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The dynamics of genetically marked Ascaris suum infections in pigs

Published online by Cambridge University Press:  18 December 2008

P. NEJSUM*
Affiliation:
Danish Centre for Experimental Parasitology, Department of Disease Biology, Copenhagen University, Denmark Genetics and Bioinformatics, Department of Animal and Veterinary Basic Sciences, Faculty of Life Sciences, Copenhagen University, Denmark
A. ROEPSTORFF
Affiliation:
Danish Centre for Experimental Parasitology, Department of Disease Biology, Copenhagen University, Denmark
T. J. C. ANDERSON
Affiliation:
Department of Genetics, Southwest Foundation for Biomedical Research, San Antonio, USA
C. JØRGENSEN
Affiliation:
Genetics and Bioinformatics, Department of Animal and Veterinary Basic Sciences, Faculty of Life Sciences, Copenhagen University, Denmark
M. FREDHOLM
Affiliation:
Genetics and Bioinformatics, Department of Animal and Veterinary Basic Sciences, Faculty of Life Sciences, Copenhagen University, Denmark
S. M. THAMSBORG
Affiliation:
Danish Centre for Experimental Parasitology, Department of Disease Biology, Copenhagen University, Denmark
*
*Corresponding author: Genetics and Bioinformatics, Department of Animal and Veterinary Basic Sciences, Faculty of Life Sciences, Copenhagen University, Denmark. Tel: +45 35283783. Fax: +45 35282774. E-mail: pn@life.ku.dk

Summary

The genotypes of both host and parasite may influence the outcome of parasitic infections, but few attempts have been made to quantify the effect of parasite genotype on macroparasite infections of socio-economic importance. We examined variation in particular traits during the infection in pigs with the parasitic nematode Ascaris suum. We infected 26 pigs with mixtures of equal proportions of embryonated eggs from 4 single female worms each with a unique mtDNA haplotype – the eggs from each female worm were a mixture of siblings and half-siblings. Pigs were necropsied on days 14, 17 and 28 following inoculation, which corresponded to time-points before, during and after the main immune responses against the nematode. A total of approximately 11 000 worms were recovered at necropsy. The location in the small intestine was recorded for all worms and the length and mtDNA haplotype were determined for about 4200 individual worms. There were significant differences in the distribution and abundance of the 4 individual haplotypes among individual pigs demonstrating strong interactions between parasite and host. We found significant differences in the abundance and position in the small intestine as well as the size of worms among haplotypes. We conclude that both parasite and host effects as well as the interplay between them play important roles in determining the characteristics and outcome of infection.

Type
Research Article
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Almasy, L. and Blangero, J. (1998). Multipoint quantitative-trait linkage analysis in general pedigrees. American Journal of Human Genetics 62, 11981211.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1985). Helminth infections of humans – mathematical models, population dynamics and control. Advances in Parasitology 24, 1101.CrossRefGoogle ScholarPubMed
Anderson, T. J. C. (1995). Ascaris infections in humans from North America: molecular evidence for cross-infection. Parasitology 110, 215219.CrossRefGoogle ScholarPubMed
Anderson, T. J. C., Komuniecki, R., Komuniecki, P. R. and Jaenike, J. (1995 a). Are mitochondria inherited paternally in Ascaris? International Journal for Parasitology 25, 10011004.CrossRefGoogle ScholarPubMed
Anderson, T. J. C., Romero-Abal, M. E. and Jaenike, J. (1995 b). Mitochondrial DNA and Ascaris microepidemiology: the composition of parasite populations from individual hosts, families and villages. Parasitology 110, 221229.CrossRefGoogle ScholarPubMed
Bellaby, T., Robinson, K. and Wakelin, D. (1996). Induction of differential T-helper-cell responses in mice infected with variants of the parasitic nematode Trichuris muris. Infection and Immunity 64, 791795.CrossRefGoogle ScholarPubMed
Bellaby, T., Robinson, K., Wakelin, D. and Behnke, J. M. (1995). Isolates of Trichuris muris vary in their ability to elicit protective immune responses to infection in mice. Parasitology 111, 353357.CrossRefGoogle ScholarPubMed
Carius, H. J., Little, T. J. and Ebert, D. (2001). Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55, 11361145.Google Scholar
Chan, M. S., Medley, G. F., Jamison, D. and Bundy, D. A. P. (1994). The evaluation of potential global morbidity attributable to intestinal nematode infections. Parasitology 109, 373387.CrossRefGoogle ScholarPubMed
Dowling, D. K., Friberg, U. and Lindell, J. (2008). Evolutionary implications of non-neutral mitochondrial genetic variation. Trends in Ecology and Evolution 23, 546554.CrossRefGoogle ScholarPubMed
Elliott, H. R., Samuels, D. C., Eden, J. A., Relton, C. L. and Chinnery, P. F. (2008). Pathogenic mitochondrial DNA mutations are common in the general population. The American Journal of Human Genetics 83, 254260.CrossRefGoogle ScholarPubMed
Flor, H. H. (1956). The complementary genic systems in flax and flax rust. Advances in Genetics 8, 2954.CrossRefGoogle Scholar
Galvani, A. P. (2005). Age-dependent epidemiological patterns and strain diversity in helminth parasites. Journal of Parasitology 91, 2430.CrossRefGoogle ScholarPubMed
Gauly, M. and Erhardt, G. (2001). Genetic resistance to gastrointestinal nematode parasites in Rhon sheep following natural infection. Veterinary Parasitology 102, 253259.CrossRefGoogle ScholarPubMed
Goudet, J. (1995). FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86, 485486.CrossRefGoogle Scholar
Grech, K., Watt, K. and Read, A. F. (2006). Host-parasite interactions for virulence and resistance in a malaria model system. Journal of Evolutionary Biology 19, 16201630.CrossRefGoogle Scholar
Johnston, C. E., Bradley, J. E., Behnke, J. M., Matthews, K. R. and Else, K. J. (2005). Isolates of Trichuris muris elicit different adaptive immune responses in their murine host. Parasite Immunology 27, 6978.CrossRefGoogle ScholarPubMed
Koyama, K. and Ito, Y. (1996). Comparative studies on immune responses to infection in susceptible B10.BR mice infected with different strains of the murine nematode parasite Trichuris muris. Parasite Immunology 18, 257263.CrossRefGoogle ScholarPubMed
Li, T. H., Guo, X. R., Xue, J., Hu, L., Qiang, H. Q., Xue, H. C., Bin, Z., Hawdon, J. M. and Xiao, S. H. (2004). Comparison of mitochondrial cytochrome oxidase 1 DNA sequences from Necator americanus hookworms maintained for 100 generations in golden hamsters (Mesocricetus auratus) and hookworms from natural human infections. Acta Tropica 92, 7175.CrossRefGoogle ScholarPubMed
Lively, C. M., Dybdahl, M. F., Jokela, J., Osnas, E. E. and Delph, L. F. (2004). Host sex and local adaptation by parasites in a snail-trematode interaction. The American Naturalist 164 (Suppl. 5), S6S18.CrossRefGoogle Scholar
Maafi, Z. T., Subbotin, S. A. and Moens, M. (2003). Molecular identification of cyst-forming nematodes (Heteroderidae) from Iran and a phylogeny based on ITS-rDNA sequences. Nematology 5, 99111.CrossRefGoogle Scholar
Miquel, N., Roepstorff, A., Bailey, M. and Eriksen, L. (2005). Host immune reactions and worm kinetics during the expulsion of Ascaris suum in pigs. Parasite Immunology 27, 7988.CrossRefGoogle ScholarPubMed
Morand, S., Manning, S. D. and Woolhouse, M. E. J. (1996). Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proceedings of the Royal Society of London, B 263, 119128.Google ScholarPubMed
Nadler, S. A., Lindquist, R. L. and Near, T. J. (1995). Genetic structure of midwestern Ascaris suum populations: a comparison of isoenzyme and RAPD markers. Journal of Parasitology 81, 385394.CrossRefGoogle ScholarPubMed
Nejsum, P., Frydenberg, J., Roepstorff, A. and Parker, E. D. (2005). Population structure in Ascaris suum (Nematoda) among domestic swine in Denmark as measured by whole genome DNA fingerprinting. Hereditas 142, 714.CrossRefGoogle ScholarPubMed
Nejsum, P., Thamsborg, S. M., Jørgensen, C., Fredholm, M. and Roepstorff, A. (2008). A novel technique for identification of Ascaris suum cohorts in pigs. Veterinary Parasitology 154, 171174.CrossRefGoogle ScholarPubMed
Paterson, S. (2005). No evidence for specificity between host and parasite genotypes in experimental Strongyloides ratti (Nematoda) infections. International Journal for Parasitology 35, 15391545.CrossRefGoogle ScholarPubMed
Paterson, S. and Viney, M. E. (2003). Functional consequences of genetic diversity in Strongyloides ratti infections. Proceedings of the Royal Society of London, B 270, 10231032.CrossRefGoogle ScholarPubMed
Roepstorff, A., Eriksen, L., Slotved, H. C. and Nansen, P. (1997). Experimental Ascaris suum infection in the pig: worm population kinetics following single inoculations with three doses of infective eggs. Parasitology 115, 443452.CrossRefGoogle ScholarPubMed
Rowe, A., McMaster, K., Emery, D. and Sangster, N. (2008). Haemonchus contortus infection in sheep: parasite fecundity correlates with worm size and host lymphocyte counts. Veterinary Parasitology 153, 285293.CrossRefGoogle ScholarPubMed
Schulenburg, H. and Ewbank, J. J. (2004). Diversity and specificity in the interaction between Caenorhabditis elegans and the pathogen Serratia marcescens. BMC Evolutionary Biology 4, 49.CrossRefGoogle ScholarPubMed
Skørping, A., Read, A. F. and Keymer, A. E. (1991). Life history covariation in intestinal nematodes of mammals. Oikos 60, 365372.CrossRefGoogle Scholar
Slotved, H. C., Barnes, E. H., Eriksen, L., Roepstorff, A., Nansen, P. and Bjørn, H. (1997). Use of an agar-gel technique for large scale application to recover Ascaris suum larvae from intestinal contents of pigs. Acta Veterinaria Scandinavica 38, 207212.CrossRefGoogle ScholarPubMed
Stear, M. J. and Bishop, S. C. (1999). The curvilinear relationship between worm length and fecundity of Teladorsagia circumcincta. International Journal for Parasitology 29, 777780.CrossRefGoogle ScholarPubMed
Thrall, P. H. and Burdon, J. J. (2003). Evolution of virulence in a plant host-pathogen metapopulation. Science 299, 17351737.CrossRefGoogle Scholar
Weir, B. S. and Cockerham, C. C. (1984). Estimating F-Statistics for the analysis of population structure. Evolution 38, 13581370.Google ScholarPubMed
Williams-Blangero, S., Subedi, J., Upadhayay, R. P., Manral, D. B., Rai, D. R., Jha, B., Robinson, E. S. and Blangero, J. (1999). Genetic analysis of susceptibility to infection with Ascaris lumbricoides. American Journal of Tropical Medicine and Hygiene 60, 921926.CrossRefGoogle ScholarPubMed