Ablastica - Metazoa without germ layers

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Abstract

The germ layers theory is a fundamental synthesis of comparative and evolutionary embryology, which is essential for proving the unity of the multicellular animals. In this article, we substantiate the point of view that among Metazoa, in addition to Diploblastica and Triploblastica, there is a third group, which lacks germ layers, and on this basis we propose to call it Ablastica.

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About the authors

A. K. Dondua

St. Petersburg State University

Email: gonobol@mail.ru

биологический факультет, кафедра эмбриологии

Russian Federation, Universitetskaya nab. 7/9, St. Petersburg, 199034

E. L. Gonobobleva

St. Petersburg State University

Author for correspondence.
Email: gonobol@mail.ru

биологический факультет, кафедра эмбриологии

Russian Federation, Universitetskaya nab. 7/9, St. Petersburg, 199034

References

  1. Беклемишев В. Н. Основы сравнительной анатомии беспозвоночных. Том 1. Проморфология. Стр. 46–49; Том 2. Органология. М.: Наука, 1964. Стр 169.
  2. Вестхайде В, Ригер Р. Зоология беспозвоночных. Т. 1. От простейших до моллюсков и артропод. М.: Изд-во КМК. 2008. 512 с.
  3. Гонобоблева Е. Л. Формирование пластов поляризованных клеток (эпителизация) в эмбриональном развитии губок // Тр. С-Петерб об-ва естествоисп. 2009. Сер. 1. Т. 97. Стр. 89–102.
  4. Ересковский А. В. Сравнительная эмбриология губок (Porifera). СПб: Изд. СПбГУ, 2005. 304 с.
  5. Иванов П. П. Общая и сравнительная эмбриология. М.-Л.: Биомедгиз, 1937. 812с.
  6. Иванова-Казас О. М. Сравнительная эмбриология беспозвоночных животных. Простейшие и низшие многоклеточные. Новосибирск: Наука, 1975. 372 с.
  7. Иванова-Казас О. М. Эволюционная эмбриология животных. СПб.: Наука, 1995. 565 с.
  8. Короткова Г. П. Общая характеристика организации губок // Труды Биол. НИИ ЛГУ. Морфогенезы у губок. 1981. № 33. С 5–91.
  9. Короткова Г. П. Половой эмбриогенез губок и закономерности его эволюции // Труды Биол. НИИ ЛГУ. Морфогенезы у губок. 1981. № 33. С 108–136.
  10. Короткова Г. П. Регенерация животных. СПб: Изд-во С.-Петерб. ун-та, 1997. 479 с.
  11. Малахов В. В. Загадочные группы морских беспозвоночных. М.: Изд-во МГУ, 1990. 145 с.
  12. Мечников И. И., 1877. О пищеварительных органах пресноводных турбеллярий // Записки Новоросс. Общ. Естествоисп. Т. 5, № 1 С. 1–12.
  13. Светлов П. Г. О значении теории зародышевых листков в современной науке // Арх. Анат. Гист. и эмбр. 1963. Т. 44. № 4. С. 7–25.
  14. Adamska M. Sponges as models to study emergence of complex animals // Curr. Opin. Genet. Dev. 2016. V. 39. P. 21–28. https://doi.org/10.1016/j.gde.2016.05.026
  15. Allman G. J. On the anatomy and physiology of Cordylophora, a contribution to our knowledge of the tubularian zoophytes // Proc. R. Soc. Lond. 1853. V. 6. № 97. P. 319–321.
  16. Amano S., Hori I. Metamorphosis of calcareous sponges. II. Cell rearrangement and differentiation in metamorphosis // Invertebr. Reprod. Dev. 1993. V. 24. P. 13–26. https://doi.org/10.1080/07924259.1993.9672327
  17. Amano S., Hori I. Metamorphosis of coeloblastula performed by multipotential larval flagellatedcells in the calcareous sponge Leucosolenia laxa. // Biol. Bull. 2001. V. 200. P. 20–32. doi: 10.2307/1543082
  18. Baer K. E. Über Entwickelungsgeschichte der Thiere. Beobachtung und Reflexion. I Theil. Königsberg: Bei den Gebrüdern Bornträger. 1828. P. 1–271
  19. Beklemishev V. N. Principles of comparative anatomy of invertebrates. Volume 2: Organology, Chicago: University of Chicago Press, 1969. P. 195.
  20. Borojevic R. Ètude expérimentale de la différenciation des cellules de l’éponge au cours de son développement // Dev. Biol. 1966. V. 14. P. 130–153.
  21. Borojevic R. Etude du développement et de la differentiation cellulaire d’éponges calcaires Calcinées (genres Clathrina et Ascandra) // Ann/ Embryol. Morph. 1969. V. 2. P. 15–36.
  22. Borojevic R. Différenciation cellulaires dans l’embryogenèse et la morphogenèse chez les Spongiaires // The biology of the Porifera. Symp. Zool. Soc. Ed. W. G. Fry. London. V. 25. P. 267–290.
  23. Boury-Esnault N., Ereskovsky A. V., Bezac C., et al. Larval development in Homoscleromorpha (Porifera, Demospongiae) first evidence of basal membrane in sponge larvae // Invert. Biol. 2003. V. 122. P. 187–202. https://doi.org/10.1111/j.1744–7410.2003.tb00084.x
  24. Brusca R., Brusca G. Invertebrates. Sinauer Associates; 2nd edition, 2003. 936 p.
  25. Calder D. R. George James Allman (1812–1898): pioneer in research on Cnidaria and freshwater Bryozoa // Zootaxa. 2015. V. 4020 N. 2. P. 201–243. doi: 10.11646/zootaxa.4020.2.1
  26. Colgren J., Nichols S. A. The significance of sponges for comparative studies of developmental evolution // WIREs Dev. Biol. 2020. V.9. e359. P. 1–16. doi: 10.1002/wdev.359
  27. Degnan B. M., Adamska M., Richards G. S., Larroux C., et al. Porifera.// In: Evolutionary Developmental Biology of Invertebrates 1: Introduction, Non-Bilateria, Acoelomorpha, Xenoturbellida, Chaetognatha. (ed. Wanninger, A.). SpringerVerlag. 2015. P. 65–106. https://doi.org/10.1007/978–3–7091–1862–7
  28. Delage Y. Embryogenese des eponges silicieus // Arch. Z. Exp. Gen. 1892. T. 10. P. 345–498.
  29. Dondua A. K., Kostyuchenko R. P. Concerning One Obsolete Tradition: Does Gastrulation in Sponges Exist? // Russ. J. Dev. Biol. V. 2013. 44. N5. P. 267–272. doi: 10.1134/S1062360413050020
  30. Edgar R., Mazor Y., Rinon A. et al. LifeMap Discovery: The Embryonic Development, Stem Cells, and Regenerative Medicine Research Portal // PLoS One. 2013 V. 8(7). P. 1–13. doi: 10.1371/journal.pone.0066629.
  31. Eerkes-Medrano D., Leys S. P. Ultrastructure and embryonic development of a syconoid calcareous sponge // Invertebr. Biol. 2006. V. 125. P. 177–194. doi: 10.1016/j.zool.2021.125984
  32. Efremova S. M. Once more on the position among Metazoa – Gastrulation and germinal layers of sponges // In: Modern problems of Poriferan biology. Eds. A. V. Ereskovsky, H. Keupp, R. Kohring. Berliner geowiss. Abh. 1997. E20. P. 7–15.
  33. Ereskovsky A. V. The Comparative Embryology of Sponges, Springer Nature, 2010. 698 p.
  34. Ereskovsky A., Borisenko I. E., Bolshakov F. V., Lavrov A. I. // Genes. 2021. V. 12, 506. https://doi.org/10.3390/genes12040506
  35. Ereskovsky A. V., Boury-Esnault N: Cleavage pattern in Oscar.ella species (Porifera, Demospongiae, Homoscleromorpha): transmission of maternal cells and symbiotic bacteria // J Nat Hist. 2002. V. 36. P. 1761–1775. https://doi.org/10.1080/00222930110069050
  36. Ereskovsky A. V., Dondua A. K. The problem of germ layers in sponges (Porifera) and some issues concerning early metazoan evolution // Zool. Anz. 2006. V. 245. I. 2. P. 65–76. https://doi.org/10.1016/j.jcz.2006.04.002
  37. Ereskovsky A. V., Tokina D. B., Bezac Ch. et al. Metamorphosis of Cinctoblastula Larvae (Homoscleromorpha, Porifera). // J. Morphol. 2007. V. 268. P. 518–528. doi: 10.1002/jmor.10506
  38. Fortunato S., Adamski M., Adamska M. Comparative analyses of developmental transcription factor repertoires in sponges reveal unexpected complexity of the earliest animals // Mar. Genomics. 2015. V. 24. P. 121–129. doi: 10.1016/j.margen.2015.07.008
  39. Franzen W. Oogenesis and larval development of Scypha ciliata (Porifera, Calcarea) // Zoomorphology. 1988. V. 107. P. 349–357. https://doi.org/10.1007/BF00312218
  40. Funayama N. Stem Cell System of Sponge // In: Stem Cells: From Hydra to Man. T.C.G. Bosch (ed.). Springer Science + Business Media B. V. 2008. P. 17–35. doi: 10.1007/978–1–4020–8274–0_2
  41. Funayama N. The stem cell system in demosponges: suggested involvement of two types of cells: archeocytes (active stem cells) and choanocytes (food-entrapping flagellated cells) // Dev. Genes Evol. 2013. V. 223. P. 23–38. doi: 10.1007/s00427–012–0417–5
  42. Godefroy N., Goff E., Martinand-Mari C. et al. Sponge digestive system diversity and evolution: filter feeding to carnivory // Cell Tissue Res. 2019. V. 377(3). P. 341–351. doi: 10.1007/s00441–019–03032–8.
  43. Gonobobleva E. L., Ereskovsky A. V. Metamorphosis of the larva of Halisarca dujardini (Demospongiae, Halisarcida) // Bull. Inst. R. Sci. nat. Belg. Biol. 2004. V. 74. P. 101–115.
  44. Haeckel E., Generelle Morphologie der Organismen. Georg Reimer, Berlin. 1866.
  45. Haeckel E. Die Gastrea-Theorie, die philogenetische Classification der Thierreichs und die Homologie der Keimblätter // Jena. Z. Naturw. 1874. Bd.8. S.1–55.
  46. Hall B. K. Germ Layers and the Germ-Layer Theory Revisited // In: Hecht, M.K., Macintyre, R.J., Clegg, M.T. (eds) Evolutionary Biology. Evolutionary Biology. Springer, Boston, MA. 1998. V. 30. P. 121–186. https://doi.org/10.1007/978–1–4899–1751–5_5
  47. Hutchins A. P., Yang Z., Li Y. et al. Models of global gene expression define major domains of cell type and tissue identity // Nucleic Acids Res. 2017. V. 45(5). P. 2354–2367. doi: 10.1093/nar/gkx054.
  48. Huxley T. G. On the anatomy and the affinities of the family of Medusae // Philosophical Trans. 1849. T.II. P. 425.
  49. Ivanova L. V. New data about morphology and metamorphosis of spongillid larvae (Porifera, Spongillidae). 2. The metamorphosis of the spongillid larvae // In: Modern problems of Poriferan biology. Eds. A. V. Ereskovsky, H. Keupp, R. Kohring. Berliner geowiss. Abh. 1997. E20. P. 73–91.
  50. Kowalevsky A. O. Embryologisсhe Studien an Würmen und Arthropoden // Mèm. Acad. Sci. St.-Petersb. 1871. Sér. 7. T. 16. S. 1–70.
  51. Kraus Y. A., Markov A. V. Gastrulation in Cnidaria: The key to an understanding of phylogeny or the chaos of secondary modifications? // Biology Bulletin Reviews. 2017. V.7. P. 7–25.
  52. Lee W. L. Reiswig H. M., Austin W. C., Lundsten L. An extraordinary new carnivorous sponge, Chondrocladia lyra, in the new subgenus Symmetrocladia (Demospongiae, Cladorhizidae), from off of northern California, USA // Invertebr. Biol. 2012. V. 131(4). P.
  53. Leininger S., Adamski M., Bergum B. et al. Developmental gene expression provides clues to relationships between sponge and eumetazoanbody plans // Nat. Commun. 2014. V. 5. P. 1–15. doi: 10.1038/ncomms4905
  54. Leys S. P., Degnan B. M. Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes // 2002. Invertebr. Biol. V. 121. N. 3. P. 171–189. https://doi.org/10.1111/j.1744–7410.2002.tb00058.x
  55. Leys S.P, Ereskovsky A. V. Embryogenesis and larval differentiation in sponges // 2006. Can. J. Zool. V. 84. N. 2. P. 262–287. https://doi.org/10.1139/z05–170
  56. Leys S.P, Hill A. The Physiology and Molecular Biology of Sponge Tissues // In; Mikel A. Becerro, Maria J. Uriz, Manuel Maldonado and Xavier Turon, editors. The Netherlands: Amsterdam, Academic Press. 2012. Adv. Mar. Biol. V. 62. P. 3–56. doi: 10.1016/B978–0–12–394283–8.00001–1
  57. Maas, O. Über die Entwicklung karbonatfreier and kalifreier Salzlösungen auf erwachsene Kalkschwämme und auf Entwicklungsstadien derselben // Roux’Arch. Entwicklungsmech. 1906. V. 22. P. 581–599.
  58. Malakhov V. V. Major stages in the Evolution of Eukaryotic Organisms // Paleontol. J. 2003. V. 37. N. 6. P. 584–591.
  59. M. Maldonado, P. Bergquist. Phylum Porifera // In Atlas of marine invertebrate larvae, (Eds: C. M. Young, M. A. Sewel, M. E. Rice), Academic, Barcelona 2001, P. 21–51.
  60. Maldonado M., Ribes M. and Duyl F. C. Nutrient Fluxes Through Sponges: Biology, Budgets, and Ecological Implications In Mikel A. Becerro, Maria J. Uriz, Manuel Maldonado and Xavier Turon, editors. The Netherlands: Amsterdam, Academic Press. 2012. Adv. Mar. Biol. V. 62. P. 113–182. doi: 10.1016/B978–0–12–394283–8.00003–5
  61. Manuel M. Early evolution of symmetry and polarity in metazoan body plans. // C. R. Biol. 2009. V. 332. I. 2–3. P. 184–209. doi: 10.1016/j.crvi.2008.07.009
  62. Metschnikoff E.,1874. Embryologische Studien an Medusen.Wien.159 S.
  63. Metschnikoff E. Vergleichend embryologische Studien. III. Über die Gastrula einiger Metazoa // Zeitschr. wiss. Zool. 1880. Bd. 37. S. 286–313.
  64. Meewis H. Contribution a l’etude de l’embryogenese des Myxospongiae: Halisarca lobularis (Schmidt) // Arch Biol Liege. 1938. V. 59. P. 1–66.
  65. Meewis H. Contribution a l’étude de l’embryogénese de Chalinulidae: Haliclona limbata. Ann. Soc. R. Zool. Belg. 1939. V. 70. P. 201–243.
  66. Meewis H. Contribution a l’étude de l’embryogénese des éponges siliceuse. Ann. Soc. R. Zool. Belg. 1941. V. 72. P. 126–149.
  67. Musser J. M., Schippers K. J., Nickel1 M. et al Profiling cellular diversity in sponges informs animal cell type and nervous system evolution // Science. 2021. V. 374. P. 717–723. doi: 10.1126/science.abj294
  68. Nájera G. S., Weijer C. J. The evolution of gastrulation morphologies // Development. 2023. V.150(7). dev200885.DOI: https://doi.org/10.1242/dev.200885
  69. Nakanishi, N., Sogabe, S., Degnan, B. Evolutionary origin of gastrulation: Insights from sponge development // BMC Biology. 2014. V. 12. N. 26. P. 1–9. doi: 10.1186/1741–7007–12–26
  70. Nielsen C. Animal Evolution: Interrelationships of the Living Phyla (third edition), Oxford: University Press, 2001. 1–563 p.
  71. Pander Ch. Dissertatio inauguralis sistens historiam metamorphoseos, quam ovum incubatum prioribusquinque diebus. Wirceburgi, 1817. 1–69 p.
  72. Rathke M. H. Flusskrebs. // Isis von Oken, 1825. Erster Band. Heft X. S. 1093–1100. Richardson M. K. Theories, laws, and models in evo-devo // J Exp Zool B Mol Dev Evol. 2021. V. 338(1–2). P. 1–26. doi: 10.1002/jez.b.23096.
  73. Riesgo A., Taylor C., Leys S. Reproduction in a carnivorous sponge: the significance of the absence of an aquiferous system to the sponge body plan // Evolution and Development. 2007. V. 9 (6). P. 618–631. https://doi.org/10.1111/j.1525–142X.2007.00200.x
  74. Sebé-Pedrós A., Chomsky E., Pang K. et al. Early metazoan cell type diversity and the evolution of multicellular gene regulation // Nat Ecol Evol. 2018. V. 2(7). P. 1176–1188. doi: 10.1038/s41559–018–0575–6.
  75. Simpson T. L. The cell biology of Sponges. New York: Springer-Verlag, 1984. 662 p.
  76. Schönberg C. H.L. No taxonomy needed: Sponge functional morphologies inform about environmental conditions // Ecol. Indic. 2021. V. 129. 107806. P. 1–30. https://doi.org/10.1016/j.ecolind.2021.107806
  77. Steinmetz P. R. A non-bilaterian perspective on the development and evolution of animal digestive systems. // Cell and tissue research. 2019. V. 377(3). P. 321–39.
  78. Tarashansky A. J., Musser J. M., Khariton M. et al. Mapping single-cell atlases throughout Metazoa unravels cell type evolution // Elife. 2021. V. 10. P. 1–24. doi: 10.7554/eLife.66747.
  79. Vacelet J, Boury-Esnault N. Carnivorous sponges // Nature. 1995. V. 373. P. 333–335. https://doi.org/10.1038/373333a0
  80. Vacelet J, Duport E. Prey capture and digestion in the carnivorous sponge Asbestopluma hypogea (Porifera: Demospongiae) // Zoomorphology. 2004. V. 123. P. 179–190. doi: 10.1242/jeb.072371
  81. Weisswnfels N. Biologie und Mikroskopische Anatomie der Süßwasserschwämme (Spongillidae). New York: Fisher. 1989. 110p.
  82. Wolff C. F. De formatione intestinorm praecipue tum et de amnio spurioiisque partibus embryonis gallinacei, nondum visis. Observationes, in ovis incubatis institutae, I – III. Novi commentarii Academiae Imp. Scientiarum Petropolitanae, t. XII. 1766–1767, 1768, s.403–507; t.XIII (1768–1769).
  83. Wolff, C. F. (1768; 1769). De formatione intestinorum praecipue, tum et de amnio spurio, aliisque partibus embryonis gallinacei nondum visis. // Novi commentarii Academiae Scientiarum Imperialis Petropolitanae. T. XII. S. 403–507; T. XIII.
  84. WPD (The World Porifera Database) // https://www.marinespecies.org/porifera/

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2. Fig. 1. The scheme of a single-scull sponge, according to Weissenfels, 1989, with changes. ap is the atrial cavity, vk is the outflow channel of the aquifer system, m is the mesochil, os is the osculum, oc is the oocyte, p is the pore, pk is the bringing channel of the aquifer system, sp is the spicule, hc is the choanocyte chamber, em is the embryo. The arrows indicate the direction of water flow through the sponge body.

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3. Fig. 2. Embryonic development of single-layered (blastula) sponge larvae. a-d – embryonic development of the calcareous sponge Ascandra minchini (Calcarea, Calcinea) and the larva calciblastula Leucosolenia (?) laxa (Calcarea, Calcinea) (based on articles: Borojevic, 1969; Amano, Hori, 1993. Drawings a-g from: Gonobobleva, 2009). Complete uniform crushing (a, b) ends with the formation of a single-layered coeloblastula (c, d). The radial planes of cell divisions of the embryo persist until the end of embryogenesis, which leads to the formation of a single-layered larva (e). Granular amoebocytes of maternal origin are present in the larva cavity. In the posterior hemisphere, among the flagellate cells, presumably photosensitive cells (e) are localized. e–k – embryonic development and larva – amphiblastula of the calcareous sponge Sycon sp (Calcarea, Calcaronea) (based on the materials of articles: Franzen, 1988; Amano, Hori, 2001; figures e-and from: Gonobobleva, 2009). Complete fragmentation leads to the formation of ~ 64 cells of the celloblastula (

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4. Fig. 3. A-D: Embryonic development and larva parenchyma of Adocia cinerea (Demospongiae, Haplosclerida) (based on the article by Meewi, 1941). a–d: differentiation and sorting of embryo cells by the example of individual cell types. Complete, uneven and disordered crushing leads to the formation of morula. At the stage of ~ 2000-4000 cells, the differentiation of embryo cells (A) begins. Scleroblasts forming larval spicules appear on the surface of the morula, which consists of morphologically homogeneous cells. B - asymmetric division of morula cells leads to the appearance of two types of cells – small and large amoeboid cells (micromeres (mi) and macromeres (ma), according to the nomenclature of Henrietta Mevi). C – the beginning of cell sorting: small cells (mi) migrate to the periphery, and large cells (ma) to the center of the embryo. Scleroblasts with spicules also move inside the embryo. G is the stage of pre–birth. Small cells have rallied on the surface and gradually form a flagellar epithelium, morphologically

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5. Fig.4. A cladogram reflecting the relationship between the primary Metazoa shows the existence of two groups, which we have named Ablastica and Blastica. The ontogenesis of Ablastica is characterized by the absence of gastrulation, germ leaves and digestive cavity. Blastica is the line in which germ leaves appear (ectoderm and endoderm in Diploblastica, or ectoderm, endoderm and mesoderm in Triploblastica). Digestion takes place in the intestine, formed from the inner germ leaf – endoderm.

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