Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-22T15:35:33.190Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogenetic analysis based on 18S rRNA gene sequences of Schellackia parasites (Apicomplexa: Lankesterellidae) reveals their close relationship to the genus Eimeria

Published online by Cambridge University Press:  04 June 2013

R. MEGÍA-PALMA ,
J. MARTÍNEZ  and
S. MERINO
R. MEGÍA-PALMA*
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-CSIC, J. Gutiérrez Abascal, 2. E-28006, Madrid, Spain
J. MARTÍNEZ
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Farmacia, Universidad de Alcalá de Henares, Alcalá de Henares, E-28871, Madrid, Spain
S. MERINO
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-CSIC, J. Gutiérrez Abascal, 2. E-28006, Madrid, Spain
*
*Corresponding author: Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-CSIC, José Gutiérrez Abascal 2, E-28006 Madrid, Spain. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In the present study we detected Schellackia haemoparasites infecting the blood cells of Lacerta schreiberi and Podarcis hispanica, two species of lacertid lizards from central Spain. The parasite morphometry, the presence of a refractile body, the type of infected blood cells, the kind of host species, and the lack of oocysts in the fecal samples clearly indicated these blood parasites belong to the genus Schellackia. Until now, the species of this genus have never been genetically characterized and its taxonomic position under the Lankesterellidae family is based on the lack of the exogenous oocyst stage. However, the phylogenetic analysis performed on the basis of the 18S rRNA gene sequence revealed that species of the genus Schellackia are clustered with Eimeria species isolated from a snake and an amphibian species but not with Lankesterella species. The phylogenetic analysis rejects that both genera share a recent common ancestor. Based on these results we suggest a revision of the taxonomic status of the family Lankesterellidae.

Keywords

EimeriidaehaplotypeshaemococcidiaLacerta schreiberilizardphylogenyPodarcis hispanicataxonomy
Type
Research Article
Information
Parasitology , Volume 140 , Issue 9 , August 2013 , pp. 1149 - 1157
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alyousif, M. S., Al-Shawa, Y. R. and Mubarak, M. (2005). Light and electron microscopy of gall bladder epithelium of the gray monitor, Varanus griseus, infected with Eimeria griseus (Apicomplexa: Eimeriidae). Journal of Biological Sciences 5, 542–546.Google Scholar
Atkinson, C. T., Thomas, N. J. and Hunter, D. B. (2008). Parasitic Diseases of Wild Birds, pp. 108, 162. Wiley–Blackwell, Ames, IA, USA.CrossRefGoogle Scholar
Barta, J. R. (2001). Molecular approaches for inferring evolutionary relationships among protistan parasites. Veterinary Parasitology 101, 175–186.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
Bristovetzky, M. and Paperna, I. (1990). Life cycle and transmission of Schellackia cf. agamae, a parasite of the starred lizard Agama stellio. International Journal for Parasitology 20, 883–892.CrossRefGoogle Scholar
Carpenter, J. W. (1993). Infectious and parasitic diseases of cranes. In Zoo and Wild Animal Medicine: Current Therapy 3 (ed. Fowler, M. E.), pp. 229–237. W. B. Saunders, Philadelphia, PA, USA.Google Scholar
Criado-Fornelio, A., Martínez-Marcos, A., Buling-Saraña, A. and Barba-Carretero, J. C. (2003). Presence of Mycoplasma haemofelis, Mycoplasma haemominutum and piroplasmids in cats from southern Europe: a molecular study. Veterinary Microbiology 93, 307–317.CrossRefGoogle ScholarPubMed
Daszak, P., Ball, S. J., Streicker, D. G. and Snow, K. R. (2011). A new species of Eimeria (Apicomplexa: Eimeriidae) from the western hognose snake, Heterodon nasicus (Serpentes: Xenodontidae), from Texas. Journal of Parasitology 97, 463–465.CrossRefGoogle Scholar
Duszynski, D. W. and Wilber, P. G. (1997). A guideline for the preparation of species descriptions in the Eimeriidae. Journal of Parasitology 83, 333–336.CrossRefGoogle ScholarPubMed
Ghimire, T. R. (2010). Redescription of genera of family Eimeriidae Minchin, 1903. International Journal of Life Sciences 4, 26–47.CrossRefGoogle Scholar
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.CrossRefGoogle ScholarPubMed
Gutell, R. R., Larsen, N. and Woese, C. R. (1994). Lessons from an evolving rRNA: 16 S and 23 S rRNA structures from a comparative perspective. Microbiological Reviews 58, 10–26.CrossRefGoogle Scholar
Harris, J., Joao, P. M., Maia, C. and Perera, A. (2012). Molecular survey of Apicomplexa in Podarcis wall lizards detects Hepatozoon, Sarcocystis, and Eimeria species. Journal of Parasitology 98, 592–597.CrossRefGoogle ScholarPubMed
Honma, H., Yokoyama, T., Inoue, M., Uebayashi, A., Matsumoto, F., Watanabe, Y. and Nakai, Y. (2007). Genetical identification of coccidia in red-crowned crane, Grus japonensis. Journal of Parasitology Research 100, 637–640.CrossRefGoogle ScholarPubMed
Jirku, M., Jirku, M., Oborník, M., Lukes, J. and Modrý, D. (2009). A model for taxonomic work on homoxenous coccidia: redescription, host apecificity, and molecular phylogeny of Eimeria ranae Dobell, 1909, with a review of Anuran-host Eimeria (Apicomplexa: Eimeriorina). Journal of Eukaryotic Microbiology 56, 39–51.CrossRefGoogle Scholar
Lainson, R., Shaw, J. J. and Ward, R. D. (1976). Schellackia landauae sp. nov. (Eimeriorina: Lankesterellidae) in the Brazilian Polychrus marmoratus (Iguanidae): experimental transmission by Culex pipiens fatigans. Parasitology 72, 225–243.CrossRefGoogle Scholar
López, G., Figuerola, J. and Soriguer, R. (2007). Time of day, age and feeding habits influence coccidian oocyst shedding in wild passerines. International Journal for Parasitology 37, 559–564.CrossRefGoogle Scholar
Marco, A. (2011). Lagarto verdinegro – Lacerta schreiberi. In Enciclopedia Virtual de los Vertebrados Españoles (ed. Salvador, A. and Marco, A.). Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org/.Google Scholar
Merino, S. and Potti, J. (1995). High prevalence of hematozoa in nestlings of a passerine species, the pied flycatcher, Ficedula hypoleuca. Auk 112, 1041–1043.CrossRefGoogle Scholar
Merino, S., Martínez, J., Martínez-de la Puente, J., Criado-Fornelio, A., Tomás, G., Morales, J., Lobato, E. and García-Fraile, S. (2006). Molecular characterization of the 18S rRNA gene of an avian Hepatozoon reveals that it is closely related to Lankesterella. Journal of Parasitology 92, 1330–1335.CrossRefGoogle ScholarPubMed
Merino, S., Hennicke, J., Martínez, J., Ludynia, K., Torres, R., Work, T. M., Stroud, S., Masello, J. F. and Quillfeldt, P. (2012). Infection by Haemoproteus parasites in four species of Frigatebirds and the description of a new species of Haemoproteus (Haemosporida: Haemoproteidae). Journal of Parasitology 98, 388–397.CrossRefGoogle ScholarPubMed
Moore, J. and Willmer, P. (1997). Convergent evolution in invertebrates. Biological Reviews 72, 1–60.CrossRefGoogle ScholarPubMed
Morrison, D. A. (2009). Evolution of the Apicomplexa: where are we now? (Review). Trends in Parasitology 25, 375–382.CrossRefGoogle Scholar
Mottalei, F., Mayberry, L. F. and Bristol, J. R. (1992). Localization of extraintestinal Eimeria nieschulzi (Apicomplexa: Eimeriidae) in the rat utilizing an indirect immunofluorescence technique. Transactions of the American Microscopical Society 111, 61–64.CrossRefGoogle Scholar
Paperna, I. and Ostrovska, K. (1989). Ultrastructural studies on sporozoite stages of Schellackia cf. agamae from liver and blood of the starred lizard Agama stellio. Australian Society for Parasitology 19, 13–19.Google Scholar
Power, M. L., Richter, C., Emery, S., Hufschmid, J. and Gillings, M. R. (2009). Eimeria trichosuri: phylogenetic position of a marsupial coccidium, based on 18S rDNA sequences. Experimental Parasitology 122, 165–168.CrossRefGoogle ScholarPubMed
Rambaut, A. and Drummond, A. J. (2007) Tracer: MCMC trace analysis tool. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Salkeld, D. J. and Schwarzkopf, L. (2005). Epizootiology of blood parasites in an Australian lizard: a mark-recapture study of a natural population. International Journal for Parasitology 35, 11–18.CrossRefGoogle Scholar
Salvador, A. (1997). Reptiles. In Fauna Ibérica, Vol. 10 (ed. Ramos, M. A. et al. Museo Nacional de Ciencias Naturales, CSIC, Madrid, Spain.Google Scholar
Smith, T. G. (1996). The genus Hepatozoon (Apicomplexa: Adeleina). Journal of Parasitology 82, 565–585.CrossRefGoogle ScholarPubMed
Stuart-Fox, D., Godinho, R., Goüy de Bellocq, J., Irwin, N. R., Brito, J. C., Moussalli, A., Siroky, P., Hugall, A. F. and Baird, S. J. E. (2009). Variation in phenotype, parasite load and male competitive ability across a cryptic hybrid zone. PLoS ONE 4, e5677.CrossRefGoogle ScholarPubMed
Svahn, K. (1975). Blood parasites of the genus Karyolysus (Coccidia, Adeleidae) in Scandinavian lizards. Description of the life cycle. Norwegian Journal of Zoology 23, 277–295.Google Scholar
Talavera, G. and Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.CrossRefGoogle ScholarPubMed
Telford, S. R. (1993). A species of Schellackia (Apicomplexa: Lankesterellidae) parasitising east and southeast Asian lizards. Systematic Parasitology 25, 109–117.CrossRefGoogle Scholar
Telford, S. M. (2008). Hemoparasites of the Reptilia: Color Atlas and Text, pp. 261–273. CRC Press, Boca Raton, FL, USA.CrossRefGoogle Scholar
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
Upton, S. J. (2000). Suborder Eimeriorina Léger, 1911. In The Illustrated Guide to the Protozoa, 2nd Edn, Vol. 1 (ed. Lee, J. J., Leedale, G. F. and Bradbury, P.). Allen Press, Lawrence, KS, USA.Google Scholar
Upton, S. J. and Oppert, C. J. (1991). Description of the oocysts of Eimeria arnyi n. sp. (Apicomplexa: Eimeriidae) from the eastern ringneck Diadophis punctatus arnyi (Serpentes: Colubridae). Systematic Parasitology 20, 195–197.CrossRefGoogle Scholar
Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. and Barton, G. J. (2009). Jalview Version 2 – a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191. doi:10.1093/bioinformatics/btp033.CrossRefGoogle ScholarPubMed
Whipps, C. M., Fournie, J. W., Morrison, D. A., Azevedo, C., Matos, E., Thebo, P. and Kent, M. L. (2012). Phylogeny of fish-infecting Calyptospora species (Apicomplexa: Eimeriorina). Parasitology Research 111, 1331–1342.CrossRefGoogle ScholarPubMed