Review of the Highly Versatile Cassiopea Xamachana System
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REVIEW published: 09 April 2018 doi: 10.3389/fevo.2018.00035 Upside-Down but Headed in the Right Direction: Review of the Highly Versatile Cassiopea xamachana Edited by: System Sandie M. Degnan, The University of Queensland, Aki H. Ohdera 1*, Michael J. Abrams 2, Cheryl L. Ames 3, David M. Baker 4, Australia Luis P. Suescún-Bolívar 5, Allen G. Collins 3,6, Christopher J. Freeman 7, Reviewed by: Edgar Gamero-Mora 8, Tamar L. Goulet 9, Dietrich K. Hofmann 10, Adrian Jaimes-Becerra 8, Adam Michael Reitzel, Paul F. Long 11, Antonio C. Marques 8,12, Laura A. Miller 13, Laura D. Mydlarz 14, University of North Carolina at Andre C. Morandini 8,12, Casandra R. Newkirk 15, Sastia P. Putri 16, Julia E. Samson 13, Charlotte, United States Sérgio N. Stampar 17, Bailey Steinworth 15, Michelle Templeman 18, Patricia E. Thomé 5, Lucas Leclere, Marli Vlok 19, Cheryl M. Woodley 20, Jane C.Y. Wong 4, Mark Q. Martindale 15, UMR7009 Laboratoire de Biologie du 21 1,22 Développement de Villefranche sur William K. Fitt and Mónica Medina * Mer, France 1 Department of Biology, Pennsylvania State University, University Park, PA, United States, 2 Division of Biology and Biological *Correspondence: Engineering, California Institute of Technology, Pasadena, CA, United States, 3 Department of Invertebrate Zoology, National Aki H. Ohdera Museum of Natural History, Smithsonian Institution, Washington, DC, United States, 4 School of Biological Sciences, The [email protected] Swire Institute of Marine Science, The University of Hong Kong, Pokfulam, Hong Kong, 5 Unidad Académica de Sistemas Mónica Medina Arrecifales Puerto Morelos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mexico [email protected] City, Mexico, 6 National Systematics Laboratory of NOAA’s Fisheries Service, National Museum of Natural History, Smithsonian Institution, Washington, DC, United States, 7 Smithsonian Marine Station, Fort Piece, FL, United States, Specialty section: 8 Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil, 9 Department of Biology, 10 This article was submitted to University of Mississippi, Oxford, MS, United States, Department of Zoology & Neurobiology, Ruhr-University Bochum, 11 Coevolution, Bochum, Germany, School of Cancer and Pharmaceutical Sciences, King’s College London, London, United Kingdom, 12 13 a section of the journal Centro de Biologia Marinha, Universidade de São Paulo, São Sebastião, Brazil, Biology Department, University of North 14 Frontiers in Ecology and Evolution Carolina at Chapel Hill, Chapel Hill, NC, United States, Department of Biology, University of Texas at Arlington, Arlington, TX, United States, 15 Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL, United States, Received: 29 January 2018 16 Department of Biotechnology, Graduate School of Engineering, Osaka University, Osaka, Japan, 17 Departamento de Accepted: 20 March 2018 Ciências Biológicas, Faculdade de Ciências e Letras de Assis, Unesp Universidade Estadual Paulista, Assis, Brazil, Published: 09 April 2018 18 TropWATER and College of Marine & Environmental Sciences, James Cook University, Townsville, QLD, Australia, Citation: 19 Department of Botany, University of British Columbia Vancouver, Vancouver, BC, Canada, 20 U.S. National Oceanic & Ohdera AH, Abrams MJ, Ames CL, Atmospheric Administration, National Ocean Service, National Centers for Coastal Ocean Science, Charleston, SC, Baker DM, Suescún-Bolívar LP, United States, 21 Odum School of Ecology, University of Georgia, Athens, GA, United States, 22 Smithsonian Tropical Collins AG, Freeman CJ, Research Institute, Smithsonian Institution, Washington, DC, United States Gamero-Mora E, Goulet TL, Hofmann DK, Jaimes-Becerra A, Long PF, Marques AC, Miller LA, The upside-down jellyfish Cassiopea xamachana (Scyphozoa: Rhizostomeae) has been Mydlarz LD, Morandini AC, predominantly studied to understand its interaction with the endosymbiotic dinoflagellate Newkirk CR, Putri SP, Samson JE, Stampar SN, Steinworth B, algae Symbiodinium. As an easily culturable and tractable cnidarian model, it is Templeman M, Thomé PE, Vlok M, an attractive alternative to stony corals to understanding the mechanisms driving Woodley CM, Wong JC, establishment and maintenance of symbiosis. Cassiopea is also unique in requiring the Martindale MQ, Fitt WK and Medina M (2018) Upside-Down but Headed in symbiont in order to complete its transition to the adult stage, thereby providing an the Right Direction: Review of the excellent model to understand symbiosis-driven development and evolution. Recently, Highly Versatile Cassiopea xamachana System. Front. Ecol. Evol. 6:35. the Cassiopea research system has gained interest beyond symbiosis in fields related to doi: 10.3389/fevo.2018.00035 embryology, climate ecology, behavior, and more. With these developments, resources Frontiers in Ecology and Evolution | www.frontiersin.org 1 April 2018 | Volume 6 | Article 35 Ohdera et al. Cassiopea xamachana System Review including genomes, transcriptomes, and laboratory protocols are steadily increasing. This review provides an overview of the broad range of interdisciplinary research that has utilized the Cassiopea model and highlights the advantages of using the model for future research. Keywords: jellyfish, symbiosis, toxinology, sleep, venom, scyphozoan systematics, bioindicator INTRODUCTION Medusa andromeda (published as a post mortem work; figures published only in Forskål (1776). The generic name Cassiopea The upside-down jellyfish Cassiopea is a benthic scyphozoan was proposed for all jellyfish with foliaceous appendages in 1810 (Rhizostomeae) commonly found in tropical and sub-tropical (Péron and Lesueur, 1810). Members of the genus Cassiopea shallow coastal ecosystems, such as mangroves and seagrass beds. were treated as a family by Tilesius (1831), and the current Cassiopea spp. are unique among scyphomedusae in that their spelling appeared ∼30 years later (Agassiz, 1862). The species- characteristic flat exumbrella rests on the sea bottom, while their level relationships of the genus Cassiopea are still unresolved convex subumbrella and oral arms face upwards. High light since most of the taxonomic studies are based on overlapping, penetrance is important for species within this genus, as the plastic, and polymorphic features (Table 1; Mayer, 1910; Kramp, jellyfish hosts one or more photosynthetic dinoflagellate species 1961). This is confounded by vague species descriptions with of the genus Symbiodinium (Hofmann et al., 1996; Lampert, species diagnoses that are descriptive rather than comparative, 2016). Similar to their coral relatives, nutrient exchange is a key although morphology has been useful in distinguishing some component supporting this cnidarian-dinoflagellate mutualism congeneric species, i.e., Cassiopea frondosa. In total, 24 nominal (Hofmann and Kremer, 1981; Welsh et al., 2009; Freeman et al., species, and varieties thereof, have been proposed to date 2016). In addition, Cassiopea spp. rely on the symbionts as a (Table 1), but only 10 species are presently considered to be developmental trigger (Hofmann et al., 1978; Colley and Trench, valid based on molecular data (Holland et al., 2004; Arai 1985). A fascination with these requisite traits of the upside- et al., 2017; Morandini et al., 2017). These studies show that down jellyfish has fueled studies on the Cassiopea-Symbiodinium populations of C. xamachana are potential introduction of interaction since the 1980s (see recent review by Lampert, 2016). Cassiopea andromeda from the Red Sea, thereby grouping While its efficacy as a system for symbiosis research is well the species into a single lineage. These species designations, known in the literature, Cassiopea is gaining momentum as a which are based on kimura 2-parameter pairwise distance, fall model species in other areas. In mathematics, the symmetric within previous estimations for other scyphozoans, ranging from morphology and relatively simple neuromuscular system of 0.00 to 0.034 for conspecifics, and 0.102–0.234 for congenerics the upside-down jellyfish make it an ideal system from which (Holland et al., 2004; Ortman et al., 2010; Gómez Daglio to develop computational fluid dynamic and neuromechanical and Dawson, 2017). Analyses with expanded taxon sampling models (Passano, 2004; Hamlet et al., 2011; Santhanakrishnan (Bayha et al., 2010; Kayal et al., 2013, 2017) have placed the et al., 2012). Additionally, Cassiopea has been presented as a monogeneric Cassiopea within the family Cassiopeidae, in an possible model organism for the study of behavioral biology unstable position within the clade Kolpophorae, along with as highlighted by recent developments with sleep behavior representatives of Mastigiidae, Thysanostomatidae, Versurigidae, (Nath et al., 2017; Figure 1). Likewise, this jellyfish genus has and Cepheidae (Figure 2). The Kolpophorae belongs to the order been gaining traction as a biomonitor/bioindicator species, with Rhizostomeae, a well-supported clade derived from within the applications for coastal ecosystem management (Templeman scyphozoan order Semaeostomeae (Bayha et al., 2010; Kayal et al., and Kingsford, 2012; Epstein et al., 2016; Klein et al., 2016a, 2013). 2017). The relative simplicity of culturing Cassiopea polyps While the polyp stage and strobilation of C. xamachana, and medusae makes this genus a highly amenable laboratory as well as the polyp stage of C. frondosa, were described by system. With newly established