<i>Electra</i> vs <i>Callopora</i>: life histories of two bryozoans with contrasting reproductive strategies in the White Sea

Shevchenko, Ekaterina T.; Varfolomeeva, Marina A.; Nekliudova, Uliana A.; Kotenko, Olga N.; Usov, Nikolay; Granovitch, Andrei I.; Ostrovsky, Andrew N.

doi:10.1080/07924259.2020.1729260

Cited by 7 publications

(7 citation statements)

References 57 publications

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“…The oocyte becomes surrounded by the follicle cells of mesodermal origin ("egg-follicle" or "primary follicle" of Borg [44]) and, together with the polypide, is enclosed inside the membranous sac. Our study in the White Sea did not sample the onset of reproduction in the local crisiid population because, as with some other bryozoans studied [90][91][92], it starts in late spring under ice. Nonetheless, in Crisiella producta we were able, apart of zooids with ovary, to detect a few zooids with early oocytes (20 μm in diameter) unconnected to the polypide and presumably destined to degenerate [44].…”

Section: Gonozooid Functioning Gametogenesis and Fertilizationmentioning

confidence: 99%

Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans

et al. 2021

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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.

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Section: Gonozooid Functioning Gametogenesis and Fertilizationmentioning

confidence: 99%

Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans

et al. 2021

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“…Secondly, the initial stages of FBs degradation were detected in June when phytoplankton is abundant in the White Sea (e.g. 87 ). We therefore propose the following scenario for the sequence of changes in FBs and their possible causes.…”

Section: Discussionmentioning

confidence: 99%

Seasonal dynamics of a complex cheilostome bryozoan symbiosis: vertical transfer challenged

Bogdanov

Vishnyakov

Kotenko

et al. 2023

Sci Rep

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Symbiotic associations are dynamic systems influenced by both intrinsic and extrinsic factors. Here we describe for the first time the developmental and seasonal changes of the funicular bodies in the bryozoan Dendrobeania fruticosa, which are unique temporary organs of cheilostome bryozoans containing prokaryotic symbionts. Histological and ultrastructural studies showed that these organs undergo strong seasonal modification in the White Sea during the ice-free period. Initially (in June) they play a trophic function and support the development of a large population of bacteria. From June to September, both funicular bodies and bacteria show signs of degradation accompanied by development of presumed virus-like particles (VLPs); these self-organize to hollow spheres inside bacteria and are also detected outside of them. Although the destruction of bacteria coincides with the development of VLPs and spheres, the general picture differs considerably from the known instances of bacteriophagy in bryozoans. We broadly discuss potential routes of bacterial infection in Bryozoa and question the hypothesis of vertical transfer, which, although widely accepted in the literature, is contradicted by molecular, morphological and ecological evidence.

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“…Degradation process was accompanied by the appearance of polyhedral VLPs in B. neritina and by the formation of structures similar to the so-called metamorphosis-associated contractile complexes (MACs) in P. sinuosa . These complexes are phage-related structures whose activity eventually results in the cell lysis, see 87 . Although the fate of FBs was not analyzed in their paper, these two VLP variants were observed both inside the bacteria and in the FB internal space by Vishnyakov and co-authors 20 .…”

Section: Discussionmentioning

confidence: 99%

“…Firstly, modified FBs were found in zooids with both degenerated and functioning polypides. Secondly, the initial stages of FBs degradation were detected in June when phytoplankton is abundant in the White Sea (e.g., 86 ). We therefore propose the following scenario for the sequence of changes in FBs and their possible causes.…”

Section: Symbiont Population Dynamics In Dendrobeania Fruticosa and I...mentioning

confidence: 99%

Seasonal dynamics of a complex cheilostome bryozoan symbiosis – vertical transfer challenged

Bogdanov

Vishnyakov

Kotenko

et al. 2022

Preprint

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Symbiotic associations are dynamic systems influenced by both intrinsic and extrinsic factors. Here we describe for the first time the developmental and seasonal changes of the funicular bodies in the bryozoan Dendrobeania fruticosa, which are unique temporary organs of cheilostome bryozoans containing prokaryotic symbionts. Histological and ultrastructural studies showed that these organs undergo strong seasonal modification in the White Sea during the ice-free period. Initially (in June) they play a trophic function and support the development of a large population of bacteria. From June to September, both funicular bodies and bacteria show signs of degradation accompanied by development of presumed virus-like particles (VLPs); these self-organize to hollow spheres inside bacteria and are also detected outside of them. Although the destruction of bacteria coincides with the development of VLPs and spheres, the general picture differs considerably from the known instances of bacteriophagy in bryozoans. We broadly discuss potential routes of bacterial infection in Bryozoa and question the hypothesis of vertical transfer, which, although popular in the literature, is contradicted by molecular, morphological and ecological evidence.

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Electra vs Callopora: life histories of two bryozoans with contrasting reproductive strategies in the White Sea

Cited by 7 publications

References 57 publications

Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans

Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans

Seasonal dynamics of a complex cheilostome bryozoan symbiosis: vertical transfer challenged

Seasonal dynamics of a complex cheilostome bryozoan symbiosis – vertical transfer challenged

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