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(Cnidaria) Exoskeleton Zoological Journal of the Linnean Society, 2016, 178, 206–225. With 4 figures An evolutionary comparative analysis of the medusozoan Downloaded from https://academic.oup.com/zoolinnean/article-abstract/178/2/206/2674323 by Universidade de São Paulo - IO user on 15 October 2018 (Cnidaria) exoskeleton MARIA A. MENDOZA-BECERRIL1*, MAXIMILIANO M. MARONNA1,MIRIAN L. A. F. PACHECO2, MARCELLO G. SIMOES~ 3, JULIANA M. LEME4, LUCILIA S. MIRANDA1, ANDRE C. MORANDINI1 and ANTONIO C. MARQUES1,5 1Department of Zoology, Institute of Biosciences, University of Sao~ Paulo, Rua do Matao,~ Trav. 14, 101, 05508-090 Sao~ Paulo, Brazil 2Department of Biology, Federal University of Sao Carlos, Rodovia Joao~ Leme dos Santos - atekm 104.000 Parque Reserva Fazenda Imperial, 18052780 Sorocaba, Sao~ Paulo, Brazil 3Department of Zoology, Laboratory of Paleozoology, Sao~ Paulo State University Botucatu, Jardim Santo Inacio (Rubiao~ Junior), 18618970 Botucatu, Sao~ Paulo, Brazil 4Department of Sedimentary and Environmental Geology, Institute of Geosciences, University of Sao~ Paulo, Rua do Lago, 562, 05508-080 Sao~ Paulo, Brazil 5Center for Marine Biology, University of Sao~ Paulo, Rodovia Manoel H. Do Rego km 131.5, CEP 11600-000 Sao~ Sebastiao,~ Sao~ Paulo, Brazil Received 16 June 2015; revised 3 January 2016; accepted for publication 7 February 2016 The benthic polyp phase of Medusozoa (Staurozoa, Cubozoa, Scyphozoa, and Hydrozoa) has endoskeletal or exoskeletal support systems, but their composition, development, and evolution is poorly known. In this contribution the variation in synthesis, structure, and function of the medusozoan exoskeleton was examined. In addition, an evolutionary hypothesis for its origin and diversification is proposed for both extinct and extant medusozoans. We also critically reviewed the literature and included data from our own histological and microstructural analyses of some groups. Chitin is a characteristic component of exoskeleton in Medusozoa, functioning as support, protection, and a reserve for various ions and inorganic and organic molecules, which may persuade biomineralization, resulting in rigid biomineralized exoskeletons. Skeletogenesis in Medusozoa dates back to the Ediacaran, when potentially synergetic biotic, abiotic, and physiological processes resulted in development of rigid structures that became the exoskeleton. Of the many types of exoskeletons that evolved, the corneous (chitin-protein) exoskeleton predominates today in polyps of medusozoans, with its greatest variation and complexity in the polyps of Hydroidolina. A new type of bilayered exoskeleton in which there is an exosarc complementing the perisarc construction is here described. © 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016, 178: 206–225 doi: 10.1111/zoj.12415 KEYWORDS: chitin – exoskeleton – glycosaminoglycan – Hydroidolina – Medusozoa – perisarc – phylo- genetics – Pseudohydrotheca. 2013a, 2014; Liu et al., 2014) and most groups INTRODUCTION already present in the Cambrian (Zhao & Bengtson, Cnidarians are an early branch of diploblastic ani- 1999; Hughes, Gunderson & Weedon, 2000; Cart- mals, which diverged from the shared ancestor of the wright et al., 2007). Cnidaria comprise two main Bilateria ~600 Mya (Ryan et al., 2013), with some clades: Anthozoa and Medusozoa (Ruggiero et al., fossil records in the Ediacaran (Van Iten et al., 2015). Anthozoa are typically benthic and marine polyps, whereas Medusozoa have a greater diversity of forms and habits, including pelagic, free-swimming *Corresponding author. E-mail: [email protected] (usually medusae), benthic and sessile (usually 206 © 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016, 178, 206–225 EXOSKELETON OF THE MEDUSOZOANS 207 polyps), all mostly marine, but with a few freshwater THE METAZOAN EXOSKELETON – species. Medusozoa encompasses the classes Stauro- SYNTHESIS zoa, Cubozoa, Scyphozoa, and Hydrozoa, whose phylogenetic relationships have been explored using Macromolecule evolution has resulted in the develop- morphology, life cycles, and nuclear and mitochondrial ment of extracellular structures with many Downloaded from https://academic.oup.com/zoolinnean/article-abstract/178/2/206/2674323 by Universidade de São Paulo - IO user on 15 October 2018 molecular markers (Marques & Collins, 2004; Collins functions, such as support, osmoregulation, defence, et al., 2006; Van Iten et al., 2006, 2014). Recently, biofilms, cell and tissue morphogenesis, and so on some molecular phylogenetic analyses indicated that (Sentandreu, Mormeneo & Ruiz-Herrera, 1994; Ruiz- Myxozoa is a cnidarian group (Chang et al., 2015; Herrera & Ortiz-Castellanos, 2010). The most signifi- Foox & Siddall, 2015; Foox et al., 2015). cant structural macromolecules in multicellular A fundamental evolutionary feature of Cnidaria is organisms are polysaccharide carbohydrates, such as the skeleton that may be present as an endoskeleton, cellulose in plants (Richmond & Somerville, 2000) exoskeleton, or hydrostatic skeleton. This is a conse- and chitin in fungi and animals, and the protein col- quence of the bauplan of two epithelial layers. The lagen, which is important for internal support in the internal gastrodermis delimits the gastrovascular Metazoa (Ehrlich, 2010a). cavity from the tentacles to the pedal disc and func- Chitin often makes up a significant fraction of tions in the absorption of nutrients as well as con- structural support structures. For example, chitin traction. The external epidermis functions in accounts for 10–30% of the total skeletal components protection from the environment and responds to in some hydrozoans and 3–15% in bryozoans (Jeuni- external stimuli (Chapman, 1974). These two epithe- aux & Voss-Foucart, 1991; Kaya et al., 2015). Chitin lial layers are separated by mesoglea, which is an is a polymer with repeating units of N-acetyl-D-gly- extracellular matrix primarily containing collagen cosamine (Muzzarelli & Muzzarelli, 2009), usually and that may or may not contain cells (Chapman, with a visible fibrous organization at different hier- 1974; Tucker, Shibata & Blankenship, 2011). archical levels (nanofibrils, microfibrils, or fibres; The epidermis is fundamental because of the many Ehrlich et al., 2010) and in three alternative forms: cell types it contains, including epithelio-muscular, antiparallel a (the most common), parallel b, and interstitial, glandular, nervous, and cnidae cells, as alternate c (Pillai, Paul & Sharma, 2009). Biosynthe- well as determining how the animal interacts with its sis of chitin includes synthesis and degradation aquatic environment (Mackie, 1984). The skeleton of catalysed by enzymes found in all living organisms Cnidaria is a key feature that plays roles in protection, (Ruiz-Herrera, Gonzalez-Prieto & Ruiz-Medrano, ion storage, fixation to substrates, swimming, flexibil- 2002; Merzendorfer & Zimoch, 2003; Tang et al., ity, and floating/drifting/dispersal, as well as other 2015). Processes of expression and functions of chitin aspects of cnidarian life (Garstang, 1946; Pyefinch & have been most studied in fungi and arthropods (e.g. Downing, 1949; Chapman, 1968, 1974; Fields & Ruiz-Herrera & Ortiz-Castellanos, 2010; Merzendor- Mackie, 1971; Blanquet, 1972; Hundgen,€ 1984; Tid- fer, 2011; Souza et al., 2011). ball, 1984; Thomas & Edwards, 1991; Marques & Mig- Chitin synthetases (Chs) are the most important otto, 2001; Fraune et al., 2010; Di Camillo et al., enzymes that form chitin, and their genes are found 2012). in several Medusozoa [e.g. Hydractinia echinata Anthozoan skeletons are reasonably well studied (Fleming, 1828), Mali et al., 2004; Hydra vulgaris (e.g. Barnes, 1970; Fukuda et al., 2003; Ramos-Silva Pallas, 1766, GenBank database, Table 1] and are et al., 2013), whereas the exoskeletons of Medusozoa present between some other Metazoa (Porifera, are much less understood. Indeed, after studies of Anthozoa, Deuterostomia) and the Choanoflagellata composition and development, a long hiatus ensued (Zakrzewski et al., 2014). Additionally, other genes before additional study of the role of the exoskeleton involved in the biosynthesis of chitin in other groups in the biology and evolution of the group, despite its of metazoans (e.g. Arthropoda; Merzendorfer & basal position in the evolution of animals (Marques, Zimoch, 2003) are also found in Medusozoa (Table 1). Morandini & Migotto, 2003; Collins et al., 2006). The presence of these genes in different groups sug- Owing to this gap in our knowledge, our goals here gests that the basic components are conserved and were to conduct detailed analyses of medusozoan these are functional since a particular moment in skeletons, highlighting the variation in origin, struc- animal evolution. Yet, Chs genes have not been ture, and function, and how disparities in these fea- found in the genomes of nonchitinous organisms tures have accompanied the evolution and (Willmer, 1990; Wagner, 1994), e.g. Trichoplax diversification of this group. To achieve these goals, adhaerens Schulze, 1883 (Placozoa; Dellaporta et al., we have brought together published and unpublished 2006; Signorovitch, Buss & Dellaporta, 2007) and data for fossil cnidarians and modern histological Mnemiopsis leidyi A. Agassiz, 1865 (Ctenophora; information for extant groups of Medusozoa. Table 1; Ryan et al., 2013; Bolte et al., 2014). © 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016, 178, 206–225 208 M. A. MENDOZA-BECERRIL Table 1. Enzymes
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