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Cnidaria: Staurozoa) Systematics of stalked jellyfishes (Cnidaria: Staurozoa) Lucı´lia S. Miranda1,*, Yayoi M. Hirano2, Claudia E. Mills3, Audrey Falconer4,5, David Fenwick6, Antonio C. Marques1,7 and Allen G. Collins8,* 1 Departamento de Zoologia, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo, Sa˜o Paulo, Brazil 2 Coastal Branch of Natural History Museum and Institute, Chiba, Katsuura, Chiba, Japan 3 Friday Harbor Laboratories and the Department of Biology, University of Washington, Friday Harbor, Washington, United States of America 4 Marine Research Group of the Field Naturalists Club of Victoria, Melbourne, Victoria, Australia 5 Sciences Department, Museum Victoria, Melbourne, Victoria, Australia 6 Penzance, Cornwall, England, United Kingdom 7 Centro de Biologia Marinha, Universidade de Sa˜o Paulo, Sa˜o Sebastia˜o, Sa˜o Paulo, Brazil 8 National Systematics Laboratory, National Marine Fisheries Service (NMFS), National Museum of Natural History, Smithsonian Institution, Washington, D.C., United States of America * These authors contributed equally to this work. ABSTRACT Staurozoan classification is highly subjective, based on phylogeny-free inferences, and suborders, families, and genera are commonly defined by homoplasies. Additionally, many characters used in the taxonomy of the group have ontogenetic and intraspecific variation, and demand new and consistent assessments to establish their correct homologies. Consequently, Staurozoa is in need of a thorough systematic revision. The aim of this study is to propose a comprehensive phylogenetic hypothesis for Staurozoa, providing the first phylogenetic classification for the group. According to our working hypothesis based on a combined set of molecular data (mitochondrial markers COI and 16S, and nuclear markers ITS, 18S, and 28S), the traditional suborders Cleistocarpida (animals with claustrum) and Eleutherocarpida (animals without claustrum) are not Submitted 9 November 2015 Accepted 29 March 2016 monophyletic. Instead, our results show that staurozoans are divided into two Published 5May2016 groups, herein named Amyostaurida and Myostaurida, which can be distinguished Corresponding author by the absence/presence of interradial longitudinal muscles in the peduncle, Lucı´lia S. Miranda, respectively. We propose a taxonomic revision at the family and genus levels that [email protected] preserves the monophyly of taxa. We provide a key for staurozoan genera and Academic editor discuss the evolution of the main characters used in staurozoan taxonomy. Tim Collins Additional Information and Declarations can be found on Subjects Biodiversity, Marine Biology, Molecular Biology, Taxonomy, Zoology page 41 Keywords Evolution, Taxonomy, Phylogeny, Medusozoa, Stauromedusae DOI 10.7717/peerj.1951 INTRODUCTION Copyright 2016 Miranda et al. Staurozoa is a class of benthic cnidarians, the so-called stalked jellyfishes (Figs. 1 and 2), Distributed under represented by approximately 50 species (Clark, 1863; Kramp, 1961; Daly et al., 2007). Creative Commons CC-BY 4.0 However, from the first stauromedusan species described (Lucernaria quadricornis Mu¨ller, 1776) until their proposition as the fifth class of Cnidaria (Marques & Collins, 2004), How to cite this article Miranda et al. (2016), Systematics of stalked jellyfishes (Cnidaria: Staurozoa). PeerJ 4:e1951; DOI 10.7717/ peerj.1951 Figure 1 Diversity of stalked jellyfishes. Calvadosia cruxmelitensis: (A) lateral view, (B) oral view (photo credit: David Fenwick); Calvadosia campanulata: (C) lateral view, (D) oral view (photo credit: David Fenwick); Calvadosia nagatensis: (E) oral view (photo credit: Yayoi Hirano); Craterolophus con- volvulus: (F, G) lateral view (photo credit: David Fenwick); Depastromorpha africana: (H) lateral view (photo credit: Yayoi Hirano); Haliclystus tenuis: (I) lateral view (photo credit: Yayoi Hirano); Haliclystus borealis: (J) lateral view (photo credit: Yayoi Hirano); Haliclystus octoradiatus: (K) oral view (photo credit: David Fenwick); Haliclystus inabai: (L) lateral view (photo credit: Yayoi Hirano); Kyopoda lamberti: (M) lateral view (photo credit: courtesy of Ronald Shimek); Lipkea sp. Japan: (N) oral view (photo credit: Yayoi Hirano); Stylocoronella riedli: (O) lateral view (proto credit: courtesy of Mat Vestjens and Anne Frijsinger); Lucernaria janetae: (P) lateral and oral views (photo credit: courtesy of Richard Lutz); Manania uchidai: (Q) lateral view (photo credit: Yayoi Hirano); Manania gwilliami: (R) oral view (photo credit: courtesy of Ronald Shimek); Manania handi: (S) lateral view (photo credit: Claudia Mills). Miranda et al. (2016), PeerJ, DOI 10.7717/peerj.1951 2/48 Figure 2 General external anatomy of stalked jellyfishes. Craterolophus convolvulus: (A) lateral view, (B) oral view. Abbreviations: am, arm; cl, calyx; gd, gonad; mn, manubrium; pd, pedal disk; pe, peduncle; tc, tentacle cluster. Photo credit: David Fenwick. Miranda et al. (2016), PeerJ, DOI 10.7717/peerj.1951 3/48 the group has had a long history of classifications, being labeled as a “puzzling group” (Gwilliam, 1956). While one species was erroneously first placed among sea cucumbers (Manania auricula as Holothuria lagenam referens Mu¨ller, 1776), most assessments prior to the 1850’s assumed that they were closely related to sea anemones (Cuvier, 1817; Cuvier, 1830) until Sars (1846) noted that the presence of gastric cirri suggested that they were allied with the jellyfishes. Reflecting this thinking, Goette (1887) included Stauromedusae as a suborder within Scyphozoa, a position that was only recently challenged. Marques & Collins (2004) proposed the class based on a phylogenetic analysis of morphological and life cycle traits, as the clade uniting the fossil group Conulatae and the Stauromedusae. In light of further evidence from the fossil record, a subsequent analysis of a similar dataset contradicted the hypothesis that Conulatae and Stauromedusae form a clade, and proposed the composition of Staurozoa to consist exclusively of the extant Stauromedusae (Van Iten et al., 2006). The same analysis suggested that Staurozoa is the sister group to all other medusozoans (Cubozoa, Hydrozoa, and Scyphozoa), a result corroborated by analyses of nuclear ribosomal data (Collins et al., 2006; see also Van Iten et al., 2014). In contrast, however, analyses of complete mitochondrial genome data (Kayal et al., 2013) suggest that Staurozoa may be the sister group of Cubozoa, and more recent phylogenomic analyses support a clade formed by Staurozoa, Cubozoa, and Scyphozoa (Zapata et al., 2015), demonstrating that more studies are necessary to reach a stable topology for Cnidaria. Although evolutionary studies have supported monophyly of the class (Collins & Daly, 2005; Collins et al., 2006; Kayal et al., 2013), comparatively little effort has been applied toward determining the systematic relationships among species of Staurozoa, with rare exceptions (Collins & Daly, 2005; Lutz et al., 2006). The current classification of Staurozoa is mainly based on the proposals of Clark (1863), Haeckel (1879), Uchida (1929) and Carlgren (1935), and is completely focused on anatomical features. Uchida (1973) proposed a hypothesis of relationship among families of stalked jellyfishes based on the characters that he regarded as important, but this analysis was not derived from specific evolutionary methods. A recent molecular inference, with limited taxon sampling, demonstrated the need for reassessing suprageneric clades, because several were found not to be monophyletic (Collins & Daly, 2005). Additionally, many characters used in the taxonomy of the group have ontogenetic and intraspecific variation, and demand consistent assessments and clarifications to establish their correct homologies (Miranda, Morandini & Marques, 2009). Consequently, staurozoan classification and taxonomy is subjective, based on phylogeny-free inferences, and families and genera may be commonly defined by homoplasies (Collins & Daly, 2005). Therefore, Staurozoa is in need of a thorough systematic revision. Inferences about the relationships among staurozoan species are especially important because of the phylogenetic status and position of Staurozoa, as a distinct clade separate from the other major cnidarian groups (Anthozoa, Cubozoa, Hydrozoa, and Scyphozoa) (Collins et al., 2006; Van Iten et al., 2006; Kayal et al., 2013; Zapata et al., 2015). The peculiar life cycle of staurozoans (Wietrzykowski, 1912; Kikinger & Salvini-Plawen, 1995; Miranda, Collins & Marques, 2010) is tightly connected to their Miranda et al. (2016), PeerJ, DOI 10.7717/peerj.1951 4/48 unique anatomy, in which characters of polypoid and medusoid stages are present in the same stauromedusa (Miranda, Collins & Marques, 2013). Our expectation is that a better understanding and interpretation of the character evolution within the group will provide crucial information for inferences in cnidarian evolution. Therefore, it is of the utmost importance to carry out an evolutionary analysis encompassing a large number of species of Staurozoa. This study presents the most comprehensive phylogenetic hypothesis for Staurozoa yet proposed and provides the first phylogenetic classification for the group. Further, we provide a key for staurozoan genera and discuss evolution of the main characters used in staurozoan taxonomy. MATERIAL AND METHODS Molecular Twenty-four species from ten genera, plus eight non-identified species (identified to genus level), from different regions of the world, were used in the molecular analyses (Table 1). Tissue samples
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