BACKGROUND: Phylogenetic relationships among myxosporeans based on ribosomal DNA data disagree with traditional taxonomic classification: a number of myxosporeans with very similar spore morphology are assigned to the same genera even though they are phylogenetically distantly related. The credibility of rDNA as a suitable marker for Myxozoa is uncertain and needs to be proved. Furthermore, we need to know the history of myxospore evolution to understand the great diversity of modern species. RESULTS: Phylogenetic analysis of elongation factor 2 supports the ribosomal DNA-based reconstruction of myxozoan evolution. We propose that SSU rDNA is a reliable marker for inferring myxozoan relationships, even though SSU rDNA analysis markedly disagrees with the current taxonomy. The analyses of character evolution of 15 morphological and 5 bionomical characters show the evolution of individual characters and uncover the main evolutionary changes in the myxosporean spore morphology and bionomy. Most bionomical and several morphological characters were found to be congruent with the phylogeny. The summary of character analyses leads to the simulation of myxozoan ancestral morphotypes and their evolution to the current species. As such, the ancestor of all myxozoans appears to have infected the renal tubules of freshwater fish, was sphaerosporid in shape, and had a spore with polar capsules that discharged slightly sideways. After the separation of Malacosporea, the spore of the common myxosporean ancestor then changed to the typical sphaerosporid morphotype. This species inhabited the marine environment as a parasite of the gall bladder of marine fish and ultimately separated into the three main myxosporean lineages evident today. Two of these lineages re-entered the freshwater environment, one as a myxosporean with Chloromyxum and another with a primitive sphaerosporid morphotype. The common ancestor of all marine myxosporeans had a ceratomyxid shape of spore. CONCLUSIONS: We support rDNA based myxozoan phylogeny by the analysis of a protein coding gene and demonstrate the reliability of rDNA as a marker explaining myxozoan relationships. Our tracing the history of myxozoan character evolution discloses ancestral morphotypes and shows their development over the course of evolution. We point out several myxozoan characters that are to a certain extent congruent with the phylogeny and determined that the discrepancy between phylogeny and current taxonomy based on spore morphology is due to an extreme myxospore plasticity occurring during myxozoan evolution.

Institute of Parasitology Biology Centre Academy of Sciences of the Czech Republic Branisovská 31 370 05 Ceské Budĕjovice Czech Republic

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Monteiro AS, Okamura B, Holland PWH. Orphan worm finds a home: Buddenbrockia is a myxozoan. Molecular Biology and Evolution. 2002;19(6):968–971. PubMed

Smothers JF, Vondohlen CD, Smith LH, Spall RD. Molecular evidence that the myxozoan protists are metazoans. Science. 1994;265(5179):1719–1721. doi: 10.1126/science.8085160. PubMed DOI

Stolc A. Actinomyxidies, nouveau groupe de Mesozoaires parent des Myxosporidies. Bull Intl Acad Sci Boheme. 1899;22:1–12.

Weill R. L 'interpretation des Cnidosporidies et Ia valeur taxonomique de Ieur cnidome. Leur cycle comparé ii Ia phase Iarvaire des Narcomeduses Cuninides. Travaux de la Station Zoologique de Wimereaux. 1938;13:727–744.

Siddall ME, Martin DS, Bridge D, Desser SS, Cone DK. The demise of a phylum of protists: Phylogeny of myxozoa and other parasitic cnidaria. Journal of Parasitology. 1995;81(6):961–967. doi: 10.2307/3284049. PubMed DOI

Hanelt B, VanSchyndel D, Adema CM, Lewis LA, Loker ES. The phylogenetic position of Rhopalura ophiocomae (Orthonectida) based on 18 S ribosomal DNA sequence analysis. Molecular Biology and Evolution. 1996;13(9):1187–1191. PubMed

Siddall ME, Whiting MF. Long-branch abstractions. Cladistics-the International Journal of the Willi Hennig Society. 1999;15(1):9–24. doi: 10.1111/j.1096-0031.1999.tb00391.x. DOI

Jimenez-Guri E, Philippe H, Okamura B, Holland PWH. Buddenbrockia is a Cnidarian worm. Science. 2007;317(5834):116–118. doi: 10.1126/science.1142024. PubMed DOI

Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J. et al.Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology. 2001;48(4):395–413. doi: 10.1111/j.1550-7408.2001.tb00173.x. PubMed DOI

Holzer AS, Sommerville C, Wootten R. Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18 S rDNA sequences. International Journal for Parasitology. 2004;34(10):1099–1111. doi: 10.1016/j.ijpara.2004.06.002. PubMed DOI

Fiala I. The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology. 2006;36(14):1521–1534. doi: 10.1016/j.ijpara.2006.06.016. PubMed DOI

Nei M, Kumar S, Takahashi K. The optimization principle in phylogenetic analysis tends to give incorrect topologies when the number of nucleotides or amino acids used is small. Proceedings of the National Academy of Sciences of the United States of America. 1998;95(21):12390–12397. doi: 10.1073/pnas.95.21.12390. PubMed DOI PMC

Philippe H, Germot A. Phylogeny of eukaryotes based on ribosomal RNA: Long-branch attraction and models of sequence evolution. Molecular Biology and Evolution. 2000;17(5):830–834. PubMed

Whipps CM, Grossel G, Adlard RD, Yokoyama H, Bryant MS, Munday BL, Kent ML. Phylogeny of the multivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. Journal of Parasitology. 2004;90(3):618–622. doi: 10.1645/GE-153R. PubMed DOI

Whipps CM, Kent ML. Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea) Journal of Eukaryotic Microbiology. 2006;53(5):364–373. doi: 10.1111/j.1550-7408.2006.00114.x. PubMed DOI

Bartosova P, Fiala I, Hypsa V. Concatenated SSU and LSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxosporea) and provide an effective tool for their molecular phylogenetics. Molecular Phylogenetics and Evolution. 2009;53(1):81–93. doi: 10.1016/j.ympev.2009.05.018. PubMed DOI

Holzer AS, Wootten R, Sommerville C. The secondary structure of the unusually long 18 S ribosomal RNA of the myxozoan Sphaerospora truttae and structural evolutionary trends in the Myxozoa. International Journal for Parasitology. 2007;37(11):1281–1295. doi: 10.1016/j.ijpara.2007.03.014. PubMed DOI

Marotta R, Ferraguti M, Erséus C, Gustavsson LM. Combined-data phylogenetics and character evolution of Clitellata (Annelida) using 18 S rDNA and morphology. Zoological Journal of the Linnean Society. 2008;154:1–26. doi: 10.1111/j.1096-3642.2008.00408.x. DOI

Vossbrinck CR, Debrunner-Vossbrinck BA. Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitologica. 2005;52(1-2):131–142. PubMed

Kent ML, Khattra J, Hedrick RP, Devlin RH. Tetracapsula renicola n. sp (Myxozoa: Saccosporidae); The PKX myxozoan - The cause of proliferative kidney disease of salmonid fishes. Journal of Parasitology. 2000;86(1):103–111. doi: 10.1645/0022-3395(2000)086[0103:TRNSMS]2.0.CO;2. PubMed DOI

Andree KB, El-Matbouli M, Hoffman RW, Hedrick RP. Comparison of 18 S and ITS-1 rDNA sequences of selected geographic isolates of Myxobolus cerebralis. International Journal for Parasitology. 1999;29(5):771–775. doi: 10.1016/S0020-7519(99)00035-1. PubMed DOI

Eszterbauer E. Genetic relationship among gill-infecting Myxobolus species (Myxosporea) of cyprinids: molecular evidence of importance of tissue-specificity. Diseases of Aquatic Organisms. 2004;58(1):35–40. doi: 10.3354/dao058035. PubMed DOI

Shulman SS. Myxosporidia of the fauna of the USSR. Moscow: Nauka; 1966.

Koie M, Karlsbakk E. Ellipsomyxa syngnathi sp n. (Myxozoa, Myxosporea) in the pipefish Syngnathus typhle and S. rostellatus (Teleostei, Syngnathidae) from Denmark. Parasitology Research. 2009;105(6):1611–1616. doi: 10.1007/s00436-009-1598-3. PubMed DOI

Gunter N, Adlard R. The demise of Leptotheca Thelohan, 1895 (Myxozoa: Myxosporea: Ceratomyxidae) and assignment of its species to Ceratomyxa Thelohan, 1892 (Myxosporea: Ceratomyxidae), Ellipsomyxa Koie, 2003 (Myxosporea: Ceratomyxidae), Myxobolus Butschli, 1882 and Sphaerospora Thelohan, 1892 (Myxosporea: Sphaerosporidae) Systematic Parasitology. 2010;75(2):81–104. doi: 10.1007/s11230-009-9227-1. PubMed DOI

Jirku M, Fiala I, Modry D. Tracing the genus Sphaerospora: rediscovery, redescription and phylogeny of the Sphaerospora ranae (Morelle, 1929) n. comb. (Myxosporea, Sphaerosporidae), with emendation of the genus Sphaerospora. Parasitology. 2007;134:1727–1739. doi: 10.1017/S0031182007003241. PubMed DOI

Lom J, Dykova I. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica. 2006;53(1):1–36. PubMed

Gunter NL, Whipps CM, Adlard RD. Ceratomyxa (Myxozoa: Bivalvulida): Robust taxon or genus of convenience? International Journal for Parasitology. 2009;39(12):1395–1405. doi: 10.1016/j.ijpara.2009.04.008. PubMed DOI

Hashimoto T, Nakamura Y, Kamaishi T, Nakamura F, Adachi J, Okamoto K, Hasegawa M. Phylogenetic place of mitochondrial-lacking protozoan, Giardia lamblia inferred from amino-acid sequences of elongation factor 2. Molecular Biology and Evolution. 1995;12(5):782–793. PubMed

Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research. 2002;30(14):3059–3066. doi: 10.1093/nar/gkf436. PubMed DOI PMC

Galtier N, Gouy M, Gautier C. SEAVIEW and PHYLO_WIN: Two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences. 1996;12(6):543–548. PubMed

Swofford DL. PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods), Version 4.0b8. Sunderland, Massachusetts: Sinauer Associates; 2001.

Zwickl DJ. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas at Austin; 2006.

Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817–818. doi: 10.1093/bioinformatics/14.9.817. PubMed DOI

Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572–1574. doi: 10.1093/bioinformatics/btg180. PubMed DOI

AWTY: A system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. http://ceb.csit.fsu.edu/awty PubMed

Rambaut A, Drummond AJ. Tracer v1.4. 2007. http://beast.bio.ed.ac.uk/Tracer

Mesquite: a modular system for evolutionary analysis. Version 2.5. http://mesquiteproject.org

Schluter D, Price T, Mooers AO, Ludwig D. Likelihood of ancestor states in adaptive radiation. Evolution. 1997;51(6):1699–1711. doi: 10.2307/2410994. PubMed DOI

Intraspecific Morphometric Variation in a New Species of Ceratomyxa Thélohan 1892 (Cnidaria) from the South Atlantic Ocean: An Ecomorphological Study Using Geometric Morphometrics

Genetic Diversity of Serine Protease Inhibitors in Myxozoan (Cnidaria, Myxozoa) Fish Parasites

The description of two new species of Chloromyxum from skates in the Argentine Sea reveals that a limited geographic host distribution causes phylogenetic lineage separation of myxozoans in Chondrichthyes

Biodiversity and host-parasite cophylogeny of Sphaerospora (sensu stricto) (Cnidaria: Myxozoa)

Species complexes and phylogenetic lineages of Hoferellus (Myxozoa, Cnidaria) including revision of the genus: A problematic case for taxonomy

Myxozoa in high Arctic: Survey on the central part of Svalbard archipelago