Догаструляционное развитие амфибий: онтогенетическое разнообразие и эволюционно-экологические аспекты

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Аннотация

В обзоре анализируются сравнительные и экологические аспекты преобразований раннего развития в классе Amphibia. Использованы данные по разнообразию онтогенезов в ряде семейств отрядов Anura и Caudata, у которых многие виды утратили связь с водной средой. Модельные представители класса Amphibia (Ambystoma mexicanum, Rana temporaria и Xenopus laevis) имеют яйца небольшого размера (диаметр не более 2.5 мм), а замедление темпов клеточных делений и потеря их синхронности происходят на стадии средней бластулы. Однако филогенетически базальные виды амфибий (Ascaphus truei, Cryptobranchus alleganiensis) характеризуются крупными (диаметр 4–6 мм) и богатыми желтком яйцами и короткой серией синхронных делений бластомеров (синхронность теряется уже на 8-клеточной стадии дробления). У них нет “среднебластульного перехода” (midblastula transition), который характерен, например, для перечисленных выше модельных видов. С другой стороны, многие эволюционно продвинутые немодельные виды хвостатых и бесхвостых амфибий (например, Desmognathus fuscus, Gastrotheca riobambae, Philoria sphagnicolus) так же, как и базальные виды, характеризуются крупными, богатыми желтком яйцами и ранней потерей синхронности клеточных делений. Филогенетический анализ предполагает, что паттерн дробления зародышей у двух наиболее подробно изученных представителей амфибий, мексиканского аксолотля (Caudata) и африканской шпорцевой лягушки (Anura), представляет гомоплазию. Среднебластульный переход, который характерен для этих двух видов, мог эволюционировать конвергентно в двух отрядах амфибий как эмбриональная адаптация к протеканию развития в стоячей воде.

Об авторах

А. Г. Десницкий

Санкт-Петербургский государственный университет, кафедра эмбриологии

Автор, ответственный за переписку.
Email: a.desnitsky@spbu.ru
Россия, 199034, Санкт-Петербург, Университетская набережная, 7/9

Список литературы

  1. Десницкий А.Г. Разнообразие начальных этапов эмбриогенеза у амфибий. СПб.: Лань, 2019. 112 с.
  2. Детлаф Т.А. Температурно-временные закономерности развития пойкилотермных животных. М.: Наука, 2001. 211 с.
  3. Иванова-Казас О.М. Эволюционная эмбриология животных. СПб.: Наука, 1995. 565 с.
  4. Сытина Л.А., Медведева И.М., Година Л.Б. Развитие сибирского углозуба. М.: Наука, 1987. 88 с.
  5. AmphibiaWeb. Information on amphibian biology and conservation. Berkeley (California): Electronic database accessible at http://amphibiaweb.org/. 2022. Accessed: 12 September 2022.
  6. Andéol Y. Early transcription in different animal species: implication for transition from maternal to zygotic control in development // Wilhelm Roux’s Arch. 1994. V. 204. № 1. P. 3–10.
  7. Barresi M.J.F., Gilbert S.F. Developmental biology. 12th ed. N.Y., Oxford: Oxford Univ. Press, 2020. 1258 p.
  8. Brauer A. Beitrӓge zur Kenntniss der Entwicklung und Anatomie der Gymnophionen. II. Die Entwicklung der äussern Form. Zool. Jahrb. Anat. 1899. Bd. 12. № 3. P. 477–508.
  9. Briggs R. Further studies on the maternal effect of the o gene in the Mexican axolotl // J. Exp. Zool. 1972. V. 181. № 2. P. 271–280.
  10. Brinkmann H., Venkatesh B., Brenner S. et al. Nuclear protein-coding genes support lungfish and not the coelacanth as the closest living relatives of land vertebrates // Proc. Natl. Acad. Sci. USA. 2004. V. 101. № 14. P. 4900–4905.
  11. Brown H.A. Temperature and development of the tailed frog, Ascaphus truei // Comp. Biochem. Physiol. 1975. V. 50. № 2. P. 397–405.
  12. Brown H.A. Developmental anatomy of the tailed frog (Ascaphus truei): a primitive frog with large eggs and slow development // J. Zool. (London). 1989. V. 217. № 4. P. 525–537.
  13. Buckley D., Alcobendas M., Garcia-Paris M. et al. Heterochrony, cannibalism, and the evolution of viviparity in Salamandra salamandra // Evol. Devel. 2007. V. 9. № 1. P. 105–115.
  14. Callery E.M. There’s more than one frog in the pond: a survey of the Amphibia and their contributions to developmental biology // Semin. Cell Devel. Biol. 2006. V. 17. № 1. P. 80–92.
  15. Callery E.M., Fang H., Elinson R.P. Frogs without polliwogs: evolution of anuran direct development // BioEssays. 2001. V. 23. № 3. P. 233–241.
  16. Chatterjee S., Elinson R.P. Commitment to nutritional endoderm in Eleutherodactylus coqui involves altered nodal signaling and global transcriptional repression // J. Exp. Zool. B. Mol. Devel. Evol. 2014. V. 322. № 1. P. 27–44.
  17. Collart C., Smith J.C., Zegerman P. Chk1 Inhibition of the replication factor Drf1 guarantees cell-cycle elongation at the Xenopus laevis mid-blastula transition // Dev. Cell. 2017. V. 42. № 1. P. 82–96.
  18. Collazo A., Marks S.B. Development of Gyrinophilus porphyriticus: identification of the ancestral developmental pattern in the salamander family Plethodontidae // J. Exp. Zool. 1994. V. 268. № 3. P. 239–258.
  19. Collazo A., Keller R. Early development of Ensatina eschscholtzii: an amphibian with a large, yolky egg // EvoDevo. 2010. V. 1. P. 6. https://doi.org/10.1186/2041-9139-1-6
  20. de Bavay J.M. The developmental stages of the sphagnum frog, Kyarranus sphagnicolus Moore (Anura: Myobatrachidae) // Austral. J. Zool. 1993. V. 41. № 2. P. 151–201.
  21. de Bussy L.P. Die ersten Entwicklungsstadien des Megalobatrachus maximus // Zool. Anz. 1905. Bd. 28. P. 523–536.
  22. de Lima A.V., Reis A.H., Amado N.G. et al. Developmental aspects of the direct-developing frog Adelophryne maranguapensis // Genesis. 2016. V. 54. № 5. P. 257–271.
  23. del Pino E.M. Modifications of oogenesis and development in marsupial frogs // Development. 1989. V. 107. № 2. P. 169–187.
  24. del Pino E.M. The extraordinary biology and development of marsupial frogs (Hemiphractidae) in comparison with fish, mammals, birds, amphibians and other animals // Mech. Dev. 2018. V. 154. P. 2–11.
  25. del Pino E.M. Embryogenesis of marsupial frogs (Hemiphractidae), and the changes that accompany terrestrial development in frogs // Res. Probl. Cell Differ. 2019. V. 68. P. 379–418.
  26. del Pino E.M. From egg to embryo in marsupial frogs // Curr. Top. Dev. Biol. 2021. V. 145. P. 91–109.
  27. del Pino E.M., Escobar B. Embryonic stages of Gastrotheca riobambae (Fowler) during maternal incubation and comparison of development with that of other egg-brooding hylid frogs // J. Morphol. 1981. V. 167. № 3. P. 277–295.
  28. del Pino E.M., Loor-Vela S. The pattern of early cleavage of the marsupial frog Gastrotheca riobambae // Development. 1990. V. 110. P. 781–789.
  29. del Pino E.M., Elinson R.P. The organizer in amphibians with large eggs: problems and perspectives // The Vertebrate Organizer / Ed. by H. Grunz. Berlin: Springer, 2003. P. 359–374.
  30. del Pino E.M., Venegas-Ferrín M., Romero-Carvajal A. et al. A comparative analysis of frog early development // Proc. Natl. Acad. Sci. USA. 2007. V. 104. № 29. P. 11882–11888.
  31. Desnitskiy A.G. Evolutionary reorganizations of ontogenesis in related frog species of the family Myobatrachidae // Russ. J. Dev. Biol. 2010. V. 41. № 3. P. 133–138.
  32. Desnitskiy A.G. On the diversity of the primary steps of embryonic development in the caudate amphibians // Russ. J. Dev. Biol. 2011. V. 42. № 4. P. 207–211.
  33. Desnitskiy A.G. On the diversity of the initial steps of embryonic development in anuran amphibians // Russ. J. Herpetol. 2012. V. 19. № 3. P. 221–231.
  34. Desnitskiy A.G. On the classification of the cleavage patterns in amphibian embryos // Russ. J. Dev. Biol. 2014. V. 45. № 1. P. 1–10.
  35. Desnitskiy A.G. On the features of embryonic cleavage in diverse fish species // Russ. J. Dev. Biol. 2015. V. 46. № 6. P. 326–332.
  36. Desnitskiy A.G. Cell cycles during early steps of amphibian embryogenesis: a review // Biosystems. 2018. V. 173. P. 100–103.
  37. Desnitskiy A.G. Surface contraction waves or cell proliferation waves in the presumptive neurectoderm during amphibian gastrulation: Mexican axolotl versus African clawed frog // Biosystems. 2020. V. 198. P. 104286. https://doi.org/10.1016/j.biosystems.2020.104286
  38. Desnitskiy A.G., Litvinchuk S.N. Comparative and phylogenetic perspectives of the cleavage process in tailed amphibians // Zygote. 2015. V. 23. № 5. P. 722–731.
  39. Dettlaff T.A., Vassetzky S.G. Animal Species for Developmental Studies: Vertebrates. N.Y.: Consultants Bureau, 1991. V. 2. 453 p. https://doi.org/10.1007/978-1-4615-3654-3
  40. Duellman W.E. Reproductive modes in anuran amphibians: phylogenetic significance of adaptive strategies // South Afr. J. Sci. 1985. V. 81. P. 174–178.
  41. Duellman W.E. Alternative life-history styles in anuran amphibians: evolutionary and ecological implications // Alternative Life-History Styles of Animals / Ed. by M.N. Bruton. Dordrecht (Netherlands): Kluwer Acad. Publ., 1989. P. 101–126.
  42. Duellman W.E., Trueb L. The biology of amphibians, 2nd ed. Baltimore and London: Johns Hopkins Univ. Press, 1994. 671 p.
  43. Dünker N., Wake M.H., Olson W.M. Embryonic and larval development in the Caecilian Ichthyophis kohtaoensis (Amphibia, Gymnophiona). A staging table // J. Morphol. 2000. V. 243. № 1. P. 3–34.
  44. Elinson R.P. Direct development in frogs: wiping the recapitulationist slate clean // Semin. Devel. Biol. 1990. V. 1. P. 263–270.
  45. Elinson R.P. Nutritional endoderm: a way to breach the holoblastic-meroblastic barrier in tetrapods // J. Exp. Zool. Part B. 2009. V. 312. № 6. P. 526–532.
  46. Elinson R.P. Metamorphosis in a frog that does not have a tadpole // Curr. Top. Dev. Biol. 2013. V. 103. P. 259–276.
  47. Elinson R.P. Development of a non-amphibious amphibian – an interview with a coquí // Int. J. Dev. Biol. 2021. V. 65. № 1–3. P. 171–176.
  48. Elinson R.P., del Pino E.M. Cleavage and gastrulation in the egg-brooding, marsupial frog, Gastrotheca riobambae // J. Embryol. Exp. Morphol. 1985. V. 90. P. 223–232.
  49. Elinson R.P., del Pino E.M., Townsend D.S. et al. A practical guide to the developmental biology of terrestrial-breeding frogs // Biol. Bull. 1990. V. 179. № 2. P. 163–177.
  50. Elinson R.P., Sabo M.C., Fisher C. et al. Germ plasm in Eleutherodactylus coqui, a direct developing frog with large eggs // Evodevo. 2011. V. 2. P. 20. https://doi.org/10.1186/2041-9139-2-20
  51. Elinson R.P., del Pino E.M. Developmental diversity of amphibians // Wiley Interdisciplinary Reviews: Devel. Biol. 2012. V. 1. № 3. P. 345–369.
  52. Exbrayat J.-M. Fertilization and embryonic development // Reproductive Biology and Phylogeny of Gymnophiona (Caecilians) / Ed. by Exbrayat J.-M. Enfield (New Hampshire, USA): Science Publishers, 2006. P. 359–386.
  53. Eycleshymer A.C. Bilateral symmetry in the egg of Necturus // Anat. Anz. 1904. V. 25. P. 230–240.
  54. Eycleshymer A.C., Wilson J.M. Normal Plates of the Development of Necturus maculosus. Jena (Germany): Verlag von Gustav Fischer, 1910. 50 p.
  55. Gasser F. Observations sur les stades initiaux du développement de l’urodèle Pyrénéen Euproctus asper // Bull. Soc. Zool. France. 1964. V. 89. P. 423–428.
  56. Gitlin D. The development of Eleutherodactylus portoricensis // Copeia. 1944. V. 1944. № 2. P. 91–98.
  57. Gomes A.D., Moreira R.G., Navas C.A. et al. Review of the reproductive biology of caecilians (Amphibia, Gymnophiona) // South Amer. J. Herpetol. 2012. V. 7. № 3. P. 191–202.
  58. Gomez-Mestre I., Pyron R.A., Wiens J.J. Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs // Evolution. 2012. V. 66. № 12. P. 3687–3700.
  59. Goodale H.D. The early development of Spelerpes bilineatus (Green) // Amer. J. Anat. 1911. V. 12. P. 173–247.
  60. Grönroos H. Zur Entwickelungsgeschichte des Erdsalamanders (Salamandra maculosa Laur.) // Anat. Hefte. 1895. Bd. 6. P. 153–247.
  61. Haddad C.F.B., Prado C.P.A. Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil // BioScience. 2005. V. 55. № 3. P. 207–217.
  62. Hedges S.B., Duellman W.E., Heinicke M.P. New World direct-developing frogs (Anura: Terrarana): Molecular phylogeny, classification, biogeography, and conservation // Zootaxa. 2008. № 1737. P. 1–182.
  63. Heinicke M.P., Duellman W.E., Hedges S.B. Major Caribbean and Central American frog faunas originated by ancient oceanic dispersal // Proc. Natl. Acad. Sci. USA. 2007. V. 104. № 24. P. 10092–10097.
  64. Heinicke M.P., Lemmon A.R., Lemmon E.M. et al. Phylogenomic support for evolutionary relationships of New World direct-developing frogs (Anura: Terraranae) // Mol. Phylogenet. Evol. 2018. V. 118. P. 145–155.
  65. Hilton W.A. Segmentation of the ovum of Desmognathus fusca // Amer. Nat. 1904. V. 38. № 451–452. P. 498–500.
  66. Hirsch N., Zimmerman L.B., Grainger R.M. Xenopus, the next generation: X. tropicalis genetics and genomics // Devel. Dyn. 2002. V. 225. № 4. P. 422–433.
  67. Humphrey R.R. Ovulation in the four-toed salamander, Hemidactylium scutatum, and the external features of cleavage and gastrulation // Biol. Bull. 1928. V. 54. № 4. P. 307–323.
  68. Iwasawa H., Kera Y. Normal stages of development of the Japanese lungless salamander, Onychodactylus japonicus (Houttuyn) // Japan. J. Herpetol. 1980. V. 8. № 3. P. 73–89.
  69. Jiang P., Nelson J.D., Leng N. et al. Analysis of embryonic development in the unsequenced axolotl: waves of transcroptomic upheaval and stability // Devel. Biol. 2017. V. 426. № 2. P. 143–154.
  70. Karadge U., Elinson R.P. Characterization of the nutritional endoderm in the direct developing frog Eleutherodactylus coqui // Devel., Genes Evol. 2013. V. 223. № 6. P. 351–362.
  71. Keller R., Shook D.R. Gastrulation in Amphibians // Gastrulation: From Cells to Embryo / Ed. by Stern C.D. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press, 2004. P. 171–203.
  72. Kemp A. The embryological development of the Queensland lungfish, Neoceratodus forsteri (Krefft) // Mem. Queensland Mus. 1982. V. 20. P. 553–597.
  73. Kershaw F., Joss G.H., Joss J.M.P. Early development in Sarcopterygian fishes // Development of Non-Teleost Fishes / Ed. by Kunz Y.W., Luer C.A. and Kapoor B.G. Enfield (NH, USA): Science Publishers, 2009. P. 275–289.
  74. Kunitomo K. Über die Entwickelungsgeschichte des Hynobius nebulosus // Anat. Hefte. 1910. Bd. 40. P. 193–283.
  75. Lefresne J., Andéol Y., Signoret J. Evidence for introduction of a variable G1 phase at the midblastula transition during early development in axolotl // Devel. Growth Differ. 1998. V. 40. № 5. P. 497–508.
  76. Liang D., Shen X.X., Zhang P. One thousand two hundred ninety nuclear genes from a genome-wide survey support lungfishes as the sister group of tetrapods // Mol. Biol. Evol. 2013. V. 30. № 8. P. 1803–1807.
  77. Liedtke H.C., Wiens J.J., Gomez-Mestre I. The evolution of reproductive modes and life cycles in amphibians // Nat. Commun. 2022. V. 13. P. 7039. https://doi.org/10.1038/s41467-022-34474-4
  78. Luo J., Xiao Y., Luo K. et al. Embryonic development and organogenesis of Chinese giant salamander, Andrias davidianus // Progr. Nat. Sci. 2007. V. 17. P. 1303–1311.
  79. Lutz B. Trends towards non-aquatic and direct development in frogs // Copeia. 1947. V. 1947. № 4. P. 242–252.
  80. Lynn W.G. The embryology of Eleutherodactylus nubicola, an anuran which has no tadpole stage // Contributions to Embryology (Publ. Carnegie Inst. Washington). 1942. V. 190. P. 27–62.
  81. Marks S.B., Collazo A. Direct development in Desmognathus aeneus (Caudata: Plethodontidae): a staging table // Copeia. 1998. V. 1998. № 3. P. 637–648.
  82. Morgan T.H. The Development of the Frog’s Egg: An Introduction to Experimental Embryology. N.Y.: MacMillan Co., 1897. 192 p.
  83. Moya I.M., Alarcón I., del Pino E.M. Gastrulation of Gastrotheca riobambae in comparison with other frogs // Devel. Biol. 2007. V. 304. № 2. P. 467–478.
  84. Nelsen O.E. Comparative Emvryology of the Vertebrates. N.Y., Toronto, London: McGraw-Hill Book Co., 1953. 982 p.
  85. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: 1. Characterization and timing of cellular changes at the midblastula stage // Cell. 1982. V. 30. № 3. P. 675–686.
  86. Nieuwkoop P.D. The organization center of the amphibian embryo: its origin, spatial organization, and morphogenetic action // Adv. Morphogen. 1973. V. 10. P. 1–39.
  87. Nieuwkoop P.D. What are the key advantages and disadvantages of urodele species compared to anurans as a model system for experimental analysis of early development? // Int. J. Devel. Biol. 1996. V. 40. № 4. P. 617–619.
  88. Nieuwkoop P.D., Faber J. Normal Table of Xenopus laevis (Daudin): Systematic and Chronological Survey of the Development from the Fertilized Egg Till the End of Metamorphosis. N.Y., London: Garland Publ. Inc., 1994. 282 p.
  89. Noble G.K. The value of life history data in the study of the evolution of the amphibia // Ann. N.Y. Acad. Sci. 1927. V. 30. № 1. P. 31–128.
  90. Nunes-de-Almeida C.H.L., Haddad C.F.B., Toledo L.F. A revised classification of the amphibian reproductive modes // Salamandra. 2021. V. 57. № 3. P. 413–427.
  91. Padial J.M., Grant T., Frost D.R. Molecular systematics of terraranas (Anura: Brachycephaloidea) with an assessment of the effects of alignment and optimality criteria // Zootaxa. 2014. V. 3825. № 1. P. 1–132.
  92. Pereira E.B., Pinto-Ledezma J.N., De Freitas C.G. et al. Evolution of the anuran foam nest: trait conservatism and lineage diversification // Biol. J. Linn. Soc. 2017. V. 122. № 4. P. 814–823.
  93. Pérez O.D., Lai N.B., Buckley D. et al. The morphology of prehatching embryos of Caecilia orientalis (Amphibia: Gymnophiona: Caeciliidae) // J. Morphol. 2009. V. 270. № 12. P. 1492–1502.
  94. Pyron R.A., Wiens J.J. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians // Mol. Phylogenet. Evol. 2011. V. 61. № 2. P. 543–583.
  95. Rugh R. The Frog; Its Reproduction and Development. Philadelphia: Blakiston Comp., 1951. 336 p.
  96. Rugh R. Experimental embryology. Techniques and Procedures. 3rd ed. Minneapolis (Minnesota): Burgess Publ. Com., 1962. 501 p.
  97. Sammouri R., Renous S., Exbrayat J.M. et al. Développement embryonnaire de Typhlonectes compressicaudus (Amphibia, Gymnophiona) // Ann. Sci. Nat. Zool. Paris. 1990. V. 11. № 3. P. 135–163.
  98. Sampson L.V. Unusual modes of breeding and development among Anura // Amer. Nat. 1900. V. 34. № 405. P. 687–715.
  99. Sampson L.V. A contribution to the embryology of Hylodes martinicensis // Amer. J. Anat. 1904. V. 3. № 4. P. 473–504.
  100. San Mauro D. A multilocus timescale for the origin of extant amphibians // Mol. Phylogenet. Evol. 2010. V. 56. № 2. P. 554–561.
  101. Sarasin P., Sarasin F. Ergebnisse naturwissenschaftlicher Forschungen auf Ceylon in den Jahren 1884–1886. Band 2. Heft 1. Zur Entwicklungsgeschichte und Anatomie der ceylonesischen Blindwȕhle Ichthyophis glutinosus. Teil 1: Einleitung, das Ei, Befruehtung und Brutpflege, Entwicklung der Körperform, Historisches, Systematisches und Vergleichendes. Wiesbaden: C.W. Kreidel’s Verlag, 1887. P. 1–40 + Tafeln 1–5.
  102. Scherz M.D., Vences M., Rakotoarison A. et al. Reconciling molecular phylogeny, morphological divergence and classification of Madagascan narrow-mouthed frogs (Amphibia: Microhylidae) // Mol. Phylogenet. Evol. 2016. V. 100. P. 372–381.
  103. Schmid M., Steinlein C., Bogart J.P. et al. The hemiphractid frogs: phylogeny, embryology, life history, and cytogenetics (review) // Cytogenet. Genome Res. 2012. V. 138. № 2–4. P. 69–367.
  104. Shen X.X., Liang D., Feng Y.J. et al. A versatile and highly efficient toolkit including 102 nuclear markers for vertebrate phylogenomics, tested by resolving the higher level relationships of the Caudata // Mol. Biol. Evol. 2013. V. 30. № 10. P. 2235–2248.
  105. Signoret J. Evidence of the first genetic activity required in axolotl development // Res. Probl. Cell Differ. 1980. V. 11. P. 71–74.
  106. Signoret J., Lefresne J. Contribution à l’étude de la segmentation de l’oeuf d’axolotl: 1. Définition de la transition blastuléenne // Ann. Embryol. Morphogen. 1971. V. 4. № 2. P. 113–123.
  107. Signoret J., Collenot A. L’organisme en développement. Des gamètes à l’embryon. Paris: Hermann, 1991. 278 p.
  108. Smith B.G. Preliminary report on the embryology of Cryptobranchus allegheniensis // Biol. Bull. 1906. V. 11. № 3. P. 146–164.
  109. Smith B.G. The origin of bilateral symmetry in the embryo of Cryptobranchus allegheniensis // J. Morphol. 1922. V. 36. № 3. P. 357–399.
  110. Smith B.G. The embryology of Cryptobranchus allegheniensis. 3. Formation of the blastula // J. Morphol. Physiol. 1926. V. 42. № 1. P. 197–252.
  111. Spemann H. Embryonic Development and Induction. New Haven: Yale Univ. Press, 1938. 401 p.
  112. Streicher J.W., Miller E.C., Guerrero P.C. et al. Evaluating methods for phylogenomic analyses, and a new phylogeny for a major frog clade (Hyloidea) based on 2214 loci // Mol. Phylogenet. Evol. 2018. V. 119. P. 128–143.
  113. Svensson G.S.O. Zur Kenntnis der Furchung bei den Gymnophionen // Acta Zool. (Stockholm). 1938. Bd. 19. № 1–2. P. 191–207.
  114. Tarkhnishvili D.N., Serbinova I.A. Normal development of the Caucasian salamander (Mertensiella caucasica) // Adv. Amphib. Res. Former Soviet Union. 1997. V. 2. P. 13–30.
  115. Toivonen S., Tarin D., Saxén L. et al. Transfilter studies on neural induction in the newt // Differentiation. 1975. V. 4. № 1. P. 1–7.
  116. Vastenhouw N.L., Cao W.X., Lipshitz H.D. The maternal-to-zygotic transition revisited // Development. 2019. V. 146: dev161471. https://doi.org/10.1242/dev.161471
  117. Vieites D., Román S.N., Wake M.H. et al. A multigenic perspective on phylogenetic relationships in the largest family of salamanders, the Plethodontidae // Mol. Phylogenet. Evol. 2011. V. 59. P. 623–635.
  118. Wake D.B., Hanken J. Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? // Int. J. Devel. Biol. 1996. V. 40. № 4. P. 859–869.
  119. Wake M.H. Fetal adaptations for viviparity in amphibians // J. Morphol. 2015. V. 276. № 8. P. 941–960.
  120. Zhang M., Skirkanich J., Lampson M.A. et al. Cell cycle remodeling and zygotic gene activation at the midblastula transition // Adv. Exp. Med. Biol. 2017. V. 953. P. 441–487.
  121. Zheng Y., Peng R., Murphy R.W. et al. Matrilineal genealogy of Hynobius (Caudata: Hynobiidae) and a temporal perspective on varying levels of diversity among lineages of salamanders on the Japanese Islands // Asian Herpetol. Res. 2012. V. 3. № 4. P. 288–302.

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