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History of myxozoan character evolution on the basis of rDNA and EF-2 data.

Fiala I, Bartosová P - BMC Evol. Biol. (2010)

Bottom Line: Most bionomical and several morphological characters were found to be congruent with the phylogeny.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branisovská 31, 370 05 Ceské Budĕjovice, Czech Republic. fiala@paru.cas.cz

ABSTRACT

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.

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Matrix of myxozoan characters evaluated in the analysis of character evolution. Myxozoan ML tree based on SSU rDNA (GenBank AccNos. are behind the species names) is completed with character matrix, which is coded as follows: Number of valves: 0 - two, 1 - more than two. Shape of spore: 0 - spherical or subspherical, 1 - flattened sphere, 2 - ellipsoidal, 3 - flattened ellipsoid, 4 - banana or crescent, 4 - stellate, 5 - spindle, 6 - droplike. Ratio of dimensions of spore width to thickness: 0 - thickness larger than width, 1 - width larger than thickness, 2 - width equal to thickness. Surface ridges and striations: 0 - absent, 1 - present. Projections of the spore: 0 - no projections, 1 - caudal appendages, 2 - filamentous, 3 - bulges. Shape of suture line: 0 - straight, 1 - curved. Number of polar capsules (PCs): 0 - one, 1 - two, 2 - three, 3 - four, 4 - five and more. Orientation of PCs to a plane of the suture: 0 -PCs in the apex of the spore are set in the sutural plane, 1 - PCs are set in a plane essentially perpendicular to the suture plane. Location of PCs and sporoplasm: 0 -PCs at anterior part and sporoplasm posteriorly, 1 - PCs at opposite ends and sporoplasm in the middle. Shape of PCs: 0 - spherical or subspherical, 1 - pyriform. Position of anterior ends of PCs: 0 - convergent, 1 - divergent. Character of polar filament: 0 - tubular, 1 -flattened. Number of sporoplasms: 0 - one, 1 - two. Mucous envelope: 0 - absent, 1 - present. Membranaceous veil: 0 - absent, 1 - present. Vegetative stages: 0 -polysporic, 1 - small mono or disporic. Site of infection: 0 - coelozoic, 1 - histozoic. Site specificity: 0 - gall bladder and biliary ducts, 1 - renal tubules, 2 - urinary bladder, 3 - muscle, 4 - intestine, 5 - gills or pseudobranchs, 6 - without site specificity, 7 - nervous system, 8 - ovary, 9 - cartilage. Host: 0 - fish, 1 - amphibian, 2 - reptile, 3 - elasmobranchs, 4 - mammal, 5 - bird. Host environment: 0 - freshwater, 1 - marine, 2 - terrestrial.
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Figure 3: Matrix of myxozoan characters evaluated in the analysis of character evolution. Myxozoan ML tree based on SSU rDNA (GenBank AccNos. are behind the species names) is completed with character matrix, which is coded as follows: Number of valves: 0 - two, 1 - more than two. Shape of spore: 0 - spherical or subspherical, 1 - flattened sphere, 2 - ellipsoidal, 3 - flattened ellipsoid, 4 - banana or crescent, 4 - stellate, 5 - spindle, 6 - droplike. Ratio of dimensions of spore width to thickness: 0 - thickness larger than width, 1 - width larger than thickness, 2 - width equal to thickness. Surface ridges and striations: 0 - absent, 1 - present. Projections of the spore: 0 - no projections, 1 - caudal appendages, 2 - filamentous, 3 - bulges. Shape of suture line: 0 - straight, 1 - curved. Number of polar capsules (PCs): 0 - one, 1 - two, 2 - three, 3 - four, 4 - five and more. Orientation of PCs to a plane of the suture: 0 -PCs in the apex of the spore are set in the sutural plane, 1 - PCs are set in a plane essentially perpendicular to the suture plane. Location of PCs and sporoplasm: 0 -PCs at anterior part and sporoplasm posteriorly, 1 - PCs at opposite ends and sporoplasm in the middle. Shape of PCs: 0 - spherical or subspherical, 1 - pyriform. Position of anterior ends of PCs: 0 - convergent, 1 - divergent. Character of polar filament: 0 - tubular, 1 -flattened. Number of sporoplasms: 0 - one, 1 - two. Mucous envelope: 0 - absent, 1 - present. Membranaceous veil: 0 - absent, 1 - present. Vegetative stages: 0 -polysporic, 1 - small mono or disporic. Site of infection: 0 - coelozoic, 1 - histozoic. Site specificity: 0 - gall bladder and biliary ducts, 1 - renal tubules, 2 - urinary bladder, 3 - muscle, 4 - intestine, 5 - gills or pseudobranchs, 6 - without site specificity, 7 - nervous system, 8 - ovary, 9 - cartilage. Host: 0 - fish, 1 - amphibian, 2 - reptile, 3 - elasmobranchs, 4 - mammal, 5 - bird. Host environment: 0 - freshwater, 1 - marine, 2 - terrestrial.

Mentions: We mapped 15 morphological and 5 bionomical characters on the SSU rDNA tree, which was constructed to cover all known phylogenetic groups of myxosporeans. The matrix includes also five unnamed, formally not characterized species, since they represent significant morphotypes and phylogenetically important taxa for the clades in which these species cluster. The summary of all characters, features, and taxa used in this analysis is shown in Figure 3. We inferred a character history for each character using likelihood ancestral state reconstruction methods to understand the process of individual character change as well as the change of the spore as a complex of characters. Figure 4 summarizes the evolutionary history of myxospore morphology and the presumed switches among bionomical characters based upon this analysis. Cladograms in additional file 4 illustrate the particular character histories for all determined characters.


History of myxozoan character evolution on the basis of rDNA and EF-2 data.

Fiala I, Bartosová P - BMC Evol. Biol. (2010)

Matrix of myxozoan characters evaluated in the analysis of character evolution. Myxozoan ML tree based on SSU rDNA (GenBank AccNos. are behind the species names) is completed with character matrix, which is coded as follows: Number of valves: 0 - two, 1 - more than two. Shape of spore: 0 - spherical or subspherical, 1 - flattened sphere, 2 - ellipsoidal, 3 - flattened ellipsoid, 4 - banana or crescent, 4 - stellate, 5 - spindle, 6 - droplike. Ratio of dimensions of spore width to thickness: 0 - thickness larger than width, 1 - width larger than thickness, 2 - width equal to thickness. Surface ridges and striations: 0 - absent, 1 - present. Projections of the spore: 0 - no projections, 1 - caudal appendages, 2 - filamentous, 3 - bulges. Shape of suture line: 0 - straight, 1 - curved. Number of polar capsules (PCs): 0 - one, 1 - two, 2 - three, 3 - four, 4 - five and more. Orientation of PCs to a plane of the suture: 0 -PCs in the apex of the spore are set in the sutural plane, 1 - PCs are set in a plane essentially perpendicular to the suture plane. Location of PCs and sporoplasm: 0 -PCs at anterior part and sporoplasm posteriorly, 1 - PCs at opposite ends and sporoplasm in the middle. Shape of PCs: 0 - spherical or subspherical, 1 - pyriform. Position of anterior ends of PCs: 0 - convergent, 1 - divergent. Character of polar filament: 0 - tubular, 1 -flattened. Number of sporoplasms: 0 - one, 1 - two. Mucous envelope: 0 - absent, 1 - present. Membranaceous veil: 0 - absent, 1 - present. Vegetative stages: 0 -polysporic, 1 - small mono or disporic. Site of infection: 0 - coelozoic, 1 - histozoic. Site specificity: 0 - gall bladder and biliary ducts, 1 - renal tubules, 2 - urinary bladder, 3 - muscle, 4 - intestine, 5 - gills or pseudobranchs, 6 - without site specificity, 7 - nervous system, 8 - ovary, 9 - cartilage. Host: 0 - fish, 1 - amphibian, 2 - reptile, 3 - elasmobranchs, 4 - mammal, 5 - bird. Host environment: 0 - freshwater, 1 - marine, 2 - terrestrial.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2927925&req=5

Figure 3: Matrix of myxozoan characters evaluated in the analysis of character evolution. Myxozoan ML tree based on SSU rDNA (GenBank AccNos. are behind the species names) is completed with character matrix, which is coded as follows: Number of valves: 0 - two, 1 - more than two. Shape of spore: 0 - spherical or subspherical, 1 - flattened sphere, 2 - ellipsoidal, 3 - flattened ellipsoid, 4 - banana or crescent, 4 - stellate, 5 - spindle, 6 - droplike. Ratio of dimensions of spore width to thickness: 0 - thickness larger than width, 1 - width larger than thickness, 2 - width equal to thickness. Surface ridges and striations: 0 - absent, 1 - present. Projections of the spore: 0 - no projections, 1 - caudal appendages, 2 - filamentous, 3 - bulges. Shape of suture line: 0 - straight, 1 - curved. Number of polar capsules (PCs): 0 - one, 1 - two, 2 - three, 3 - four, 4 - five and more. Orientation of PCs to a plane of the suture: 0 -PCs in the apex of the spore are set in the sutural plane, 1 - PCs are set in a plane essentially perpendicular to the suture plane. Location of PCs and sporoplasm: 0 -PCs at anterior part and sporoplasm posteriorly, 1 - PCs at opposite ends and sporoplasm in the middle. Shape of PCs: 0 - spherical or subspherical, 1 - pyriform. Position of anterior ends of PCs: 0 - convergent, 1 - divergent. Character of polar filament: 0 - tubular, 1 -flattened. Number of sporoplasms: 0 - one, 1 - two. Mucous envelope: 0 - absent, 1 - present. Membranaceous veil: 0 - absent, 1 - present. Vegetative stages: 0 -polysporic, 1 - small mono or disporic. Site of infection: 0 - coelozoic, 1 - histozoic. Site specificity: 0 - gall bladder and biliary ducts, 1 - renal tubules, 2 - urinary bladder, 3 - muscle, 4 - intestine, 5 - gills or pseudobranchs, 6 - without site specificity, 7 - nervous system, 8 - ovary, 9 - cartilage. Host: 0 - fish, 1 - amphibian, 2 - reptile, 3 - elasmobranchs, 4 - mammal, 5 - bird. Host environment: 0 - freshwater, 1 - marine, 2 - terrestrial.
Mentions: We mapped 15 morphological and 5 bionomical characters on the SSU rDNA tree, which was constructed to cover all known phylogenetic groups of myxosporeans. The matrix includes also five unnamed, formally not characterized species, since they represent significant morphotypes and phylogenetically important taxa for the clades in which these species cluster. The summary of all characters, features, and taxa used in this analysis is shown in Figure 3. We inferred a character history for each character using likelihood ancestral state reconstruction methods to understand the process of individual character change as well as the change of the spore as a complex of characters. Figure 4 summarizes the evolutionary history of myxospore morphology and the presumed switches among bionomical characters based upon this analysis. Cladograms in additional file 4 illustrate the particular character histories for all determined characters.

Bottom Line: Most bionomical and several morphological characters were found to be congruent with the phylogeny.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branisovská 31, 370 05 Ceské Budĕjovice, Czech Republic. fiala@paru.cas.cz

ABSTRACT

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.

Show MeSH
Related in: MedlinePlus