolutionary Aspects

E. I. Vorobyeva, J. R. Hinchliffe

Abstract


In this paper, we consider the pattern of skeletal development and morphology in the limbs of the hynobiid species, Salamandrella keyserlingii, with the overall aim of analyzing tetrapod limb evolution in context of the phylogeny. In comparison with anurans the urodeles demonstrate caenogenetic adaptation in distal structures of the limbs. As the most primitive family of Caudata hynobiids are of special interest since a study of early stages is likely to display some plesiomorphic features. In common with other larval salamanders Salamandrella has early development of digits 1 + 2. However, in contrast to them this species displays a number of distinctive characters, including larval adaptations and features which can be considered as phylogenetically primitive for caudates and sometimes for uniseriate sarcopterygians in general. The main peculiarities of Salamandrella can been summarized as follows:

1) early formation of the mesenchyme mass between the zeugopod bifurcation as the base for the proximodistal differentiation of preaxial, median and postaxial columns;

2) initial connection of the median column with postaxial one in the region of intermedium condensation;

3) early formation of the intermedium condensation in close contact with ulnar/fibular condensation;

4) dominance of the posterior or postaxial branch (ulnare/fibulare) in the early limb development;

5) comparatively late formation of the basale commune which arises primarily as a small distal 2 condensation at the base of the digit 2 and later fuses with distal 1 condensation;

6) fusion of the skeletal elements in longitudinal rather than in transverse direction; usually amalgamation of the median elements with postaxial than with preaxial ones;

7) frequent (in 75%) amalgamation of the intermedium with ulnare;

8) presence of two central elements in the standard morphology;

9) presence of a well developed, long temporary epidermal fin between first and second digits used in balance and locomotion of the larvae. This is caenogenetic adaptation.

The comparison of Salamandrella with other caudates and some fossil sarcopterygians led us to conclusion that many developmental pattern of its limb (1 – 4) can been considered as an ancestral features. It may be supposed that such characters of urodeles as the precocious appearance of anterior digits and basale commune, the gap between them and proximal (zeugopod/stylopod) portion, distal-to-proximal sequence in development of carpal and tarsal elements have a secondary character, probably correlated with their caenogenetic adaptations, and do not support the hypothesis of the polyphyly of tetrapods.


Keywords


Caudata (Urodela); limb development; variation; evolution

Full Text:

PDF

References


Alberch P. and Gale E. (1985), «A developmental analysis of an evolutionary trend: digital reduction in amphibians», Evolution, 39, 8 – 23.

Blanko M. and Alberch P. (1992), «Caenogenesis, developmental variability and evolution of the carpus and tarsus of the marbled newt, Triturus marmoratus», Evolution, 46, 677 – 687.

Borkhvardt V. G. (1994), «Development of the limbs in larvae of siberian salamander, Salamandrella keyserlingii (Amphibia, Hynobiidae)», Zool. Zh., 73(3), 53 – 67 [in Russian].

Borkhvardt V. G., Moiseeva A. A., and Ledentsov A. B. (1992), «Development of mesopodial skeleton in siberian newt Salamandrella keyserlingii (Amphibia, Hynobiidae) at the postmetamorphic stages», Zool. Zh., 71(2), 64 – 73 [in Russian].

Borkhvardt V. G. and Ivashintsova I. V. (1993), «Some regularities in the variation of the paw skeleton of siberian salamander, Salamandrella keyserlingii (Amphibia, Hynobiidae», Zool. Zh., 72(6), 66 – 73 [in Russian].

Borkhvardt V. G., Moiseeva A. A. and Ledentsov A. B. (1994), «Development of the limbs in larvae of siberian salamander, Salamandrella keyserlingii (Amphibia, Hynobiidae)», Zool. Zh., 73(5), 53 – 67 [in Russian].

Chang M. M. (1991), «Rhipidistians, dipnoans and tetrapods», in: Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb (eds.), Comstock Publ. Ass., Ithaca, pp. 3 – 38.

Coates M. and Clack J. (1990), «Polydactyly in the earliest known tetrapod limbs», Nature, 347, 66 – 69.

Jarvik E. (1980), Basic Structure and Evolution of Vertebrates, Vol. 2, Acad. Press, New York.

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

Hanken J. (1982), «Appendicular skeletal morphology in minute Salamanders, genus Thorius (Amphibia, Plethodontidae): growth regulation, adult size determination and natural variation», J. Morphol., 174(1), 57 – 77.

Hanken J. (1983), «High incidence of limb skeletal variation in a peripheral population of the red-backed salamander Plethodon cinereus (Amphibia: Plethodontidae) from Nova Scotia», Can. J. Zool., 61, 1925 – 1931.

Hanken J. and Dinsmore C. E. (1986) «Geographic variation in the limb skeleton of the red-backed salamander, Plethodon cinereus», J. Herpetol., 20, 97 – 101.

Hasumi M. and Iwasawa H. (1993), «Geographic variation in the Pes of the Salamander Hynobius lichenatus and Pentadactyl Hynobius nigrescence», Zool. Sci., 10(6), 1017 – 1027.

Hinchliffe J. R. (1991), «Developmental approaches to the problem of transformation of limb structure in evolution», in: Developmental Patterning of the Vertebrate Limb, J. R. Hinchliffe, J. M. Hurle, and D. Summerbell (eds.), Plenum Press, New York, pp. 313 – 323.

Hinchliffe J. R. and Griffiths P. J. (1983), «The prechondrogenic patterns in tetrapod limb development and their phylogenetic significance», in: Development and Evolution, B. Goodwin, N. Holder and C. C. Wylie (eds.), Cambridge Univ. Press, Cambridge, pp. 99 – 121.

Holmgren. N. (1933), «On the origin of the tetrapod limb», Acta Zool., 14, 185 – 295.

Lebedkina N. S. (1964), «Development of the dermal bones in the cranial basis of Caudata fam. Hynobiidae», Trudy Zool. Inst. Akad. Nauk, 33, 75 – 172 [in Russian].

Rienesl J. and Wagner G. (1992), «Constancy and change of basipodial variation patterns: a comparative study of crested and marbled newts — Triturus cristatus, Triturus marmoratus — and their natural hybrids», J. Evol. Biol., 5, 307 – 324.

Rosen D., Forey P., Gardiner B., and Patterson C. (1981), «Lungfishes, tetrapods, palaeontology and plesiomorphy», Bull. Am. Mus. Nat. Hist., 167, 163 – 273.

Schmalhausen I. I. (1910), «Die Entwicklung des Extremitaten Skeleton von Salamandrella keyserlingii», Anat. Anz., 37.

Schmalhausen I. I. (1915), Development of the Extremities of the Amphibia and Their Significance to the Question of the Origin of the Vertebrates, Izd. RAN, Moscow [in Russian].

Schmalhausen I. I. (1917), «On the extremities of Ranidens sibiricus Kessl», Rus. Zool. Zh., 2, 129 – 135.

Schubin N. H. (1991), «Implications of the «Bauplan» for development and evolution of the tetrapod limb», in: Developmental Patterning of the Vertebrate Limb, J. R. Hinchliffe, J. M. Hurle and D. Summerbell (eds.), Plenum Press, New York, pp. 411 – 422.

Schubin N. (1995), «The evolution of paired fins and the origin of tetrapod limbs», in: Evolutionary Biology, Vol. 28, Max K. Hecht et al. (eds.), Plenum Press, London – New York, pp. 39 – 86.

Schubin N. H. and Alberch P. (1986), «A morphogenetic approach to the origin and basic organization of the tetrapod limb», in: Evolutionary Biology, Vol. 20, Max K. Hecht et al. (eds.), Plenum Press, London – New York, pp. 318 – 320.

Shubin N. H., Wake D. W., and Crawford A. J. (1995), «Morphological variation in the limbs of Taricha granulosa (Caudata: Salamandridae): evolutionary and phylogenetic implications», Evolution, 49(5), 874 – 884.

Schultze H.-P. (1991), «Controversial hypotheses on the origin of tetrapods», in: Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb (eds.), Comstock Publ. Assoc., Ithaca, pp. 29 – 67.

Sytina L. A., Medvedeva I. M., and Godina L. B. (1987), Development of Hynobius keyserlingii, Nauka, Moscow [in Russian].

Vorobyeva E. I. (1991), «The fin-limb transformation: paleontological and embryological evidence», in: Developmental Patterning of the Vertebrate Limb, J. R. Hinchliffe, J. M. Hurle, and D. Summerbell (eds.), Plenum Press, New York, pp. 339 – 345.

Vorobyeva E. I. (1995), «Evolutionary morphological peculiarities of the species», in: The Siberian newt (Salamandrella keyserlingii), E. I. Vorobyeva (ed.), Vol. 2, Nauka, Moscow, pp. 6 – 28 [in Russian].

Vorobyeva E. I. and Borkhvardt V. G. (1994), «Morphology and development of appendages», in: The Siberian Newt Salamandrella keyserlingii, E. I. Vorobyeva (ed.), Vol. 1, Nauka, Moscow, pp. 334 – 341 [in Russian].

Vorobyeva E. I. and Hinchliffe R. J. (1995), «The fin-limb transition and sarcopterygian relationships», Geobios Mem. Sp., 19, 289 – 292.

Vorobyeva E. I. and Schultze H.-P. (1991), «Description and systematics of panderichthyid fishes with comments on their relationship to tetrapods», in: Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb (eds.), Comstock Publ. Associates, Ithaca, pp. 68 – 109.

Vorobyeva E. I., Borkhvardt V. G., and Hinchliffe R. J. (1995), «Limb development in the Siberian newt (Salamandrella keyserlingii)», in: Abstrs. of the XII Int. Symp. on Morphol. Sci., Aristotle Univ. Thessaloniki, p. 234.




DOI: https://doi.org/10.30906/1026-2296-1996-3-1-68-81

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