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History of Evolutionary Developmental Biology

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Abstract

Foundations of evolutionary developmental biology (evo-devo) were laid by K. von Baer, the author of the law of embryonic similarity in various animal species. Subsequent exploration of this problem was related to the proof of the relationship between the invertebrate and vertebrate animals (A.O. Kowalevsky). The next phase of evo-devo progress was the creation of the theory of phylembryogenesis (A.N. Severtsov) and the concept of integrity of the organism in onto- and phylogenesis (I.I. Schmalhausen). In the context of evo-devo, the idea of epigenetic regulation in ontogenesis is of great importance (C. Waddington). At the present stage of evo-devo development, associated with names of S. Gould, P. Alberch, K. McNamara, etc., the importance of heterochrony is explored, in particular, the molecular mechanisms of heterochrony formation (“heterochronic genes” and microRNAs).

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REFERENCES

  1. Abzhanov, A. and Tabin, C.J., Shh and Fgf8 act synergetically to drive cartilage outgrowth during cranial development, Dev. Biol., 2004, vol. 273, pp. 134–148.

    Article  CAS  PubMed  Google Scholar 

  2. Abzhanov, A., Protas, M., Grant, B.R., et al., Bmp4 and morphological variation of beaks in Darwin’s finches, Science, 2004, vol. 305, pp. 1462–1465.

    Article  CAS  PubMed  Google Scholar 

  3. Abzhanov, A., Kuo, W.P., Hartmann, C., et al., The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches, Nature, 2006, vol. 442, pp. 563–567.

    Article  CAS  PubMed  Google Scholar 

  4. Afanas’eva, G.A. and Nevesskaya, L.A., Analysis of the causes of different consequences of crisis situations using articulate brachiopods and bivalves as an example, in Sistemnye perestroiki i evolyutsiya biosfery (System Rearrangements and Evolution of the Biosphere), Moscow: Nedra, 1994, vol. 1, pp. 101–108.

  5. Ahi, E.P., Signalling pathways in trophic skeletal development and morphogenesis: insights from studies on teleost fish, Dev. Biol., 2016, vol. 420, pp. 11–31.

    Article  CAS  PubMed  Google Scholar 

  6. Alberch, P., Gould, S.J., Oster, G.F., and Wake, D.B., Size and shape in ontogeny and phylogeny, Paleontology, 1979, vol. 5, pp. 296–317.

    Google Scholar 

  7. Alberch, P., The generative and regulatory role of development in evolution, in Environmental Adaptation and Evolution, Stuttgart: Fischer, 1982, pp. 19–26.

    Google Scholar 

  8. Alberch, P. and Blanco, M.J., Evolutionary patterns in ontogenetic transformation, Int. J. Dev. Biol., 1996, vol. 40, pp. 845–859.

    CAS  PubMed  Google Scholar 

  9. Ambros, V. and Horvitz, H.R., Heterochronic mutants of nematode Caenorhabditis elegans,Science, 1984, vol. 226, pp. 409–416.

    Article  CAS  PubMed  Google Scholar 

  10. De Beer, G.R., Embryology and Evolution, Oxford: Clarendon Press, 1930.

    Google Scholar 

  11. De Beer, G.R., Embryos and Ancestors, Oxford: Clarendon Press, 1958.

    Google Scholar 

  12. Bengston, S. and Zhao, Y., Fossilized metazoan embryos from the earliest Cambrian, Science, 1997, vol. 277, pp. 1645–1648.

    CAS  Google Scholar 

  13. Bhullar, B.-A.S., Morris, Z.S., Sefton, E.M., et al., A molecular mechanism for the origin of a key evolutionary innovation, the bird deack and palate, revealed by an integrative approach to major transitions in vertebrate history, Evolution, 2015, vol. 69, pp. 1665–1677.

    Article  PubMed  Google Scholar 

  14. Blanco, M. and Alberch, P., Evolutionary patterns in ontogenetic transformation: from lows to regulation, Int. J. Dev. Biol., 1996, vol. 40, pp. 845–858.

    PubMed  Google Scholar 

  15. Caugill, E.E. and Johnston, L.A., Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs, Curr. Biol. CB, 2008, vol. CB 18, pp. 943–950.

  16. Darwin, C., The Descent of Man and Selection in Relation to Sex, 2nd ed., London: John Murray, 1874.

    Book  Google Scholar 

  17. Dobrzhansky, T.G., Genetics and the Origin of Species, New York: Columbia Univ. Press, 1937.

    Google Scholar 

  18. Dondua, A.K., Biologiya razvitiya (Developmental Biology), St. Petersburg: St. Peterb. Gos. Univ., 2005, vols. 1, 2.

  19. Eldredge, N. and Gould, S.J., Punctuated Equilibria: An Alternative to Phyletic Gradualism, in Models in Paleontology, Schopf, T.J.M., Ed., San Francisco: Freeman, Cooper and Company, 1972.

    Google Scholar 

  20. Filatov, D.P., The role of the volume factor in accelerating of some morphogeneses, Zh. Eksp. Biol., 1931, vol. 7, pp. 137–162.

    Google Scholar 

  21. Filatov, D.P Mechanics of development as a method for studying some problems of evolution, Zh. Obshch. Biol., 1943, vol. 7, pp. 137–162.

    Google Scholar 

  22. Gignac, P.M. and Erickson, G.M., Ontogenetic biteforce modeling of alligator mississippiensis: implications for dietary transitions in large-bodied vertebrate and the evolution of crocodilian feeding, J. Zool., 2016, vol. 299, pp. 229–238.

    Article  Google Scholar 

  23. Gilbert, S.F., Opitz, J.M., and Raff, R.A., Resynthesizing evolutionary and developmental biology, Russ. J. Dev. Biol., 1997, vol. 23, no. 5, pp. 265–280.

    Google Scholar 

  24. Gilbert, S.F., Biologiya razvitiya (Developmental Biology), Inform-Planeta, Politekhnika, 2010.

  25. Goldschmidt, R.B., Physiological Genetics, New York: McGraw-Hill, 1938.

    Google Scholar 

  26. Goldschmidt, R.B., Evolution as viewed by one geneticist, Am. Sci., 1952, vol. 40, pp. 84–94.

    Google Scholar 

  27. Goodman, C.S. and Coughlin, B.C., The evolution of evo-devo biology, Proc. Natl. Acad. Sci. U. S. A., 2000, vol. 97, no. 9, pp. 4424–4425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gould, S.J., Punctuated equilibrium in fact and theory, Skeptic, vol. 1, no. 3, pp. 48–65.

  29. Gould, S.J., Ontogeny and Phylogeny, Cambridge: Cambridge Univ. Press, 1977.

    Google Scholar 

  30. Gould, S.J., The Structure of Evolutionary Theory, Cambridge, USA: Harvard Univ. Press, 2002.

    Book  Google Scholar 

  31. Hall, B.K., Evolutionary Developmental Biology, Dordrecht: Kluwer Acad. Publ., 1998.

    Google Scholar 

  32. Hall, B.K., Evo-devo: evolutionary developmental mechanisms, Int. J. Dev. Biol., 2003, vol. 47, pp. 491–495.

    PubMed  Google Scholar 

  33. Hertel, J. and Stadler, P.F., The expansion of animal microRNA families revisited, Life, 2015, vol. 5, pp. 905–920.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hu, D. and Marcucio, R.S., Unique organization of the functional ectodermal zone in birds and mammals, Dev. Biol., 2009, vol. 325, pp. 200–210.

    Article  CAS  PubMed  Google Scholar 

  35. Huxley, J.S., Problems of Relative Growth, London: Methuen and Company, 1932.

    Google Scholar 

  36. Ikegami, K., Ohgane, J., Tanaka, S., et al., Interplay between DNA methylation, histone modification and chromatin remodeling in stem cells and during development, Int. J. Dev. Biol., 2009, vol. 53, pp. 77–96.

    Article  CAS  Google Scholar 

  37. Isaeva, V.V., Ozernyuk, N.D., and Rozhnov, S.V., Evidence for evolutionary changes in ontogeny: paleontological, comparative-morphological, and molecular aspects, Biol. Bull. (Moscow), 2013, vol. 40, no. 3, pp. 243–252.

    Article  Google Scholar 

  38. Ivanova-Kazas, O.M., Evolyutsionnaya embriologiya zhivotnykh (Evolutionary Embryology of Animals), St. Petersburg: Nauka, 1995.

  39. Jacob, F., Evolution and tinkering, Science, 1977, vol. 196, pp. 1161–1166.

    Article  CAS  PubMed  Google Scholar 

  40. Kato, M. and Slack, F.J., MicroRNAs: small molecules with big roles—C. elegans to human cancer, Biol. Cell., 2008, vol. 100, pp. 71–81.

    Article  CAS  PubMed  Google Scholar 

  41. Keri, N., Epigenetika (Epigenetics), Rostov-on-Don, 2012.

    Google Scholar 

  42. Kirschner, M.W. and Gerhart, J.C., The Plausibility of Life, New Haven, London: Yale Univ. Press, 2005.

    Google Scholar 

  43. Kittelmann, S. and McGregor, P., Modulation and evolution of animal development through microRNA regulation of gene expression, Genes, 2019, vol. 10, no. 4, p. 321.https://doi.org/10.1016/j.tree.2019.04.003

    Article  CAS  PubMed Central  Google Scholar 

  44. Korochkin, L.I., Vvedenie v genetiku razvitiya (Introduction to Developmental Genetics), Moscow: Nauka, 1999.

  45. Kouzarides, T., Chromatin modifications and their function, Cell, 2007, vol. 15, pp. 175–191.

    Google Scholar 

  46. Kowalevsky, A., Entwicklungescyichte der einfachen Ascidien, Mem. l’Acad. St. Petersbourg, 1866, Ser. 7, vol. 10, pp. 1–19.

  47. Kraus, Yu.A. and Rodimov, A.A., Heterochronies and heterotopias of morphogenetic processes of the cellular level—a source of diversity and variability of gastrulation of cnidarians, in Kletochnye, molekulyarnye i evolyutsionnye aspekty morfogeneza (Cellular, Molecular, and Evolutionary Aspects of Morphogenesis), Moscow: Tov. Nauchn. Izd. KMK, 2007, pp. 97–99.

  48. Levit, G.S., The roots of evo-devo in Russia: it there a characteristic “Russian tradition?”, Theor. Biosci., 2007, vol. 126, pp. 131–140.

    Article  Google Scholar 

  49. Lewis, E.B., A gene complex controlling segmentation in Drosophila,Nature, 1978, vol. 276, pp. 565–570.

    Article  CAS  PubMed  Google Scholar 

  50. Lewis, E.B., Regulation of the genes of the bithorax complex in Drosophila,Cold Spring Harbor Symp. Quant. Biol., 1985, vol. 50, pp. 155–164.

    Article  CAS  PubMed  Google Scholar 

  51. Love, A.C., Morphological and paleontological perspectives for a history of evo-devo, in From Embryology to Evo-Devo, Laubichler, M.D. and Maienschtein, J., Eds., Cambridge: MIT Press, 2007, pp. 267–307.

    Google Scholar 

  52. Mayr, E., Animal Species and Evolution, Cambridge: Belknap Press, 1963.

    Book  Google Scholar 

  53. Margueron, R., Trojer, P., and Reinberg, D., The key to development: interpreting the histone code?, Curr. Opin. Gen. Dev., 2005, vol. 15, pp. 163–176.

    Article  CAS  Google Scholar 

  54. McKinney, L.M. and McNamara, K.J., Heterochrony: Evolution of Ontogeny, New York: Plenum, 1991.

    Book  Google Scholar 

  55. McNamara, K.J., A guide to the nomenclature of heterogeneity, J. Paleontol., 1986, vol. 60, pp. 4–13.

    Article  Google Scholar 

  56. McNamara, K.J., Shapes of Time: The Evolution of Growth and Development, Baltimore: John Hopkins Univ. Press, 1997.

    Google Scholar 

  57. McNamara, K.J., Changing times, changing places: heterochrony and heterotopy, Paleobiology, 2002, vol. 28, pp. 551–558.

    Article  Google Scholar 

  58. Minelli, A., Evo-devo and its significance for animal evolution and phylogeny, in Evol. Dev. Biol. Inverteb., Wanninger, A., Ed., Wienn: Springer, 2015a, vol. 1, pp. 1–24.

  59. Minelli, A., Morphological misfits and the architecture of development, in Macroevolution: Explanation, Interpretation and Evidence, Serrelli, E. and Gontier, N., Eds., Htidelberg: Springer, 2015b, pp. 329–343.

  60. Monk, M., Baubelik, M., and Lehnert, S., Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineage mouse embryo development, Development, 1987, vol. 99, pp. 371–382.

    CAS  PubMed  Google Scholar 

  61. Monk, M., Germine-derived DNA methylation and early embryo epigenetic reprogramming: the selected survival of imprints, Int. J. Biochem. Cell Biol., 2015, vol. 41, pp. 128–138.

    Article  CAS  Google Scholar 

  62. Morgan, T.H., The rise of genetics, Science, 1932a, vol. 76, pp. 261–288.

    Article  CAS  PubMed  Google Scholar 

  63. Morgan, T.H., Genetics and physiology of development, Am. Nat., 1932b, vol. 60, pp. 489–515.

    Article  Google Scholar 

  64. Morris, Z.S., Vliet, K.A., Abzhanov, A., et al., Heterochronic shifts and conserved embryonic shape underlie crocodilian craniofacial disparity and convergence, Proc. R. Soc. B, 2019, vol. 286, p. 20182389.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Ngu, R.K., Dean, W., Dawson, C., et al., Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5, Nat. Cell Biol., 2008, vol. 10, no. 11, pp. 1280–1290.

    Article  CAS  Google Scholar 

  66. Ohno, S., Evolution by Gene Duplication, Berlin: Springer Verlag, 1970.

    Book  Google Scholar 

  67. Ozernyuk, N.D. and Isaeva, V.V., Evolyutsiya ontogeneza (Evolution of Ontogeny), Moscow: Tov. Nauchn. Izd. KMK, 2016.

  68. Ozernyuk, N.D., Correlation of ontogenetic and evolutionary processes in view of achievements of modern genetics: role of gene duplication, Biol. Bull. (Moscow), 2010, vol. 37, no. 2, pp. 100–105.

    Article  Google Scholar 

  69. Ozernyuk, N.D., Heterochronies and evolutionary innovations—modularity, morphogenetic fields of gene action, and molecular mechanisms, in Morfogenez: getero-khronii, geterotopii i allometriya (Morphogenesis: Heterochronies, Heterotopias, and Allometry), Moscow: Paleontol. Inst. Ross. Akad. Nauk, 2014, pp. 49–60.

  70. Ozernyuk, N.D., Evolutionary mechanisms: modularity, morphogenetic fields, gene regulation, Paleontol. J., 2015, vol. 49, pp. 1524–1529.

    Article  Google Scholar 

  71. Ozernyuk, N.D. and Myuge, N.S., Evolutional principles of homology in regulatory genes of myogenesis, Biol. Bull. (Moscow), 2012, vol. 39, no. 4, pp. 316–322.

    Article  Google Scholar 

  72. Ozernyuk, N.D. and Myuge, N.S., Large-scale genome duplications and paralog divergence in fish, Russ. J. Genet., 2013, vol. 49, no. 1, pp. 63–69.

    Article  CAS  Google Scholar 

  73. Pasquinelli, A.E., MicroRNAs and their targets: recognition and emerging reciprocal relationship, Nat. Rev. Genet., 2012, vol. 13, pp. 271–283.

    Article  CAS  PubMed  Google Scholar 

  74. Raff, R.A. and Raff, E.C., Evolution in the light of embryos: seeking the origins of novelties in ontogeny, in Form and Function in Developmental Evolution, Laubichler, M.D. and Maienschein, J., Eds., Cambridge: Cambridge Univ. Press, 2009, pp. 83–111.

    Google Scholar 

  75. Raff, R.A. and Kaufman, T.C., Embryos, Genes, and Evolution, New York: Macmillan, 1983.

    Google Scholar 

  76. Reinhart, B.J., Slack, F.J., and Basson, M., The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans,Nature, 2000, vol. 408, pp. 86–89.

    Article  CAS  PubMed  Google Scholar 

  77. Rozhnov, S.V., The role of heterochrony in the establishment of body plan in higher echinoderm taxa, Biol. Bull. (Moscow), 2009, vol. 36, no. 2, pp. 117–127.

    Article  Google Scholar 

  78. Rozhnov, S.V., Role of modularity and heterochronies in the formation of higher metazoan taxa according to fossil records, in Morfogenez: geterokhronii, geterotopii i allometriya ((Morphogenesis: Heterochronies, Heterotopias, and Allometry), Moscow: Paleontol. Inst. Ross. Akad. Nauk, 2014, pp. 61–82.

  79. Schmalhausen, I.I., Organizm kak tseloe v individual’nom razvitii (The Organism as a Whole in the Individual Development), Moscow: Akad. Nauk SSSR, 1938.

  80. Schmalhausen, I.I., Faktory evolyutsii. Teoriya stabiliziruyushchego otbora (Factors of Evolution. The Theory of Stabilizing Selection), Moscow: Nauka, 1968.

  81. Schmalhausen, I.I., Puti i zakonomernosti evolyutsionnogo protsessa. Izbrannye trudy (Pathways and Patterns of the Evolutionary Process. Selected Works), Moscow: Nauka, 1983.

  82. Severtsov, N.A., Morfologicheskie zakonomernosti evolyutsii (Morphological Patterns of Evolution), Moscow: 1939.

    Google Scholar 

  83. Shubin, N. and Alberch, P., A morphogenetic approach to the origin and basic organization of tetrapod limb, Evol. Biol., 1986, vol. 20, pp. 319–387.

    Google Scholar 

  84. Slack, F.J. and Ruvkun, G., Heterochronic genes in development and evolution, Biol. Bull., 1998, vol. 195, pp. 375–376.

    Article  CAS  PubMed  Google Scholar 

  85. Smirnov, S.V., Pedomorphosis as a mechanism of evolutionary transformation of organisms, in Sovremennaya evolyutsionnaya morfologiya (Modern Evolutionary Morphology), Kiev: Naukova Dumka, 1991, pp. 88–103.

  86. Smirnov, S.V., Metamorphosis of urodeles and evolution of the mechanisms of its regulation, in Evolyutsionnye faktory formirovaniya raznoobraziya zhivotnogo mira (Evolutionary Factors of Wildlife Diversity Formation), Moscow: Tov. Nauchn. Izd. KMK, 2005, pp. 124–134.

  87. Smith, K.K., Thime’s arrow: heterochrony and evolution of development, Int. J. Dev. Biol., 2003, vol. 47, pp. 613–621.

    PubMed  Google Scholar 

  88. Sperling, E.A. and Peterson, K.J., microRNAs and metazoan phylogeny, in Animal Evolution, Genomes, Threes and Fossils, Telford, M.J. and Littewood, D.T.J., Eds., Oxford: Oxford Univ. Press, 2009, pp. 157–170.

  89. Stanley, S.M., Macroevolution: Pattern and Process, San Francisco: W.H. Freeman, 1979.

    Google Scholar 

  90. Takita, M., Yano, W., James, H.F., et al., Cranial shape evolution in adaptive radiations of birds: comparative morphometrics of Darwin’s finches and Hawaiian honeycreepers, Philos. Trans. R. Soc. London B., 2016, vol. 372, p. 20150481.

    Article  Google Scholar 

  91. Vanyushin, B.F., DNA methylation and epigenetics, Russ. J. Genet., 2006, vol. 42, no. 9, pp. 985–997.

    Article  CAS  Google Scholar 

  92. Vorob’eva, E.I., Modern evolutional developmental biology: mechanical and molecular genetic or phenotypic approaches, Russ. J. Dev. Biol., 2010a, vol. 41, no. 5, pp. 283–290.

    Article  Google Scholar 

  93. Vorob’eva, E.I., Evo-devo and the I.I. Schmalhausen concept of the evolution of ontogeny, Biol. Bull. (Moscow), 2010b, vol. 37, no. 2, pp. 106–113.

    Article  Google Scholar 

  94. Vrba, E.S., Ecology, development and evolution: perspectives from the fossil record, in Environment, Development and Evolution, Hall, B.K., Pearson, B.J., and Muller, G.B., Eds., Cambridge: MIT Press, 2003.

    Google Scholar 

  95. Waddington, C., Canalization of development and the inheritance of acquired character, Nature, 1942, vol. 50, pp. 563–565.

    Article  Google Scholar 

  96. Waddington, C., The strategy of the genes, in A Discussion of Some Aspects of Theoretical Biology, London: Georg Allen and Unwin, 1957.

    Google Scholar 

  97. Waddington, C.H., Morfogenez i genetika (Morphogenesis and Genetics), Moscow: Mir, 1964.

  98. Waddington, C.H., Basic biological concepts, in Na puti k teoreticheskoi biologii (On the Way to Theoretical Biology), Astaurov, B.L., Ed., Moscow: Mir, 1970, pp. 11–36.

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    N. D. Ozernyuk

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Ozernyuk, N.D. History of Evolutionary Developmental Biology. Russ J Dev Biol 50, 341–350 (2019). https://doi.org/10.1134/S1062360419060067

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