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


Journal

Journal of morphology
ISSN: 1097-4687
Titre abrégé: J Morphol
Pays: United States
ID NLM: 0406125

Informations de publication

Date de publication:
02 2019
Historique:
received: 25 09 2018
revised: 06 12 2018
accepted: 15 12 2018
entrez: 18 1 2019
pubmed: 18 1 2019
medline: 11 4 2020
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 30653716
doi: 10.1002/jmor.20943
pmc: PMC6949948
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

278-299

Informations de copyright

© 2019 The Authors. Journal of Morphology published by Wiley Periodicals, Inc.

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Auteurs

Uliana A Nekliudova (UA)

Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, Vienna, Austria.
Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Saint Petersburg, Russia.

Thomas F Schwaha (TF)

Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, Vienna, Austria.

Olga N Kotenko (ON)

Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Saint Petersburg, Russia.

Daniela Gruber (D)

Core Facility Cell Imaging and Ultrastructure Research, Faculty of Life Sciences, University of Vienna, Vienna, Austria.

Norbert Cyran (N)

Core Facility Cell Imaging and Ultrastructure Research, Faculty of Life Sciences, University of Vienna, Vienna, Austria.

Andrew N Ostrovsky (AN)

Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Saint Petersburg, Russia.
Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, University of Vienna, Vienna, Austria.

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Classifications MeSH