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From incipient to substantial: evolution of placentotrophy in a phylum of aquatic colonial invertebrates.

ABSTRACT: Matrotrophy has long been known in invertebrates, but it is still poorly understood and has never been reviewed. A striking example of matrotrophy (namely, placentotrophy) is provided by the Bryozoa, a medium-sized phylum of the aquatic colonial filter feeders. Here I report on an extensive anatomical study of placental analogues in 21 species of the bryozoan order Cheilostomata, offering the first review on matrotrophy among aquatic invertebrates. The first anatomical description of incipient placentotrophy in invertebrates is presented together with the evidence for multiple independent origins of placental analogues in this order. The combinations of contrasting oocytic types (macrolecithal or microlecithal) and various degrees of placental development and embryonic enlargement during incubation, found in different bryozoan species, are suggestive of a transitional series from the incipient to the substantial placentotrophy accompanied by an inverse change in oogenesis, a situation reminiscent of some vertebrates. It seems that matrotrophy could trigger the evolution of sexual zooidal polymorphism in some clades. The results of this study show that this phylum, with its wide variety of reproductive patterns, incubation devices, and types of the simple placenta-like systems, offers a promising model for studying parallel evolution of placentotrophy in particular, and matrotrophy in general.

SUBMITTER: Ostrovsky AN

PROVIDER: S-EPMC3698692 | biostudies-literature | 2013 May

REPOSITORIES: biostudies-literature

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From incipient to substantial: evolution of placentotrophy in a phylum of aquatic colonial invertebrates.

Ostrovsky Andrew N AN

Evolution; international journal of organic evolution 20130204 5

Matrotrophy has long been known in invertebrates, but it is still poorly understood and has never been reviewed. A striking example of matrotrophy (namely, placentotrophy) is provided by the Bryozoa, a medium-sized phylum of the aquatic colonial filter feeders. Here I report on an extensive anatomical study of placental analogues in 21 species of the bryozoan order Cheilostomata, offering the first review on matrotrophy among aquatic invertebrates. The first anatomical description of incipient p ...[more]

PMID: 23617914

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Project description:Molecular techniques are currently the leading tools for reconstructing phylogenetic relationships, but our understanding of ancestral, plesiomorphic and apomorphic characters requires the study of the morphology of extant forms for testing these phylogenies and for reconstructing character evolution. This review highlights the potential of soft body morphology for inferring the evolution and phylogeny of the lophotrochozoan phylum Bryozoa. This colonial taxon comprises aquatic coelomate filter-feeders that dominate many benthic communities, both marine and freshwater. Despite having a similar bauplan, bryozoans are morphologically highly diverse and are represented by three major taxa: Phylactolaemata, Stenolaemata and Gymnolaemata. Recent molecular studies resulted in a comprehensive phylogenetic tree with the Phylactolaemata sister to the remaining two taxa, and Stenolaemata (Cyclostomata) sister to Gymnolaemata. We plotted data of soft tissue morphology onto this phylogeny in order to gain further insights into the origin of morphological novelties and character evolution in the phylum. All three larger clades have morphological apomorphies assignable to the latest molecular phylogeny. Stenolaemata (Cyclostomata) and Gymnolaemata were united as monophyletic Myolaemata because of the apomorphic myoepithelial and triradiate pharynx. One of the main evolutionary changes in bryozoans is a change from a body wall with two well-developed muscular layers and numerous retractor muscles in Phylactolaemata to a body wall with few specialized muscles and few retractors in the remaining bryozoans. Such a shift probably pre-dated a body wall calcification that evolved independently at least twice in Bryozoa and resulted in the evolution of various hydrostatic mechanisms for polypide protrusion. In Cyclostomata, body wall calcification was accompanied by a unique detachment of the peritoneum from the epidermis to form the hydrostatic membraneous sac. The digestive tract of the Myolaemata differs from the phylactolaemate condition by a distinct ciliated pylorus not present in phylactolaemates. All bryozoans have a mesodermal funiculus, which is duplicated in Gymnolaemata. A colonial system of integration (CSI) of additional, sometimes branching, funicular cords connecting neighbouring zooids via pores with pore-cell complexes evolved at least twice in Gymnolaemata. The nervous system in all bryozoans is subepithelial and concentrated at the lophophoral base and the tentacles. Tentacular nerves emerge intertentacularly in Phylactolaemata whereas they partially emanate directly from the cerebral ganglion or the circum-oral nerve ring in myolaemates. Overall, morphological evidence shows that ancestral forms were small, colonial coelomates with a muscular body wall and a U-shaped gut with ciliary tentacle crown, and were capable of asexual budding. Coloniality resulted in many novelties including the origin of zooidal polymorphism, an apomorphic landmark trait of the Myolaemata.

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Dataset Information

From incipient to substantial: evolution of placentotrophy in a phylum of aquatic colonial invertebrates.

Publications

From incipient to substantial: evolution of placentotrophy in a phylum of aquatic colonial invertebrates.

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