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Benefits of fidelity: does host specialization impact nematode parasite life history and fecundity?

Published online by Cambridge University Press:  24 January 2013

J. KOPRIVNIKAR  and
H. S. RANDHAWA
J. KOPRIVNIKAR*
Affiliation:
Department of Biology, Brandon University, 270 18th Street, Brandon, Manitoba, CanadaR7A 6A9
H. S. RANDHAWA
Affiliation:
Ecology Degree Programme, Department of Botany, University of Otago, PO Box 56 Dunedin, New Zealand9054
*
*Corresponding author: Department of Biology, Brandon University, 270 18th Street, Brandon, Manitoba, CanadaR7A 6A9. Tel: +1 204 727 9787. Fax: +1 204 728 7346. E-mail: [email protected]
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Summary

The range of hosts used by a parasite is influenced by macro-evolutionary processes (host switching, host–parasite co-evolution), as well as ‘encounter filters’ and ‘compatibility filters’ at the micro-evolutionary level driven by host/parasite ecology and physiology. Host specialization is hypothesized to result in trade-offs with aspects of parasite life history (e.g. reproductive output), but these have not been well studied. We used previously published data to create models examining general relationships among host specificity and important aspects of life history and reproduction for nematodes parasitizing animals. Our results indicate no general trade-off between host specificity and the average pre-patent period (time to first reproduction), female size, egg size, or fecundity of these nematodes. However, female size was positively related to egg size, fecundity, and pre-patent period. Host compatibility may thus not be the primary determinant of specificity in these parasitic nematodes if there are few apparent trade-offs with reproduction, but rather, the encounter opportunities for new host species at the micro-evolutionary level, and other processes at the macro-evolutionary level (i.e. phylogeny). Because host specificity is recognized as a key factor determining the spread of parasitic diseases understanding factors limiting host use are essential to predict future changes in parasite range and occurrence.

Keywords

diseasefecundityspecificitycompatibilitytrade-offphylogenetic influencesmicro-evolutionmacro-evolution
Type
Research Article
Information
Parasitology , Volume 140 , Issue 5 , April 2013 , pp. 587 - 597
Copyright
Copyright © Cambridge University Press 2013

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References

REFERENCES

Adamson, M. L. (1989). Evolutionary biology of the Oxyurida (Nematoda): biofacies of a haplodiploid taxon. Advances in Parasitology 28, 175–228.CrossRefGoogle ScholarPubMed
Agosta, S. J., Janz, N. and Brooks, D. R. (2010). How specialists can be generalists: resolving the ‘parasite paradox’ and implications for emerging infectious disease. Zoologia 27, 151–162.Google Scholar
Amarante, A. F. T., Rocha, R. A. and Bricarello, P. A. (2007). Relationship of intestinal histology with the resistance to Trichostrongylus colubriformis infection in three breeds of sheep. Pesquisa Veterinaria Brasileira 27, 43–48.CrossRefGoogle Scholar
Anderson, D. R. (2008). Model Based Inference in the Life Sciences: A Primer on Evidence. Springer, New York, USA.Google Scholar
Anderson, R. C. (1992). Nematode Parasites of Vertebrates: their Development and Transmissions. Commonwealth Agricultural Bureaux, Farnham, Hants, UK.Google Scholar
Anderson, R. M. and May, R. M. (1982). Directly transmitted infectious diseases: control by vaccination. Science 215, 1053–1060.Google Scholar
Anderson, R. M. and May, R. M. (1992). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford, UK.Google Scholar
Andrews, J. R. H. (1969). A guide to the identification of helminth parasites recorded from wild ruminants in New Zealand. Tuatara 17, 67–81.Google Scholar
Andrews, J. S. (1939). Life history of the nematode Cooperia curticei, and the development of resistance in sheep. Journal of Agriculture Research 58, 771–785.Google Scholar
Audebert, F., Cassone, J., Kerboeuf, D. and Durette-Desset, M. C. (2004). Development of Nematodirus spathiger (Nematoda, Molineoidea) in the rabbit and comparison with other Nematodirus spp. parasites of ruminants. Parasitology Research 94, 112–117.Google Scholar
Bates, D. and Maechler, M. (2009). lme4: Linear Mixed-Effects Models using S4 classes. Available at http://CRAN.R-project.org/package=lme4.Google Scholar
Begon, M., Harper, J. L. and Townsend, C. R. (1996). Ecology: Individuals, Populations and Communities, 3rd Edn. Blackwell Science, Oxford, UK.Google Scholar
Bernays, E. and Graham, M. (1988). On the evolution of host specificity in phytophagous arthropods. Ecology 69, 886–892.Google Scholar
Berntzen, A. K. (1965). Comparative growth and development of Trichinella spiralis in vitro and in vivo, with a redescription of the life cycle. Experimental Parasitology 16, 74–106.Google Scholar
Blaxter, M. L., De Ley, P., Garey, J. R., Liuk, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M, Frisse, L. M., Vida, J. T. and Thomas, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature, London 392, 71–75.Google Scholar
Borji, H., Raji, A. R. and Naghibi, A. G. (2011). The comparative morphology of Marshallagia marshalli and Ostertagia occidentalis (Nematoda: Strongylida, Trichostrongylidae) by scanning electron microscopy. Parasitology Research 108, 1391–1395.CrossRefGoogle ScholarPubMed
Brooks, D. R. and McLennan, D. A. (1991). Phylogeny, Ecology, and Behavior. A Research Program in Comparative Biology. The University of Chicago Press, Chicago, IL, USA.Google Scholar
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd Edn. Springer-Verlag, New York, USA.Google Scholar
Burrows, R. B. (1962). Comparative morphology of Ancylostoma tubaeforme (Zeder, 1800) and Ancylostoma caninum . Journal of Parasitology 48, 715–718.Google Scholar
Bush, A. O. and Kennedy, C. R. (1994). Host fragmentation and helminth parasites: hedging your bets against extinction. International Journal for Parasitology 24, 1333–1343.Google Scholar
Combes, C. (1991). Evolution of parasite life cycles. In Parasite-Host Associations: Coexistence or Conflict? (ed. Toft, C. A., Aeschlimann, A. and Bolis, L.), pp. 62–82. Oxford University Press, Oxford, UK.Google Scholar
Combes, C. (1995). Interactions Durables: Ecologie et Evolution du Parasitisme. Masson, Paris, France.Google Scholar
Combes, C. (2001). Parasitism: The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, IL, USA.Google Scholar
Coyne, M. J., Smith, G. and Johnstone, C. (1991). Fecundity of gastrointestinal trichostrongylid nematodes of sheep in the field. American Journal of Veterinary Research 52, 1182–1188.Google Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287, 443–449.Google Scholar
de Gruijter, J. M., Blotkamp, J., Gasser, R. B., Amponsah, S. and Polderman, A. M. (2006). Morphological variability within Oesophagostomum bifurcum among different primate species from Ghana. Journal of Helminthology 80, 357–361.Google Scholar
Desdevises, D., Morand, S. and Legendre, P. (2002). Evolution and determinants of host specificity in the Genus Lamellodiscus (Monogenea). Biological Journal of the Linnean Society, 77, 431–443.CrossRefGoogle Scholar
Dobson, C. (1964). Host endocrine interactions with nematode infections. I. Effects of sex, gonadectomy, and thyroidectomy on experimental infections in lambs. Experimental Parasitology 15, 200–212.CrossRefGoogle ScholarPubMed
Ehrenford, F. A. (1954). The life cycle of Nematospiroides dubius Baylis (Nematoda: Heligmosomidae). Journal of Parasitology 40, 480–481.Google Scholar
Euzet, L. and Combes, C. (1980). Les problèmes de l'espèce chez les animaux parasites. Bulletin de la Société Zoologique de France 40, 239–285.Google Scholar
Feliu, C., Spakulova, M., Casanova, J. C., Renaud, F., Morand, S., Hugot, J. P., Santalla, F. and Durand, P. (2000). Genetic and morphological heterogeneity in small rodent whipworms in south western Europe: characterization of Trichuris muris and description of Trichuris arvicolae n. sp. (Nematoda: Trichuridae). Journal of Parasitology 86, 442–449.Google Scholar
Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist 125, 1–15.CrossRefGoogle Scholar
Fenton, A., Viney, M. E. and Lello, J. (2010). Detecting interspecific macroparasite interactions from ecological data: patterns and process. Ecology Letters 13, 606–615.Google Scholar
Foreyt, W. J. (2001). Veterinary Parasitology Reference Manual, 5th Edn. Iowa State University Press, Ames, Iowa, USA.Google Scholar
Fowler, M. E. (2010). Medicine and Surgery of Camelids. Wiley-Blackwell Publishing, Ames, IA, USA.Google Scholar
Futuyma, D. J. and Moreno, G. (1988). The evolution of ecological specialization. Annual Review of Ecology and Systematics 19, 207–233.Google Scholar
Garland, T., Harvey, P. H. and Ives, A. R. (1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41, 18–32.CrossRefGoogle Scholar
Gemmill, A. W., Viney, M. E. and Read, A. F. (2000). The evolutionary ecology of host-specificity: experimental studies with Strongyloides ratti . Parasitology 120, 429–437.Google 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.Google Scholar
Haley, A. J. (1961). Biology of the rat nematode Nippostrongylus brasiliensis (Travassos, 1914) I. Systematics, hosts and geographical distribution. Journal of Parasitology 47, 727–732.Google Scholar
Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. and Challenger, W. (2008). GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131.Google Scholar
Herreras, M. V., Montero, F. E., Marcogliese, D. J., Raga, J. A. and Balbuena, J. A. (2007 a). Comparison of a manual and an automated method to estimate the number of uterine eggs in anisakid nematodes: to Coulter or not to Coulter. Is that the question? Journal of Parasitology 93, 423–425.Google Scholar
Herreras, M. V., Montero, F. E., Marcogliese, D. J., Raga, J. A. and Balbuena, J. A. (2007 b). Phenotypic tradeoffs between egg number and egg size in three parasitic anisakid nematodes. Oikos 116, 1737–1747.Google Scholar
Hoberg, E. P. and Brooks, D. R. (2008). A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems. Journal of Biogeography 35, 1533–1550.Google Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MrBayes. Bayesian inference of phylogeny. Bioinformatics 17, 754–755.Google Scholar
Huelsenbeck, J. P., Ronquist, F., Nielson, R. and Bollback, J. P. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 2310–2314.CrossRefGoogle ScholarPubMed
John, J. L. (1994). The avian spleen: a neglected organ. Quarterly Reviews of Biology 69, 327–351.Google Scholar
Kelly, D. W., Paterson, R. A., Townsend, C. R., Poulin, R. and Tompkins, D. M. (2009). Parasite spillback: a neglected concept in invasion ecology? Ecology 90, 2047–2056.Google Scholar
Krepel, H. P. and Polderman, A. M. (1992). Egg production of Oesophagostomum bifurcum, a locally common parasite of humans in Togo. American Journal of Tropical Medicine and Hygiene 46, 469–472.Google Scholar
Lawton, J. H. (1978). Host-plant influences on insect diversity: the effects of time and space. Symposia of the Royal Entomological Society London 9, 105–125.Google Scholar
Lichtenfels, J. R. and Pilitt, P. A. (1991). A redescription of Ostertagia bison is (Nematoda: Trichostrongyloidea) and a key to species of Ostertagiinae with a tapering lateral synlophe from domestic ruminants in North America. Journal of the Helminthological Society of Washington, 58, 231–234.Google Scholar
Love, S. C. J. and Hutchinson, G. W. (2003). Pathology and diagnosis of internal parasites in ruminants. Gross Pathology of Ruminants, Proceedings 350, Post Graduate Foundation in Veterinary Science, pp. 309–338. University of Sydney, Sydney, Australia.Google Scholar
Maddison, D. R. and Maddison, W. P. (2005). MacClade 4, Version 4.07. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Maddison, W. P. (1990). A method for testing the correlated evolution of two binary characters: are gains or losses concentrated on certain branches of a phylogenetic tree? Evolution 44, 539–557.Google Scholar
Maddison, W. P. and Maddison, D. R. (2007). Mesquite: a Modular System for Evolutionary Analysis. Version 2.5. Available at http://mesquiteproject.org.Google Scholar
May, H. G. (1921). Observations on the nematode genus Nematodirus, with descriptions of new species. Proceedings of the U.S. National Museum 58, 577–578.Google Scholar
McCoy, K. D., Boulinier, T., Tirard, C. and Michalakis, Y. (2001). Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae . Molecular Ecology 14, 395–405.Google Scholar
Meeusen, E. N. T. and Balic, A. (2000). Do eosinophils have a role in the killing of helminth parasites? Parasitology Today 16, 95–101.Google Scholar
Midford, P. E., Garland, T. Jr. and Maddison, W. P. (2005). PDAP Package of Mesquite. Version 1.07. Available at www.mesquiteproject.org Google Scholar
Møller, A. P. and Erritzøe, J. (1996). Parasite virulence and host immune defence: host immune response is related to nest re-use in birds. Evolution 50, 2066–2072.Google Scholar
Morand, S. (1996 a). Biodiversity of parasites in relation with their life cycle. In The Genesis and Maintenance of Biological Diversity (ed. Hochberg, M., Clobert, J. and Barbault, R.), pp. 243–260. Oxford University Press, Oxford, UK.Google Scholar
Morand, S. (1996 b). Life-history traits in parasitic nematodes: a comparative approach for the search of invariants. Functional Ecology 10, 210–218.Google Scholar
Morand, S. and Poulin, R. (2003). Phylogenies, the comparative method and parasite evolutionary ecology. Advances in Parasitology 54, 281–302.Google Scholar
Morand, S. and Sorci, G. (1998). Determinants of life-history evolution in nematodes. Parasitology Today 14, 193–196.Google Scholar
Morgan, E. (2003). Parasites of saiga antelopes and domestic livestock in Kazakhstan. Ph.D. thesis, University of Warwick, Coventry, UK.Google Scholar
Muller, R. and Wakelin, D. (2002). Worms and Human Disease. CABI Publishing Series, Wallingford, UK.CrossRefGoogle Scholar
Mupeyo, B., Barry, T. N., Pomroy, W. E., Ramírez-Restrepo, C. A., López-Villalobos, N. and Pernthaner, A. (2011). Effects of feeding willow (Salix spp.) upon death of established parasites and parasite fecundity. Animal Feed Science and Technology 164, 8–20.Google Scholar
Perlman, S. J. and Jaenike, J. (2001). Competitive interactions and persistence of two nematode species that parasitize Drosophila recens . Ecology Letters 4, 577–584.CrossRefGoogle Scholar
Popiolek, M., Szczesna, J., Kotusz, J., Kusznierz, J. and Witkowski, A. (2007). The level of infection with gastro-intestinal nematodes in Svalbard reindeers from Hornsund area. Spitsbergen Polish Polar Research 28, 277–282.Google Scholar
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, 793–808.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
Poulin, R. (1992). Determinants of host-specificity in parasites of freshwater fishes. International Journal for Parasitology 22, 753–758.Google Scholar
Poulin, R. (1995). Evolution of parasite life history traits: myths and reality. Parasitology Today 11, 342–345.Google Scholar
Poulin, R. (1996). The evolution of life history strategies in parasitic animals. Advances in Parasitology 37, 107–134.Google Scholar
Poulin, R. (2005). Relative infection levels and taxonomic distances among the host species used by a parasite: insights into parasite specialization. Parasitology 130, 109–115.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ, USA.Google Scholar
Poulin, R. and Hamilton, W. J. (1997). Ecological correlates of body size and egg size in parasitic Ascothoracida and Rhizocephala (Crustacea). Acta Oecologia 18, 621–635.Google Scholar
Poulin, R. and Keeney, D. B. (2008). Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 24–28.Google Scholar
Poulin, R. and Mouillot, D. (2003). Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126, 473–480.Google Scholar
Poulin, R. and Mouillot, D. (2004). The relationship between specialization and local abundance: the case of helminth parasites of birds. Oecologia 140, 372–378.Google Scholar
Poulin, R. and Mouillot, D. (2005). Host specificity and the probability of discovering species of helminth parasites. Parasitology 130, 709–715.Google Scholar
Poulin, R. and Morand, S. (2004). The diversity of parasites. The Quarterly Review of Biology 75, 277–293.Google Scholar
Poulin, R., Krasnov, B. R., Shenbrot, G. I., Mouillot, D. and Khokhlova, I. S. (2006). Evolution of host specificity in fleas: is it directional and irreversible? International Journal for Parasitology 36, 185–191.Google Scholar
Poulin, R., Guilhaumon, F., Randhawa, H. S., Luque, J. L. and Mouillot, D. (2011). Identifying hotspots of parasite diversity from species–area relationships: host phylogeny versus host ecology. Oikos 120, 740–747.Google Scholar
Purvis, A. and Garland, T. Jr. (1993). Polytomies in comparative analyses of continuous data. Systematic Biology 42, 569–575.CrossRefGoogle Scholar
R Development Core Team (2012). R: A Language and Environment for Statistical Computing. Version 2.15·0. Available at http://www.r-project.org. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Read, A. F. and Skorping, A. (1995). The evolution of tissue migration by parasitic nematode larvae. Parasitology 111, 359–371.Google Scholar
Roberts, L. S. and Janovy, J. Jr. (2009). Foundations of Parasitology, 8th Edn. McGraw-Hill, New York, USA.Google Scholar
Rohde, K. (1979). A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. American Naturalist 114, 648–671.Google Scholar
Saif, Y. M.., Fadly, A. M., Glisson, J. R., McDougald, L. R., Nolan, L. K. and Swayne, D. E. (2008). Diseases of Poultry, 12th Edn. Iowa State University Press, Ames, IA, USA.Google Scholar
Skorping, A., Read, A. F. and Keymer, A. E. (1991). Life history covariation in intestinal nematodes of mammals. Oikos 60, 365–372.Google Scholar
Sorci, G., Skarstein, F., Morand, S. and Hugot, J. -P. (2003). Correlated evolution between host immunity and parasite life histories in primates and oxyurid parasites. Proceedings of the Royal Society of London, B 270, 2481–2484.Google Scholar
Sowemino, O. A. and Asaolu, S. O. (2008). The daily egg production of Ancyclostoma caninum and the distribution of the worm along the digestive tract of the dog. Research Journal of Parasitology 3, 92–97.Google Scholar
Stear, M. J., Strain, S. and Bishop, S. C. (1999). Mechanisms underlying resistance to nematode infection. International Journal for Parasitology 29, 51–56.Google Scholar
Stoll, N. R. (1946). Necator americanus and Ancylostoma duodenale in Guam, Leyte and Okinawa, with a note on hookworm egg sizes. Journal of Parasitology 32, 490–496.Google Scholar
Tetley, J. H. (1941). The differentiation of the eggs of the trichostrongylid species Nematodirus filicollis and N . spathiger. Journal of Parasitology 27, 473–480.Google Scholar
Tetley, J. H. (1950). The differentiation of the eggs of Haemonchus contortus and Ostertagia species of the sheep and a note on the relative generic egg-laying rates. Parasitology 40, 273–275.Google Scholar
Thienpont, D., Rochette, F. and Vanparijs, O. F. J. (1986). Diagnosing Helminthiasis by Coprological Examination, 2nd Edn. Janseen Research Foundation, Beerse, Belgium.Google Scholar
Thompson, J. N. (1994). The Coevolutionary Process. University of Chicago Press, Chicago, IL, USA.Google Scholar
Threlkeld, W. L. (1934). The life history of Ostertagia circumcincta. Technical Bulletin No. 5, Virginia Polytechnic Institute, Virginia. Agricultural Experimental Station, Blacksburg, VA, USA.Google Scholar
Tinsley, R. C. (2004). Platyhelminth parasite reproduction: some general principles derived from monogeneans. Canadian Journal of Zoology 82, 270–291.Google Scholar
Torchin, M. E. and Mitchell, C. E. (2004). Parasites, pathogens, and invasions by plants and animals. Frontiers in Ecology and the Environment 2, 183–190.CrossRefGoogle Scholar
Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J. & Kuris, A. M. (2003). Introduced species and their missing parasites. Nature, London 421, 628–630.CrossRefGoogle ScholarPubMed
Trouve, S., Sasal, P., Jourdane, J., Renaud, F. and Morand, S. (1998). The evolution of life-history traits in parasitic and free-living platyhelminthes: a new perspective. Oecologia 115, 370–378.Google Scholar
Ward, S. A. (1992). Assessing functional explanations of host specificity. American Naturalist 139, 883–891.CrossRefGoogle Scholar
Yoshikawa, H., Yamada, M., Matsumoto, Y. and Yoshida, Y. (1989). Variations in egg size of Trichuris trichuria . Parasitology Research 75, 649–654.CrossRefGoogle Scholar
Zajac, A. and Conboy, G. A. (2012). Veterinary Clinical Parasitology, 8th Edn. Iowa State University Press, Ames, IA, USA.Google Scholar
Ziem, J. B. (2006). Controlling human oesophagostomiasis in northern Ghana. Ph.D. thesis, Leiden University, Leiden, the Netherlands.Google Scholar