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Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans
BACKGROUND: Placentation has evolved multiple times among both chordates and invertebrates. Although they are structurally less complex, invertebrate placentae are much more diverse in their origin, development and position. Aquatic colonial suspension-feeders from the phylum Bryozoa acquired placen...
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2021
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8042935/ https://www.ncbi.nlm.nih.gov/pubmed/33845757 http://dx.doi.org/10.1186/s12862-021-01775-z |
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author | Nekliudova, U. A. Schwaha, T. F. Kotenko, O. N. Gruber, D. Cyran, N. Ostrovsky, A. N. |
author_facet | Nekliudova, U. A. Schwaha, T. F. Kotenko, O. N. Gruber, D. Cyran, N. Ostrovsky, A. N. |
author_sort | Nekliudova, U. A. |
collection | PubMed |
description | BACKGROUND: Placentation has evolved multiple times among both chordates and invertebrates. Although they are structurally less complex, invertebrate placentae are much more diverse in their origin, development and position. Aquatic colonial suspension-feeders from the phylum Bryozoa acquired placental analogues multiple times, representing an outstanding example of their structural diversity and evolution. Among them, the clade Cyclostomata is the only one in which placentation is associated with viviparity and polyembryony—a unique combination not present in any other invertebrate group. RESULTS: The histological and ultrastructural study of the sexual polymorphic zooids (gonozooids) in two cyclostome species, Crisia eburnea and Crisiella producta, revealed embryos embedded in a placental analogue (nutritive tissue) with a unique structure—comprising coenocytes and solitary cells—previously unknown in animals. Coenocytes originate via nuclear multiplication and cytoplasmic growth among the cells surrounding the early embryo. This process also affects cells of the membranous sac, which initially serves as a hydrostatic system but later becomes main part of the placenta. The nutritive tissue is both highly dynamic, permanently rearranging its structure, and highly integrated with its coenocytic ‘elements’ being interconnected via cytoplasmic bridges and various cell contacts. This tissue shows evidence of both nutrient synthesis and transport (bidirectional transcytosis), supporting the enclosed multiple progeny. Growing primary embryo produces secondary embryos (via fission) that develop into larvae; both the secondary embyos and larvae show signs of endocytosis. Interzooidal communication pores are occupied by 1‒2 specialized pore-cells probably involved in the transport of nutrients between zooids. CONCLUSIONS: Cyclostome nutritive tissue is currently the only known example of a coenocytic placental analogue, although syncytial ‘elements’ could potentially be formed in them too. Structurally and functionally (but not developmentally) the nutritive tissue can be compared with the syncytial placental analogues of certain invertebrates and chordates. Evolution of the cyclostome placenta, involving transformation of the hydrostatic apparatus (membranous sac) and change of its function to embryonic nourishment, is an example of exaptation that is rather widespread among matrotrophic bryozoans. We speculate that the acquisition of a highly advanced placenta providing massive nourishment might support the evolution of polyembryony in cyclostomes. In turn, massive and continuous embryonic production led to the evolution of enlarged incubating polymorphic gonozooids hosting multiple progeny. |
format | Online Article Text |
id | pubmed-8042935 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-80429352021-04-14 Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans Nekliudova, U. A. Schwaha, T. F. Kotenko, O. N. Gruber, D. Cyran, N. Ostrovsky, A. N. BMC Ecol Evol Research Article BACKGROUND: Placentation has evolved multiple times among both chordates and invertebrates. Although they are structurally less complex, invertebrate placentae are much more diverse in their origin, development and position. Aquatic colonial suspension-feeders from the phylum Bryozoa acquired placental analogues multiple times, representing an outstanding example of their structural diversity and evolution. Among them, the clade Cyclostomata is the only one in which placentation is associated with viviparity and polyembryony—a unique combination not present in any other invertebrate group. RESULTS: The histological and ultrastructural study of the sexual polymorphic zooids (gonozooids) in two cyclostome species, Crisia eburnea and Crisiella producta, revealed embryos embedded in a placental analogue (nutritive tissue) with a unique structure—comprising coenocytes and solitary cells—previously unknown in animals. Coenocytes originate via nuclear multiplication and cytoplasmic growth among the cells surrounding the early embryo. This process also affects cells of the membranous sac, which initially serves as a hydrostatic system but later becomes main part of the placenta. The nutritive tissue is both highly dynamic, permanently rearranging its structure, and highly integrated with its coenocytic ‘elements’ being interconnected via cytoplasmic bridges and various cell contacts. This tissue shows evidence of both nutrient synthesis and transport (bidirectional transcytosis), supporting the enclosed multiple progeny. Growing primary embryo produces secondary embryos (via fission) that develop into larvae; both the secondary embyos and larvae show signs of endocytosis. Interzooidal communication pores are occupied by 1‒2 specialized pore-cells probably involved in the transport of nutrients between zooids. CONCLUSIONS: Cyclostome nutritive tissue is currently the only known example of a coenocytic placental analogue, although syncytial ‘elements’ could potentially be formed in them too. Structurally and functionally (but not developmentally) the nutritive tissue can be compared with the syncytial placental analogues of certain invertebrates and chordates. Evolution of the cyclostome placenta, involving transformation of the hydrostatic apparatus (membranous sac) and change of its function to embryonic nourishment, is an example of exaptation that is rather widespread among matrotrophic bryozoans. We speculate that the acquisition of a highly advanced placenta providing massive nourishment might support the evolution of polyembryony in cyclostomes. In turn, massive and continuous embryonic production led to the evolution of enlarged incubating polymorphic gonozooids hosting multiple progeny. BioMed Central 2021-04-12 /pmc/articles/PMC8042935/ /pubmed/33845757 http://dx.doi.org/10.1186/s12862-021-01775-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Nekliudova, U. A. Schwaha, T. F. Kotenko, O. N. Gruber, D. Cyran, N. Ostrovsky, A. N. Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans |
title | Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans |
title_full | Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans |
title_fullStr | Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans |
title_full_unstemmed | Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans |
title_short | Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans |
title_sort | three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8042935/ https://www.ncbi.nlm.nih.gov/pubmed/33845757 http://dx.doi.org/10.1186/s12862-021-01775-z |
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