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Phylogenetic relationships among Eimeria spp. (Apicomplexa, Eimeriidae) infecting rabbits: evolutionary significance of biological and morphological features

Published online by Cambridge University Press:  04 February 2008

J. KVIČEROVÁ ,
M. PAKANDL  and
V. HYPŠA
J. KVIČEROVÁ*
Affiliation:
Biological Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
M. PAKANDL
Affiliation:
Biological Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
V. HYPŠA
Affiliation:
Biological Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
*
*Corresponding author: Biological Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic. Tel: +420 38 7775448. Fax: +420 38 5310388. E-mail: janaq@paru.cas.cz
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Summary

Monophyly of all 11 valid Eimeria species from rabbits (Oryctolagus cuniculus Linnaeus, 1758) was revealed based on nuclear 18S rDNA sequence data. This finding implies that these species, which vary considerably in terms of their morphology and biology, diversified on a single host or several closely related species. Phylogenetic analysis divided rabbit Eimeria species into 2 sister lineages, corresponding to the presence/absence of the oocyst residuum. Other morphological or biological traits (oocyst shape and size, presence/absence of oocyst inner structures, pathogenicity, infection site, pre-patent and patent periods, sporulation time, and number of asexual generations) do not explicitly correlate with the phylogeny of rabbit coccidia.

Keywords

coccidiaEimeriaoocystsOryctolagushost specificity18S rDNAphylogenetic analysis
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 4 , April 2008 , pp. 443 - 452
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

Banks, J. C., Palma, R. L. and Paterson, A. M. (2006). Cophylogenetic relationships between penguins and their chewing lice. Journal of Evolutionary Biology 19, 156–166.CrossRefGoogle ScholarPubMed
Barta, J. R. (1989). Phylogenetic analysis of the class Sporozoea (phylum Apicomlexa Levine 1970): evidence for the independent evolution of heteroxenous life cycles. Journal of Parasitology 75, 195–206.CrossRefGoogle Scholar
Barta, J. R., Martin, D. S., Liberator, P. A., Dashkevicz, M., Anderson, J. W., Feighner, S. D., Elbrecht, A., Perkins-Barrow, A., Jenkins, M. C., Danforth, H. D., Ruff, M. D. and Profous-Juchelka, H. (1997). Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal of Parasitology 83, 262–271.CrossRefGoogle ScholarPubMed
Barta, J. R., Martin, D. S., Carreno, R. A., Siddall, M. E., Profous-Juchelka, H., Hozza, M., Powles, M. A. and Sundermann, C. (2001). Molecular phylogeny of the other tissue coccidia: Lankesterella and Caryospora. Journal of Parasitology 87, 121–127.CrossRefGoogle ScholarPubMed
Carreno, R. A., Martin, D. S. and Barta, J. R. (1999). Cryptosporidium is more closely related to the gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small-subunit ribosomal RNA gene sequences. Parasitology Research 85, 899–904.CrossRefGoogle Scholar
Ceré, N., Licois, D. and Humbert, J. F. (1995). Study of the inter- and intraspecific variation of Eimeria spp. from the rabbit using random amplified polymorphic DNA. Parasitology Research 91, 324–328.CrossRefGoogle Scholar
Ceré, N., Humbert, J. F., Licois, D., Corvione, M., Afanassieff, M. and Chanteloup, N. (1996). A new approach for the identification and the diagnosis of Eimeria media parasite of the rabbit. Experimental Parasitology 82, 132–138.CrossRefGoogle ScholarPubMed
Ceré, N., Licois, D. and Humbert, J. F. (1997). Comparison of the genomic fingerprints generated by the random amplification of polymorphic DNA between precocious lines and parental strains of Eimeria spp. from the rabbit. Parasitology Research 83, 300–302.CrossRefGoogle ScholarPubMed
Coudert, P., Licois, D. and Streun, A. (1979). Characterization of Eimeria species. I. Isolation and study of pathogenicity of a pure strain of Eimeria perforans (Leuckart, 1879; Sluiter and Swellengrebel, 1912). Zeitschrift für Parasitenkunde 59, 227–234.CrossRefGoogle ScholarPubMed
Coudert, P., Licois, D. and Drouet-Viard, F. (1995). Eimeria species and strains of the rabbits. In Biotechnology. Guidelines on Techniques in Coccidiosis Research (ed. Eckert, J., Braun, R., Shirley, M. W. and Coudert, P.), pp. 52–71. COST 89/820, Luxembourg.Google Scholar
Doležel, D., Koudela, B., Jirků, M., Hypša, V., Oborník, M., Votýpka, J., Modrý, D., Šlapeta, J. R. and Lukeš, J. (1999). Phylogenetic analysis of Sarcocystis spp. of mammals and reptiles supports the coevolution of Sarcocystis spp. with their final hosts. International Journal for Parasitology 29, 795–798.CrossRefGoogle ScholarPubMed
Duszynski, D. W. and Upton, S. J. (2001). The common coccidia of wild mammals. Cyclospora, Eimeria (Eimeriidae) and Cryptosporidium (Cryptosporidiidae) spp. In Parasitic Diseases of Wild Mammals (ed. Samuel, W. M., Pybus, M. J. and Kocan, A. A.), pp. 416–433. Iowa State University Press, Ames, IA, USA.CrossRefGoogle Scholar
Eberhard, M. L., Da Silva, A. J., Lilley, B. G. and Pieniazek, N. J. (1999). Morphologic and molecular characterization of new Cyclospora species from Ethiopian monkeys: C. cercopitheci sp. n., C. colobi sp. n., and C. papionis, sp. n. Emerging Infectious Diseases 5, 651–657.CrossRefGoogle Scholar
Eckert, J., Braun, R., Shirley, M. W. and Coudert, P. (1995). Biotechnology. Guidelines on Techniques in Coccidiosis Research. COST 89/820, Luxembourg.Google Scholar
Entzeroth, R. and Scholtyseck, E. (1977). The life cycle of E. stiedai from rabbits in hares. Fifth International Congress on Protozoology, New York City 26.6.-2.7.Google Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hnida, J. A. and Duszynski, D. W. (1999 a). Taxonomy and systematics of some Eimeria species of murid rodents as determined by the ITS1 region of the ribosomal gene complex. Parasitology 199, 349–357.CrossRefGoogle Scholar
Hnida, J. A. and Duszynski, D. W. (1999 b). Taxonomy and phylogeny of some Eimeria (Apicomplexa: Eimeriidae) species of rodents as determined by polymerase chain reaction/restriction-fragment-length polymorphism analysis of 18s rDNA. Parasitology Research 85, 887–894.CrossRefGoogle Scholar
Hoberg, E., Brooks, D. R. and Siegel-Causey, D. (1997). Host-parasite cospeciation: history, principles, and prospects. In General Principles and Avian Models Host-Parasite Evolution (ed. Clayton, D. H. and Moore, J.), pp. 212–235. Oxford University Press, Oxford.CrossRefGoogle Scholar
Holmdahl, O. J., Morrison, D. A., Ellis, J. T. and Huong, L. T. (1999). Evolution of ruminant Sarcocystis (Sporozoa) parasites based on small subunit rDNA sequences. Molecular Phylogenetics and Evolution 11, 27–37.CrossRefGoogle ScholarPubMed
Jirků, M., Modrý, D., Šlapeta, J. R., Koudela, B. and Lukeš, J. (2002). The phylogeny of Goussia and Choleoeimeria (Apicomplexa; Eimeriorina) and the evolution of excystation structures in coccidia. Protist 153, 379–390.CrossRefGoogle ScholarPubMed
Johnson, K. P. and Clayton, D. H. (2001). Coevolutionary history of ecological replicates: comparing phylogenies of wing and body lice to Columbiform hosts. In Tangled Trees: Phylogeny, Cospeciation, and Coevolution (ed. Page, R. D. M.), pp. 262–286. Chicago University Press, Chicago, IL.Google Scholar
Jousson, O., Bartoli, P. and Pawlowski, J. (2000). Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). Journal of Evolutionary Biology 13, 778–785.CrossRefGoogle Scholar
Joyner, L. P. (1982). Host and site specificity. In The Biology of the Coccidia (ed. Long, P. L.), pp. 35–62. University Park Press, Baltimore, Maryland, USA.Google Scholar
Kopečná, J., Jirků, M., Oborník, M., Tokarev, Y. S., Lukeš, J. and Modrý, D. (2006). Phylogenetic analysis of coccidian parasites from invertebrates: search for missing links. Protist 157, 173–183. doi: 10.1016/j.protis.2006.02.005.CrossRefGoogle ScholarPubMed
Leander, B. S., Lloyd, S. A. J., Marshall, W. and Landers, S. C. (2006). Phylogeny of marine gregarines (Apicomplexa) – Pterospora, Lithocystis and Lankesteria – and the origin(s) of coelomic parasitism. Protist 157, 45–60. doi: 10.1016/j.protis.2005.10.002.CrossRefGoogle ScholarPubMed
Li, G., Xiao, S., Zhou, R., Li, W. and Wadeh, H. (2007). Molecular characterization of Cyclospora-like organism from dairy cattle. Parasitology Research 100, 955–961.CrossRefGoogle ScholarPubMed
Licois, D. and Coudert, P. (1982). Coccidioses et diarrhées du lapin à l'engraissement. Bull GTV 5, 109–122.Google Scholar
Licois, D. and Mongin, P. (1980). An hypothesis of the pathogenesis of diarrhoea in the rabbit based on a study of intestinal contents. Reproduction Nutrition Development 20, 1209–1216.CrossRefGoogle ScholarPubMed
Long, P. L. and Joyner, L. P. (1984). Problems in the identification of species of Eimeria. Journal of Protozoology 31, 535–541.CrossRefGoogle ScholarPubMed
Marquardt, W. C. (1973). Host and site specificity. In The Coccidia (ed. Hammond, D. M. and Long, P. L.), pp. 23–43. University Park Press, Baltimore, Maryland, USA.Google Scholar
Matsubayashi, M., Takami, K., Niichiro, A., Kimata, I., Tani, H., Sasai, K. and Baba, E. (2005). Molecular characterization of crane coccidia, Eimeria gruis and E. reichenowi, found in feces of migratory cranes. Parasitology Research 97, 80–83.CrossRefGoogle Scholar
Metzner, R. (1903). Untersuchungen an Coccidium cuniculi. Archiv für Protistenkunde 2, 13–72.Google Scholar
Minning, W. (1936). Zur Entstehung der Coccidienknoten in der Leber von Kaninchen. Zeitschrift für Parasitenkunde 9, 61–72.CrossRefGoogle Scholar
Morrison, D. A., Bornstein, S., Thebo, P., Wernery, U., Kinne, J. and Mattsson, J. G. (2004). The current status of the small subunit rRNA phylogeny of the coccidia (Sporozoa). International Journal for Parasitology 34, 501–514.CrossRefGoogle ScholarPubMed
Mugridge, M. B., Morrison, D. A., Jakel, T., Heckeroth, A. R., Tenter, A. M. and Johnson, A. M. (2000). Effects of sequence alignment and structural domains of ribosomal DNA on phylogeny reconstruction for the protozoan family Sarcocystidae. Molecular Biology and Evolution 17, 1842–1853.CrossRefGoogle ScholarPubMed
Nieberding, C., Morand, S., Libois, R. and Michaux, J. R. (2004). A parasite reveals cryptic phylogeographic history of its host. Proceedings of the Royal Society of London, B 271, 2559–2568.CrossRefGoogle ScholarPubMed
Nieberding, C., Libois, R., Douady, C. J., Morand, S. and Michaux, J. R. (2005). Phylogeography of a nematode (Heligmosomoides polygyrus) in the western Palearctic region: persistence of northern cryptic populations during ice ages? Molecular Ecology 14, 765–779.CrossRefGoogle ScholarPubMed
Norton, C. C., Catchpole, N. and Rose, M. E. (1977). Eimeria stiedai in rabbits: the presence of an oocyst residuum. Parasitology 75, 1–7.CrossRefGoogle ScholarPubMed
Olsen, G. J. and Woese, C. R. (1993). Ribosomal RNA: a key to phylogeny. FASEB Journal 7, 113–123.CrossRefGoogle ScholarPubMed
Page, R. D. M. (1996 a). Temporal congruence revisited: comparison of mitochondrial DNA sequence divergence in cospeciating pocket gophers and their chewing lice. Systematic Biology 45, 151–167.CrossRefGoogle Scholar
Page, R. D. M. (1996 b). TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.Google ScholarPubMed
Pakandl, M. (1988). Description of Eimeria vejdovskyi sp. n. and redescription of Eimeria media Kessel, 1929 from the rabbit. Folia Parasitologica 35, 1–9.Google Scholar
Pakandl, M. and Coudert, P. (1999). Life cycle of Eimeria vejdovskyiPakandl, 1988: electron microscopy study. Parasitology Research 85, 850–854.CrossRefGoogle ScholarPubMed
Pakandl, M., Černík, F. and Coudert, P. (2003). The rabbit coccidium Eimeria flavescens Marotel and Guilhon, 1941: an electron microscopic study of its life cycle. Parasitology Research 91, 304–311.CrossRefGoogle ScholarPubMed
Pakandl, M., Ahmed, N. E., Licois, D. and Coudert, P. (1996 c). Eimeria magna Pérard 1925: study of the endogenous development of parental and precocious strains. Veterinary Parasitology 65, 213–222.CrossRefGoogle ScholarPubMed
Pakandl, M., Gaca, K., Drouet-Viard, F. and Coudert, P. (1996 a). Eimeria coecicola Cheissin 1947: endogenous development in gut-associated lymphoid tissue. Veterinary Research 82, 347–351.Google ScholarPubMed
Pakandl, M., Gaca, K., Licois, D. and Coudert, P. (1996 b). Eimeria media Kessel 1929: comparative study of endogenous development between precocious and parental strains. Veterinary Research 27, 465–472.Google ScholarPubMed
Pakandl, M. and Jelínková, A. (2006). The rabbit coccidium Eimeria piriformis: Selection of a precocious line and life-cycle study. Veterinary Parasitology 137, 351–354.CrossRefGoogle ScholarPubMed
Paterson, A. M., Wallis, G. P., Wallis, L. J. and Gray, L. D. (2000). Seabird and louse coevolution: complex histories revealed by 12S rRNA sequences and reconciliation analyses. Systematic Biology 49, 383–399.CrossRefGoogle ScholarPubMed
Pellérdy, L. P. (1965). Oryctolagus. In Coccidia and Coccidiosis (ed. North, H. F. and Farkas, I.), pp. 323–330. Akademiai Kiado, Budapest.Google Scholar
Pellérdy, L. P. and Dürr, U. (1970). Zum endogenen Entwicklungszyklus von Eimeria stiedai (Lindemann 1865) Kisskalt & Hartmann, 1907. Acta Veterinaria of the Academy of Sciences of Hungary 20, 227–244.Google ScholarPubMed
Proctor, H. C. (1999). Gallilichus jonesi sp.n. (Acari: Ascouracaridae): a new species of feather mite from the quills of the Australian brush-turkey (Aves: Megapodiidae). Australian Journal of Entomology 38, 77–84.CrossRefGoogle Scholar
Reduker, D. W., Duszynski, D. W. and Yates, T. L. (1987). Evolutionary relationships among Eimeria spp. (Apicomplexa) infecting cricetid rodents. Canadian Journal of Zoology 65, 722–735.CrossRefGoogle Scholar
Rutherford, R. L. (1943). The life-cycle of four intestinal coccidia of the domestic rabbit. Journal of Parasitology 29, 10–32.CrossRefGoogle Scholar
Scholtyseck, E., Entzeroth, R. and Pellérdy, L. (1979). Transmission of Eimeria stiedai from the rabbit (Oryctolagus cuniculus) to the hare (Lepus europaeus). Acta Veterinaria of the Academy of Sciences of Hungary 27, 365–373.Google Scholar
Schrenzel, M. D., Maalouf, G. A., Gaffney, P. M., Tokarz, D., Keener, L. L., McClure, D., Griffey, S., McAloose, D. and Rideout, B. A. (2005). Molecular characterization of isosporoid coccidian (Isospora and Atoxoplasma spp.) in passerine birds. The Journal of Parasitology 91, 635–647.CrossRefGoogle ScholarPubMed
Šlapeta, J. R., Modrý, D., Votýpka, J., Jirků, M., Lukeš, J. and Koudela, B. (2003). Evolutionary relationships among cyst-forming coccidia Sarcocystis spp. (Alveolata: Apicomplexa: Coccidea) in endemic African tree vipers and perspective for evolution of heteroxenous life cycle. Molecular Phylogenetics and Evolution 27, 464–475.CrossRefGoogle ScholarPubMed
Sugár, L., Murai, E. and Mészáros, P. (1978). Über die Endoparasiten der wildleben Leporidae Ungarns. Parasitologica Hungarica 11, 63–85.Google Scholar
Swofford, D. L. (2001). Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sinauer Associates, Sunderland, Massachusetts, USA.Google Scholar
Tenter, A. M., Baverstock, P. R. and Johnson, A. M. (1992). Phylogenetic relationships of Sarcocystis species from sheep, goats, cattle and mice based on ribosomal RNA sequences. International Journal for Parasitology 22, 503–510.CrossRefGoogle ScholarPubMed
Tenter, A. M., Barta, J. R., Beveridge, I., Duszynski, D. W., Mehlhorn, H., Morrison, D. A., Thompson, R. C. A. and Conrad, P. A. (2002). The conceptual basis for a new classification of the coccidia. International Journal for Parasitology 32, 595–616.CrossRefGoogle ScholarPubMed
Varga, I. (1976). Experimental transmission of E. stiedai to the hare. Acta Veterinaria of the Academy of Sciences of Hungary 26, 105–112.Google Scholar
Vítovec, J. and Pakandl, M. (1989). The pathogenicity of rabbit coccidium Eimeria coecicola Cheissin, 1947. Folia Parasitologica (Praha) 36, 289–293.Google ScholarPubMed
Votýpka, J., Hypša, V., Jirků, M., Flegr, J., Vávra, J. and Lukeš, J. (1998). Molecular phylogenetic relatedness of Frenkelia spp. (Protozoa, Apicomplexa) to Sarcocystis falcatula Stiles 1893: is the genus Sarcocystis paraphyletic? Journal of Eukaryotic Microbiology 45, 137–141. www.ncbi.nlm.nih.govCrossRefGoogle ScholarPubMed
Zhao, X. and Duszynski, D. W. (2001 a). Phylogenetic relationships among rodent Eimeria species determined by plastid ORF470 and nuclear 18S rDNA sequences. International Journal for Parasitology 31, 715–719.CrossRefGoogle ScholarPubMed
Zhao, X. and Duszynski, D. W. (2001 b). Molecular phylogenies suggest the oocyst residuum can be used to distinguish two independent lineages of Eimeria spp in rodents. Parasitology Research 87, 638–643.Google ScholarPubMed