Abstract
Now that we have strong evidence for the phylogenetic placement of Myxozoa within the Cnidaria it is of great interest to explore their evolutionary history. In particular, what cnidarian features may have facilitated the transition to an endoparasitic lifestyle and can we identify a potential cnidarian sister group? In this chapter we summarise evidence for characters linking myxozoans to cnidarians and identify cnidarian traits that may have promoted endoparasitism including: their diploblastic condition, their capacity for regeneration, transdifferentiation, and dormancy, the production of novel propagative stages, cell-within-cell development, and asexual reproduction. Equating the basic cnidarian life cycle (benthic polyps and planktonic medusae) with the complex myxozoan life cycle is problematic because of great plasticity in cnidarian development, which can entail the loss of stages and associated transfer of function. The sexual phase of myxozoans involves the production of isogametes but divergent views on their subsequent fusion lead to questions about whether sexual reproduction involves selfing or outcrossing and if it may result in the development of multicellular chimaeras. The apical structures of myxozoan polar capsules closely resemble those of medusozoan but not those of anthozoan nematocysts, thus supporting a medusozoan affinity for Myxozoa.
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References
Abd-Elfattah A, Fontes I, Kumar G, Soliman H, Hartikainen H, Okamura B, El-Matbouli M (2014) Vertical transmission of Tetracapsuloides bryosalmonae (Myxozoa), the causative agent of salmonid proliferative kidney disease. Parasitology 141:482–490
Aerne B, Stidwill R, Tardent P (1991) Nematocyst discharge in Hydra does not require the presence of nerve cells. J Exp Zool 141:137–141
Agrawal AF, Lively CM (2001) Parasites and the evolution of self-fertilization. Evolution 55:869–879
Arai MN (2009) The potential importance of podocysts to the formation of scyphozoan blooms: a review. Hydrobiologia 616:241–246
Bavestrello G, Sommer C, Sarà M (1992) Bi-directional conversion in Turritopsis nutricula (Hydrozoa). Sci Mar 56:137–140
Beckmann A, Özbek S (2012) The nematocyst: a molecular map of the cnidarian stinging organelle. Int J Dev Biol 56:577–582. doi:10.1387/ijdb.113472ab
Bernstein H, Bernstein C, Monod RE (2011) Meiosis as an evolutionary adaptation for DNA repair. In: Kruman I (ed) DNA Repair, InTech
Billiard S, López-Villavicencio M, Devier B, Hood ME, Fairhead C, Giraud T (2011) Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biol Rev 86:421–442
Boero F, Bouillon J, Piraino S (1992) On the origins and evolution of hydromedusan life cycles (Cnidaria, Hydrozoa). In: Dallai R (ed) Sex origin and evolution. Symposia and Monographs U.Z.I, vol 6, pp 59–68
Boero F, Bouillon J, Piraino S, Schmid V (2002) Asexual reproduction in the Hydrozoa (Cnidaria). In: RN Hughes (ed) Reproductive biology of invertebrates. Progress in asexual reproduction, vol XI. Oxford & IBH Publishing Co. Pvt. Ltd, New Delhi, pp 141–158
Boero F, Hewitt CL (1992) A hydrozoan, Zanclella bryozoophila n. gen., n. sp. (Zancleidae), symbiotic with a bryozoan, with a discussion of the Zancleoidea. Can J Zool 70:1645–1651
Bosch TCG (2008) Stem cells in immortal Hydra. In: Bosch TCG (ed) Stem cells. From Hydra to man. Springer Netherlands, Berlin, pp 37–57
Bouillon J, Medeal MD, Pages F, Gili J-M, Boero F, Gravili C (2004). Fauna of the Mediterranean Hydrozoa. Sci Mar 68(Suppl 2):5–438
Brooks DR, McLennan DA (1993) Parascript: Parasites and the language of evolution. Smithsonian Institution Press, Washington DC
Brown SP, Renaud F, Guégan J-F, Thomas F (2001) Evolution of trophic transmission in parasites: the need to reach a mating place? J Evol Biol 14:815–820
Canning EU, Curry A, Feist SW, Longshaw M, Okamura B (2000) A new class and order of myxozoans to accommodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). J Eukaryot Microbiol 47:456–468
Canning EU, Curry A, Hill SLL, Okamura B (2007) Ultrastructure of Buddenbrockia allmani n. sp. (Myxozoa, Malacosporea), a parasite of Lophopus crystallinus (Bryozoa, Phylactolaemata). J Eukaryot Microbiol 54:247–262
Canning EU, Curry A, Okamura B (2008) Early development of the myxozoan Buddenbrockia plumatellae in the bryozoans Hyalinella punctata and Plumatella fungosa, with comments on taxonomy and systematics of the Myxozoa. Folia Parasit 45:241–255
Canning EU, Okamura B (2004) Biodiversity and evolution of the Myxozoa. Adv Parasitol 56:43–131
Canning EU, Tops S, Curry A, Wood TS, Okamura B (2002) Ecology, development and pathogenicity of Buddenbrockia plumatellae Schröder, 1910 (Myxozoa, Malacosporea) (syn. Tetracapsula bryozoides) and establishment of Tetracapsuloides n. gen. for Tetracapsula bryosalmonae. J Eukaryot Microbiol 49:280–295
Cannon Q, Wagner E (2003) Comparison of discharge mechanisms of cnidarian cnidae and cyxozoan polar capsules. Rev Fish Sci 11:185–219
Carré C, Carré C (1990) Complex reproductive cycle in Eucheilota paradoxica (Hydrozoa: Leptomedusae): medusae, polyps and frustules produced from medusa stage. Mar Biol 104:303–310
Casal G, Costa G, Azevedo C (2007) Ultrastructural description of Ceratomyxa tenuispora (Myxozoa), a parasite of the marine fish Aphanopus carbo (Trichiuridae), from the Atlantic coast of Madeira Island (Portugal). Folia Parasit 54:165–171
Chapman GB, Tilney LG (1959a) Cytological studies of the nematocysts of Hydra. I. Desmonemes, isorhizas, cnidocils, and supporting structures. J Biophys Biochem Cytol 5:69–78
Chapman GB, Tilney LG (1959b) Cytological studies of the nematocysts of Hydra. II. The stenoteles. J Biophys Biochem Cytol 5:79–84
Collins AG, Schuchert P, Marques AC, Jankowski T, Medina M, Schierwater B (2006) Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst Biol 55:97–115
Crnokrak P, Barrett SC (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358
Czaker R (2011) Dicyemid’s dilemma: structure versus genes. The unorthodox structure of dicyemid reproduction. Cell Tissue Res 343:649–658
David CN, Özbek S, Adamczyk P, Meier S, Pauly B, Chapman J, Hwang JS, Gojobori T, Holstein TW (2008) Evolution of complex structures: minicollagens shape the cnidarian nematocyst. Trends Genet 24:431–438
de Kinkelin P, Gay M, Forman S (2002) The persistence of infectivity of Tetracapsula bryosalmonae-infected water for rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 25:477–482
Desser SS, Molnar K, Weller I (1983) Ultrastructure of sporogenesis of Thelohanellus nikolskii Akhmerov, 1955 (Myxozoa: Myxosporea) from the common carp, Cyprinus carpio. J Parasitol 69:504–518
El-Matbouli M, Hoffmann RW (1991) Effects of freezing, aging, and passage through the alimentary canal of predatory animals on the viability of Myxobolus cerebralis spores. J Aquat Anim Health 3:260–262
El-Matbouli M, Hoffmann RW (1998) Light and electron microscopic studies on the chronological development of Myxobolus cerebralis to the actinosporean stage in Tubifex tubifex. Int J Parasitol 28:195–217
Fautin DG (1991) Developmental pathways of anthozoans. Hydrobiologia 216(217):143–149
Fautin DG (2002) Reproduction of Cnidaria. Can J Zool 80:1735–1754
Fautin DG (2009) Structural diversity, systematics, and evolution of cnidae. Toxicon 54:1054–1064
Feist SW, Longshaw M (2006) Phylum Myxozoa. In: Fish diseases and disorders. Protozoan and metazoan infections, vol. 1, 2nd ed. CABI Publishing, Wallingford, pp 230–296
Ferguson JC (1982) A comparative study of the net metabolic benefits derived from the uptake and release of free amino acids by marine invertebrates. Biol Bull 162:1–17
Furuya H, Tsuneki K (2007) Developmental patterns of the hermaphroditic gonad in dicyemid mesozoans (Phylum Dicyemida). Inv Biol 126:295–306
Grover, R Marguer JF, Allemand D, Ferrier-Pagès (2008) Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata. J Exp Biol 211:860–865
Gruhl A, Okamura B (2012) Development and myogenesis of the vermiform Buddenbrockia (Myxozoa) and implications for cnidarian body plan evolution. EvoDevo 3:10. doi:10.1186/2041-9139-3-10
Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35:282–290
Hausmann K (1978) Extrusive organelles in protists. Int Rev Cytol 52:197–276
Hausmann K (2002) Review food acquisition, food ingestion and food digestion by protists. Jpn J Protozool 35:85–95
Hessinger DA, Ford MT (1988) Ultrastructure of the small cnidocyte of the Portuguese man-of-war (Physalia physalis) tentacle. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, New York, pp 75–94
Heyward AJ, Babcock RC (1986) Self and cross fertilisation in scleractinian corals. Mar Biol 90:191–195
Hill SLL, Okamura B (2007) Endoparasitism in colonial hosts: patterns and processes. Parasitology 134:841–852
Hinsch GW, Moore JA (1992) The structure of the reproductive mesenteries of the sea anemone Ceriantheopsis americanus. Invertebr Reprod Dev 21:25–32
Holland JW, Okamura B, Hartikainen H, Secombes CJ (2011) A novel minicollagen gene links cnidarians and myxozoans. Proc Roy Soc Ser B 278:546–553
Holstein T, Hausmann K (1988) The cnidocil apparatus of hydrozoans: a progenitor of higher metazoan mechanoreceptors. In: Hessinger DA, Lenhoff HM (eds) Biology of nematocysts. Academic Press, San Diego, pp 53–73
Holstein TW (2012) A view to kill. BMC Biology 10:18
Hoppenrath M, Yubuki N, Bachvaroff TR, Leander BS (2010) Re-classification of Pheopolykrikos hartmannii as Polykrikos (Dinophyceae) based partly on the ultrastructure of complex extrusomes. Eur J Protistol 46:29–37
Hurst LD, Hamilton WD (1992) Cytoplasmic fusion and the nature of the sexes. Proc R Soc B 247:189–194
Hwang JS, Nagai S, Hayakawa S, Takaku Y, Gojobori T (2008) The search for the origin of cnidarian nematocysts in dinoflagellates. In: Pontarotti P (ed) Evolutionary biology from concept to application. Springer, Berlin, pp 135–152
Jaenike J (1978) An hypothesis to account for the maintenance of sex within populations. Evol Theor 3:191–194
Kallert DM, Bauer W, Haas W, El-Matbouli M (2011) No shot in the dark: myxozoans chemically detect fresh fish. Int J Parasitol 41:271–276
Kallert DM, El-Matbouli M, Haas W (2005) Polar filament discharge of Myxobolus cerebralis actinospores is triggered by combined non-specific mechanical and chemical cues. Parasitology 131:609–616
Kallert DM, Ponader S, Adelt S, Kaese P, Geyer R, Haas W, El-Matbouli M (2010) Analysis of rainbow trout Oncorhynchus mykiss epidermal mucus and evaluation of semiochemical activity for polar filament discharge in Myxobolus cerebralis actinospores. J Fish Biol 77:1579–1598
Kayal E, Roure B, Philippe H, Collins AG, Lavrov DV (2013) Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evol Biol 13:5. doi:10.1186/1471-2148-13-5
Kent ML, Khattra J, Hedrick RP, Devlin RH (2000) Tetracapsula renicola n. sp. (Myxozoa: Saccosporidae); the PKD myxozoan-the cause of proliferative kidney disease of salmonid fish. J Parasitol 86:103–111
Kubota S (2011) Repeating rejuvenation in Turritopsis, an immortal hydrozoan (Cnidaria, Hydrozoa). Biogeography 13:101–103
Levitan DR (1993) The importance of sperm limitation to the evolution of egg size in marine invertebrates. Amer Nat 141:517–536
Lom J (1990) Phylum Myxozoa. In: Margulis L, Corliss JO, Melkonian M, Chapman DJ (eds) Handbook of Protoctista. Jones and Bartlett, Boston, pp 36–52
Lom J, Dyková I (1997) Ultrastructural features of the actinosporean phase of Myxosporea (Phylum, Myxozoa): a comparative study. Acta Protozool 36:83–103
Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasit 53:1–36
Lom J, Yokoyama H, Dyková I (1997) Comparative ultrastructure of Aurantiactinomyxon and Raabeia, actinosporean stages of myxozoan life cycles. Arch Protistenkd 148:173–189
Mali B, Millane C, Plickert G, Frohme M, Frank U (2011) A polymorphic, thrombospondin domain-containing lectin is an oocyte marker in Hydractinia: implications for germ cell specification and sex determination. Int J Dev Biol 55:103–108
Mariscal RN (1974) Nematocysts. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology: reviews and new perspectives. Academic Press, New York, pp 129–178
Mariscal RN (1984) Cnidaria: Cnidae. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument. Invertebrates, vol I. Springer, New York, pp 57–68
Marquès A (1987) La sexualité chez les Actinomyxidies: étude chez Neoactinomyxon eiseniellae (Ormières et Frézil, 1969), Actinosporea, Noble, 1980; Myxozoa, Grassé, 1970. Ann Sci Nat Zool Paris 8:81–101
McGurk C, Morris DJ, Auchinachie NA, Adams A (2006) Development of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) in bryozoan hosts (as examined by light microscopy) and quantitation of infective dose to rainbow trout (Oncorhynchus mykiss). Vet Parasitol 135:249–257
McKinney FK (2009) Bryozoan-hydroid symbiosis and a new ichnogenus, Caupokeras. Ichnos 16:193–201
Michod RE, Bernstein H, Nedelcu AM (2008) Adaptive value of sex in microbial pathogens. Infect Genet Evol 8:267–285
Mikrjukov KA (1995) Structure, function, and formation of extrusive organelles—microtoxicysts in the rhizopod Penardia cometa. Protoplasma 188:186–191
Milde S, Hemmrich G, Anton-Erxleben F, Khalturin K, Wittlieb J, Bosch TCG (2009) Characterization of taxonomically restricted genes in a phylum-restricted cell type. Genome Biol 10:8
Miller K, Grange K (1997) Population genetic studies of antipatharian black corals from Doubtful and Nancy Sounds, Fiordland, New Zealand. In: Proceedings of the 6th international conference on coelenterate biology. The Leeuwenhorst, Nordwijkerhout, The Netherlands, 16–21 July 1995. Nationaal Natuurhistorisch Museum, Leiden, The Netherlands, pp 271–278
Moebius K (1866) Über den Bau, den Mechanismus und die Entwicklung der Nesselkapseln einiger Polypen und Quallen. Abh naturwiss Verein in Hamburg 5:1–22
Morandini AC, Marques AC (2010) Revision of the genus Chrysaora Péron & Lesueur, 1810 (Cnidaria: Scyphozoa). Zootaxa 2464:1–97
Morran LT, Parmenter MC, Phillips PC (2009) Mutation load and rapid adaptation favour outcrossing over self-fertilization. Nature 462:350–352
Morran LT, Schmidt OG, Gelarden IA, Parrish RC II, Lively CM (2011) Running with the red queen: host-parasite coevolution selects for biparental sex. Science 333:216–218
Morris DJ (2012) A new model for myxosporean (Myxozoa) development explains the endogenous budding phenomenon, the nature of cell within cell life stages and the evolution of parasitism from a cnidarian ancestor. Int J Parasitol 42:829–840
Morris DJ, Freeman MA (2010) Hyperparasitism has wide-ranging implications for studies on the invertebrate phase of myxosporean (Myxozoa) life cycles. Int J Parasitol 40:357–369
Okamura B (1996) Occurrence, prevalence, and effects of the myxozoan Tetracapsula bryozoides Canning, Okamura and Curry, 1996, parasitic in the freshwater bryozoan Cristatella mucedo Cuvier (Bryozoa, Phylactolaemata). Folia Parasit 43:262–266
Okamura B, Curry A, Wood TS, Canning EU (2002) Ultrastructure of Buddenbrockia identifies it as a myxozoan and verifies the bilaterian origin of the Myxozoa. Parasitology 124:215–223
Özbek S (2011) The cnidarian nematocyst: a miniature extracellular matrix within a secretory vesicle. Protoplasma 248:635–640
Park E, Hwang D-S, Lee J-S, Song J-I, Seo T-K, Won Y-J (2012) Estimation of divergence times in cnidarian evolution based on mitochondrial protein-coding genes and the fossil record. Mol Phylogenet Evol 62:329–345
Parker GA, Baker RR, Smith VGF (1972) The origin and evolution of gamete dimorphism and the male-female phenomenon. J Theor Biol 36:529–553
Pearse VB (2001) Prodigies of propagation: the many modes of clonal replication in boloceroidid sea anemones (Cnidaria, Anthozoa, Actiniaria). Inv Repr Dev 41:201–213
Piraino S, Boero F, Aeschbach B, Schmid V (1996) Reversing the life cycle: medusae transforming into polyps and cell transdifferentiation in Turritopsis nutricula (Cnidaria, Hydrozoa). Biol Bull 190:302–312
Piraino S, De Vito D, Schmich J, Bouillon J, Boero F (2004) Reverse development in Cnidaria. Can J Zool 82:1748–1754
Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton, NJ
Puill-Stephan E, van Oppen MJH, Pichavant-Rafini K, Willis BL (2012) High potential for formation and persistence of chimeras following aggregated larval settlement in the broad cast spawning coral, Acropora millepora. Proc R Soc B 279:699–708
Raikova EV (2008) Cytological peculiarities of Polypodium hydriforme (Cnidaria). J Mar Biol Assoc UK 88:1695–1702
Rangel LF, Cech G, Szekely C, Santos MY (2011) A new actinosporean type Unicapsulactinomyxon (Myxozoa) infecting the marine polychaete, Diopatra neapolitana (Polychaeta: Onuphidae) in the Aveiro Estuary (Portugal). Parasitol 138:698–712
Rauch G, Kalbe M, Reusch BH (2005) How a complex life cycle can improve a parasite’s sex life. J Evol Biol 18:1069–1075
Reft AJ, Daly M (2012) Morphology, distribution, and evolution of apical structure of nematocysts in hexacorallia. J Morphol 273:121–136
Ringuette MJ, Koehler A, Desser SS (2011) Shared antigenicity between the polar filaments of myxosporeans and other Cnidaria. J Parasitol 97:163–166
Ruppert EE, Fox RS, Barnes RD (2004) Invertebrate zoology. A functional evolutionary appoach, 7th edn. Brooks/Cole-Thomson Learning, Belmont
Schlesinger A, Kramarsky-Winter E, Rosenfeld H, Armoza-Zvoloni R, Loya Y (2010) Sexual plasticity and self-fertilization in the sea anemone Aiptasia diaphana. PLoS ONE 5(7):e11874. doi:10.1371/journal.pone.0011874
Sherlock RE, Robison BH (2000) Effects of temperature on the development and survival of Nanomia bijuga (Hydrozoa, Siphonophora). Inv Biol 119:379–385
Shostak S, Kolluri V (1995) Symbiogenetic origins of cnidarian cnidocysts. Symbiosis 19:1–29
Shul’man SS (1990) Myxosporidia of the USSR. Russian Translations Series 75. Balkema AA, Rotterdam
Siddall ME, Martin DS, Bridge D, Desser SS, Cone DK (1995) The demise of a phylum of protists: phylogeny of Myxozoa and other parasitic cnidaria. J Parasitol 81:961–967
Takabayashi N, Morrell PL (2001) Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. Am J Bot 88:1143–1150
Tops S, Curry A, Okamura B (2005) Diversity and systematics of the Malacosporea (Myxozoa). Inv Biol 124:285–295
Weill R (1934) Contribution à l’étude des cnidaires et de leurs nématocystes. Trav Sta Zool Wimereux 10(11):1–701
Werner B (1963) Effect of some environmental factors on differentiation and determination in marine Hydrozoa, with a note on their evolutionary significance. Ann New York Acad Sc 105:461–488
Westfall JA (1965) Nematocysts of the sea anemone Metridium. Am Zool 5:377–393
Westfall JA (1966) The differentiation of nematocysts and associated structures in the Cnidaria. Z Zellforsch Mikrosk Anat 75:381–403
Westfall JA, Bradbury PC, Townsend JW (1983) Ultrastructure of the dinoflagellate Polykrikos. J Cell Sci 63:245–261
Woolsey E (2012) Self-fertilization suppresses thermal tolerance in embryos of reef-building coral. In: Yellowlees D, Hughes TP (eds) Proceedings of the 12th international coral reef symposium. James Cook University, Cairns
Acknowledgments
We thank Stephen Atkinson for images of myxosporean polar capsules and Stephen Feist for image of plasmotomy. We are also grateful to Alan Curry for ultrastructural documentation of malacosporean development over many years, including several images incorporated here. Work on polar capsules was supported by a Marie Curie Intra-European Fellowship (272772) to Alexander Gruhl and Beth Okamura. Ultrastructural investigations of malacosporeans were supported by the Natural Environment Research Council (GR3/11065, GR3/11068, NER/A/S/1999/00075, NER/B/S/2000/00336) and the Department of Environment, Food and Rural Affairs (FC 1112). Work on nematocysts was supported by NSF postdoctoral grant (PRFB-130664) directed to Abigail J Reft and NSF grant (EF-0531763) to Marymegan Daly (Ohio State University).
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Okamura, B., Gruhl, A., Reft, A.J. (2015). Cnidarian Origins of the Myxozoa. In: Okamura, B., Gruhl, A., Bartholomew, J. (eds) Myxozoan Evolution, Ecology and Development. Springer, Cham. https://doi.org/10.1007/978-3-319-14753-6_3
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