First ultrastructural evidence of placental nutrition in a ctenostome bryozoan: example of Amathia verticillata

Abstract

Matrotrophy and its most advanced mode-placentation-is a masterpiece of nature contributing to offspring fitness. It has been studied mainly in vertebrates, whereas so-called placental analogues in invertebrates are poorly known. Here we use an ultrastructural approach to report the first evidence of placentation in the ctenostome bryozoan Amathia verticillata. This marine colonial suspension-feeder incubates its progeny in the tentacle sheath, which is transformed into a brood chamber. When the fertilized egg is deposited into the brood cavity, the tentacle sheath wall, originally consisting of flattened epithelial cells, is modified into an embryophore (placental analogue) via cell multiplication and hypertrophy. The embryophore (nutritive) cells develop a massive secretory apparatus and acquire 'microvillous' apical membranes indicating the presence of exocytosis. In turn, the embryo surface cells also form a complex network of irregular projections and foldings. Coated pits beneath this network indicate active endocytosis. The developing embryo is adjacent to the embryophore and the narrow slit between them is filled with dense and flocculent (presumably nutritive) material. The embryo increases up to 24-fold in size indicating substantial matrotrophic provisioning. We compare the ultrastructural details of placentation in A. verticillata with those known in cheilostome bryozoans, and review the major structural principles of placentation in Bryozoa in general. We then discuss possible ways of nutrient transport to the embryophore in various bryozoan clades.

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

“…Phylactolaemata brood their embryos in an internal brood sac (reviewed in [ 20 , 119 , submitted]), as do some placental ctenostome and cheilostome Gymnolaemata (reviewed in [ 16 , 36 , 120 ]). Some ctenostomes also brood their progeny in the tentacle sheath modified into a placental analogue (reviewed in [ 26 ]). Finally, most placental cheilostomes incubate their young in skeletal brood chambers (ovicells) (reviewed in [ 16 , 19 ]).…”

“…The dynamics of placentation is also quite contrasting: in most cheilostomes and some ctenostomes, placental analogues function without affecting the polypide (whether ordinary or rudimentary) recycling: they develop repeatedly for each embryo and degrade after larval release. In contrast, in ctenostomes nourishing embryos in the modified tentacle sheath, the polypide degenerates before or after deposition of a zygote in the brooding site (tentacle sheath, brooding pouch) [ 16 , 26 , 120 , 125 ]. In Epistomiidae, the polypide degenerates irreversibly in the enlarged/swollen female zooid that produces a single larva [ 22 ].…”

Life in a tube: morphology of the ctenostome bryozoan Hypophorella expansa

“…Broadcasting is less common among Bryozoa, whereas most species (including ctenostomes) incubate their embryos (cf. [41, 43–45]). Broadcasting in H. expansa includes the production of many small oligolecithal oocytes and a presumed feeding larva, the cyphonautes [7, 9].…”

Key novelties in the evolution of the aquatic colonial phylum Bryozoa: evidence from soft body morphology

“…The distribution of oogenetic modes, types of embryonic incubation and larval anatomy imply numerous independent shifts from a broadcast‐spawning pattern with a feeding larval stage to embryonic incubation with lecithotrophic larvae (Taylor, ; Reed, ; Ostrovsky, 2013 a ). Placentation has evolved independently many times among Gymnolaemata, and at least once in the Phylactolaemata and once in the Stenolaemata (Ostrovsky et al ., , ; Ostrovsky, 2013 a , b ; Schwaha et al ., ). These changes were accompanied by shifts in oogenesis from oligolecithal to macrolecithal and occasionally by reversals back to oligolecithal oogenesis (Moosbrugger et al ., ; Ostrovsky, 2013 a , b ; Nekliudova et al ., ).…”