Abstract
Literature on the earliest steps of fish embryogenesis (including a number of “non-model” species) has been considered. The main attention has been paid to the loss of cleavage division synchrony and the first latitudinal cleavage furrow. In teleostean embryos, the features of their meroblastic cleavage are not rigidly associated with egg size. The midblastula transition (in a form clearly enough) occurs in some chondrostean and teleostean fishes, but it has not been detected in the representatives of sarcopterygian and chondrichthyan fishes.
Similar content being viewed by others
References
Aanes, H., Collas, P., and Aleström, P., Transcriptome dynamics and diversity in the early zebrafish embryo, Brief. Funct. Genomics, 2014, vol. 13, pp. 95–105.
Aizawa, K., Shimada, A., Naruse, K, et al., The medaka midblastula transition as revealed by the expression of the paternal genome, Gene Expr. Patt., 2003, vol. 3, pp. 43–47.
Arakawa, T., Kanno, Y., Akiyama, N, et al., Stages of embryonic development of the ice goby (shiro-uo), Leucopsarion petersii, Zool. Sci., 1999, vol. 16, pp. 761–773.
Arezo, M.J., Pereiro, L., and Berois, N., Early development in the annual fish Cynolebias viarius, J. Fish. Biol., 2005, vol. 66, pp. 1357–1370.
Armstrong, P.B. and Child, J.S, Stages in the normal development of Fundulus heteroclitus, Biol. Bull., 1965, vol. 128, pp. 143–168. Ballard, W.W. and
Needham, R.G, Normal embryonic stages of Polyodon spathula (Walbaum), J. Morphol., 1964, vol. 114, pp. 465–477.
Ballard, W.W, Stages and rates of normal development in the holostean fish, Amia calva, J. Exp. Zool., 1986, vol. 238, pp. 337–354.
Ballard, W.W., Mellinger, J., and Lechenault, H, A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae), J. Exp. Zool., 1993, vol. 267, pp. 318–336.
Benyumov, A.O., Dubrovskaya, T.A., Barmintsev, V.A., and Shan Lizyuan, The duration of the first mitotic cycles and the staging of embryogenesis in Danio rerio, Ontogenez, 1995, vol. 26, no. 2, pp. 132–138.
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. Nat. Acad. Sci. USA, 2004, vol. 101, pp. 4900–4905. Carter, C.A. and
Wourms, J.P, Cell behavior during early development in the South American annual fishes of the genus Cynolebias, J. Morphol., 1991, vol. 210, pp. 247–266.
Collazo, A., Bolker, J.A., and Keller, R, A phylogenetic perspective on teleost gastrulation, Am. Nat., 1994, vol. 144, pp. 133–152.
Cooper, M.S. and Virta, V.C, Evolution of gastrulation in the ray-finned (actinopterygian) fishes, J. Exp. Zool. Part B. Mol. Dev. Evol., 2007, vol. 308, pp. 591–608.
Cunningham, J.E.R. and Balon, E.K, Early ontogeny of Adinia xenica (Pisces, Cyprinodontiformes): 1. The development of embryos in hiding, Env. Biol. Fish, 1985, vol. 14, pp. 115–166.
Dalle Nogare, D.E., Pauerstein, P.T., and Lane, M.E., G2 acquisition by transcription-independent mechanism at the zebrafish midblastula transition, Devel. Biol., 2009, vol. 326, pp. 131–142.
Desnitskiy, A.G, On the classification of the cleavage patterns in amphibian embryos, Russ. J. Devel. Biol., 2014, vol. 45, pp. 1–10.
Desnitskiy, A.G. and Litvinchuk, S.N, Comparative and phylogenetic perspectives of the cleavage process in tailed amphibians, Zygote, 2014, pp. 1–10. doi: http:// dx.doi.org/10.1017/S0967199414000379
Dettlaff, T.A., Ginsburg, A.S., and Shmal’gauzen, O.I., Razvitie osetrovykh ryb (Development of Sturgeons), Moscow: Nauka, 1981.
Diedhiou, S. and Bartsch, P, Staging of the early development of Polypterus (Cladistia: Actinopterygii), in Development of Non-Teleost Fishes, Kunz, Y.W., Luer, C.A., and Kapoor, B.G., Eds., Enfield (NH, USA): Science Publishers, 2009, pp. 104–169.
Dondua, A.K., Rott, N.N., and Gorodilov, Yu.N., Desynchronization of cell division during the early development of the axoloty, loach and salmon, Ontogenez, 1977, vol. 8, no. 1, pp. 11–20.
Eycleshymer, A.C, The cleavage of the egg of Lepidosteus osseus, Anat. Anz., 1899, vol. 16, pp. 529–536.
Fujimoto, T., Kataoka, T., Otani, S, et al., Embryonic stages from cleavage to gastrula in the loach Misgurnus anguillicaudatus, Zool. Sci., 2004, vol. 21, pp. 747–755.
Fujimoto, T., Kataoka, T., Sakao, S, et al., Developmental stages and germ cell lineage of the loach (Misgurnus anguillicaudatus), Zool. Sci., 2006, vol. 23, pp. 977–989.
Gerhart, J.C, Mechanisms regulating pattern formation in the amphibian egg and early embryo, in Biological Regulation and Development, Goldberger, R.F., Ed., New York: Springer, 1980, vol. 2, pp. 133–316.
Ginsburg, A.S. and Dettlaff, T.A, The Russian sturgeon Acipencer güldenstädti. Part 1. Gametes and early development up to time of hatching, in Animal Species for Developmental Studies, Dettlaff, T.A. and Vassetzky, S.G., Eds., New York: Consultants Bureau, 1991, vol. 2, pp. 15–65.
Gorodilov, Yu.N. and Lil’p, I.G, Duration of the cell cycles and mitotic phases during the cleavage period of the salmon Salmo salar L., Ontogenez, 1978, vol. 9, no. 4, pp. 363–375.
Gorodilov, Y.N., Terjesen, B.F., Krasnov, A., and Takle, H, Description of embryogenesis of Atlantic cod, Gadus morhua, Open Mar. Biol. J., 2008, vol. 2, pp. 43–53.
Van Haarlem, R., Van Wijk, R., and Fikkert, A.H.M., Analysis of the variability in cleavage times and demonstration of a mitotic gradient during the cleavage stages of Nothobranchius guentheri, Cell Tissue Kinet., 1981, vol. 14, pp. 285–300.
Van Haarlem, R., Early ontogeny of the annual fish genus Nothobranchius: cleavage plane orientation and epiboly, J. Morphol., 1983, vol. 176, pp. 31–42.
Hall, T.E., Smith, P., and Johnston, I.A, Stages of embryonic development in the Atlantic cod, Gadus morhua, J. Morphol., 2004, vol. 259, pp. 255–270.
Hisaoka, K.K. and Firlit, C.F, Further studies on the embryonic development of the zebrafish, Brachydanio rerio (Hamilton-Buchanan), J. Morphol., 1960, vol. 107, pp. 205–225.
Honji, R.M., Tolussi, C.E., Mello, P.H, et al., Embryonic development and larval stages of Steindachneridion parahybae (Siluriformes: Pimelodidae)—implications for the conservation and rearing of this endangered neotropical species, Neotrop. Ichthyol., 2012, vol. 10, pp. 313–327.
Ignatieva, G.M. and Rott, N.N, The temporal pattern of interphase prolongation and nuclear activities during early embryogenesis in Teleostei, Wilhelm Roux’s Arch. Dev. Biol., 1970, vol. 165, pp. 103–109.
Ignatieva, G.M, The rainbow trout Salmo gairdneri, in Animal Species for Developmental Studies, Dettlaff, T.A. and Vassetzky, S.G., Eds., New York: Consultants Bureau, 1991, vol. 2, pp. 89–124.
Iwamatsu, T, Stages of normal development in the medaka Oryzias latipes, Mech. Dev., 2004, vol. 121, pp. 605–618. Jaroszewska, M. and
Dabrowski, K, Early ontogeny of Semionotiformes and Amiiformes (Neopterygii: Actinopterygii), in Development of Non-Teleost Fishes, Kunz, Y.W., Luer, C.A., and Kapoor, B.G., Eds., Enfield (NH, USA): Science Publishers, 2009, pp. 230–274.
Kageyama, T, Mitotic behavior and pseudopodial activity of cells in the embryo of Oryzias latipes during blastula and gastrula stages, J. Exp. Zool., 1987, vol. 244, pp. 243–252.
Kane, D.A. and Kimmel, C.B, The zebrafish midblastula transition, Development, 1993, vol. 119, pp. 447–456.
Kemp, A, The embryological development of the Queensland lungfish, Neoceratodus forsteri (Krefft), Mem. Queensland Mus., 1982, vol. 20, pp. 553–597.
Kerr, J.G, The external features in the development of Lepidosiren paradoxa, Fitz., Phil. Trans. Roy. Soc. London: Ser. B, 1900, vol. 192, pp. 299–330.
Kershaw, F., Joss, G.H., and Joss, J.M.P, Early development in Sarcopterygian fishes, in Development of Non-Teleost Fishes, Kunz, Y.W., Luer, C.A., and Kapoor, B.G., Eds., Enfield (NH, USA): Science Publishers, 2009, pp. 275–289.
Kimmel, C.B., Ballard, W.W., Kimmel, S.R, et al., Stages of embryonic development of the zebrafish, Devel. Dyn., 1995, vol. 203, pp. 253–310.
Korzh, V.P. and Minin, A.A, A short history of loach or why remember morphogenetic function of nuclei? The 50th Anniversary of A.A. Neyfakh’s discovery of the morphogenetic function of the nucleus, Russ. J. Dev. Biol., 2010, vol. 41, no. 2, pp. 122–129.
Kostomarova, A.A, The loach Misgurnus fossilis, in Animal Species for Developmental Studies, Dettlaff, T.A. and Vas-setzky, S.G., Eds., New York: Consultants Bureau, 1991, vol. 2, pp. 125–144.
Kraeussling, M., Wagner, T.U., and Schartl, M., Highly asynchronous and asymmetric cleavage divisions accompany early transcriptional activity in pre-blastula medaka embryos, PLoS One, 2011, vol. 6, no. 7, p. e21741. doi: 10.1371/journal.pone.0021741
Kunz, Y.W., Developmental Biology of Teleost Fishes, Dordrecht: (the Netherlands): Springer, 2004.
Liang, D., Shen, X.X., and 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, vol. 30, pp. 1803–1807.
Long, W.L. and Ballard, W.W., Normal embryonic stages of the longnose gar, Lepisosteus osseus, BMC Devel. Biol., 2001, vol. 1: 6.
Martinez, G.M. and Bolker, J.A, Embryonic and larval staging of summer flounder (Paralichthys dentalus), J. Morphol., 2003, vol. 255, pp. 162–176.
Meijide, F.J. and Guerrero, G.A, Embryonic and larval development of a substrate-brooding cichlid Cichlasoma dimerus (Heckel, 1840) under laboratory conditions, J. Zool. (London), 2000, vol. 252, pp. 481–493.
Mendieta-Serrano, M.A., Schnabel, D., Lomeli, H., and Salas-Vidal, E, Cell proliferation patterns in early zebrafish development, Anat. Rec., 2013, vol. 296, pp. 759–773.
Miller, A.E, The cleavage of the egg of Lepidosiren paradoxa, Quart. J. Micr. Sci., 1923, vol. 67, pp. 497–505.
Morrison, C.M., Miyake, T., and Wright, J.R, Histological study of the development of the embryo and early larva of Oreochromis niloticus (Pisces: Cichlidae), J. Morphol., 2001, vol. 247, pp. 172–195.
Near, T.J., Eytan, R.I., Dornburg, A., et al., Resolution of ray-finned fish phylogeny and timing of diversification, Proc. Nat. Acad. Sci. U.S.A., 2012, vol. 109, pp. 13698–13703.
Newport, J. and Kirschner, M, A major developmental transition in early Xenopus embryos: 1. Characterization and timing of cellular changes at the midblastula stage, Cell, 1982, vol. 30, pp. 675–686.
Ninhaus-Silveira, A., Foresti, F., and de Azevedo, A., Structural and ultrastructural analysis of embryonic development of Prochilodus lineatus (Valenciennes, 1836) (Characiforme; Prochilodontidae), Zygote, 2006, vol. 14, pp. 217–229.
Nogueira, L.B., Azevedo, P.G., Canelhas, M.R, et al., Induced spawning and early ontogeny in hatcheryreared catfish Zungaro jahu (Siluriformes: Pimelodidae), Neotrop. Ichthyol., 2012, vol. 10, pp. 89–98.
Oliveira-Almeida, I.R., Buzollo, H, Silva, Costa R., et al., Structural analysis of embryogenesis of Leiarius marmoratus (Siluriformes: Pimelodidae), Zygote, 2014, pp. 1–16. doi: http://dx.doi.org/10.1017/S0967199414000392
Olivier, N., Luendo-Oroz, M.A., Duloquin, L, et al., Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy, Science, 2010, vol. 329, pp. 967–971.
Ostaszewska, T. and Dabrowski, K, Early development of Acipenseriformes (Chondrostei: Actinopterygii), in Development of Non-teleost Fishes, Kunz, Y.W., Luer, C.A., and Kapoor, B.G., Eds., Enfield (NH, USA): Science Publishers, 2009, pp. 170–229.
Rott, N.N. and Sheveleva, G.A, Changes in the rate of cell divisions in the course of early development of diploid and haploid loach embryos, J. Embryol. Exp. Morphol., 1968, vol. 20, pp. 141–150.
Rott, N.N, Cell cycles in the early embryogenesis of the peled, Ontogenez, 1979, vol. 10, no. 3, pp. 209–219.
Rott, N.N, Mitotic activity of cells in different parts of the blastoderm peled, Ontogenez, 1981, vol. 12, no. 5, pp. 485–489.
Rugh, R., Experimental Embryology. Techniques and Procedures, 3rd ed., Minneapolis (Minnesota): Burgess Publ. Com, 1962.
Sallan, L.C, Major issues in the origins of ray-finned fish (Actinopterygii) biodiversity, Biol. Rev., 2014, vol. 89, pp. 950–971.
Shadrin, A.M. and Emel’yanova, N.G, Embryonic-larval development and some data on the reproductive biology of Abudefduf sexfasciatus (Pomacentridae: Perciformes), J. Ichthyol., 2007, vol. 47, no. 1, pp. 67–80.
Shardo, J.D, Comparative embryology of teleostean fishes. 1. Development and staging of the American shad, Alosa sapidissima (Wilson, 1811), J. Morphol., 1995, vol. 225, pp. 125–167.
Signoret, J. and Lefresne, J, Contribution à l’étude de la segmentation de l’oeuf d’axolotl: 1. Définition de la transition blastuléenne, Ann. Embryol. Morphogen., 1971, vol. 4, pp. 113–123.
Takeuchi, M., Okabe, M., and Aizawa, S, The genus Polypterus (Bichirs): a fish group diverged at the stem of ray-finned fishes (Actinopterygii), in Emerging Model Organisms: A Laboratory Manual, Gann, A. and Crotty, D., Eds., Cold Spring Harbor (NY, USA): CSHL Press, 2008, vol. 1, pp. 447–469.
Takeuchi, M., Takahashi, M., Okabe, M., and Aizawa, S, Germ layer patterning in bichir and lamprey; an insight into its evolution in vertebrates, Devel. Biol., 2009, vol. 332, pp. 90–102.
Tong, X.H., Xu, S.H., Liu, Q.H, et al., Stages of embryonic development and changes in enzyme activities in embryogenesis of turbot (Scophthalmus maximus L.), Aquacult. Int., 2013, vol. 21, pp. 129–142.
Trinkaus, J.P, The midblastula transition, the YSL transition and the onset of gastrulation in Fundulus, Development, 1992, Suppl. 1992, pp. 75–80.
Whitman, C.O. and Eycleshymer, A.C., The egg of Amia and its cleavage, J. Morphol., 1897, vol. 12, pp. 309–354.
Wourms, J.P, Developmental biology of annual fishes. 1. Stages in the normal development of Austrofundulus myersi Dahl, J. Exp. Zool., 1972, vol. 182, pp. 143–168.
Wourms, J.P, Reproduction and development in chondrichthyan fishes, Am. Zool., 1977, vol. 17, pp. 379–410.
Wyffels, J.T, Embryonic development of chondrichthyan fishes—a review, in Development of Non-Teleost Fishes, Kunz, Y.W., Luer, C.A., and Kapoor, B.G., Eds., Enfield (NH, USA): Science Publishers, 2009, pp. 1–103.
Yamamoto, K, Cleavage pattern and formation of the blastocoel in the egg of the eel, Anguilla japonica, Jap. J. Ichthyol., 1981, vol. 27, pp. 301–308.
Yanwirsal, H., Reproductive styles of Osteoglossomorpha with emphasis on Notopterus notopterus and Osteoglossum bicirrhosum, dissertation dr. rer. agr., Berlin: HumboldtUniv., 2013.
Zamir, E., Kam, Z., and Yarden, A, Transcription-dependent induction of G1 phase during the zebra fish midblastula transition, Mol. Cell. Biol., 1997, vol. 17, pp. 529–536.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © A.G. Desnitskiy, 2015, published in Ontogenez, 2015, Vol. 46, No. 6, pp. 385–392.
The article was translated by the author.
Rights and permissions
About this article
Cite this article
Desnitskiy, A.G. On the features of embryonic cleavage in diverse fish species. Russ J Dev Biol 46, 326–332 (2015). https://doi.org/10.1134/S106236041506003X
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S106236041506003X