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

Abstract

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.

The epithelial layers of the body wall in hornerid bryozoans (Stenolaemata: Cyclostomatida)

“…We did not detect any cell contacts, and ultrastructurally these cells resemble loose epidermal cells of the terminal membrane and the distal part of the vestibulum. Some of these cells appear to stretch towards the zooid walls, which implies similarity with ‘mesothelial’ cells reported by Nekliudova et al ( 2021 ).…”

“…In many cases, we observed a conglomerate of non‐epithelial cells and/or non‐cellular material in the distal portion of the polypide, occupying the exosaccal cavity between the terminal membrane and the lower vestibulum. Similar, but presumably strictly cellular, agglomerations were recently reported as the ‘upper cell complex’ in crisiids (Nekliudova et al, 2021 ). In addition, loosely arranged cells are located on the exosaccal side of the proximal, epithelialised portion of the vestibular wall.…”

“…At the same time, the original observations by Borg ( 1926a , 1926b ) cannot be dismissed, and indeed were partly confirmed here and also by Nekliudova et al ( 2021 ) in substance if not in interpretation. Although numerous TEM images confirm the lack of collagenous ECM supporting much of the epidermis, we saw squamous, seemingly epidermal, cells making up a loose ‘secondary layer’ in various parts of the colony.…”

Composite branch construction by dual autozooidal budding modes in hornerids (Bryozoa: Cyclostomatida)

“…Micro-CT and soft-tissue sections show that the most-proximal part of a lateral autozooidal chamber usually coincides directly with a mural pore, suggesting the first skeletal walls may have formed around the pore (Figure 7D, F). In thin sections of mature autozooids these first pores are seen to be occupied by a pore cell (Figure 7F, and see Tamberg et al, 2022); although potentially these are formed secondarily, as cyclostome communication pores may be open early in ontogeny (Nekliudova et al, 2021, p. 20). If a pore is not located directly at the proximal-most tip of a zooidal chamber (i.e., the budding locus), one is invariably present very close by and normally within 5 μm.…”

“…Another possibility is that hornerid pores have a nutritional role for the developing (non-feeding) polypide (see Batson et al, 2021). For instance, interzooidal pores, in combination with mesothelial cell networks, have recently been shown to function as a de facto funiculus system in crisiids (Nekliudova et al, 2021).…”