Thyroid Hormone Mediation in Skull Development of Siberian Newt, Salamandrella keyserlingi (Urodela: Hynobiidae), with Comparison to Other Species

Sergei V. Smirnov, Anna B. Vassilieva, Kseniya M. Merkulova


Sequence and timing of cranial bones appearance and metamorphic transformation were compared in larvae of Siberian newt, Salamandrella keyserlingi (Urodela, Hynobiidae), reared under different levels of thyroid hormone (TH): i) normal, ii) high (in 1 and 10 ng/ml T3), and iii) low (in 0.02% thiourea, TU, which inhibits thyroid gland activity resulting in TH deficiency). Cranial bones exhibit differential reaction to changes in TH level. Bones appearing in early larval ontogeny display no or only slight response to TH changes. At different TH regimes, they arise at the same stages and at the same age. Bones appearing later show reaction to TH changes: their appearance is accelerated and retarded in TH- and TU-treated larvae, correspondingly. The major response to TH alterations is displayed by ontogenetic events involved into metamorphic remodeling: they are greatly accelerated under TH-treatment and retarded in TH-deficiency. Most metamorphic events fail to occur under TH-deficiency. Comparison of TH-related changes in skull development of Ambystoma mexicanum (Ambystomatidae), Triturus vulgaris (Salamandridae), and S. keyserlingi showed that in these species the same bones differ in reaction to TH changes. A corollary of these differences is that in urodeles TH-dependence and TH-sensitivity of cranial bones change both in ontogeny and phylogeny.


skull development; thyroid hormone; ossification sequence; Siberian newt

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Alberch P., Lewbart G. A., and Gale E. A. (1985), «The fate of larval chondrocytes during the metamorphosis of the epibranchial in the salamander, Eurycea bislineata», J. Embryol. Exp. Morphol., 88, 71 – 83.

Cubbage C. C. and Mabee P. M. (1996), «Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae)», J. Morphol., 229, 121 – 160.

Dundee H. A. (1957), «Partial metamorphosis induced in Typhlomolge rathbuni», Copeia, 1957, 52 – 53.

Dundee H. A. (1962), «Response of the neotenic salamander Haideotriton wallacei to a metamorphic agent», Science, 135, 1060 – 1061.

Gaudin A. J. (1978), «The sequence of cranial ossification in the California toad, Bufo boreas (Amphibia, Anura, Bufonidae)», J. Herpetol., 12, 309 – 318.

Hanken J. and Hall B. K. (1984), «Variation and timing of the cranial ossification sequence of the Oriental fire-bellied toad, Bombina orientalis (Amphibia, Discoglossidae)», J. Morphol., 182, 245 – 255.

Hanken J. and Hall B. K. (1988), «Skull development during anuran metamorphosis. II. Role of thyroid hormone in osteogenesis», Anat. Embryol., 178, 219 – 227.

Keller R. (1946), «Morphogenetische Untersuchungen am Skelett von Siredon mexicanus Shaw mit besonderer Berucksichtigung des Ossifikationsmodus beim neotenen Axolotl», Rev. Suiss Zool., 53, 329 – 426 (cit. after Rose, 2003).

Kemp N. E. and Hoyt J. A. (1965a), «Influence of thyroxine on ossification of the parasphenoid bone in the skull of Rana pipiens», Am. Zool., 5, 710.

Kemp N. E. and Hoyt J. A. (1965b), «Influence of thyroxine on order of ossification of bones of the skull of Rana pipiens», Am. Zool., 5, 719.

Kemp N. E. and Hoyt J. A. (1969), «Sequence of ossification in the skeleton of growing and metamorphosing tadpoles of Rana pipiens», J. Morphol., 129, 415 – 444.

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

Lebedkina N. S. (1986), «Development of correlative systems in phylogeny and ontogeny», in: E. I. Vorobyeva and N. S. Lebedkina (eds.), Animal Morphology and Evolution [in Russian], Nauka, Moscow, pp. 95 – 101.

Lebedkina N. S. (2004), Evolution of the Amphibian Skull, Pensoft Publ., Sofia.

Medvedeva I. M. (1975), The Olfactory Organ in Amphibians and its Phylogenetic Significance [in Russian], Nauka, Leningrad.

Rose C. S. (1995a), «Skeletal morphogenesis in the urodele skull: II. Effect of developmental stage in TH-induced remodeling», J. Morphol., 223, 149 – 166.

Rose C. S. (1995b), «Skeletal morphogenesis in the urodele skull: III. Effect of hormone dosage in TH-induced remodeling», J. Morphol., 223, 243 – 261.

Rose C. S. (1996), «An endocrine-based model for developmental and morphogenetic diversification in metamorphic and paedomorphic urodeles», J. Zool., 239, 253 – 284.

Rose C. S. (2003), «The developmental morphology of salamander skulls», in: H. Heatwole (ed.), Amphibian Biology. Vol. 5. Osteology, Surrey Beatty and Sons, Australia, pp. 1684 – 1781.

Schoch R. R. (2006), «Skull ontogeny: developmental patterns of fishes conserved across major tetrapod clades», Evol. Devel., 8, 524 – 536.

Smirnov S. V. and Vassilieva A. B. (2003), «Skeletal and dental ontogeny in the smooth newt, Triturus vulgaris (Urodela: Salamandridae): role of thyroid hormone in its regulation», Russ. J. Herpetol., 10(2), 93 – 110.

Smirnov S. V. and Vassilieva A. B. (2005), «Skull development in normal, TH-exposed, and goitrogen-treated axolotls, Ambystoma mexicanum», Russ. J. Herpetol., 12(2), 113 – 126.

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

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

Yeatman H. C. (1967), «Artificially metamorphosed neotenic cave salamanders», J. Tenn. Sci., 42, 16 – 22.



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