Sexual reproduction of the placental brooder Celleporella hyalina (Bryozoa, Cheilostomata) in the White Sea

Abstract

The evolution of parental care is a central field in many ecological and evolutionary studies, but integral approaches encompassing various life‐history traits are not common. Else, the structure, development and functioning of the placental analogues in invertebrates are poorly understood. Here, we describe the life‐history, sexual colony dynamics, oogenesis, fertilization and brooding in the boreal‐Arctic cheilostome bryozoan Celleporella hyalina . This placental brooder incubates its progeny in calcified protective chambers (ovicells) formed by polymorphic sexual zooids. We conducted a detailed ultrastructural study of the ovary and oogenesis, and provide evidence of both auto‐ and heterosynthetic mechanisms of vitellogenesis. We detected sperm inside the early oocyte and within funicular strands, and discuss possible variants of fertilization. We also detail the development and functioning of the placental analogue (embryophore) in the various stages of embryonic incubation as well as embryonic histotrophic nourishment. In contrast to all known cheilostome placentas, the main part of embryophore of C. hyalina is not a single cell layer. Rather, it is a massive “nutritive tissue” whose basal part is associated with funicular strands presumably providing transport function. C. hyalina shows a mixture of reproductive traits with macrolecithal oogenesis and well‐developed placenta. These features give it an intermediate position in the continuum of variation of matrotrophic provisioning between lecithotrophic and placentotrophic cheilostome brooders. The structural and developmental differences revealed in the placental analogue of C. hyalina , together with its position on the bryozoan molecular tree, point to the independent origin of placentation in the family Hippothoidae.

Abstract

Histological sections of the female polymorphic zooids of Celleporella hyalina showing consecutive stages of embryonic growth and embryophore (placental analogue) development in the brood chamber (ovicell). Early embryo and placental analogue in the early stage are seen in the upper image. The bottom image shows advanced embryo that occupies most of the brood cavity. Well‐developed placental analogue is in the mid‐stage. Later on it can occupy almost half of the female zooid.