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.
Highlights
The mode and timing of parental investment in developing progeny are among the most important aspects of sexual reproduction (Lodé, 2012; Pollux, Pires, Banet, & Reznick, 2009)
The placental analogue in C. hyalina strongly differs from all those previously described in matrotrophic cheilostomes
This is confirmed by its position in the bryozoan molecular tree, where it clusters with non-placental taxa (Taylor & Waeschenbach, 2015; Waeschenbach, Taylor, & Littlewood, 2012)
Summary
The mode and timing of parental investment in developing progeny are among the most important aspects of sexual reproduction (Lodé, 2012; Pollux, Pires, Banet, & Reznick, 2009). This study focuses on the reproductive biology of the common boreal-Arctic cheilostome Celleporella hyalina (Linnaeus, 1767) It demonstrates a prominent example of placentation due to its specialized sexually polymorphic zooids. The development and structure of the ovicells, along with certain aspects of oogenesis and embryonic incubation, were studied on the specimens from the White Sea by Ostrovsky (1998, 2013a, 2013b) using SEM and histological techniques. Both oogenesis and placental nourishment, while providing a comparative basis for our study, were described rather superficially. We for the first time report the main life-history traits of this bryozoan species in the White Sea, yielding an integral picture of its sexual reproduction
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