Brief History of Ctenophora

  • Protocol
  • First Online:
Ctenophores

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2757))

  • 294 Accesses

Abstract

Ctenophores are the descendants of the earliest surviving lineage of ancestral metazoans, predating the branch leading to sponges (Ctenophore-first phylogeny). Emerging genomic, ultrastructural, cellular, and systemic data indicate that virtually every aspect of ctenophore biology as well as ctenophore development are remarkably different from what is described in representatives of other 32 animal phyla. The outcome of this reconstruction is that most system-level components associated with the ctenophore organization result from convergent evolution. In other words, the ctenophore lineage independently evolved as high animal complexities with the astonishing diversity of cell types and structures as bilaterians and cnidarians. Specifically, neurons, synapses, muscles, mesoderm, through gut, sensory, and integrative systems evolved independently in Ctenophora. Rapid parallel evolution of complex traits is associated with a broad spectrum of unique ctenophore-specific molecular innovations, including alternative toolkits for making an animal. However, the systematic studies of ctenophores are in their infancy, and deciphering their remarkable morphological and functional diversity is one of the hot topics in biological research, with many anticipated surprises.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Protocol
EUR 44.95
Price includes VAT (Germany)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 209.00
Price includes VAT (Germany)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
EUR 267.49
Price includes VAT (Germany)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References 

  1. Krumbach T (1925) Erste und einzige Klasse der Actinaria Vierte Klasse des Stammes der Coelenterata. Ctenophora. In: Kukenthal W, Krumbach T (eds) Handbuch der Zoologie. de Gruyter, Berlin, pp 905–995

    Google Scholar 

  2. Harbison GR (1985) On the classification and evolution of the Ctenophora. In: Morris SC et al (eds) The origins and relationships of lower invertebrates. Clarendon Press, Oxford, pp 78–100

    Google Scholar 

  3. Podar M et al (2001) A molecular phylogenetic framework for the phylum Ctenophora using 18S rRNA genes. Mol Phylogenet Evol 21(2):218–230

    Article  CAS  PubMed  Google Scholar 

  4. Li Y et al (2021) Rooting the animal tree of life. Mol Biol Evol 38(10):4322–4333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Moroz LL et al (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature 510(7503):109–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Schultz DT et al (2023) Ancient gene linkages support ctenophores as sister to other animals. Nature 618(7963):110–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Whelan NV et al (2015) Error, signal, and the placement of Ctenophora sister to all other animals. Proc Natl Acad Sci U S A 112(18):5773–5778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Whelan NV et al (2017) Ctenophore relationships and their placement as the sister group to all other animals. Nat Ecol Evol 1(11):1737–1746

    Article  PubMed  PubMed Central  Google Scholar 

  9. Jamieson AJ, Lindsay DJ, Kitazato H (2023) Maximum depth extensions for hydrozoa, Tunicata and Ctenophora. Mar Biol 170(3):33

    Article  Google Scholar 

  10. Aghamaali MR et al (2011) Cloning, sequencing, expression and structural investigation of mnemiopsin from Mnemiopsis leidyi: an attempt toward understanding Ca2+−regulated photoproteins. Protein J 30(8):566–574

    Article  CAS  PubMed  Google Scholar 

  11. Burakova LP, Kolmakova AA, Vysotski ES (2022) Recombinant light-sensitive photoprotein berovin from ctenophore Beroe abyssicola: bioluminescence and absorbance characteristics. Biochem Biophys Res Commun 624:23–27

    Article  CAS  PubMed  Google Scholar 

  12. Burakova LP et al (2021) Unexpected Coelenterazine degradation products of Beroe abyssicola photoprotein photoinactivation. Org Lett 23(17):6846–6849

    Article  CAS  PubMed  Google Scholar 

  13. Burakova LP, Vysotski ES (2019) Recombinant Ca(2+)-regulated photoproteins of ctenophores: current knowledge and application prospects. Appl Microbiol Biotechnol 103(15):5929–5946

    Article  CAS  PubMed  Google Scholar 

  14. Jafarian V et al (2011) A unique EF-hand motif in mnemiopsin photoprotein from Mnemiopsis leidyi: implication for its low calcium sensitivity. Biochem Biophys Res Commun 413(2):164–170

    Article  CAS  PubMed  Google Scholar 

  15. Markova SV et al (2012) The light-sensitive photoprotein berovin from the bioluminescent ctenophore Beroe abyssicola: a novel type of Ca(2+) -regulated photoprotein. FEBS J 279(5):856–870

    Article  CAS  PubMed  Google Scholar 

  16. Mohammadi Ghanbarlou R et al (2018) Molecular mechanisms governing the evolutionary conservation of Glycine in the 6(th) position of loops IotaIotaIota and IotaV in photoprotein mnemiopsin 2. J Photochem Photobiol B 187:18–24

    Article  CAS  PubMed  Google Scholar 

  17. Molakarimi M et al (2019) Reaction mechanism of the bioluminescent protein mnemiopsin1 revealed by X-ray crystallography and QM/MM simulations. J Biol Chem 294(1):20–27

    Article  CAS  PubMed  Google Scholar 

  18. Pashandi Z et al (2017) Photoinactivation related dynamics of ctenophore photoproteins: insights from molecular dynamics simulation under electric-field. Biochem Biophys Res Commun 490(2):265–270

    Article  CAS  PubMed  Google Scholar 

  19. Powers ML et al (2013) Expression and characterization of the calcium-activated photoprotein from the ctenophore Bathocyroe fosteri: insights into light-sensitive photoproteins. Biochem Biophys Res Commun 431(2):360–366

    Article  CAS  PubMed  Google Scholar 

  20. Schnitzler CE et al (2012) Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes. BMC Biol 10:107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Stepanyuk GA et al (2013) Spatial structure of the novel light-sensitive photoprotein berovin from the ctenophore Beroe abyssicola in the Ca(2+)-loaded apoprotein conformation state. Biochim Biophys Acta 1834(10):2139–2146

    Article  CAS  PubMed  Google Scholar 

  22. Ward WW, Seliger HH (1974) Properties of mnemiopsin and berovin, calcium-activated photoproteins from the ctenophores Mnemiopsis sp. and Beroe ovata. Biochemistry 13(7):1500–1510

    Article  CAS  PubMed  Google Scholar 

  23. Ward WW, Seliger HH (1974) Extraction and purification of calcium-activated photoproteins from the ctenophores Mnemiopsis sp. and Beroe ovata. Biochemistry 13(7):1491–1499

    Article  CAS  PubMed  Google Scholar 

  24. Madin LP et al (2013) Scuba diving in blue water: a window on ecology and evolution in the epipelagic ocean. Research and Discoveries: The Revolution of Science Through Scuba

    Google Scholar 

  25. Harbison G, Madin L, Swanberg N (1978) On the natural history and distribution of oceanic ctenophores. Deep-Sea Res 25(3):233–256

    Article  Google Scholar 

  26. Welch V et al (2006) Optical properties of the iridescent organ of the comb-jellyfish Beroe cucumis (Ctenophora). Phys Rev E Stat Nonlinear Soft Matter Phys 73(4 Pt 1):041916

    Article  Google Scholar 

  27. Hernandez-Nicaise M-L (1991) Ctenophora. In: Harrison FWFW, Westfall JA (eds) Microscopic anatomy of invertebrates: Placozoa, Porifera, Cnidaria, and Ctenophora. Wiley, New York, pp 359–418

    Google Scholar 

  28. Heimbichner Goebel WL et al (2020) Scaling of ctenes and consequences for swimming performance in the ctenophore Pleurobrachia bachei. Invertebr Biol 139(3):e12297

    Article  Google Scholar 

  29. Colin SP et al (2010) Stealth predation and the predatory success of the invasive ctenophore Mnemiopsis leidyi. Proc Natl Acad Sci U S A 107(40):17223–17227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Gemmell BJ et al (2019) A ctenophore (comb jelly) employs vortex rebound dynamics and outperforms other gelatinous swimmers. R Soc Open Sci 6(3):181615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hyman LH (1940) Invertebrates: protozoa through Ctenophora, vol 1. McGraw-Hill, New York/London, p 726

    Google Scholar 

  32. Schultz DT et al (2021) A chromosome-scale genome assembly and karyotype of the ctenophore Hormiphora californensis. G3 (Bethesda) 11(11)

    Google Scholar 

  33. Ryan JF et al (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342(6164):1242592

    Article  PubMed  PubMed Central  Google Scholar 

  34. Hoencamp C et al (2021) 3D genomics across the tree of life reveals condensin II as a determinant of architecture type. Science 372(6545):984–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Moroz LL (2014) The genealogy of genealogy of neurons. Commun Integr Biol 7(6):e993269

    Article  PubMed  Google Scholar 

  36. Moroz LL (2015) Convergent evolution of neural systems in ctenophores. J Exp Biol 218(Pt 4):598–611

    Article  PubMed  PubMed Central  Google Scholar 

  37. Moroz LL, Kohn AB (2016) Independent origins of neurons and synapses: insights from ctenophores. Philos Trans R Soc Lond Ser B Biol Sci 371(1685):20150041

    Article  Google Scholar 

  38. Horridge GA (1964) The giant mitochondria of ctenophore comb plates. Q J Microsc Sci 105:301–310

    Google Scholar 

  39. Kohn AB et al (2012) Rapid evolution of the compact and unusual mitochondrial genome in the ctenophore, Pleurobrachia bachei. Mol Phylogenet Evol 63(1):203–207

    Article  CAS  PubMed  Google Scholar 

  40. Lavrov DV, Pett W (2016) Animal mitochondrial DNA as we do not know it: mt-genome organization and evolution in Nonbilaterian lineages. Genome Biol Evol 8(9):2896–2913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Arafat H et al (2018) Extensive mitochondrial gene rearrangements in Ctenophora: insights from benthic Platyctenida. BMC Evol Biol 18(1):65

    Article  PubMed  PubMed Central  Google Scholar 

  42. Christianson LM et al (2022) Hidden diversity of Ctenophora revealed by new mitochondrial COI primers and sequences. Mol Ecol Resour 22(1):283–294

    Article  CAS  PubMed  Google Scholar 

  43. Formaggioni A, Luchetti A, Plazzi F (2021) Mitochondrial genomic landscape: a portrait of the mitochondrial genome 40 years after the first complete sequence. Life (Basel) 11(7)

    Google Scholar 

  44. Muthye V, Lavrov DV (2018) Characterization of mitochondrial proteomes of nonbilaterian animals. IUBMB Life 70(12):1289–1301

    Article  CAS  PubMed  Google Scholar 

  45. Pett W et al (2011) Extreme mitochondrial evolution in the ctenophore Mnemiopsis leidyi: insight from mtDNA and the nuclear genome. Mitochondrial DNA 22(4):130–142

    Article  CAS  PubMed  Google Scholar 

  46. Schultz DT et al (2020) Conserved novel ORFs in the mitochondrial genome of the ctenophore Beroe forskalii. PeerJ 8:e8356

    Article  PubMed  PubMed Central  Google Scholar 

  47. Wang M, Cheng F (2019) The complete mitochondrial genome of the ctenophore Beroe cucumis, a mitochondrial genome showing rapid evolutionary rates. Mitochondrial DNA B Resour 4(2):3774–3775

    Article  PubMed  PubMed Central  Google Scholar 

  48. Alamaru A et al (2017) Molecular diversity of benthic ctenophores (Coeloplanidae). Sci Rep 7(1):6365

    Article  PubMed  PubMed Central  Google Scholar 

  49. Schroeder A et al (2021) Suitability of a dual COI marker for marine zooplankton DNA metabarcoding. Mar Environ Res 170:105444

    Article  CAS  PubMed  Google Scholar 

  50. Mukherjee K, Moroz LL (2023) Transposon-derived transcription factors across metazoans. Front Cell Dev Biol 11:1113046

    Article  PubMed  PubMed Central  Google Scholar 

  51. Mukherjee K, Moroz LL (2023) Parallel evolution of transcription factors in basal metazoans. Ctenophores: Methods and Protocols, Methods Mol Biol, vol. 2757, https://doi.org/10.1007/978-1-0716-3642-8_20. This volume

  52. Becklemishev VM (1964) Foundation for comprative anatomy of invertebrates, vol 1–2, 3rd edn. Nauka, Moscow. (in Russian)

    Google Scholar 

  53. Brusca RC, Giribet G, Moore W (2022) Invertebrates, 4th edn. Sinauer Associates of Oxford University Press, p 1104

    Book  Google Scholar 

  54. Parry LA et al (2021) Cambrian comb jellies from Utah illuminate the early evolution of nervous and sensory systems in ctenophores. iScience 24(9):102943

    Article  PubMed  PubMed Central  Google Scholar 

  55. Ou Q et al (2015) A vanished history of skeletonization in Cambrian comb jellies. Sci Adv 1(6):e1500092

    Article  PubMed  PubMed Central  Google Scholar 

  56. Tang F et al (2011) Eoandromeda and the origin of Ctenophora. Evol Dev 13(5):408–414

    Article  PubMed  Google Scholar 

  57. Zhao Y et al (2019) Cambrian sessile, suspension feeding stem-group ctenophores and evolution of the comb jelly body plan. Curr Biol 29(7):1112–1125 e2

    Article  PubMed  Google Scholar 

  58. Fu D et al (2019) The Qingjiang biota – a burgess shale-type fossil Lagerstatte from the early Cambrian of South China. Science 363(6433):1338–1342

    Article  CAS  PubMed  Google Scholar 

  59. Stanley GD, Sturmer W (1983) The first fossil ctenophore from the lower devonian of West Germany. Nature 303:518–520

    Article  Google Scholar 

  60. Stanley GD, Stürmer W (1987) A new fossil ctenophore discovered by X-rays. Nature 328(6125):61–63

    Article  Google Scholar 

  61. Haddock SH (2007) Comparative feeding behavior of planktonic ctenophores. Integr Comp Biol 47(6):847–853

    Article  PubMed  Google Scholar 

  62. Cordeiro M et al (2022) Oceanic lobate ctenophores possess feeding mechanics similar to the impactful coastal species Mnemiopsis leidyi. Limnol Oceanogr 67(12):2706–2717

    Google Scholar 

  63. Reeve MR, Walter MA (1979) Nutritional ecology of ctenophores – a review of recent research. In: Russell FS, Yonge M (eds) Advances in marine biology. Academic, pp 249–287

    Google Scholar 

  64. Swanberg N (1974) The feeding behavior of Beroe ovata. Mar Biol 24:69–76

    Article  Google Scholar 

  65. Carre D, Carre C, Mills CE (1989) Novel cnidocysts of narcomedusae and a medusivorous ctenophore, and confirmation of kleptocnidism. Tissue Cell 21(5):723–734

    Article  CAS  PubMed  Google Scholar 

  66. Mills CE, Miller RL (1984) Ingestion of a medusa (Aegina citrea) by the nematocyst-containing ctenophore Haeckelia rubra (formerly Euchlora rubra): phylogenetic implications. Mar Biol 78(2):215–221

    Google Scholar 

  67. Carré C, Carré D (1980) Les cnidocystes du cténophore Euchlora rubra (Kölliker 1853). Cah Biol Mar 21:221–226

    Google Scholar 

  68. Potter B et al (2023) Quantifying the feeding behavior and trophic impact of a widespread oceanic ctenophore. Sci Rep 13(1):2292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Yip SY (1984) The feeding of Pleurobrachia pileus Müller (Ctenophora) from Galway Bay. Proc R Ir Acad Sect B Biol Geol Chem Sci 84B:109–122

    Google Scholar 

  70. Waggett R, Costello J (1999) Capture mechanisms used by the lobate ctenophore, Mnemiopsis leidyi, preying on the copepod Acartia tonsa. J Plankton Res 21(11):2037–2052

    Article  Google Scholar 

  71. Kremer P, Reeve MR, Syms MA (1986) The nutritional ecology of the ctenophore Bolinopsis vitrea: comparisons with Mnemiopsis mccradyi from the same region. J Plankton Res 8(6):1197–1208

    Article  Google Scholar 

  72. Kremer P, Canino M, Gilmer R (1986) Metabolism of epipelagic tropical ctenophores. Mar Biol 90:403–412

    Article  Google Scholar 

  73. Jaspers C et al (2018) Resilience in moving water: effects of turbulence on the predatory impact of the lobate ctenophore Mnemiopsis leidyi. Limnol Oceanogr 63(1):445–458

    Article  Google Scholar 

  74. Buecher E, Gasser B (1998) Estimation of predatory impact of Pleurobrachia rhodopis (cydippid ctenophore) in the northwestern Mediterranean Sea: in situ observations and laboratory experiments. J Plankton Res 20(4):631–651

    Article  Google Scholar 

  75. Swanberg N, Båmstedt U (1989) The role of prey stratification in the predation pressure by the cydippid ctenophore Mertensia ovum in the Barents Sea. In: Coelenterate biology: recent research on Cnidaria and Ctenophora: proceedings of the fifth international conference on coelenterate biology, vol 1991. Springer

    Google Scholar 

  76. Townsend J et al (2020) Ink release and swimming behavior in the oceanic ctenophore Eurhamphaea vexilligera. Biol Bull 238(3):206–213

    Article  CAS  PubMed  Google Scholar 

  77. Sutherland KR et al (2014) Ambient fluid motions influence swimming and feeding by the ctenophore Mnemiopsis leidyi. J Plankton Res 36(5):1310–1322

    Article  Google Scholar 

  78. Matsumoto G, Harbison G (1993) In situ observations of foraging, feeding, and escape behavior in three orders of oceanic ctenophores: Lobata, Cestida, and Beroida. Mar Biol 117:279–287

    Article  Google Scholar 

  79. Matsumoto G, Hamner W (1988) Modes of water manipulation by the lobate ctenophore Leucothea sp. Mar Biol 97:551–558

    Article  Google Scholar 

  80. Matsumoto G (1991) Swimming movements of ctenophores, and the mechanics of propulsion by ctene rows. Hydrobiologia 216:319–325

    Article  Google Scholar 

  81. Hamner W et al (1987) Ethological observations on foraging behavior of the ctenophore Leucothea sp. in the open sea 1. Limnol Oceanogr 32(3):645–652

    Article  Google Scholar 

  82. Colin SP et al (2015) Elevating the predatory effect: sensory-scanning foraging strategy by the lobate ctenophore Mnemiopsis leidyi. Limnol Oceanogr 60(1):100–109

    Article  Google Scholar 

  83. Swift HF et al (2009) Feeding behavior of the ctenophore Thalassocalyce inconstans: revision of anatomy of the order Thalassocalycida. Mar Biol 156(5):1049–1056

    Article  Google Scholar 

  84. Decker MB, Breitburg DL, Purcell JE (2004) Effects of low dissolved oxygen on zooplankton predation by the ctenophore Mnemiopsis leidyi. Mar Ecol Prog Ser 280:163–172

    Article  Google Scholar 

  85. Thuesen EV, Rutherford LD, Brommer PL (2005) The role of aerobic metabolism and intragel oxygen in hypoxia tolerance of three ctenophores: Pleurobrachia bachei, Bolinopsis infundibulum and Mnemiopsis leidyi. J Mar Biol Assoc U K 85(3):627–633

    Article  Google Scholar 

  86. Båmstedt U, Martinussen MB (2015) Ecology and behavior of Bolinopsis infundibulum (Ctenophora; Lobata) in the Northeast Atlantic. Hydrobiologia 759:3–14

    Article  Google Scholar 

  87. Titelman J et al (2012) Predator-induced vertical behavior of a ctenophore. Hydrobiologia 690:181–187

    Article  Google Scholar 

  88. Falkenhaug T, Stabell OB (1996) Chemical ecology of predator-prey interactions in ctenophores. Mar Freshw Behav Phy 27(4):249–260

    Article  Google Scholar 

  89. Moss AG, Rapoza RC, Muellner L (2001) A novel cilia-based feature within the food grooves of the ctenophore Mnemiopsis mccradyi Mayer. Hydrobiologia 451:287–294

    Article  Google Scholar 

  90. Leonardi ND, Thuesen EV, Haddock SHD (2020) A sticky thicket of glue cells: a comparative morphometric analysis of colloblasts in 20 species of comb jelly (phylum Ctenophora). Cienc Mar 46(4):211–225

    Article  CAS  Google Scholar 

  91. Townsend J et al (2020) Colloblasts act as a biomechanical sensor for suitable prey in Pleurobrachia. bioRxiv:2020.06. 27.175059

    Google Scholar 

  92. Presnell JS et al (2016) The presence of a functionally tripartite through-gut in Ctenophora has implications for metazoan character trait evolution. Curr Biol 26(20):2814–2820

    Article  CAS  PubMed  Google Scholar 

  93. Tamm SL (2014) Cilia and the life of ctenophores. Invertebr Biol 133(1):1–46

    Article  Google Scholar 

  94. Dubas F, Stein PG, Anderson PA (1988) Ionic currents of smooth muscle cells isolated from the ctenophore Mnemiopsis. Proc R Soc Lond B Biol Sci 233(1271):99–121

    Article  CAS  PubMed  Google Scholar 

  95. Stein PG, Anderson PA (1984) Maintenance of isolated smooth muscle cells of the ctenophore Mnemiopsis. J Exp Biol 110:329–334

    Article  CAS  PubMed  Google Scholar 

  96. Hernandez-Nicaise ML, Mackie G, Meech RW (1980) Giant smooth muscle cells of Beroe. J General Physiol 75:79–105

    Google Scholar 

  97. Bilbaut A et al (1988) Membrane currents that govern smooth muscle contraction in a ctenophore. Nature 331(6156):533–535

    Article  CAS  PubMed  Google Scholar 

  98. Anderson PAV (1984) The electrophysiology of single smooth muscle cells isolated from Mnemiopsis. J Compar Physiol B 154:257–268

    Google Scholar 

  99. Meech RW (2015) Electrogenesis in the lower Metazoa and implications for neuronal integration. J Exp Biol 218(Pt 4):537–550

    Article  PubMed  PubMed Central  Google Scholar 

  100. Meech RW, Bilbaut A, Hernandez-Nicaise ML. Electrophysiology of ctenophore smooth muscle. In: Ctenophores: Methods and Protocols, Methods in Molecular Biology, vol. 2757, https://doi.org/10.1007/978-1-0716-3642-8_15 (in press)

  101. Tamm S, Tamm S (1991) Macrociliary tooth patterns in beroid ctenophores. Biol Bull 181(2):355–356

    Article  CAS  PubMed  Google Scholar 

  102. Norekian TP, Moroz LL (2019) Neural system and receptor diversity in the ctenophore Beroe abyssicola. J Comp Neurol 527(12):1986–2008

    Article  PubMed  Google Scholar 

  103. Norekian TP, Moroz LL (2023) Scanning electron microscopy of ctenophores: Illustrative atlas. in Ctenophores: Methods and Protocols, Methods in Molecular Biology, vol. 2757, https://doi.org/10.1007/978-1-0716-3642-8_6. This volume.

  104. Jokura K, Inaba K (2020) Structural diversity and distribution of cilia in the apical sense organ of the ctenophore Bolinopsis mikado. Cytoskeleton (Hoboken) 77(10):442–455

    Article  CAS  PubMed  Google Scholar 

  105. Noda N, Tamm SL (2014) Lithocytes are transported along the ciliary surface to build the statolith of ctenophores. Curr Biol 24(19):R951–R952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Krisch B (1973) Über das Apikalorgan (statocyste) der ctenophore Pleurobrachia pileus. Z Zellforsh 142:241–262

    Article  CAS  Google Scholar 

  107. Tamm SL (1982) Ctenophora. In: Electrical conduction and behavior in “simple” invertebrates. Clarendon Press, Oxford, pp 266–358

    Google Scholar 

  108. Norekian TP, Moroz LL (2019) Neuromuscular organization of the ctenophore Pleurobrachia bachei. J Comp Neurol 527(2):406–436

    Article  CAS  PubMed  Google Scholar 

  109. Norekian TP, Moroz LL (2020) Comparative neuroanatomy of ctenophores: neural and muscular systems in Euplokamis dunlapae and related species. J Comp Neurol 528(3):481–501

    Article  PubMed  Google Scholar 

  110. Tamm SL (1983) Motility and mechanosensitivity of macrocilia in the ctenophore Beroe. Nature 305(5933):430–433

    Article  CAS  PubMed  Google Scholar 

  111. Tamm SL, Tamm S (1981) Ciliary reversal without rotation of axonemal structures in ctenophore comb plates. J Cell Biol 89(3):495–509

    Article  CAS  PubMed  Google Scholar 

  112. Jokura K et al (2019) CTENO64 is required for coordinated paddling of ciliary comb plate in ctenophores. Curr Biol 29(20):3510–3516 e4

    Article  CAS  PubMed  Google Scholar 

  113. Jokura K et al (2022) Two distinct compartments of a ctenophore comb plate provide structural and functional integrity for the motility of giant multicilia. Curr Biol 32(23):5144–5152 e6

    Article  CAS  PubMed  Google Scholar 

  114. Hertwig R (1880) Ueber den Bau der Ctenophoren. Jenaische Z Naturwiss 14:393–457

    Google Scholar 

  115. Hertwig O, Hertwig R (1878) Das Nervensystem und die Sinnesorgane der Medusen (The nervous system and the sensory organs of the Medusa). Vogel, Leipzig, p 157

    Google Scholar 

  116. Hertwig O, Hertwig R (1879) Die Actinien anatomisch und histologisch mit besonderer Berucksichtigung des Nervenmuskelsystems untersucht. Jenaische Z. Naturwiss. 13:457–640

    Google Scholar 

  117. Hertwig O, Hertwig R (1880) Die Actinien anatomisch und histologisch mit besonderer Berucksichtigung des Nervenmuskelsystems untersucht. Jenaische Z. Naturwiss. 14:39–89

    Google Scholar 

  118. Parker GH (1919) The elementary nervous systems. Lippincott, Philadelphia, p 229

    Book  Google Scholar 

  119. Moroz LL (2009) On the independent origins of complex brains and neurons. Brain Behav Evol 74(3):177–190

    Article  PubMed  PubMed Central  Google Scholar 

  120. Moroz LL, Kohn AB (2015) Unbiased view of synaptic and neuronal gene complement in ctenophores: are there pan-neuronal and pan-synaptic genes across metazoa? Integr Comp Biol 55(6):1028–1049

    PubMed  PubMed Central  Google Scholar 

  121. Hernandez-Nicaise ML (1968) Specialized connexions between nerve cells and mesenchymal cells in ctenophores. Nature 217(5133):1075–1076

    Article  CAS  PubMed  Google Scholar 

  122. Hernandez-Nicaise ML (1973) The nervous system of ctenophores. III. Ultrastructure of synapses. J Neurocytol 2(3):249–263

    Article  CAS  PubMed  Google Scholar 

  123. Hernandez-Nicaise ML (1973) The nervous system of ctenophores. I. Structure and ultrastructure of the epithelial nerve-nets. Z Zellforsch Mikrosk Anat 137(2):223–250

    Article  CAS  PubMed  Google Scholar 

  124. Hernandez-Nicaise ML (1973) The nervous system of ctenophores. II. The nervous elements of the mesoglea of beroids and cydippids (author’s transl). Z Zellforsch Mikrosk Anat 143(1):117–133

    Article  CAS  PubMed  Google Scholar 

  125. Hernandez-Nicaise ML (1974) Ultrastructural evidence for a sensory-motor neuron in Ctenophora. Tissue Cell 6(1):43–47

    Article  CAS  PubMed  Google Scholar 

  126. Jager M et al (2011) New insights on ctenophore neural anatomy: immunofluorescence study in Pleurobrachia pileus (Muller, 1776). J Exp Zool B Mol Dev Evol 316B(3):171–187

    Article  PubMed  Google Scholar 

  127. Norekian TP, Moroz LL (2016) Development of neuromuscular organization in the ctenophore Pleurobrachia bachei. J Comp Neurol 524(1):136–151

    Article  PubMed  Google Scholar 

  128. Norekian TP, Moroz LL (2021) Development of the nervous system in the early hatching larvae of the ctenophore Mnemiopsis leidyi. J Morphol 282(10):1466–1477

    Article  PubMed  Google Scholar 

  129. Moroz LL, Romanova DY (2022) Alternative neural systems: what is a neuron? (ctenophores, sponges and placozoans). Front Cell Dev Biol 10:1071961

    Article  PubMed  PubMed Central  Google Scholar 

  130. Moroz LL (2012) Phylogenomics meets neuroscience: how many times might complex brains have evolved? Acta Biol Hung 63(Suppl 2):3–19

    Article  PubMed  PubMed Central  Google Scholar 

  131. Moroz LL (2018) NeuroSystematics and periodic system of neurons: model vs reference species at single-cell resolution. ACS Chem Neurosci 9(8):1884–1903

    Article  CAS  PubMed  Google Scholar 

  132. Moroz LL (2021) Multiple origins of neurons from secretory cells. Front Cell Dev Biol 9:669087

    Article  PubMed  PubMed Central  Google Scholar 

  133. Moroz LL, Romanova DY (2021) Selective advantages of synapses in evolution. Front Cell Dev Biol 9:726563

    Article  PubMed  PubMed Central  Google Scholar 

  134. Burkhardt P et al (2023) Syncytial nerve net in a ctenophore adds insights on the evolution of nervous systems. Science 380(6642):293–297

    Article  CAS  PubMed  Google Scholar 

  135. Horridge GA (1965) Non-motile sensory cilia and neuromuscular junctions in a ctenophore independent effector organ. Proc R Soc Lond Biol 162:333–350

    Article  Google Scholar 

  136. Horridge GA, Mackay B (1964) Neurociliary synapses in Pleurobrachia (Ctenophora). Q J Microsc Sci 105:163–174

    Google Scholar 

  137. Moroz LL, Mukherjee K, Romanova DY (2023) Nitric oxide signaling in ctenophores. Front Neurosci 17:1125433

    Article  PubMed  PubMed Central  Google Scholar 

  138. Norekian TP, Moroz LL (2023) Recording cilia activity in ctenophores: effects of nitric oxide and low molecular weight transmitters. Front Neurosci 17:1125476

    Article  PubMed  PubMed Central  Google Scholar 

  139. Moroz LL, Romanova DY, Kohn AB (1821) Neural versus alternative integrative systems: molecular insights into origins of neurotransmitters. Philos Trans R Soc Lond Ser B Biol Sci 2021(376):20190762

    Google Scholar 

  140. Moroz LL et al (2021) Evolution of glutamatergic signaling and synapses. Neuropharmacology 199:108740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Sachkova MY et al (2021) Neuropeptide repertoire and 3D anatomy of the ctenophore nervous system. Curr Biol 31(23):5274–5285 e6

    Article  CAS  PubMed  Google Scholar 

  142. Hayakawa E et al (2022) Mass spectrometry of short peptides reveals common features of metazoan peptidergic neurons. Nat Ecol Evol 6(10):1438–1448

    Article  PubMed  PubMed Central  Google Scholar 

  143. Harbison GR, Miller RL (1986) Not all ctenophores are hermaphrodites. Studies on the systematics, distribution, sexuality and development of two species of Ocyropsis. Mar Biol 90(3):413–424

    Article  Google Scholar 

  144. Carre D, Sardet C (1984) Fertilization and early development in Beroe ovata. Dev Biol 105(1):188–195

    Article  CAS  PubMed  Google Scholar 

  145. Carre D, Rouviere C, Sardet C (1991) In vitro fertilization in ctenophores: sperm entry, mitosis, and the establishment of bilateral symmetry in Beroe ovata. Dev Biol 147(2):381–391

    Article  CAS  PubMed  Google Scholar 

  146. Sardet C, Carré D, Rouvière C (1990) Reproduction and development in ctenophores. Exp Embryol Aquat Plants Anim:83–94

    Google Scholar 

  147. Kowalevsky A (1866) Entwickelungsgeschichte der Rippenquallen, vol 10. Memoires L’Academie Imperial des Sciences de St.-Petersbourg, St.-Petersbourg

    Google Scholar 

  148. Agassiz A (1874) Embryology of the ctenophorae. Memoirs Am Acade Arts Sci 10(3):357–398

    Google Scholar 

  149. Chun C (1880) Die Ctenophoren des Golfes von Neapel. Fauna Flora Neapel. Monogr:1–313

    Google Scholar 

  150. Metchnikoff E (1885) Vergleichend-embryologische Studien. 4. Über die Gastrulation und Mesodermbildung der Ctenophoren. 5 Über die Bildung der Wanderzellen bei Asterien und Echiniden. Z Wiss Zool 42:648–673

    Google Scholar 

  151. Driesch H, Morgan TH (1895) Zur Analysis der ersten Entwickelungsstadien des Ctenophoreneies: I. Von der Entwickelung einzelner Ctenophorenblastomeren. Arch Mikrosk Anat 2:204–215

    Google Scholar 

  152. Ziegler HE (1898) Experimentelle Studien über die Zellteilung. Arch f Entwicklungsmech d Organismen 7:34–64

    Article  Google Scholar 

  153. Fischel A (1903) Entwickelung und Organ-Differenzirung. Archiv für Entwicklungsmechanik der Organismen 15(4):679–750

    Article  Google Scholar 

  154. Yatsu N (1911) Observations and experiments on the ctenophore egg: II. Notes on early cleavage stages and experiments on cleavage. 日本動物学彙報 7(5):333–346

    Google Scholar 

  155. Yatsu N (1912) Observations and experiments on the ctenophore egg. Annot Zool Japon 8:5

    Google Scholar 

  156. Reverberi G (1957) Mitochondrial and enzymatic segregation through the embryonic development in ctenophores

    Google Scholar 

  157. Reverberi G, Ortolani G (1965) The development of the ctenophores egg. Riv Biol 58:113–137

    Google Scholar 

  158. Dunlap H (1966) Oogenesis in the Ctenophora. Ph.D. thesis, University of Washington, Seattle

    Google Scholar 

  159. Freeman GP, Reynolds GT (1973) The development of bioluminescence in the ctenophore Mnemiopsis leidyi. Dev Biol 31(1):61–100

    Article  CAS  PubMed  Google Scholar 

  160. Dunlap H (1974) Ctenophora. In: Giese AC, Pearse JP (eds) Reproduction in marine invertebrates. Academic, New York, pp 201–265

    Google Scholar 

  161. Strathmann MF (2017) Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae. University of Washington Press

    Google Scholar 

  162. Martindale MQ, Henry JQ (2015) Ctenophora. In: Wanninger A (ed) Evolutionary developmental biology of invertebrates 1: introduction, non-Bilateria, Acoelomorpha, Xenoturbellida, Chaetognatha. Springer, Vienna, pp 179–201

    Chapter  Google Scholar 

  163. Freeman G (1977) The establishment of the oral-aboral axis in the ctenophore embryo, vol 42, p 237

    Google Scholar 

  164. Martindale MQ, Henry JQ (1997) Reassessing embryogenesis in the Ctenophora: the inductive role of e1 micromeres in organizing ctene row formation in the ‘mosaic’ embryo, Mnemiopsis leidyi. Development 124(10):1999–2006

    Google Scholar 

  165. Martindale MQ, Henry JQ (1999) Intracellular fate map** in a basal metazoan, the ctenophore Mnemiopsis leidyi, reveals the origins of mesoderm and the existence of indeterminate cell lineages. Dev Biol 214(2):243–257

    Article  CAS  PubMed  Google Scholar 

  166. Salinas-Saavedra M, Martindale MQ (2020) Par protein localization during the early development of Mnemiopsis leidyi suggests different modes of epithelial organization in the metazoa. elife 9:9

    Article  Google Scholar 

  167. Derelle R, Manuel M (2007) Ancient connection between NKL genes and the mesoderm? Insights from Tlx expression in a ctenophore. Dev Genes Evol 217(4):253–261

    Article  CAS  PubMed  Google Scholar 

  168. Burton PM (2008) Insights from diploblasts; the evolution of mesoderm and muscle. J Exp Zool B Mol Dev Evol 310(1):5–14

    Article  PubMed  Google Scholar 

  169. Giribet G, Edgecombe GD (2020) The invertebrate tree of life. Princeton University Press

    Book  Google Scholar 

  170. Mortensen T (1912) Ctenophora Danish Ingolf-expedition. 5A(2):1–96

    Google Scholar 

  171. Edgar A, Ponciano JM, Martindale MQ (2022) Ctenophores are direct developers that reproduce continuously beginning very early after hatching. Proc Natl Acad Sci U S A 119(18):e2122052119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Soto-Angel JJ et al (2023) Are we there yet to eliminate the terms larva, metamorphosis, and dissogeny from the ctenophore literature? Proc Natl Acad Sci U S A 120(4):e2218317120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Mortensen T (1913) On regeneration in ctenophores. Vidensk Medd Fra Dan Nat Foren I Kjøbenhavn 66:45–51

    Google Scholar 

  174. Coonfield B (1936) Regeneration in Mnemiopsis leidyi. Agassiz The Biological Bulletin 71(3):421–428

    Article  Google Scholar 

  175. Coonfield BR (1937) The regeneration of plate rows in Mnemiopsis leidyi, Agassiz. Proc Natl Acad Sci U S A 23(3):152–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Freeman G (1967) Studies on regeneration in the cree** ctenophore, Vallicula multiformis. J Morphol 123(1):71–83

    Article  CAS  PubMed  Google Scholar 

  177. Korotkova GP, Pylilo IV (1970) Regenerative phenomena in Ctenophora larvae. Vestn Leningr Univ Biol 1:21–28

    CAS  PubMed  Google Scholar 

  178. Henry JQ, Martindale MQ (2000) Regulation and regeneration in the ctenophore Mnemiopsis leidyi. Dev Biol 227(2):720–733

    Article  CAS  PubMed  Google Scholar 

  179. Tamm SL (2012) Regeneration of ciliary comb plates in the ctenophore Mnemiopsis leidyi. i. Morphology. J Morphol 273(1):109–120

    Article  PubMed  Google Scholar 

  180. Komai T (1922) Studies on two aberrant ctenophores: Coeloplana and Gastrodes. The Author

    Book  Google Scholar 

  181. Tanaka H (1931) Reorganization in regenerating pieces of Coeloplana. Kyoto Imp Univ Coll Sci Ser B 7(Pt.):5

    Google Scholar 

  182. Alie A et al (2011) Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: ancient association of “germline genes” with stemness. Dev Biol 350(1):183–197

    Article  CAS  PubMed  Google Scholar 

  183. Tanaka, H Reorganization in regenerating pieces of Coeloplana, Memoirs Coll Sci Kyoto Imp Univ Ser B, 1932. 7(5): p. 223–246

    Google Scholar 

  184. Dawydoff C (1938) Multiplication asexuée chez les Ctenoplana. Acad Sci Paris Compt Rend 206:127–128

    Google Scholar 

  185. Ramon-Mateu J et al (2022) Studying Ctenophora WBR using Mnemiopsis leidyi. Methods Mol Biol 2450:95–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Ramon-Mateu J et al (2019) Regeneration in the ctenophore Mnemiopsis leidyi occurs in the absence of a blastema, requires cell division, and is temporally separable from wound healing. BMC Biol 17(1):80

    Article  PubMed  PubMed Central  Google Scholar 

  187. Angel J-JS et al (2023) Stable laboratory culture system for the ctenophore Mnemiopsis leidyi. In Ctenophores: Methods and Protocols, Methods Mol Biol, vol. 2757 (This volume)

    Google Scholar 

  188. Presnell JS et al (2022) Multigenerational laboratory culture of pelagic ctenophores and CRISPR-Cas9 genome editing in the lobate Mnemiopsis leidyi. Nat Protoc 17(8):1868–1900

    Article  CAS  PubMed  Google Scholar 

  189. Patry WL et al (2020) Diffusion tubes: a method for the mass culture of ctenophores and other pelagic marine invertebrates. PeerJ 8:e8938

    Article  PubMed  PubMed Central  Google Scholar 

  190. Bubel M, Knowles T, Patry WL (2019) Ctenophore culture at the Monterey Bay Aquarium

    Google Scholar 

  191. Baker LD, Reeve MR (1974) Laboratory culture of the lobate ctenophore Mnemiopsis mccradyi with notes on feeding and fecundity. Mar Biol 26:57–62

    Article  Google Scholar 

  192. Courtney A, Merces GO, Pickering M (2020) Characterising the behaviour of the Ctenophore Pleurobrachia pileus in a Laboratory Aquaculture System. bioRxiv:2020.05. 25.114744

    Google Scholar 

  193. Dieter AC, Vandepas LE, Browne WE (2022) Isolation and maintenance of in vitro cell cultures from the ctenophore Mnemiopsis leidyi. Methods Mol Biol 2450:347–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Vandepas LE et al (2017) Establishing and maintaining primary cell cultures derived from the ctenophore Mnemiopsis leidyi. J Exp Biol 220(Pt 7):1197–1201

    PubMed  Google Scholar 

  195. Moroz LL (2015) Biodiversity meets neuroscience: from the sequencing ship (Ship-Seq) to deciphering parallel evolution of neural systems in Omic’s era. Integr Comp Biol 55(6):1005–1017

    PubMed  PubMed Central  Google Scholar 

  196. Norekian TP, Moroz LL (2023) Illustrative neuroanatomy of ctenophores: Immunohistochemistry. In Ctenophores: Methods and Protocols, Methods Mol Biol, vol. 2757, https://doi.org/10.1007/978-1-0716-3642-8_5

  197. Moroz LL (2023) Syncytial nets vs. chemical signaling: emerging properties of alternative integrative systems. Front Cell Dev Biol 11, 1320209. https://doi.org/10.3389/fcell.2023.1320209

  198. Moroz LL, Collins R, Paulay G Ctenophora: Illustrated Guide and Taxonomy. In: Ctenophores: Methods and Protocols, Methods Mol Biol vol. 2757, https://doi.org/10.1007/978-1-0716-3642-8_2, this volume

  199. Kohn AB, Moroz LL (2024) Gap Junctions in Ctenophora. In: Ctenophores: Methods and Protocols, Methods Mol Biol vol. 2757, https://doi.org/10.1007/978-1-0716-3642-8_16. This volume

Download references

Acknowledgments

The author thanks the OGAP team led by Capt. Peter Molnar (vessel SAM), Tyler Meade, Matthew Stromberg as well as Mr. James F. Jacoby (vessel Miss Phebe II) and Mr. Steven Sablonski (vessel Copacetic) with help to collect ctenophores around the globe. This work was supported by the Human Frontiers Science Program (RGP0060/2017) and the National Science Foundation (IOS-1557923) grants to LLM. Research reported in this publication was also supported in part by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under award number R01NS114491 (to LLM). The content is solely the author’s responsibility and does not necessarily represent the official views of the National Institutes of Health.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leonid L. Moroz .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2024 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Moroz, L.L. (2024). Brief History of Ctenophora. In: Moroz, L.L. (eds) Ctenophores. Methods in Molecular Biology, vol 2757. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3642-8_1

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-3642-8_1

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-3641-1

  • Online ISBN: 978-1-0716-3642-8

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Navigation