Skull Development in Normal, TH-Exposed, and Goitrogen-Treated Axolotls, Ambystoma mexicanum

Sergei V. Smirnov, Anna B. Vassilieva

Abstract


Normal development of the Ambystoma mexicanum skull was compared with those in axolotls reared at different TH concentrations and in the TH-deficiency. Cranial bones show different TH-dependence. The latter is at best low (if ever) in the early-appearing bones; it somewhat increases in later ones and becomes strong in the nasal and septomaxilla, the last dermal bones to arise. Bones appearing after this peak TH-dependency revert back to be TH-independent. Similar ontogenetic dynamics of TH-dependency is displayed by metamorphosing urodeles. Axolotls retain this typical pattern though their plasma TH level and TH profile differ from those in metamorphosing salamanders. However, if compared with metamorphosing congenerics, changes in the thyroid activity (manifested as changes in TH level and profile) cause changes in the timing and sequence of cranial ossification. To be normally developed, dermal bones associated with nasal capsule require the presence of the underlying cartilage. Their underdevelopment in axolotl results from the underdevelopment of the TH-dependent nasal capsule rather than immediately from TH-deficiency. Our observations favor the assumption that urodele evolution is accompanied by the progressive increase of TH-mediation in the skull ontogeny. Also, they favor that formation of the vomeropalatine in TH-induced axolotls is artifact of TH-induction rather than a feature of their normal development.

Keywords


thyroid hormone; thiuorea; skull; ontogeny; axolotl; urodele

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References


Alberch P., Gale E. A., and Larsen P. R. (1986), «Plasma T4 and T3 levels in naturally metamorphosing Eurycea bislineata (Amphibia; Plethodontidae)», Gen. Comp. Endocrinol., 61, 153 – 163.

Bonebrake J. E. and Brandon R. A. (1971), «Ontogeny of cranial ossification in the small-mouthed salamander, Ambystoma texanum (Matthes)», J. Morphol., 133, 189 – 204.

Boorse G. C. and Denver R. J. (2002), «Acceleration of Ambystoma tigrinum metamorphosis by corticotropin-releasing hormone», J. Exp. Zool., 293, 94 – 98.

Brown D. D. (1997), «The role of thyroid hormone in zebrafish and axolotl development», Proc. Natl. Acad. Sci. USA, 94, 13011 – 13016.

Clemen G. (1979), «Experimentelle Veränderungen am knöchernen Gaumenbogen der Axolotl-Larve und ihre Auswirkungen während der Metamorphose», Zool Anz. Jena, 203, 23 – 24.

Clemen G. and Greven H. (1994), «The buccal cavity of larval and metamorphosed Salamandra salamandra: structural and developmental aspects», Mertensiella, 4, 83 – 109.

Flick R. W. (1992), Effects of Hybridization between the Salamanders Ambystoma tigrinum and A. texanum on skull development and morphology. Masters Thesis, Southern Illinois Univ., Carbondale (cit. after Rose, 2003).

Galton V. A. (1992), «Thyroid hormone receptors and iodothyronine deiodinases in the developing Mexican axolotl, Ambystoma mexicanum», Gen. Comp. Endocrinol., 85, 62 – 70.

Gundernatsch J. F. (1912), «Feeding experiments on tadpoles. I. The influence of specific organs given as food on growth and differentiation. A contribution to the knowledge of organs with internal secretion», Wilhelm Roux Arch. Entwicklungsmech. Organismen, 35, 457 – 483.

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

Larras-Regard E. (1985), «Hormonal determination of neoteny in facultative neotenic urodeles», in: M. Balls and M. Bownes (eds.), Metamorphosis, Clarendon Press, Oxford, pp. 294 – 312.

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

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

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

Nace G. W. (1970), «The use of amphibians in biomedical research», in: Ch. C. Middleton (ed.), Animal Models for Biomedical Research. III, National Academy of Sciences, Washington, pp. 103 – 124.

Papendieck H. I. C. M. (1954), «Contributions to the cranial morphology of Ambystoma macrodactylum Baird», Ann. Univ. Stellenbosch., 30, 151 – 178.

Reilly S. M. (1987), «Ontogeny of the hyobranchial apparatus in the salamanders Ambystoma talpoideum (Ambystomatidae) and Notophthalmus viridescens (Salamandridae): The ecological morphology of two neotenic strategies», J. Morphol., 191, 205 – 214.

Rose C. S. (1985a), «Skeletal morphogenesis in the urodele skull: II. Effect of developmental stage in TH-induced remodeling», J. Morphol., 223, 149 – 166.

Rose C. S. (1985b), «Skeletal morphogenesis in the urodele skull: III. Effect of hormone dosage in TH-induced remodeling», J. Morphol., 223, 243 – 261.

Rose C. S. (1986), «An endocrine-based model for developmental and morphogenetic diversification in metamorphic and paedomorphic urodeles», J. Zool. Lond., 239, 253 – 284.

Rose C. S. (1999), «Hormonal control in larval development and evolution — Amphibians», in: B. K. Hall and M. H. Wake (eds.), The Origin and Evolution of Larval Forms, Acad. Press, San Diego, pp. 167 – 216.

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.

Rosenkilde P. (1985), «The role of hormones in the regulation of amphibian metamorphosis», in: M. Balls and M. Bownes (eds.), Metamorphosis, Clarendon Press, Oxford, pp. 221 – 259.

Smirnov S. V. (2005), «The urodele metamorphosis: regulatory mechanisms and evolution», in: N. Ananjeva and O. Tsinenko (eds.), Herpetologica Petropolitana. Proc. of the 12th Ord. Gen. Meeting Soc. Eur. Herpetol., August 12 – 16, 2003, St. Petersburg, Russ. J. Herpetol., 12(Suppl.), 304 – 306.

Smirnov S. V. and Vassilieva A. B. (2002), «The bony skull of the Siberian salamander, Salamandrella keyserlingi (Amphibia: Urodela: Hynobiidae) and the role of thyroid hormones in its development», Dokl. Biol. Sci., 385, 387 – 389.

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.

Theron J. G. (1952), «On the cranial morphology of Ambystoma maculatum (Shaw)», South African J. Sci., 48, 345 – 365.

Wakahara M. (1994), «Spermatogenesis is extraordinarily accelerated in metamorphosis-arrested larvae of a salamander, Hynobius retardatus», Experientia, 50, 94 – 98.

Wintrebert P. (1910a), «Sur le déterminisme de la métamorphose chez les Amphibiens. XII. L’évolution du vomer et di ptérygo-palatin chez Ambystoma tigrinum», Comptes Rendues Hebdomad. Séanc. Mem. Soc. Biol., 68, 178 – 180.

Wintrebert P. (1910b), «Sur le déterminisme de la métamorphose chez les Amphibiens. XIII. La disparition du palatin et la transformation du vomer chez Salamandra maculosa Laur»., Comptes Rendues Hebdomad. Séanc. Mem. Soc. Biol., 68, 300 – 302.




DOI: https://doi.org/10.30906/1026-2296-2005-12-2-113-126

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