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The Biology of Glass Sponges

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The Biology of Glass Sponges The Biology of Glass Sponges S. P. Leys* G., O. Mackie{ and H. M. Reiswig{ ,{ *Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada {Department of Biology, University of Victoria, Victoria V8W 3N5, Canada {Natural History Section, Royal British Columbia Museum, Victoria V8W 9W2, Canada 1. Introduction . 3 2. General Organisation . 5 2.1. Gross morphology. 5 2.2. Structure of the body wall. 5 3. Cells and Syncytia . 9 3.1. Definitions. 9 3.2. Plugged junctions . 10 3.3. Hexactinellid plugs compared with other junctions . 13 3.4. Trabecular syncytium. 15 3.5. Sclerocytes and sclerosyncytium. 17 3.6. Archaeocytes. 18 3.7. Cells with inclusions. 18 3.8. Choanocytes . 20 3.9. Mesohyl. 24 4. Tissue Dynamics . 24 4.1. Reaggregation of dissociated sponge tissue. 24 4.2. Fusion. 27 4.3. Cytoskeleton . 29 4.4. Organelle transport. 33 4.5. Comparison with cellular sponges. 37 4.6. Immune response. 38 5. Physiology. 39 5.1. Hexactinellids as experimental animals. 39 ADVANCES IN MARINE BIOLOGY VOL 52 0065-2881/07 $35.00 # 2007 Elsevier Ltd. All rights reserved DOI: 10.1016/S0065-2881(06)52001-2 2 S. P. LEYS ET AL. 5.2. Food and wastes . 40 5.3. Production and control of feeding currents . 50 6. The Siliceous Skeleton . 59 6.1. Discrete spicules . 59 6.2. Megascleres and microscleres . 60 6.3. Spicule locations . 66 6.4. Fused silica networks . 68 6.5. Silication . 76 7. Ecology. 85 7.1. Habitats: distribution and abundance . 85 7.2. Succession: glass sponge skeletons as substrates . 87 7.3. Reefs or bioherms . 90 7.4. Growth rates and seasonal regression . 94 7.5. Predation, mortality and regeneration . 96 7.6. Recruitment . 99 7.7. Symbioses: animal–plant associations. 101 8. Reproduction . 104 8.1. Sexual reproduction . 104 8.2. Asexual reproduction . 116 9. Classification and Phylogeny. 116 9.1. Classification of recent Hexactinellida . 116 9.2. Classification of fossil Hexactinellida . 119 9.3. Phylogeny of Hexactinellida within Porifera. 125 9.4. Phylogeny within Hexactinellida . 128 10. Conclusions . 131 Acknowledgements . 132 References . 132 As the most ancient extant metazoans, glass sponges (Hexactinellida) have attracted recent attention in the areas of molecular evolution and the evolution of conduction systems but they are also interesting because of their unique histolo- gy: the greater part of their soft tissue consists of a single, multinucleate syncytium that ramifies throughout the sponge. This trabecular syncytium serves both for transport and as a pathway for propagation of action potentials that trigger flagellar arrests in the flagellated chambers. The present chapter is the first comprehensive modern account of this group and covers work going back to the earliest work dealing with taxonomy, gross morphology and histology as well as dealing with more recent studies. The structure of cellular and syncytial tissues and the formation of specialised intercellular junctions are described. Experimental work on reaggregation of dissociated tissues is also covered, a process during which histocompatibility, fusion and syncytialisation have been investigated, and where the role of the cytoskeleton in tissue architecture and transport processes has been studied in depth. The siliceous skeleton is given special attention, with an account of discrete spicules and fused silica networks, their diversity and distribution, their importance as taxonomic features and the process of silication. Studies on particle capture, transport of internalised food THE BIOLOGY OF GLASS SPONGES 3 objects and disposal of indigestible wastes are reviewed, along with production and control of the feeding current. The electrophysiology of the conduction system coordinating flagellar arrests is described. The review covers salient features of hexactinellid ecology, including an account of habitats, distribution, abundance, growth, seasonal regression, predation, mortality, regeneration, recruitment and symbiotic associations with other organisms. Work on the recently discovered hexactinellid reefs of Canada’s western continental shelf, analogues of long-extinct Jurassic sponge reefs, is given special attention. Reproductive biology is another area that has benefited from recent investiga- tions. Seasonality, gametogenesis, embryogenesis, diVerentiation and larval biology are now understood in broad outline, at least for some species. The process whereby the cellular early larva becomes syncytial is described. A final section deals with the classification of recent and fossil glass sponges, phyloge- netic relationships within the Hexactinellida and the phylogenetic position of the group within the Porifera. Palaeontological aspects are covered in so far as they are relevant to these topics. 1. INTRODUCTION Glass sponges, Hexactinellida, are emerging as an important group of ani- mals which, because of their ancient heritage, can shed light on fundamental questions such as the origin of multicellular animals, molecular evolution, and the evolution of conduction systems. Glass sponges are unusual animals with a skeleton of silicon dioxide whose triaxonal (cubic), six-rayed symme- try and square axial proteinaceous filament distinguishes them from other siliceous sponges. The fossil record suggests glass sponges were established by the Late Proterozoic, thrived during the middle Cambrian, diversified during the Jurassic when they formed vast reefs in the Tethys Sea and reached their maximum radiation and diversity during the Late Cretaceous. Estimated rates of molecular evolution place their origin even earlier at 800 million years ago (Ma). However, it is their soft tissues that are really remarkable. They are interestingly diVerent from all other animals (including other sponges) in having syncytial tissues that arise by fusion of early embryonic cells. The larva and adult have an elegant combination of multinucleate and cellular cytoplasmic regions unknown in any other animal. The continuity of this tissue not only allows food to be transported around the animal symplas- tically.
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