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Phylogeny of Medusozoa and the evolution of cnidarian life cycles
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Abstract To investigate the evolution of cnidarian life cycles, data from the small subunit of the ribosome are used to derive a phylogenetic hypothesis for Medusozoa. These data indicate that Cnidaria is monophyletic and composed of Anthozoa and Medusozoa. While Cubozoa and Hydrozoa are well supported clades, Scyphozoa appears to be paraphyletic. Stauromedusae is possibly the sister group of either Cubozoa or all other medusozoans. The phylogenetic results suggest that: the polyp probably preceded the medusa in the evolution of Cnidaria; within Hydrozoa, medusa development involving the entocodon is ancestral; within Trachylina, the polyp was lost and subsequently regained in the parasitic narcomedusans; within Siphonophorae, the float originated prior to swimming bells; stauromedusans are not likely to be descended from ancestors that produced medusae by strobilation; and cubozoan polyps are simplified from those of their ancestors, which possessed polyps with gastric septa and four mesogleal muscle bands and peristomial pits.
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“The absence of precambrian planktonic metazoans is consistent with our Early Cambrian estimate for the origin of the last common ancestor of living cnidarians, a population of animals whose life cycle lacked a medusa stage and thus was entirely benthic (49).”
From Estimating metazoan divergence times with a molecular clock (2004) · cites this paper as [49]
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“Based on morphological and 18S ribosomal RNA data, the Anthozoa appear to be the most ancestral class within the phylum (Bridge et al., 1995;Collins, 2002).”
From Evolutionary aspects of developmentally regulated helix-loop-helix transcription factors in striated muscle of jellyfish (2003) · cites this paper as Collins, 2002
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InfluentialSelf-citationGenesis and Expansion of Metazoan Transcription Factor Gene Classes
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Self-citationCnidarian phylogenetic relationships as revealed by mitogenomics
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“Table 2 The use of several statistical tests verifying the validity of some groups in cnidarians AliMG AU KH SH Cnidaria 0.27 0.15 0.86 Anthozoa 0.63 0.41 0.93 Hexacorallia 0.48 0.32 0.86 Scleractinia 0.25 0.17 0.53 Acraspeda* 0.80 0.59 0.99 Rhizostomeae 0.24 0.17 0.64 Scyphozoa 0.10 0.08 0.42 Scyphozoa + Cubozoa + Hy…”
BackgroundResultInfluentialSelf-citationAncient Venom Systems: A Review on Cnidaria Toxins
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“Based upon mitochondrial DNA (mtDNA) data [15] and life cycles [8,16], cnidarians are divided into two extant subphyla: Anthozoa and Medusozoa.”
BackgroundLavrov, D. V., & Pett, W. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw195 · Cited by 234
“Within Medusozoa four major clades are recognized: Scyphozoa (jellyfishes), Staurozoa (stalked jellyfishes), Cubozoa (box jellyfishes), and Hydrozoa (hydroids, fire corals, freshwater jellyfishes, siphonophores, etc.) (Collins 2002).”
BackgroundPhylogenomic Analyses Support Traditional Relationships within Cnidaria
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Self-citationMolecular evidence for deep evolutionary roots of bilaterality in animal development
Matus, D. Q., Pang, K., Marlow, H. Q., Dunn, C. W., Thomsen, G. H., & Martindale, M. Q. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601257103 · Cited by 227
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“been confirmed by other data (Bridge et al., 1995; Collins, 2002).”
ResultRising starlet: the starlet sea anemone,Nematostella vectensis
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“Recent exceptions are the genus Dactylometra and the species Pelagia colorata, which are now both considered members of the confamilial genus Chrysaora (Gershwin & Collins, 2002).”
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“Based on comparisons of the anatomy, morphogenesis and palaeoautecology of conulariids and extant taxa, many investigators (e.g. Kiderlen 1937; Moore & Harrington 1956; Werner 1973«; Bischoff 1978; von Salvini-Plawen 1978; Bouillon 1981; Van Iten 1991a, \992a,h\ Jerre 1994; Wade 1994; Bergström 1995; McKinney et al. 1…”
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“…data were used for V. velella 18S (Collins, 2002, GenBank AF358087), P. porpita 18S (Collins, 2002, AF358086), Staurocladia wellingtoni 18S (Collins, 2002, AF358084), S. wellingtoni 16S (Schuchert, 2005, AJ580934), Hydra circumcincta 18S (Medina et al., 2001, AF358080), and H. vulgaris 16S…”
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“…Hydrozoa revealed multiple instances of loss, and sometimes regain, in prominent aspects of the hydrozoan life cycle (Cunningham and Buss 1993; Collins 2002; Collins et al. 2006; Dunn et al. 2005; Govindarajan et al. 2006; Leclère et al. 2007; Cartwright et al. 2008; Collins et al. 2008;…”
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“Initial phylogenetic analyses suggested that monodisc strobilation was specific to Rhizostomeae (Collins, 2002), and arose from ancestral polydisc strobilation (Marques & Collins, Biological Reviews 93 (2018) 1228–1250 © 2018 The Authors.”
BackgroundMethodInfluentialHow corals made rocks through the ages
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“…Corallimopharia, Anthipatharia, Actiniaria, Zoanthiniaria), Ceriantharia, and Octocorallia and is thought to be a sister group to all other cnidarians, including Cubozoa (box jellyfish), Hydrozoa (jellyfish and hydroids), and Scyphozoa (true jellyfish; Collins, 2002; Kayal et al., 2018).”
Background16S rRNA is a better choice than COI for DNA barcoding hydrozoans in the coastal waters of China
Zheng, L., He, J., Lin, Y., Cao, W., & Zhang, W. (2014) · Acta Oceanologica Sinica · doi:10.1007/s13131-014-0415-8 · Cited by 99
Collins, A. G., Bentlage, B., Lindner, A., LINDSAY, D. J., Haddock, S. H. D., Jarms, G., Norenburg, J. L., Jankowski, T., & Cartwright, P. (2008) · Journal of the Marine Biological Association of the United Kingdom · doi:10.1017/s0025315408001732 · Cited by 96
Self-citationStierwald, M., Yanze, N., Bamert, R. P., Kammermeier, L., & Schmid, V. J. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.06.018 · Cited by 95
The fossil record of cnidarian medusae
Young, G. A., & Hagadorn, J. W. (2010) · Palaeoworld · doi:10.1016/j.palwor.2010.09.014 · Cited by 95
Shao, Z., Graf, S., Chaga, O. Y., & Lavrov, D. V. (2006) · Gene · doi:10.1016/j.gene.2006.06.021 · Cited by 93
“There are approximately 200 species in this class, which are traditionally divided into four orders (Brusca and Brusca, 2002), although one of these orders (Stauromedusae) may represent an independent lineage within the phylum (Collins, 2002; Marques and Collins, 2004; Collins and Daly, 2005).”
BackgroundPotential of DNA Sequences to Identify Zoanthids (Cnidaria: Zoantharia)
Sinniger, F., Reimer, J. D., & Pawlowski, J. W. (2008) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.25.1253 · Cited by 92
A golden age of gelata: past and future research on planktonic ctenophores and cnidarians
Haddock, S. H. D. (2007) · Springer eBooks · doi:10.1007/978-1-4020-2762-8_62 · Cited by 92
Ponce, D., Brinkman, D. L., Potriquet, J., & Mulvenna, J. P. (2016) · Toxins · doi:10.3390/toxins8040102 · Cited by 91
“The phylum is divided into two subphyla, Anthozoa and Medusozoa (comprising the four remaining Classes), based on differences in mitochondrial genomes and life cycles [1,2].”
BackgroundExpression of Pax gene family members in the anthozoan cnidarian, Nematostella vectensis
Matus, D. Q., Pang, K., Daly, M., & Martindale, M. Q. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2006.00135.x · Cited by 91
“…placozoans (e.g., Trichoplax) are both reported to be the sister-group to bilaterally symmetrical animals (Wainright et al. 1993; Medina et al. 2001; Collins 2002; Collins and Daly 2005), although mitochondrial genomic data suggests a more ancient origin for the Placozoa (Dellaporta et al. 2006).”
BackgroundReverse development in Cnidaria
Piraino, S., De Vito, D., Schmich, J., Bouillon, J., & Boero, F. (2004) · Canadian Journal of Zoology · doi:10.1139/z04-174 · Cited by 87
“Reversible metamorphosis in Anthozoa Anthozoa are considered the ancestral group of Cnidaria (Bridge et al. 1992; Collins 2002).”
BackgroundRecent Insights into Cnidarian Phylogeny
Collins, A. G. (2009) · Smithsonian contributions to the marine sciences · doi:10.5479/si.01960768.38.139 · Cited by 88
Self-citationPhylogeny of Capitata and Corynidae (Cnidaria, Hydrozoa) in light of mitochondrial 16S rDNA data
Collins, A. G., Winkelmann, S., Hadrys, H., & Schierwater, B. (2005) · Zoologica Scripta · doi:10.1111/j.1463-6409.2005.00172.x · Cited by 83
Self-citationCartwright, P., & Collins, A. G. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm071 · Cited by 84
Self-citationRevision of the genus Chrysaora Péron & Lesueur, 1810 (Cnidaria: Scyphozoa)
Morandini, A. C., & Marques, A. C. (2010) · Zootaxa · doi:10.11646/zootaxa.2464.1.1 · Cited by 81
Corumbella, an Ediacaran-grade organism from the Late Neoproterozoic of Brazil
Babcock, L. E., Grunow, A. M., Sadowski, G. R., & Leslie, S. A. (2005) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2003.01.001 · Cited by 78
Molecular phylogenetics in Hydra, a classical model in evolutionary developmental biology
Hemmrich, G., Anokhin, B. A., Zacharias, H., & Bosch, T. C. G. (2006) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2006.10.031 · Cited by 78
Ohdera, A. H., Ames, C. L., Dikow, R. B., Kayal, E., Chiodin, M., Busby, B., La, S., Pirro, S., Collins, A. G., Medina, M., et al. (2019) · GigaScience · doi:10.1093/gigascience/giz069 · Cited by 77
“Active areas of 45 research include the basis of venom evolution and diversification [2-4], mechanisms of 46 independent evolution of image-forming vision (lens eyes) [5-7], and the emergence of a 47 pelagic adult stage within a biphasic (or multiphasic) life cycle [8].”
Self-citationPhylogenetic placement of the enigmatic parasite, Polypodium hydriforme, within the Phylum Cnidaria
Evans, N., Lindner, A., Ev, R., Collins, A. G., & Cartwright, P. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-139 · Cited by 76
“In this study, Polypodium falls within the medusozoan clade of cnidarians, although the non-cnidarian placozoan, Trichoplax [19,20], also fell within this clade, rendering Cnidaria paraphyletic.”
Self-citationDevelopment of the rhopalial nervous system in Aurelia sp.1 (Cnidaria, Scyphozoa)
Nakanishi, N., Hartenstein, V., & Jacobs, D. K. (2009) · Development Genes and Evolution · doi:10.1007/s00427-009-0291-y · Cited by 76
“, jellyfishes) (Collins 2002).”
BackgroundInfluentialEye evolution: a question of genetic promiscuity
Nilsson, D. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.07.004 · Cited by 76
“On the other hand, it remains possible that an original, and yet unknown, role of Hox genes naturally lends itself to setting up bilateral symmetry, and that this has happened independently in Bilateria and some Cnidaria.”
BackgroundInfluentialA character-based analysis of the evolution of jellyfish blooms: adaptation and exaptation
Dawson, M. N., & Hamner, W. M. (2008) · Hydrobiologia · doi:10.1007/s10750-008-9591-x · Cited by 75
“…Newick format subtrees drawn from published results were as follows: ((Staurozoa1,Staurozoa2),((Hydrozoa1,Hydrozoa2), (Cubozoa1,Cubozoa2),((Coronatae1,Coronatae2), (Semaeostomeae1,(Semaeostomeae2,Rhizostomeae)) ))) from analyses of 18S rDNA by Hamner & Dawson (2008; see also Collins, 2002, Fig.”
BackgroundMethodInfluentialWhat Are Jellyfishes and Thaliaceans and Why Do They Bloom?
Lucas, C. H., & Dawson, M. N. (2013) · Springer eBooks · doi:10.1007/978-94-007-7015-7_2 · Cited by 76
Coherence, correspondence, and the renaissance of morphology in phylogenetic systematics
Assis, L. C. S. (2009) · Cladistics · doi:10.1111/j.1096-0031.2009.00261.x · Cited by 73
“In several groups, life stages are unknown, generating an important limitation while constructing data matrices and in phylogenetic reconstruction (Bridge et al., 1995; Nielsen, 1998; Collins, 2002; Freitas and Brown, 2004; Wahlberg et al., 2005).”
BackgroundMethodKayal, E., Bentlage, B., Cartwright, P., Yanagihara, A. A., LINDSAY, D. J., Hopcroft, R. R., & Collins, A. G. (2015) · PeerJ · doi:10.7717/peerj.1403 · Cited by 74
Self-citationTiny sea anemone from the Lower Cambrian of China
Han, J., Kubota, S., Uchida, H.-O., Stanley, G. D., Yao, X., Shu, D., Li, Y., & Yasui, K. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013276 · Cited by 72
“The anthozoan and medusozan clades within the Cnidaria are adopted from [60].”
BackgroundGovindarajan, A. F., Boero, F., & Halanych, K. M. (2006) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.11.012 · Cited by 72
“Two species of Hydridae (Collins, 2000, 2002) were used to root the Leptomedusae analysis.”
MethodStraehler-Pohl, I., & Jarms, G. (2005) · Marine Biology · doi:10.1007/s00227-005-0031-4 · Cited by 72
Evolutionary crossroads in developmental biology
Patel, N. H. (2012) · Development · doi:10.1242/dev.085464 · Cited by 77
Müller, P., Seipel, K., Yanze, N., Reber-Müller, S., Streitwolf-Engel, R., Stierwald, M., Spring, J. Ü., & Schmid, V. (2003) · Developmental Biology · doi:10.1016/s0012-1606(02)00091-x · Cited by 69
Pratlong, M., Haguenauer, A., Chabrol, O., Klopp, C., Pontarotti, P., & Aurelle, D. (2015) · Molecular Ecology Resources · doi:10.1111/1755-0998.12383 · Cited by 72
“These relationships correspond to the most usual phylogeny of cnidarians (Collins 2002; Technau et al. 2005) although two recent papers uncovered a closer relationship of octocorals with medusozoans rather than with hexacorals (Park et al.”
ResultEckelbarger, K. J., & Hodgson, A. N. (2021) · Invertebrate Reproduction & Development · doi:10.1080/07924259.2021.1927861 · Cited by 66
Insights from diploblasts; the evolution of mesoderm and muscle
Burton, P. M. (2007) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21150 · Cited by 69
Zrzavý, J. (2003) · Cladistics · doi:10.1016/s0748-3007(03)00007-0 · Cited by 67
“The comprehensive phylogenetic analysis of the cnidarian SSU sequences (Collins, 2002) indeed retrieves monophyletic Cnidaria and Hydrozoa (¼Hydroidolina and Trachylina, the latter including the Narcomedusae) but an uncertain position of Polypodium and Myxozoa outside the Hydrozoa (A.G. Collins,…”
BackgroundMiranda, L. S., Collins, A. G., & Marques, A. C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010182 · Cited by 64
“While there is great variation in medusozoan life cycles, there exist some broad-scale patterns of congruence between life cycle differences and the origins of major medusozoan taxa [1,2], suggesting that evolutionary changes in life cycle have sometimes corresponded to the establishment of distinct lineages.”
BackgroundSelf-citationTronolone, V. B., Morandini, A. C., & Migotto, Á. E. (2002) · Biota Neotropica · doi:10.1590/s1676-06032002000200008 · Cited by 60
“COLLINS, A.G., 2002.”
BackgroundInfluentialLogashina, Y. A., Solstad, R. G., Mineev, K. S., Korolkova, Y. V., Mosharova, I. V., Dyachenko, I. A., Паликов, В. А., Palikova, Y. A., Мурашев, А. Н., Arseniev, A. S., et al. (2017) · Toxins · doi:10.3390/toxins9050154 · Cited by 60
Early Cambrian Pentamerous Cubozoan Embryos from South China
Han, J., Kubota, S., Li, G., Yao, X., Yang, X., Shu, D., Li, Y., Kinoshita, S., Sasaki, O., Komiya, T., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070741 · Cited by 58
Hox, Wnt, and the evolution of the primary body axis: insights from the early-divergent phyla
Ryan, J. F., & Baxevanis, A. D. (2007) · Biology Direct · doi:10.1186/1745-6150-2-37 · Cited by 65
“[95] 2002 MP (Po,(Po,(Ct,(Cn,(Tr, Bi))))) TrBi”
Mazza, M. E., Pang, K., Martindale, M. Q., & Finnerty, J. R. (2007) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21158 · Cited by 57
Development and epithelial organisation of muscle cells in the sea anemone Nematostella vectensis
Jahnel, S. M., Walzl, M., & Technau, U. (2014) · Frontiers in Zoology · doi:10.1186/1742-9994-11-44 · Cited by 57
“The striking structural similarity of striated muscles in Cnidaria and Bilateria has led to the suggestion that striated muscles of Cnidaria and Bilateria are homologous [4].”
BackgroundInfluentialAdoption of conserved developmental genes in development and origin of the medusa body plan
Kraus, J. E. M., Fredman, D., Wang, W., Khalturin, K., & Technau, U. (2015) · EvoDevo · doi:10.1186/s13227-015-0017-3 · Cited by 54
“a Phylogenetic relationship of the cnidarian taxa (blue box) [14, 55, 56].”
BackgroundFigueroa, D. F., & Baco, A. R. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu286 · Cited by 54
“…classification and with phylogenetic reconstructions based on nuclear markers, which strongly support a monophyletic Anthozoa comprised of the Octocorallia and Hexacorallia (France et al. 1996; Odorico and Miller 1997; Berntson et al. 1999; Won et al. 2001; Collins 2002; Daly et al. 2007).”
BackgroundInfluential
Metadata
- Authors
- Collins, A. G.
- Affiliations
- University of California, Berkeley (US)
- Corresponding author
- Collins, A. G.
- ORCID
- Collins, A. G.
- Venue
- Journal of Evolutionary Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2002-05-01
- Volume
- 15
- Issue
- 3
- Pages
- 418-432
- ISSN
- 1010-061X (ISSN-L)
- 1420-9101
- OpenAlex
- W2098787235
- Cited by
- 355
- References
- 62
- Citations by year
- 2026: 11 · 2025: 8 · 2024: 9 · 2023: 12 · 2022: 16 · 2021: 10 · 2020: 6 · 2019: 13 · 2018: 15 · 2017: 19 · 2016: 21 · 2015: 27 · 2014: 15 · 2013: 9 · 2012: 7
- FWCI
- 17.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Journal of Evolutionary Biology (publishedVersion)
- Funders
- National Science Foundation (9814845)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Invertebrate Taxonomy and Ecology
- Keywords
- Medusozoa, Anthozoa, Cubozoa, Hydrozoa, Scyphozoa, Siphonophorae, strobilation, monophyly
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