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

U.A. Nekliudova, T.F. Schwaha, O.N. Kotenko, D. Gruber, N. Cyran, A.N. Ostrovsky

Research output

3 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)278-299
Number of pages22
JournalJournal of Morphology
Volume280
Issue number2
DOIs
Publication statusPublished - Feb 2019

Fingerprint

Bryozoa
Placentation
Oogenesis
oogenesis
sexual reproduction
Oceans and Seas
Reproduction
fertilization (reproduction)
placenta
Fertilization
Placenta
life history
Vitellogenesis
brooders
vitellogenesis
reproductive traits
Invertebrates
automobiles
Oocytes
Spermatozoa

Scopus subject areas

  • Animal Science and Zoology
  • Developmental Biology

Cite this

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title = "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.",
keywords = "colonial aquatic invertebrates, life-history, matrotrophy, oogenesis, placental analogue, FERTILIZATION, VITELLOGENIC MECHANISMS, PHYLOGEOGRAPHY, GAMETOGENESIS, PATTERNS, VIVIPARITY, WATER-BORNE SPERM, MOLECULAR PHYLOGENY, EVOLUTION, HISTORY",
author = "U.A. Nekliudova and T.F. Schwaha and O.N. Kotenko and D. Gruber and N. Cyran and A.N. Ostrovsky",
year = "2019",
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language = "English",
volume = "280",
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journal = "Journal of Morphology",
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TY - JOUR

T1 - Sexual reproduction of the placental brooder Celleporella hyalina (Bryozoa, Cheilostomata) in the White Sea

AU - Nekliudova, U.A.

AU - Schwaha, T.F.

AU - Kotenko, O.N.

AU - Gruber, D.

AU - Cyran, N.

AU - Ostrovsky, A.N.

PY - 2019/2

Y1 - 2019/2

N2 - 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.

AB - 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.

KW - colonial aquatic invertebrates

KW - life-history

KW - matrotrophy

KW - oogenesis

KW - placental analogue

KW - FERTILIZATION

KW - VITELLOGENIC MECHANISMS

KW - PHYLOGEOGRAPHY

KW - GAMETOGENESIS

KW - PATTERNS

KW - VIVIPARITY

KW - WATER-BORNE SPERM

KW - MOLECULAR PHYLOGENY

KW - EVOLUTION

KW - HISTORY

UR - http://www.scopus.com/inward/record.url?scp=85060143432&partnerID=8YFLogxK

UR - http://www.mendeley.com/research/sexual-reproduction-placental-brooder-celleporella-hyalina-bryozoa-cheilostomata-white-sea

U2 - 10.1002/jmor.20943

DO - 10.1002/jmor.20943

M3 - Article

VL - 280

SP - 278

EP - 299

JO - Journal of Morphology

JF - Journal of Morphology

SN - 0362-2525

IS - 2

ER -