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

. 2018 Jun 15 ; 11 (1) : 347. [epub] 20180615

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid29903034

Grantová podpora
505/12/G112 Czech Science Foundation
16-20744S Czech Science Foundation
634429 H2020 European Research Council
K112301 Hungarian National Research, Development and Innovation Office

Odkazy

PubMed 29903034
PubMed Central PMC6002976
DOI 10.1186/s13071-018-2863-z
PII: 10.1186/s13071-018-2863-z
Knihovny.cz E-zdroje

BACKGROUND: Myxozoa are extremely diverse microscopic parasites belonging to the Cnidaria. Their life-cycles alternate between vertebrate and invertebrate hosts, predominantly in aquatic habitats. Members of the phylogenetically well-defined Sphaerospora (sensu stricto) clade predominantly infect the urinary system of marine and freshwater fishes and amphibians. Sphaerosporids are extraordinary due to their extremely long and unique insertions in the variable regions of their 18S and 28S rDNA genes and due to the formation of motile proliferative stages in the hosts' blood. To date, DNA sequences of only 19 species have been obtained and information on the patterns responsible for their phylogenetic clustering is limited. METHODS: We screened 549 fish kidney samples from fish of various geographical locations, mainly in central Europe, to investigate sphaerosporid biodiversity microscopically and by 18S rDNA sequences. We performed multiple phylogenetic analyses to explore phylogenetic relationships and evolutionary trends within the Sphaerospora (s.s.) clade, by matching host and habitat features to the resultant 18S rDNA trees. The apparent co-clustering of species from related fish hosts inspired us to further investigate host-parasite co-diversification, using tree-based (CoRE-PA) and distance-based (ParaFit) methods. RESULTS: Our study considerably increased the number of 18S rDNA sequence data for Sphaerospora (s.s.) by sequencing 17 new taxa. Eight new species are described and one species (Sphaerospora diminuta Li & Desser, 1985) is redescribed, accompanied by sufficient morphological data. Phylogenetic analyses showed that sphaerosporids cluster according to their vertebrate host order and habitat, but not according to geography. Cophylogenetic analyses revealed a significant congruence between the phylogenetic trees of sphaerosporids and of their vertebrate hosts and identified Cypriniformes as a host group of multiple parasite lineages and with high parasite diversity. CONCLUSIONS: This study significantly contributed to our knowledge of the biodiversity and evolutionary history of the members of the Sphaerospora (s.s.) clade. The presence of two separate phylogenetic lineages likely indicates independent historical host entries, and the remarkable overlap of the larger clade with vertebrate phylogeny suggests important coevolutionary adaptations. Hyperdiversification of sphaerosporids in cypriniform hosts, which have undergone considerable radiations themselves, points to host-driven diversification.

Zobrazit více v PubMed

Zhang ZQ. Animal biodiversity: An introduction to higher-level classification and taxonomic richness. Zootaxa. 2011;3148:7–12. PubMed

Fiala I, Bartošová-Sojková P, Whipps CM. Classification and phylogenetics of Myxozoa. In: Okamura B, Gruhl A, Bartholomew JL, editors. Myxozoan evolution, ecology and development. Cham Heidelberg New York Dordrecht London: Springer International Publishing AG Switzerland; 2015. pp. 85–110.

Lom J, Dyková I. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol. 2006;53:1–36. doi: 10.14411/fp.2006.001. PubMed DOI

Jirků M, Fiala I, Modrý 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. PubMed

Bartošová P, Fiala I, Jirků M, Cinková M, Caffara M, Fioravanti ML, et al. Sphaerospora sensu stricto: Taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa) Mol Phylogenet Evol. 2013;68:93–105. doi: 10.1016/j.ympev.2013.02.026. PubMed DOI

Holzer AS, Pecková H, Patra S, Brennan NP, Yanes-Roca C, Main KL. Severe glomerular disease in juvenile grey snapper Lutjanus griseus L. in the Gulf of Mexico caused by the myxozoan Sphaerospora motemarini n. sp. Int J Parasitol Parasites Wildl. 2013;2:124–130. doi: 10.1016/j.ijppaw.2013.03.003. PubMed DOI PMC

Sanders JL, Jaramillo AG, Ashford JE, Feist SW, Lafferty KD, Kent ML. Two myxozoans from the urinary tract of topsmelt, Atherinops affinis. J Parasitol. 2015;101:577–586. doi: 10.1645/15-726. PubMed DOI

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

Eszterbauer E, Sipos D, Forró B, Bartošová P, Holzer A. Molecular characterization of Sphaerospora molnari (Myxozoa), the agent of gill sphaerosporosis in common carp Cyprinus carpio. Dis Aquat Organ. 2013;104:59–67. doi: 10.3354/dao02584. PubMed DOI

Jirků M, Bartošová-Sojková P. Ultrastructure and localisation of late-sporogonic developmental stages of Sphaerospora ranae (Myxosporea: Sphaerosporidae) Folia Parasitol. 2014;61:311–321. doi: 10.14411/fp.2014.047. PubMed DOI

Özer A, Wootten R. The life cycle of Sphaerospora truttae (Myxozoa: Myxosporea) and some features of the biology of both the actinosporean and myxosporean stages. Dis Aquat Organ. 2000;40:33–9. PubMed

Molnár K, El-Mansy A, Székely C, Baska F. Experimental identification of the actinosporean stage of Sphaerospora renicola Dyková & Lom, 1982 (Myxosporea: Sphaerosporidae) in oligochaete alternate hosts. J Fish Dis. 1999;22:143–53.

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

Eszterbauer E, Marton S, Rácz OZ, Letenyei M, Molnár K. Morphological and genetic differences among actinosporean stages of fish-parasitic myxosporeans (Myxozoa): difficulties of species identification. Sys Parasitol. 2006;65:97–114. doi: 10.1007/s11230-006-9041-y. PubMed DOI

Desser SS, Lom J, Dyková I. Developmental stages of Sphaerospora ohlmacheri (Whinery, 1893) n. comb. (Myxozoa:Myxosporea) in the renal tubules of bullfrog tadpoles, Rana catesbeiana, from Lake of Two Rivers, Algonquin Park, Ontario. Can J Zool. 1986;64:2213–2217. doi: 10.1139/z86-335. DOI

Holzer AS, Bartošová-Sojková P, Born-Torrijos A, Lövy A, Hartigan A, Fiala I. The joint evolution of the Myxozoa and their alternate hosts: a cnidarian recipe for success and vast biodiversity. Mol Ecol. 2018;27:1651–66. PubMed

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

Evans NM, Holder MT, Barbeitos MS, Okamura B, Cartwright P. The phylogenetic position of Myxozoa: exploring conflicting signals in phylogenomic and ribosomal data sets. Mol Biol Evol. 2010;27:2733–2746. doi: 10.1093/molbev/msq159. PubMed DOI

Chang ES, Neuhof M, Rubinstein ND, Diamant A, Philippe H, Huchon D, et al. Genomic insights into the evolutionary origin of Myxozoa within Cnidaria. Proc Natl Acad Sci USA. 2015;112:14912–14917. doi: 10.1073/pnas.1511468112. PubMed DOI PMC

Takeuchi F, Sekizuka T, Ogasawara Y, Yokoyama H, Kamikawa R, Inagaki Y, et al. The mitochondrial genomes of a myxozoan genus Kudoa are extremely divergent in Metazoa. PLoS One. 2015;10:e0132030. doi: 10.1371/journal.pone.0132030. PubMed DOI PMC

Lom J, Arthur JR. A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis. 1989;12:151–156. doi: 10.1111/j.1365-2761.1989.tb00287.x. DOI

Sitja-Bobadilla A, Alvarez-Pellitero P. Revised classification and key species of the genus Sphaerospora Davies, 1917 (Protozoa: Myxosporea) Res Rev Parasitol. 1994;54:67–80.

Asahida T, Kobayashi T, Saitoh K, Nakayama I. Tissue preservation and total DNA extraction from fish stored at ambient temperature using buffers containing high concentration of Urea. Fish Sci. 1996;62:727–730. doi: 10.2331/fishsci.62.727. DOI

Holzer AS, Bartošová P, Pecková H, Tyml T, Atkinson S, Bartholomew J, et al. ‘Who’s who’ in renal sphaerosporids (Bivalvulida: Myxozoa) from common carp, Prussian carp and goldfish - molecular identification of cryptic species, blood stages and new members of Sphaerospora sensu stricto. Parasitology. 2013;140:46–60. 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 Res. 2002;30:3059–3066. doi: 10.1093/nar/gkf436. PubMed DOI PMC

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC

Stamatakis A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–2690. doi: 10.1093/bioinformatics/btl446. PubMed DOI

Posada D. JModelTest: phylogenetic model averaging. Mol BIol Evol. 2008;25:1253–1256. doi: 10.1093/molbev/msn083. PubMed DOI

Swofford DL. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sunderland, Massachusetts: Sinauer Associates; 2002.

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

Rambaut A, Suchard MA, Xie D, Drummond AJ. Tracer v1.6. 2014.

Merkle D, Middendorf M, Wieseke N. A parameter-adaptive dynamic programming approach for inferring cophylogenies. BMC Bioinformatics. 2010;11(Suppl. 1):S60. doi: 10.1186/1471-2105-11-S1-S60. PubMed DOI PMC

Legendre P, Desdevises Y, Bazin E. A statistical test for host-parasite coevolution. Syst Biol. 2002;51:217–234. doi: 10.1080/10635150252899734. PubMed DOI

Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;20:289–290. doi: 10.1093/bioinformatics/btg412. PubMed DOI

Li LX, Desser SS. The protozoan parasites of fish from two lakes in Algonquin Park. Ontario. Can J Zool. 1985;63:1846–1858. doi: 10.1139/z85-275. DOI

Lom J, Desser SS, Dyková I. Some little-known and new protozoan parasites of fish from Lake Sasajewun, Algonquin Park, Ontario. Can J Zool. 1989;67:1372–1379. doi: 10.1139/z89-195. DOI

Xiao C, Desser SS. Sphaerospora ovophila n. sp. and Myxobolus algonquinensis n. sp. (Myxozoa, Myxosporea), ovarian parasites of fish from Algonquin Park, Ontario, Canada. J Eukaryot Microbiol. 1997;44:157–61.

ICZN International Commission on Zoological Nomenclature: Amendment of articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. Bull Zool Nomencl. 2012;69:161–169. PubMed

El-Matbouli M, Hoffmann R, Kern R. Sphaerospora bramae sp. nov. (Myxosporea: Sphaerosporidae) in the kidney of common bream (Abramis brama) Bull Eur Ass Fish Pathol. 1995;15:197–199.

Kudo R. Studies on Myxosporidia. A synopsis of genera and species of Myxosporidia. Ill Biol Monogr. 1919;5:1–265.

Lom J, Pavlásková M, Dyková I. Notes on kidney-infecting species of the genus Sphaerospora Thélohan (Myxosporea), including a new species S. gobionis sp. nov., and on myxosporean life cycle stages in the blood of some freshwater fish. J Fish Dis. 1985;8:221–232. doi: 10.1111/j.1365-2761.1985.tb01217.x. DOI

Baska F, Molnár K. Blood stages of Sphaerospora spp. (Myxosporea) in cyprinid fishes. Dis Aquat Organ. 1988;5:23–28. doi: 10.3354/dao005023. DOI

El-Matbouli M, Hoffmann RW. Sphaerospora scardinii n. sp. (Myxosporea, Sphaerosporidae) observed in the kidney of rudd Scardinius erythrophthalmus. Dis Aquat Organ. 1992;14:23–29. doi: 10.3354/dao014023. DOI

Longshaw M. Studies of myxozoan parasites of freshwater fish and invertebrate hosts. PhD Thesis. England: University of Plymouth; 2004. p. 355.

Zaika VE. The question of endemicity among the parasites of the fishes in Lake Baikal. Dokl Akad Nauk SSSR. 1961;141:236–239.

Molnár K. Renal sphaerosporosis in the common carp Cyprinus carpio L. J Fish Dis. 1980;3:11–19. doi: 10.1111/j.1365-2761.1980.tb00179.x. DOI

Hanajavanit C, Bermingham M, Mulcahy MF. Epidemiology of squamous cell carcinomas in rudd Scardinius erythrophthalmus from SE Ireland. Dis Aquat Organ. 2008;80:145–156. doi: 10.3354/dao01909. PubMed DOI

Kulemina IV. New species of endoparasitic protozoa from the fry of the Lake Seliger. Zool Zh. 1969;48:1295–1298.

Kashkovsky VV, Razmashkin DA, Skripchenko GE. Diseases and parasites of fishes in Siberian and Ural fish farms. Sverdlovsk: Sredne-Uralskoe Knizhnoe Izdatelstvo; 1974.

Kepr T. Parasitic Protozoa of cyprinid fishes: Protozoa of the roach Rutilus rutilus (Linnaeus, 1758) in Czechoslovakia. Folia Parasitol. 1991;38:11–21. PubMed

Near TJ, Eytan RI, Dornburg A, Kuhn KL, Moore JA, Davis MP, et al. Resolution of ray-finned fish phylogeny and timing of diversification. Proc Natl Acad Sci USA. 2012;109:13698–13703. doi: 10.1073/pnas.1206625109. PubMed DOI PMC

Betancur-R R, Wiley EO, Arratia G, Acero A, Bailly N, Miya M, et al. Phylogenetic classification of bony fishes. BMC Evol Biol. 2017;17:162. doi: 10.1186/s12862-017-0958-3. PubMed DOI PMC

U-Taynapun K, Chirapongsatonkul N, Maneesaay P, Itami T, Tantikitti C. A new host record of Sphaerospora epinepheli (Myxosporea: Bivalvulida) occurring on orange-spotted grouper Epinephelus coioides from Thailand: epidemiology, histopathology and phylogenetic position. Vet Parasitol. 2012;188:215–224. doi: 10.1016/j.vetpar.2012.04.002. PubMed DOI

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

Bartošová P, Fiala I. Molecular evidence for the existence of cryptic species assemblages of several myxosporeans (Myxozoa) Parasitol Res. 2011;108:573–583. doi: 10.1007/s00436-010-2100-y. PubMed DOI

Patra S, Hartigan A, Morris DJ, Kodádková A, Holzer AS. Description and experimental transmission of Tetracapsuloides vermiformis n. sp. (Cnidaria: Myxozoa) and guidelines for describing malacosporean species including reinstatement of Buddenbrockia bryozoides n. comb. (syn. Tetracapsula bryozoides) Parasitology. 2017;144:497–511. doi: 10.1017/S0031182016001931. PubMed DOI

McGeorge JM, Sommerville C, Wootten R. Epizootiology of Sphaerospora truttae (Myxozoa: Myxosporea) infections of Atlantic salmon Salmo salar at freshwater smolt producing hatcheries in Scotland. Dis Aquat Organ. 1996;26:33–41. doi: 10.3354/dao026033. DOI

Fantham HB, Porter A, Richardson LR. Some myxosporidia found in certain freshwater fishes in Quebec Province, Canada. Parasitology. 1939;31:1–77.

Shul’man SS. Myxosporidia of the USSR. Moscow-Lenningrad: Nauka Publishers. Translated version published for the United States Department of the Interior and National Science Foundation. New Delhi: Amerind Publishing Co. Pvt. Ltd; 1966. p. 631.

Molnár K. Sphaerospora danubialis sp. n. (Myxosporea: Sphaerosporidae) from the kidney of freshwater percid fishes. Parasitol Hung. 1991;24:53–58.

Fomena A, Bouix G. New Myxosporidea species (Myxozoa) from freshwater teleosts in southern Cameroon (Central Africa) J Afr Zool. 1994;108:481–491.

Supamattaya K, Fischerscherl T, Hoffmann RW, Boonyaratpalin S. Sphaerospora epinepheli n. sp. (Myxosporea: Sphaerosporidae) observed in grouper (Epinephelus malabaricus) J Protozool. 1991;38:448–454. doi: 10.1111/j.1550-7408.1991.tb04815.x. PubMed DOI

Holzer AS, Sommerville C, Wootten R. Molecular studies on the seasonal occurrence and development of five myxozoans in farmed Salmo trutta L. Parasitology. 2006;132:193–205. doi: 10.1017/S0031182005008917. PubMed DOI

Stout CC, Tan M, Lemmon AR, Lemmon EM, Armbruster JW. Resolving Cypriniformes relationships using an anchored enrichment approach. BMC Evol Biol. 2016;16:244. doi: 10.1186/s12862-016-0819-5. PubMed DOI PMC

Forró B, Eszterbauer E. Correlation between host specificity and genetic diversity for the muscle-dwelling fish parasite Myxobolus pseudodispar: examples of myxozoan host-shift? Folia Parasitol. 2016;63:019. doi: 10.14411/fp.2016.019. PubMed DOI

Tun T, Yokoyama H, Ogawa K, Wakabayashi H. Myxosporeans and their hyperparasitic microsporeans in the intestine of emaciated tiger puffer. Fish Pathol. 2000;35:145–156. doi: 10.3147/jsfp.35.145. DOI

Lom J, Dyková I, Pavlásková M, Grupcheva G. Sphaerospora molnari sp. n. (Myxozoa, Myxosporea), an agent of gill, skin and blood sphaerosporosis of common carp in Europe. Parasitology. 1983;86:529–535. doi: 10.1017/S003118200005071X. DOI

Fiala I, Bartošová P. History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evol Biol. 2010;10:13. doi: 10.1186/1471-2148-10-228. PubMed DOI PMC

Cohn L. Zur Kenntniss der Myxosporidien. Zentralbl Bakter Parasitenkd. 1902;1:628–632.

Fantham HB, Porter A. On a myxosporidian. Sphærospora periophthalmi, sp. n., found in African and Indian Mudskippers (Pisces), and its possible significance. Proc Zool Soc Lond. 1943;112:113–119.

Moser M, Kent ML, Dennis D. Gall-bladder Myxosporea in coral-reef fishes from Heron Island, Australia. Aust J Zool. 1989;37:1–13. doi: 10.1071/ZO9890001. DOI

Sarkar NK, Ghosh S. Two new coelozoic Myxosporida (Myxozoa: Myxosporea) from estuarine teleost fishes (Mugilidae) of West Bengal, India. Proc Zool Soc Calcutta. 1991;44:131–135.

Brickle P, Kalavati C, MacKenzie K. Two new species of myxozoan parasites (Myxosporea, Bivalvulida) from toothfish Dissostichus eleginoides Smitt, 1898 (Pisces, Nototheniidae) Acta Parasitol. 2001;46:250–253.

Su X, White RWG. New myxosporeans (Myxozoa: Myxosporea) from marine fishes of Tasmania, Australia. Acta Protozool. 1994;33:251–259.

Chen C, Ma C. Myxozoa, Myxosporea. Fauna Sinica. Beijing: Science Press; 1998. p. 993.

Jacob E, Bremen HB. Eine bislang unbekannte Sphaerosporose des Flussaals, hervorgerufen durch Sphaerospora reichenowi nova species, mit eigenartigem Sitz im Darm. Berl Munch Tierarztl Wochenschr. 1953;66:326–328.

Chen C, Hsieh S. A new genus and two new species of family Myxobolidae from freshwater fishes of China (Myxosporidia: Myxobolidae) Acta Zootaxon Sinica. 1984;9:113–117.

Arthur JR, Lom J. Sphaerospora araii n. sp. (Myxosporea: Sphaerosporidae) from the kidney of a longnose skate (Raja rhina Jordan and Gilbert) from the Pacific Ocean off Canada. Can J Zool. 1985;63:2902–2906. doi: 10.1139/z85-434. DOI

Schuurmans-Stekhoven JJH. Über einige Myxosporidien des Stichlings. Arch Protistenk. 1920;41:321–329.

Moshu AY. Description of Sphaerospora luciopercae sp. n. (Protista: Myxosporea) - parasite of the European pikeperch Stizostedion lucioperca (L.). Bul Akad Stiinte Republicci Moldova. Stinnte Biologice si Chimice. 1992;2:54–6.

Whipps CM, Adlard RD, Bryant MS, Lester RJG, Findlay V, Kent ML. First report of three Kudoa species from eastern Australia: Kudoa thyrsites from mahi mahi (Coryphaena hippurus), Kudoa amamiensis and Kudoa minithyrsites n. sp. from sweeper (Pempheris ypsilychnus) J Eukaryot Microbiol. 2003;50:215–219. doi: 10.1111/j.1550-7408.2003.tb00120.x. PubMed DOI

Henderson M, Okamura B. The phylogeography of salmonid proliferative kidney disease in Europe and North America. Proc R Soc Lond B-Biol Sci. 2004;271:1729–1736. doi: 10.1098/rspb.2004.2677. PubMed DOI PMC

Liu XH, Batueva MD, Zhao YL, Zhang JY, Zhang QQ, Li TT, et al. Morphological and molecular characterisation of Myxobolus pronini n. sp. (Myxozoa: Myxobolidae) from the abdominal cavity and visceral serous membranes of the gibel carp Carassius auratus gibelio (Bloch) in Russia and China. Parasit Vectors. 2016;9:562. doi: 10.1186/s13071-016-1836-3. PubMed DOI PMC

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

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

Alama-Bermejo G, Raga JA, Holzer AS. Host-parasite relationship of Ceratomyxa puntazzi n. sp. (Myxozoa: Myxosporea) and sharpsnout seabream Diplodus puntazzo (Walbaum, 1792) from the Mediterranean with first data on ceratomyxid host specificity in sparids. Vet Parasitol. 2011;182:181–192. doi: 10.1016/j.vetpar.2011.05.012. PubMed DOI

de Vienne DM, Refrégier G, López-Villavicencio M, Tellier A, Hood ME, Giraud T. Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytol. 2013;198:347–385. doi: 10.1111/nph.12150. PubMed DOI

Vega GC, Wiens JJ. Why are there so few fish in the sea? P Roy Soc Lond B Biol. 2012;279:2323–2329. doi: 10.1098/rspb.2012.0075. PubMed DOI PMC

Cooper N, Griffin R, Franz M, Omotayo M, Nunn CL. Phylogenetic host specificity and understanding parasite sharing in primates. Ecol Lett. 2012;15:1370–1377. doi: 10.1111/j.1461-0248.2012.01858.x. PubMed DOI

Huang S, Bininda-Emonds ORP, Stephens PR, Gittleman JL, Altizer S. Phylogenetically related and ecologically similar carnivores harbour similar parasite assemblages. J Anim Ecol. 2014;83:671–680. doi: 10.1111/1365-2656.12160. PubMed DOI

Reyjol Y, Hugueny B. D. Pont, Bianco PG, Beier U, Caiola N, et al. Patterns in species richness and endemism of European freshwater fish. Global Ecol Biogeogr. 2007;16:65–75. doi: 10.1111/j.1466-8238.2006.00264.x. DOI

Freyhof J, Brooks E. Luxembourg: Publications Office of the European Union. 2011. European Red List of freshwater fishes.

Tedersoo L, Bahram M, Dickie IE. Does host plant richness explain diversity of ectomycorrhizal fungi? Re-evaluation of Gao et al. (2013) data sets reveals sampling effects. Mol Ecol. 2014;23:992–995. doi: 10.1111/mec.12660. PubMed DOI

Gleeson R, Adlard R. Morphological and genetic analysis of three new species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea) from carcharhinid sharks off Australia. Syst Parasitol. 2011;80:117–124. doi: 10.1007/s11230-011-9316-9. PubMed DOI

Gleeson RJ, Adlard RD. Phylogenetic relationships amongst Chloromyxum Mingazzini, 1890 (Myxozoa: Myxosporea), and the description of six novel species from Australian elasmobranchs. Parasitol Int. 2012;61:267–274. doi: 10.1016/j.parint.2011.10.008. PubMed DOI

Kodádková A, Bartošová-Sojková P, Holzer AS, Fiala I. Bipteria vetusta n. sp. - an old parasite in an old host: tracing the origin of myxosporean parasitism in vertebrates. Int J Parasitol. 2015;45:269–276. doi: 10.1016/j.ijpara.2014.12.004. PubMed DOI

Molnár K. Sphaerospora siluri n. sp. (Myxosporea: Sphaerosporidae) in the kidney of the sheatfish (Silurus glanis) Acta Vet Hung. 1993;41:341–347. PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...