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

Uliana A. Nekliudova, Thomas Schwaha, Olga N. Kotenko, Daniela Gruber, Norbert Cyran, Andrew N. Ostrovsky

Результат исследований: Научные публикации в периодических изданияхстатья

Аннотация

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 to 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 hydrocompensatory apparatus but later becomes part of the placenta. Although permanently rearranging its structure, the nutritive tissue is highly integrated, and its coenocytic ‘elements’ are 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 buds secondary embryos that develop to larvae, both showing signs of endocytosis. Interzooidal communication pores are occupied by 1‒2 specialized pore-cells probably involved in the intracolonial transport of nutrients.

Conclusions
Cyclostome nutritive tissue is currently the only known example of a coenocytic placental analogue, although syncytial ‘elements’ could potentially be formed 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 hydrocompensatory apparatus (membranous sac) and substitution 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.
Язык оригиналаанглийский
Число страниц64
ЖурналBMC Evolutionary Biology
СостояниеОтправлено - 2020

Предметные области Scopus

  • Земледелие и биологические науки (все)

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