First ultrastructural evidence of placental nutrition in a ctenostome bryozoan: example of Amathia verticillata

Thomas Schwaha, M. Moosbrugger, M.G. Walzl, A.N. Ostrovsky

Research output

1 Citation (Scopus)

Abstract

Matrotrophy and its most advanced mode—placentation—is a masterpiece of nature contributing to offspring fitness. It has been studied mainly in vertebrates, whereas so-called placental analogues in invertebrates are poorly known. Here we use an ultrastructural approach to report the first evidence of placentation in the ctenostome bryozoan Amathia verticillata. This marine colonial suspension-feeder incubates its progeny in the tentacle sheath, which is transformed into a brood chamber. When the fertilized egg is deposited into the brood cavity, the tentacle sheath wall, originally consisting of flattened epithelial cells, is modified into an embryophore (placental analogue) via cell multiplication and hypertrophy. The embryophore (nutritive) cells develop a massive secretory apparatus and acquire ‘microvillous’ apical membranes indicating the presence of exocytosis. In turn, the embryo surface cells also form a complex network of irregular projections and foldings. Coated pits beneath this network indicate active endocytosis. The developing embryo is adjacent to the embryophore and the narrow slit between them is filled with dense and flocculent (presumably nutritive) material. The embryo increases up to 24-fold in size indicating substantial matrotrophic provisioning. We compare the ultrastructural details of placentation in A. verticillata with those known in cheilostome bryozoans, and review the major structural principles of placentation in Bryozoa in general. We then discuss possible ways of nutrient transport to the embryophore in various bryozoan clades.
Original languageEnglish
Pages (from-to)221-232
Number of pages12
JournalZoomorphology
Volume138
Issue number2
DOIs
Publication statusPublished - 2019

Fingerprint

Placentation
embryo (animal)
Embryonic Structures
Bryozoa
nutrition
nutrient transport
exocytosis
Zygote
Exocytosis
endocytosis
cells
Invertebrates
Endocytosis
hypertrophy
Hypertrophy
Vertebrates
Suspensions
epithelial cells
Epithelial Cells
invertebrates

Scopus subject areas

  • Animal Science and Zoology
  • Developmental Biology

Cite this

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title = "First ultrastructural evidence of placental nutrition in a ctenostome bryozoan: example of Amathia verticillata",
abstract = "Matrotrophy and its most advanced mode—placentation—is a masterpiece of nature contributing to offspring fitness. It has been studied mainly in vertebrates, whereas so-called placental analogues in invertebrates are poorly known. Here we use an ultrastructural approach to report the first evidence of placentation in the ctenostome bryozoan Amathia verticillata. This marine colonial suspension-feeder incubates its progeny in the tentacle sheath, which is transformed into a brood chamber. When the fertilized egg is deposited into the brood cavity, the tentacle sheath wall, originally consisting of flattened epithelial cells, is modified into an embryophore (placental analogue) via cell multiplication and hypertrophy. The embryophore (nutritive) cells develop a massive secretory apparatus and acquire ‘microvillous’ apical membranes indicating the presence of exocytosis. In turn, the embryo surface cells also form a complex network of irregular projections and foldings. Coated pits beneath this network indicate active endocytosis. The developing embryo is adjacent to the embryophore and the narrow slit between them is filled with dense and flocculent (presumably nutritive) material. The embryo increases up to 24-fold in size indicating substantial matrotrophic provisioning. We compare the ultrastructural details of placentation in A. verticillata with those known in cheilostome bryozoans, and review the major structural principles of placentation in Bryozoa in general. We then discuss possible ways of nutrient transport to the embryophore in various bryozoan clades.",
keywords = "Aquatic colonial invertebrates, Brooding, Matrotrophy, Placenta, Vesicularioidea, CELLEPORELLA-HYALINA BRYOZOA, REPRODUCTIVE PATTERNS, GAMETOGENESIS, VIVIPARITY, ANATOMY, SEXUAL REPRODUCTION, ORIGIN, EVOLUTION, CHEILOSTOMATA, MORPHOLOGY",
author = "Thomas Schwaha and M. Moosbrugger and M.G. Walzl and A.N. Ostrovsky",
year = "2019",
doi = "10.1007/s00435-019-00438-4",
language = "English",
volume = "138",
pages = "221--232",
journal = "Zoomorphology",
issn = "0340-6725",
publisher = "Springer",
number = "2",

}

First ultrastructural evidence of placental nutrition in a ctenostome bryozoan: example of Amathia verticillata. / Schwaha, Thomas; Moosbrugger, M.; Walzl, M.G.; Ostrovsky, A.N.

In: Zoomorphology, Vol. 138, No. 2, 2019, p. 221-232.

Research output

TY - JOUR

T1 - First ultrastructural evidence of placental nutrition in a ctenostome bryozoan: example of Amathia verticillata

AU - Schwaha, Thomas

AU - Moosbrugger, M.

AU - Walzl, M.G.

AU - Ostrovsky, A.N.

PY - 2019

Y1 - 2019

N2 - Matrotrophy and its most advanced mode—placentation—is a masterpiece of nature contributing to offspring fitness. It has been studied mainly in vertebrates, whereas so-called placental analogues in invertebrates are poorly known. Here we use an ultrastructural approach to report the first evidence of placentation in the ctenostome bryozoan Amathia verticillata. This marine colonial suspension-feeder incubates its progeny in the tentacle sheath, which is transformed into a brood chamber. When the fertilized egg is deposited into the brood cavity, the tentacle sheath wall, originally consisting of flattened epithelial cells, is modified into an embryophore (placental analogue) via cell multiplication and hypertrophy. The embryophore (nutritive) cells develop a massive secretory apparatus and acquire ‘microvillous’ apical membranes indicating the presence of exocytosis. In turn, the embryo surface cells also form a complex network of irregular projections and foldings. Coated pits beneath this network indicate active endocytosis. The developing embryo is adjacent to the embryophore and the narrow slit between them is filled with dense and flocculent (presumably nutritive) material. The embryo increases up to 24-fold in size indicating substantial matrotrophic provisioning. We compare the ultrastructural details of placentation in A. verticillata with those known in cheilostome bryozoans, and review the major structural principles of placentation in Bryozoa in general. We then discuss possible ways of nutrient transport to the embryophore in various bryozoan clades.

AB - Matrotrophy and its most advanced mode—placentation—is a masterpiece of nature contributing to offspring fitness. It has been studied mainly in vertebrates, whereas so-called placental analogues in invertebrates are poorly known. Here we use an ultrastructural approach to report the first evidence of placentation in the ctenostome bryozoan Amathia verticillata. This marine colonial suspension-feeder incubates its progeny in the tentacle sheath, which is transformed into a brood chamber. When the fertilized egg is deposited into the brood cavity, the tentacle sheath wall, originally consisting of flattened epithelial cells, is modified into an embryophore (placental analogue) via cell multiplication and hypertrophy. The embryophore (nutritive) cells develop a massive secretory apparatus and acquire ‘microvillous’ apical membranes indicating the presence of exocytosis. In turn, the embryo surface cells also form a complex network of irregular projections and foldings. Coated pits beneath this network indicate active endocytosis. The developing embryo is adjacent to the embryophore and the narrow slit between them is filled with dense and flocculent (presumably nutritive) material. The embryo increases up to 24-fold in size indicating substantial matrotrophic provisioning. We compare the ultrastructural details of placentation in A. verticillata with those known in cheilostome bryozoans, and review the major structural principles of placentation in Bryozoa in general. We then discuss possible ways of nutrient transport to the embryophore in various bryozoan clades.

KW - Aquatic colonial invertebrates

KW - Brooding

KW - Matrotrophy

KW - Placenta

KW - Vesicularioidea

KW - CELLEPORELLA-HYALINA BRYOZOA

KW - REPRODUCTIVE PATTERNS

KW - GAMETOGENESIS

KW - VIVIPARITY

KW - ANATOMY

KW - SEXUAL REPRODUCTION

KW - ORIGIN

KW - EVOLUTION

KW - CHEILOSTOMATA

KW - MORPHOLOGY

UR - http://www.scopus.com/inward/record.url?scp=85063207370&partnerID=8YFLogxK

U2 - 10.1007/s00435-019-00438-4

DO - 10.1007/s00435-019-00438-4

M3 - Article

VL - 138

SP - 221

EP - 232

JO - Zoomorphology

JF - Zoomorphology

SN - 0340-6725

IS - 2

ER -