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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.

SUBMITTER: Nekliudova UA

PROVIDER: S-EPMC6949948 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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

Nekliudova Uliana A UA Schwaha Thomas F TF Kotenko Olga N ON Gruber Daniela D Cyran Norbert N Ostrovsky Andrew N AN

Journal of morphology 20190201 2

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 i ...[more]

PMID: 30653716

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Project description:BackgroundBugula is a speciose genus of marine bryozoans, represented by both endemic and cosmopolitan species distributed in tropical and temperate waters and important to marine biologists because of the occurrence of many species in harbor and fouling communities, therefore as potential invaders. The southeastern Brazilian coast in the southern Atlantic hosts the highest known diversity of the genus, a status intimately associated with the intensity of collecting efforts.MethodologyMorphological data based on the examination of living specimens, scanning electron and light microscopic images, and morphometric analyses were used to assess the diversity of Bugula along the coastal areas of southern, northeastern, and southeastern Brazil. In this study, morphological species boundaries were based mainly on avicularian characters. For two morphologically very similar species, boundaries are partially supported by 16 S rDNA molecular data.ResultsNine species are newly described from Brazil, as follows: Bugula bowiei n. sp. ( = Bugula turrita sensu Marcus, 1937) from the southern, northeastern, and southeastern coasts; Bugula foliolata n. sp. ( = Bugula flabellata sensu Marcus, 1938), Bugula guara n. sp., Bugula biota n. sp. and Bugula ingens n. sp from the southeastern coast; Bugula gnoma n. sp. and Bugula alba n. sp. from the northeastern coast; Bugula rochae n. sp. ( = Bugula uniserialis sensu Marcus, 1937) from the southern coast; and Bugula migottoi n. sp., from the southeastern and southern coasts.ConclusionThe results contribute to the morphological characterization and the knowledge of the species richness of the genus in the southwestern Atlantic (i.e., Brazil), through the description of new species in poorly sampled areas and also on the southeastern coast of that country. Additionally, the taxonomic status of the Brazilian specimens attributed to B. flabellata, B. turrita and B. uniserialis are clarified by detailed studies on zooidal and avicularia morphology.

Project description:BACKGROUND: The phylogenetic position of Bryozoa is one of the most controversial issues in metazoan phylogeny. In an attempt to address this issue, the first bryozoan mitochondrial genome from Flustrellidra hispida (Gymnolaemata, Ctenostomata) was recently sequenced and characterized. Unfortunately, it has extensive gene translocation and extremely reduced size. In addition, the phylogenies obtained from the result were conflicting, so they failed to assign a reliable phylogenetic position to Bryozoa or to clarify lophophorate phylogeny. Thus, it is necessary to characterize further mitochondrial genomes from slowly-evolving bryozoans to obtain a more credible lophophorate phylogeny. RESULTS: The complete mitochondrial genome (15,433 bp) of Bugula neritina (Bryozoa, Gymnolaemata, Cheilostomata), one of the most widely distributed cheliostome bryozoans, is sequenced. This second bryozoan mitochondrial genome contains the set of 37 components generally observed in other metazoans, differing from that of F. hispida (Bryozoa, Gymnolaemata, Ctenostomata), which has only 36 components with loss of tRNAser(ucn) genes. The B. neritina mitochondrial genome possesses 27 multiple noncoding regions. The gene order is more similar to those of the two remaining lophophorate phyla (Brachiopoda and Phoronida) and a chiton Katharina tunicate than to that of F. hispida. Phylogenetic analyses based on the nucleotide sequences or amino acid residues of 12 protein-coding genes showed consistently that, within the Lophotrochozoa, the monophyly of the bryozoan class Gymnolaemata (B. neritina and F. hispida) was strongly supported and the bryozoan clade was grouped with brachiopods. Echiura appeared as a subtaxon of Annelida, and Entoprocta as a sister taxon of Phoronida. The clade of Bryozoa + Brachiopoda was clustered with either the clade of Annelida-Echiura or that of Phoronida + Entoprocta. CONCLUSION: This study presents the complete mitochondrial genome of a cheliostome bryozoan, B. neritina. The phylogenetic analyses suggest a close relationship between Bryozoa and Brachiopoda within the Lophotrochozoa. However, the sister group of Bryozoa + Brachiopoda is still ambiguous, although it has some attractions with Annelida-Echiura or Phoronida + Entoprocta. If the latter is a true phylogeny, lophophorate monophyly including Entoprocta is supported. Consequently, the present results imply that Brachiozoa (= Brachiopoda + Phoronida) and the recently-resurrected Bryozoa concept comprising Ectoprocta and Entoprocta may be refuted.

Dataset Information

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

Publications

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

Similar Datasets

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