TY - JOUR

T1 - The placental analogue and the pattern of sexual reproduction in the cheilostome bryozoan Bicellariella ciliata (Gymnolaemata)

AU - Moosbrugger, Martin

AU - Schwaha, Thomas

AU - Walzl, Manfred G.

AU - Obst, Matthias

AU - Ostrovsky, Andrew N.

N1 - Funding Information: We would like to thank the Core Facility Cell Imaging and Ultrastructure Research Unit, Faculty of Life Sciences, University of Vienna, for providing working facilities, and especially Professor, Dr. W. Klepal for her advice on this work. Special thanks are given to X. Shunkina, Department of Invertebrate Zoology, St Petersburg State University, for image processing. Financial support is provided by the FWF project P 22696-B17 (Austria) and the RFBR grant 10-04-00085a (Russia). MO thanks the Swedish Taxonomy Initiative (Grant no. dha 15/06 1.4) for the support.

PY - 2012/10/25

Y1 - 2012/10/25

N2 - Background: Matrotrophy or extraembryonic nutrition - transfer of nutrients from mother to embryo during gestation - is well known and thoroughly studied among vertebrates, but still poorly understood in invertebrates. The current paper focuses on the anatomy and ultrastructure of the oogenesis and placentotrophy as well as formation of the brood chamber (ovicell) in the cheilostome bryozoan Bicellariella ciliata (Linnaeus, 1758). Our research aimed to combine these aspects of the sexual reproduction into an integral picture, highlighting the role of the primitive placenta-like system in the evolution of bryozoan reproductive patterns.Results: Follicular and nutrimentary provisioning of the oocyte occur during oogenesis. Small macrolecithal oocytes are produced, and embryos are nourished in the ovicell via a simple placental analogue (embryophore). Every brooding episode is accompanied by the hypertrophy of the embryophore, which collapses after larval release. Nutrients are released and uptaken by exocytosis (embryophore) and endocytosis (embryo). Embryos lack specialized area for nutrient uptake, which occurs through the whole epidermal surface. The volume increase between the ripe oocyte and the larva is ca. 10-fold.Conclusions: The ovicell is a complex organ (not a special polymorph as often thought) consisting of an ooecium (protective capsule) and an ooecial vesicle (plugging the entrance to the brooding cavity) that develop from the distal and the fertile zooid correspondingly. Combination of macrolecithal oogenesis and extraembryonic nutrition allows attributing B. ciliata to species with reproductive pattern IV. However, since its oocytes are small, this species represents a previously undescribed variant of this pattern, which appears to represent a transitional state from the insipient matrotrophy (with large macrolecithal eggs) to substantial one (with small microlecithal ones). Altogether, our results substantially added and corrected the data obtained by the previous authors, providing a new insight in our understanding of the evolution of matrotrophy in invertebrates.

AB - Background: Matrotrophy or extraembryonic nutrition - transfer of nutrients from mother to embryo during gestation - is well known and thoroughly studied among vertebrates, but still poorly understood in invertebrates. The current paper focuses on the anatomy and ultrastructure of the oogenesis and placentotrophy as well as formation of the brood chamber (ovicell) in the cheilostome bryozoan Bicellariella ciliata (Linnaeus, 1758). Our research aimed to combine these aspects of the sexual reproduction into an integral picture, highlighting the role of the primitive placenta-like system in the evolution of bryozoan reproductive patterns.Results: Follicular and nutrimentary provisioning of the oocyte occur during oogenesis. Small macrolecithal oocytes are produced, and embryos are nourished in the ovicell via a simple placental analogue (embryophore). Every brooding episode is accompanied by the hypertrophy of the embryophore, which collapses after larval release. Nutrients are released and uptaken by exocytosis (embryophore) and endocytosis (embryo). Embryos lack specialized area for nutrient uptake, which occurs through the whole epidermal surface. The volume increase between the ripe oocyte and the larva is ca. 10-fold.Conclusions: The ovicell is a complex organ (not a special polymorph as often thought) consisting of an ooecium (protective capsule) and an ooecial vesicle (plugging the entrance to the brooding cavity) that develop from the distal and the fertile zooid correspondingly. Combination of macrolecithal oogenesis and extraembryonic nutrition allows attributing B. ciliata to species with reproductive pattern IV. However, since its oocytes are small, this species represents a previously undescribed variant of this pattern, which appears to represent a transitional state from the insipient matrotrophy (with large macrolecithal eggs) to substantial one (with small microlecithal ones). Altogether, our results substantially added and corrected the data obtained by the previous authors, providing a new insight in our understanding of the evolution of matrotrophy in invertebrates.

KW - Bicellariella ciliata

KW - Bryozoa

KW - Matrotrophy

KW - Oogenesis

KW - Ovicell

KW - Placental analogue

UR - http://www.scopus.com/inward/record.url?scp=84867745659&partnerID=8YFLogxK

U2 - 10.1186/1742-9994-9-29

DO - 10.1186/1742-9994-9-29

M3 - Article

VL - 9

JO - Frontiers in Zoology

JF - Frontiers in Zoology

SN - 1742-9994

M1 - 29

ER -