Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-24T10:45:15.177Z Has data issue: false hasContentIssue false

Detection of multiple infections by Monocystis strains in a single earthworm host using ribosomal internal transcribed spacer sequence variation

Published online by Cambridge University Press:  20 August 2009

T. P. VELAVAN*
Affiliation:
Department of Animal Evolutionary Ecology, University of Tübingen, Germany Institute for Tropical Medicine, Department of Parasitology, Tübingen, Germany
H. SCHULENBURG
Affiliation:
Department of Animal Evolutionary Ecology, University of Tübingen, Germany Zoological Institute, Christian Albrechts University, Kiel, Germany
N. K. MICHIELS
Affiliation:
Department of Animal Evolutionary Ecology, University of Tübingen, Germany
*
*Corresponding author: Department of Animal Evolutionary Ecology, Zoological Institute, University of Tübingen, Auf der Morgenstelle 28 E, 72076 Tübingen, Germany. Tel: +49 7071 2974841. Fax: +49 7071 295634. E-mail: [email protected]

Summary

Monocystis sp. are sporocyst-forming apicomplexan parasites common in seminal vesicles of the earthworm Lumbricus terrestris where they may account for temporary castration. This study describes the internal transcribed spacer (ITS) region of the ribosomal cistron of Monocystis sp. This region, including ITS-1, the 5·8S ribosomal RNA gene, and ITS-2, was PCR amplified, cloned, and sequenced for Monocystis sp. isolated from the seminal vesicles of several wild-caught L. terrestris. Our analysis revealed substantial polymorphisms, also within single host organisms, indicating intra-host diversity of parasites. These genetic markers are the first that allow distinction of Monocystis sp. genotypes, opening new avenues for the study of parasite diversity within and between hosts.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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

Altizer, S. M. (2001). Migratory behaviour and host-parasite co-evolution in natural populations of monarch butterflies infected with a protozoan parasite. Evolutionary Ecology Research 3, 611632.Google Scholar
Altizer, S., Foufopoulos, J. and Gager, A. (2001). Conservation and diseases. In Encyclopedia of Biodiversity, Vol. 2 (ed. Levin, S. A.), pp. 109126. Academic Press, San Diego, CA, USA.CrossRefGoogle Scholar
Bandyopadhyay, P.K., Bhowmik, B. and Mitra, A. K. (2006). Biology of Monocystis clubae sp nov. (Apicomplexa: Eugregarinida) from an Indian earthworm Lampito mauritii (Annelida: Oligochaeta) of India. Zootaxa 1120, 5155.CrossRefGoogle Scholar
Bandyopadhyay, P. K. and Mitra, A. K. (2005). Observations on two new species of Monocystis Stein, 1848 (Protozoa: Apicomplexa: Monocystidae) Monocystis darjeelingensis sp.n. and M. ranaghatensis sp.n. from earthworms (Annelida: Oligochaeta) of West Bengal, India. Animal Biology 55, 123132.CrossRefGoogle Scholar
Breidenbach, J. (2002). Normalanatomie und- histologie des Lumbriciden Lumbricus terrestris L. (Annelida: Oligochaeta). Doctoral thesis. University of Münster, Münster, Germany.Google Scholar
Bush, A. O., Fernandez, J. C., Esch, G. W. and Seed, R. J. (2001). Parasitism: the diversity and ecology of animal parasites. Cambridge: Cambridge University Press.Google Scholar
Cariello, N. F., Swenberg, T. A. and Skopek, T. R. (1991). Fidelity of the Thermococcus litoralis DNA polymerase (Vent) in polymerase chain reaction determined by denaturing gradient gel electrophoresis. Nucleic Acids Research 19, 41934198.CrossRefGoogle ScholarPubMed
Criscione, C. D. and Blouin, M. S. (2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198202.Google ScholarPubMed
Delmotte, F., Bucheli, E. and Shykoff, J. (1999). Host and parasite population structure in a natural plant-pathogen system. Heredity 82, 300308.CrossRefGoogle Scholar
Dover, G. A. (1982). Molecular drive: a cohesive mode of species evolution. Nature, London 299, 111117.CrossRefGoogle ScholarPubMed
Edwards, C. A. and Bohlen, P. J. (1996). Biology and Ecology of Earthworms, 3rd Edn.Chapman & Hall, London, UK.Google Scholar
Ellis, J. T., McMillan, D., Ryce, C., Payne, S., Atkinson, R. and Harper, P. A. W. (1999). Development of a single tube nested polymerase chain reaction assay for the detection of Neospora caninum DNA, International Journal for Parasitology 29, 15891596.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783791.CrossRefGoogle ScholarPubMed
Field, S. G. and Michiels, N. K. (2005). Parasitism and growth in the earthworm Lumbricus terrestris: fitness costs of the gregarine parasite Monocystis sp. Parasitology 130, 17.CrossRefGoogle ScholarPubMed
Flamant, F., Heizmann, P. and Nigon, V. (1984). Rearrangement of chloroplast ribosomal cistrons by unequal crossing-over in Euglena gracilis. Current Genetics 8, 9–13.CrossRefGoogle ScholarPubMed
Gandon, S., Capoweiz, Y., Dubois, Y., Michalakis, Y. and Olivien, I. (1996). Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society of London, B 263, 10031009.Google Scholar
Gaspar da Silva, D., Barton, E., Bunbury, N., Lunness, P., Bell, D. J. and Tyler, K. M. (2007). Molecular identity and heterogeneity of Trichomonad parasites in a closed avian population, Infection, Genetics and Evolution 7, 433440.CrossRefGoogle Scholar
Gerbi, S. A. (1986). Evolution of ribosomal DNA. In Molecular Evolutionary Genetics (ed. Maclntyre, R.), pp. 419517. Plenum Press, New York, USA.Google Scholar
Goggin, C. L. (1994). Variation in the two internal transcribed spacers and 5·8S ribosomal RNA from five isolates of the marine parasite Perkinsus (Protista, Apicomplexa). Molecular and Biochemical Parasitology 65, 179182.CrossRefGoogle ScholarPubMed
Grauer, D. and Li, W. H. (2000). Fundamentals of Molecular Evolution, 2nd Edn.Sinauer Associates, Inc., Sunderland, MA, USA.Google Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.CrossRefGoogle ScholarPubMed
Hamilton, W. D., Axelrod, R. and Tanese, R. (1990). Sexual reproduction as an adaptation to resist parasites. Proceedings of the National Academy of Sciences, USA 87, 35663573.CrossRefGoogle ScholarPubMed
Hillis, D. M. and Bull, J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42, 182192.CrossRefGoogle Scholar
Hnida, J. A. and Duszynski, D. W. (1999). Taxonomy and systematics of some Eimeria species of murid rodents as determined by the ITS1 region of the ribosomal gene complex. Parasitology 119, 349357.CrossRefGoogle ScholarPubMed
Lively, C. M. (1999). Migration, virulence, and the geographic mosaic of adaptation by parasites. The American Naturalist 153, S34S47.CrossRefGoogle ScholarPubMed
Mackinnon, D. L. and Hawes, R. J. S. (1961). Class Sporozoa. In An Introduction to the Study of Protozoa. pp. 156213. Oxford University Press, London, UK.Google Scholar
Mes, T. H. M. and Cornelissen, A. W. C. A. (2004). Non-homogenized ITS regions in the parasitic nematode Cooperia oncophora. Parasitology 129, 213222.CrossRefGoogle ScholarPubMed
Posada, D. and Buckley, T. R. (2004). Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Systematic Biology 53, 793808.CrossRefGoogle ScholarPubMed
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (2000). The diversity of parasites. Quarterly Review of Biology 75, 277293.CrossRefGoogle ScholarPubMed
Rooney, A. P. (2004). Mechanisms underlying the evolution and maintenance of functionally heterogeneous 18S rRNA genes in apicomplexans. Molecular Biology and Evolution 21, 17041711.CrossRefGoogle ScholarPubMed
Schmidt, G. D. and Roberts, L. S. (2000). Foundations of Parasitology. 6th Edn.McGraw-Hill Publishing, Boston, MA, USA.Google Scholar
Schneider, S., Roessli, D. and Excoffier, L. (2000). arlequin ver: 2000 a Software for Population Genetic Data Analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva, Switzerland.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.CrossRefGoogle ScholarPubMed
Tamura, K. and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.Google ScholarPubMed
Thompson, J. D., Gibson, T. J., Piewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.CrossRefGoogle ScholarPubMed
Thompson, J. N. (1994). The Coevolutionary Process. University of Chicago Press, Chicago, IL, USA.CrossRefGoogle Scholar
Yang, Z. (1993). Maximum likelihood estimation of the phylogeny from DNA sequences when substitution rates differ over sites. Molecular Biology and Evolution 10, 13961401.Google ScholarPubMed