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. 2016 May 5:4:e1951.
doi: 10.7717/peerj.1951. eCollection 2016.

Systematics of stalked jellyfishes (Cnidaria: Staurozoa)

Lucília S Miranda #  1 , Yayoi M Hirano  2 , Claudia E Mills  3 , Audrey Falconer  4   5 , David Fenwick  6 , Antonio C Marques  1   7 , Allen G Collins #  8
Affiliations

Systematics of stalked jellyfishes (Cnidaria: Staurozoa)

Lucília S Miranda et al. PeerJ. .

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 monophyletic. Instead, our results show that staurozoans are divided into two groups, herein named Amyostaurida and Myostaurida, which can be distinguished by the absence/presence of interradial longitudinal muscles in the peduncle, respectively. We propose a taxonomic revision at the family and genus levels that preserves the monophyly of taxa. We provide a key for staurozoan genera and discuss the evolution of the main characters used in staurozoan taxonomy.

Keywords: Evolution; Medusozoa; Phylogeny; Stauromedusae; Taxonomy.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
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 convolvulus: (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).
Figure 2
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.
Figure 3
Figure 3. Parsimony phylogenetic hypothesis.
Analysis based on combined data of mitochondrial markers COI and 16S, and nuclear markers ITS, 18S (SSU), and 28S (LSU). Single most parsimonious tree, length: 1682.18 steps. Bootstrap indices under parsimony at each node. ANT, Antarctica; AUS, Australia; EPR, East Pacific Rise; GER, Germany; JAP, Japan; NZ, New Zealand; SAF, South Africa; UK, the United Kingdom; USA, the United States of America.
Figure 4
Figure 4. Maximum likelihood phylogenetic hypothesis.
Analysis based on combined data of mitochondrial markers COI and 16S, and nuclear markers ITS, 18S (SSU), and 28S (LSU). Bootstrap indices under maximum likelihood at each node. ANT, Antarctica; AUS, Australia; EPR, East Pacific Rise; GER, Germany; JAP, Japan; NZ, New Zealand; SAF, South Africa; UK, the United Kingdom; USA, the United States of America.
Figure 5
Figure 5. Bayesian phylogenetic hypothesis.
Analysis based on combined data of mitochondrial markers COI and 16S, and nuclear markers ITS, 18S (SSU), and 28S (LSU). Posterior probability at each node. ANT, Antarctica; AUS, Australia; EPR, East Pacific Rise; GER, Germany; JAP, Japan; NZ, New Zealand; SAF, South Africa; UK, the United Kingdom; USA, the United States of America.
Figure 6
Figure 6. Support of each individual molecular marker for the main groups observed in the combined analyses.
White squares represent non monophyletic groups, and gray squares represent monophyletic groups. First row: individual molecular markers under parsimony analyses; second row: individual molecular markers under maximum likelihood analyses; third row: individual molecular markers under Bayesian analyses. PA, parsimony; ML, maximum likelihood; BA, Bayesian. “?” indicates groups whose monophyly could not be corroborate for a particular molecular marker (only one species).
Figure 7
Figure 7. New proposal of classification based on molecular phylogenetic analyses.
“?” indicates groups not included in the analysis, classified according to morphological evidence. EPR, East Pacific Rise; UK, the United Kingdom; USA, the United States of America.
Figure 8
Figure 8. Historical proposals of classifications for Staurozoa.
Classification proposed in this study (F), based on molecular phylogenetic analysis and on additional morphological evidence. In red, new names proposed by the author of respective classification.
Figure 9
Figure 9. Claustrum connecting adjacent septa.
Craterolophus convolvulus: (A) beginning of claustrum delimitation (indicated by black arrow) between adjacent septa (sp) in peduncle; (B) claustrum (cs) completely delimited at base of calyx, enclosing accessory radial pockets (ar); Manania uchidai: (C) claustrum (cs) completely delimited at base of calyx, enclosing accessory radial pockets (ar); (D) claustrum (cs) between accessory radial pockets (ar) and principal radial pockets (pr) (associated with gonads) in calyx, and a central manubrium (mn); Calvadosia sp. 2 NZ: (E) absence of claustrum connecting adjacent septa (sp) in peduncle; (F) absence of claustrum at the base of calyx between adjacent septa (sp); (G) gastric radial pocket (gp) associated with gonads (gd). Cross-sections. Photo credit: Lucília Miranda.
Figure 10
Figure 10. Interradial longitudinal muscles in peduncle.
Manania uchidai: (A) presence of interradial longitudinal muscles (mu); Calvadosia cruciformis: (B) absence of interradial longitudinal muscles (indicated by arrow). Cross-sections. Photo credit: Lucília Miranda.
Figure 11
Figure 11. Hypothesis of character evolution for staurozoan genera.
ACCTRAN optimization of selected morphological and life-history features according to our molecular phylogenetic analyses. Synapomorphies and symplesiomorphies are based on Collins & Daly (2005). The presence of claustrum as a potential symplesiomorphy of Staurozoa (Collins & Daly, 2005) is equivocal, and the state in outgroups needs careful reconsideration based on detailed histological studies. If considered a symplesiomorphy of Staurozoa, claustrum was lost in Calvadosia, Haliclystus, and in the clade Lucernaria + Lipkea (most parsimonious reconstruction). Anchors are adhesive structures resulting from metamorphosis of eight primary tentacles (perradial and interradial). Coronal muscle divided into eight sections by the adradial arms or entire. The species with 4/1-chambered peduncle have four chambers basally and one chamber in the middle of the peduncle.
Figure 12
Figure 12. Coronal muscle.
Craterolophus convolvulus: (A) divided coronal muscle (cm); Lipkea sp. Japan: (B) entire coronal muscle (cm); Manania uchidai: (C) external (exumbrellar) coronal muscle (cm) in relation to anchor (an); Depastromorpha africana: (D) internal (subumbrellar) coronal muscle in relation to anchor (an). Photo credit: Lucília Miranda.
Figure 13
Figure 13. Primary tentacles and anchors.
Craterolophus convolvulus: (A) absence of primary tentacles and anchors (indicated by black arrow) between arms; Calvadosia cruciformis: (B) presence of primary tentacles (pt); Manania uchidai: (C) anchors (an) with a knobbed remnant of primary tentacles; Depastromorpha africana: (D) anchors (an) with a knobbed remnant of primary tentacles; Haliclystus tenuis: (E) anchors (an). Photo credit: Lucília Miranda.
Figure 14
Figure 14. Chambers in the peduncle.
Haliclystus tenuis: (A) four perradial chambers (pc) in peduncle; Calvadosia corbini: (B) one central gastric chamber (indicated by arrow) in the middle region of peduncle. Cross-sections. Photo credit: Lucília Miranda.
Figure 15
Figure 15. Pad-like adhesive structures.
Calvadosia tasmaniensis: (A–B) pad (pa) on the tip of an arm separate from the secondary tentacles (tc); Calvadosia cruxmelitensis: (C) pad (pa) on the tip of an arm, with secondary tentacles (tc) arising directly from it; Craterolophus convolvulus: (D) pads (pa) in the outermost secondary tentacles (tc); Calvadosia vanhoeffeni: (E) pads (pa) in the outermost secondary tentacles (tc); Calvadosia campanulata: (F) pads (pa) in the outermost secondary tentacles (tc). Photo credit: Lucília Miranda.
Figure 16
Figure 16. Evolution of pad-like adhesive structures in Kishinouyeidae.
Most parsimonious reconstruction of pad-like adhesive structures in Kishinouyeidae according to our molecular phylogenetic hypothesis.
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Grants and funding

This study was supported by FAPESP 2010/07362-7 (LSM), 2010/52324-6 (ACM), 2011/50242-5 (ACM), 2013/50484-4 (ACM); CNPq 474672/2007-7 (ACM), 142270/2010-5 (LSM), 563106/2010-7 (ACM), 562143/2010-6 (ACM), 477156/2011-8 (ACM), 305805/2013-4 (ACM), 165066/2014-8 (LSM), 445444/2014-2 (ACM); CAPES/PDSE: 16499/12-3 (LSM); and NSF Grant AToL EF-0531779 (to P. Cartwright, AGC, and D. Fautin). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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