Hostname: page-component-cc8bf7c57-j4qg9 Total loading time: 0 Render date: 2024-12-12T01:49:41.890Z Has data issue: false hasContentIssue false
  • English
  • Français

An evolutionary perspective on gastrointestinal nematodes of sheep

Published online by Cambridge University Press:  19 April 2011

M.J. Stear ,
D. Singleton  and
L. Matthews
M.J. Stear*
Affiliation:
Boyd Orr Centre for Population and Ecosystem Health, College of Medical, Veterinary and Life Sciences, University of Glasgow, Garscube Estate, Bearsden Road, Glasgow, G61 1QH, UK
D. Singleton
Affiliation:
Boyd Orr Centre for Population and Ecosystem Health, College of Medical, Veterinary and Life Sciences, University of Glasgow, Garscube Estate, Bearsden Road, Glasgow, G61 1QH, UK
L. Matthews
Affiliation:
Boyd Orr Centre for Population and Ecosystem Health, College of Medical, Veterinary and Life Sciences, University of Glasgow, Garscube Estate, Bearsden Road, Glasgow, G61 1QH, UK
*
*E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The purpose of this paper was to discuss from an evolutionary perspective the interaction between domestic sheep (Ovis aries) and their gastrointestinal nematodes. Although evolution is the central theme of biology, there has been little attempt to consider how evolutionary forces have shaped and continue to shape the relationships between domestic animals and their parasite community. Mathematical modelling of the host–parasite relationship indicated that the system is remarkably robust to perturbations in its parameters. This robustness may be a consequence of the long coevolution of host and parasites. Although nematodes can potentially evolve faster than the host, coevolution is not dominated by the parasite and there are several examples where breeds of cattle or sheep have evolved high levels of resistance to disease. Coevolution is a more equal partnership between host and nematode than is commonly assumed. Coevolution between parasites and the host immune system is often described as an arms race where both host immune response genes and parasite proteins evolve rapidly in response to each other. However, initial results indicate that nematode antigens are not evolving rapidly; the arms race between the immune system and nematodes, if it exists, is happening very slowly. Fisher's fundamental theorem of natural selection states that genes with positive effects on fitness will be fixed by natural selection. Consequently, heritable variation in fitness traits is expected to be low. Contrary to this argument, there is considerable genetic variation in resistance to nematode infection. In particular, the heritabilities of nematode-specific IgA and IgE activity are moderate to high. The reasons for this apparent violation of the fundamental theorem of natural selection are not clear but several possible explanations are explored. Faecal nematode egg counts increase at the beginning of the grazing season – a phenomenon known as the periparturient rise. This increase benefits host and parasite and appears to be a consequence of coevolution. In conclusion, an evolutionary perspective can shed light on many aspects of the host–parasite relationship in domestic animals.

Type
Research Papers
Information
Journal of Helminthology , Volume 85 , Issue 2 , June 2011 , pp. 113 - 120
Copyright
Copyright © Cambridge University Press 2011

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

Bahirathan, M., Miller, J.E., Barras, S.R. & Kearney, M.T. (2000) Variation in susceptibility of Suffolk and Gulf Coast Native suckling lambs to naturally acquired strongylate nematode infections. Veterinary Parasitology 65, 259–268.Google Scholar
Baker, R.L., Mwamachi, D.M., Audho, J.O., Aduda, E.O. & Thorpe, W. (1999) Genetic resistance to gastro-intestinal nematode parasites in Red Maasai, Dorper and Red Maasai × Dorper ewes in the sub-humid tropics. Animal Science 69, 335–344.Google Scholar
Bishop, S.C. & Stear, M.J. (2001) Inheritance of faecal egg counts during early lactation in Scottish Blackface ewes facing mixed, natural nematode infections. Animal Science 73, 389–395.CrossRefGoogle Scholar
Bishop, S.C., Bairden, K., McKellar, Q.A., Park, M. & Stear, M.J. (1996) Genetic parameters for faecal egg count following mixed, natural, predominantly Ostertagia circumcincta infection and relationships with liveweight in young lambs. Animal Science 63, 423–428.Google Scholar
Bishop, S.C., Jackson, F., Coop, R.L. & Stear, M.J. (2004) Genetic parameters for resistance to nematode infections in Texel lambs and their utility in breeding programmes. Animal Science 78, 185–194.Google Scholar
Bisset, S.A., Morris, C.A., McEwan, J.C. & Vlassoff, A. (2001) Breeding sheep in New Zealand that are less reliant on anthelmintics to maintain health and productivity. New Zealand Veterinary Journal 49, 236–246.Google Scholar
Blaxter, M., Dorris, M. & De Ley, P. (2000) Patterns and processes in the evolution of animal parasitic nematodes. Nematology 2, 43–55.Google Scholar
Coop, R.L., Sykes, A.R. & Angus, K.W. (1982) The effect of three levels of Ostertagia circumcincta larvae on growth rate, food intake and body composition of growing lambs. Journal of Agricultural Science (Cambridge) 98, 247–255.Google Scholar
Coop, R.L., Graham, R.B., Jackson, F., Wright, S.E. & Angus, K.W. (1985) Effect of experimental Ostertagia circumcincta infection on the performance of grazing lambs. Research in Veterinary Science 38, 282–287.Google Scholar
Cornell, S.J. (2006) Modelling nematode populations: 20 years of progress. Trends in Parasitology 21, 542–545.Google Scholar
Donaldson, J., van Houtert, M.F.J. & Sykes, A.R. (1998) The effect of nutrition on the periparturient parasite status of mature ewes. Animal Science 67, 523–533.Google Scholar
Dorris, M., De Ley, P. & Blaxter, M.L. (1999) Molecular analysis of nematode diversity and the evolution of parasitism. Parasitology Today 15, 188–193.Google Scholar
Dunne, D.W. & Cooke, A. (2005) A worm's eye view of the immune system: consequences for evolution of human autoimmune disease. Nature Reviews Immunology 5, 420–425.Google Scholar
Fernández, M.H. & Vrba, E.S. (2005) A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biological Reviews 80, 269–302.Google Scholar
Fisher, R.A. (1930) The genetical theory of natural selection. Oxford, Oxford University Press.Google Scholar
Gaba, S., Gruner, L. & Cabaret, J. (2006) The establishment rate of a sheep nematode: revisiting classics using a meta-analysis of 87 experiments. Veterinary Parasitology 140, 302–311.CrossRefGoogle Scholar
Gamble, H.R. & Zajac, A.M. (1992) Resistance of St. Croix lambs to Haemonchus contortus in experimentally and naturally acquired infections. Veterinary Parasitology 41, 211–225.Google Scholar
Gauly, M., Kraus, M., Vervelde, L., van Leeuwen, M.A.W. & Erhardt, G. (2002) Estimating genetic differences in natural resistance in Rhön and Merinoland sheep following experimental Haemonchus contortus infection. Veterinary Parasitology 106, 55–67.Google Scholar
Hoberg, E.P. & Lichtenfels, J.R. (1994) Phylogenetic systematic analysis of the trichostrongylidae (nematoda), with an initial assessment of coevolution and biogeography. Journal of Parasitology 80, 976–996.Google Scholar
Hoberg, E.P., Monsen, K.J., Kutz, S. & Blouin, M.S. (1999) Structure, biodiversity, and historical biogeography of nematode faunas in holartic ruminants: morphological and molecular diagnoses for Teladorsagia boreoarcticus n. sp. (Nematodea: Ostertagiinae), a dimorphic cryptic species in muskoxen (Ovibos moschatus). Journal of Parasitology 85, 910–934.Google Scholar
Huntley, J.F., Redmond, J., Welfare, W., Brennan, G., Jackson, F., Kooyman, F. & Vervelde, L. (2001) Studies on the immunoglobulin E responses to Teladorsagia circumcincta in sheep: purification of a major high molecular weight allergen. Parasite Immunology 23, 227–235.Google Scholar
Janis, C.M. (1993) Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annual Review of Ecology and Systematics 24, 467–500.Google Scholar
Leignel, V., Cabaret, J. & Humbert, J.F. (2002) New molecular evidence that Teladorsagia circumcincta (Nematoda: Trichostrongylidea) is a species complex. Journal of Parasitology 88, 135–140.Google Scholar
Miller, J.E. & Horohov, D.W. (2006) Immunological aspects of nematode parasite control in sheep. Journal of Animal Science 84, E124–E132.Google Scholar
Mugambi, J.M., Wanyangu, S.W., Bain, R.K., Owango, M.O., Duncan, J.L. & Stear, M.J. (1996) Response of Dorper and Red Maasai lambs to trickle Haemonchus contortus infections. Research in Veterinary Science 61, 218–221.Google Scholar
Murphy, L., Eckersall, P.D., Bishop, S.C., Pettit, J.J., Huntley, J., Burchmore, R. & Stear, M.J. (2010) Genetic variation among lambs in peripheral IgE activity against the larval stages of Teladorsagia circumcincta. Parasitology 137, 1249–1260.Google Scholar
Nginyi, J.M., Duncan, J.L., Mellor, D.J., Stear, M.J., Wanyangu, S.W., Bain, R.K. & Gatongi, P.M. (2001) Epidemiology of parasitic gastrointestinal infections of ruminants on smallholder farms in central Kenya. Research in Veterinary Science 70, 33–39.Google Scholar
Nicholas, F.W. (1987) Veterinary genetics. Oxford, Oxford University Press.Google Scholar
Nicholas, F.W. (2010) Introduction to veterinary genetics. Chichester, Wiley-Blackwell.Google Scholar
Nieuwhof, G.J. & Bishop, S.C. (2005) Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact. Animal Science 81, 23–29.Google Scholar
Pál, C., Papp, B. & Lercher, M.J. (2006) An integrated view of protein evolution. Nature Reviews Genetics 7, 337–348.Google Scholar
Perry, B.D. & Randolph, T.F. (1999) Improving the assessment of the economic impact of parasitic diseases and of their control in production animals. Veterinary Parasitology 84, 145–168.Google Scholar
Raadsma, H.W., Gray, G.D. & Woolaston, R.R. (2009) Breeding for disease resistance in Merino sheep in Australia. Revue Scientifique et Technique de l'Office International des Epizooties 17, 315–328.Google Scholar
Sayers, G. & Sweeney, T. (2005) Gastrointestinal nematode infection in sheep – a review of the alternatives to anthelmintics in parasite control. Animal Health Research Reviews 6, 159–171.Google Scholar
Sayers, G., Good, B., Hanrahan, J.P., Ryan, M., Angles, J.M. & Sweeney, T. (2005a) Major histocompatibility complex DRB1 gene: its role in nematode resistance in Suffolk and Texel sheep breeds. Parasitology 131, 403–409.Google Scholar
Sayers, G., Good, B., Hanrahan, J.P., Ryan, M. & Sweeney, T. (2005b) Intron 1 of the interferon γ gene: its role in nematode resistance in Suffolk and Texel sheep breeds. Research in Veterinary Science 79, 191–196.Google Scholar
Shaw, R.J., McNeill, M.M., Maass, D.R., Hein, W.R., Barber, T.K., Wheeler, M., Morris, C.A. & Shoemaker, C.B. (2003) Identification and characterisation of an apartyl protease inhibitor homologue as a major allergen of Trichostrongylus colubriformis. International Journal for Parasitology 33, 1233–1243.Google Scholar
Singleton, D.R., Stear, M.J. & Matthews, L. (2010) A mechanistic model of developing immunity to Teladorsagia circumcincta infection in lambs. Parasitology DOI 10.1017/50031182010001289, in press.Google Scholar
Smith, J.A., Wilson, K., Pilkington, J.G. & Pemberton, J.M. (1999) Heritable variation in resistance to gastrointestinal nematodes in an unmanaged mammal population. Proceedings of the Royal Society of London B Biological Sciences 266, 1283–1290.Google Scholar
Stear, M.J. & Bishop, S.C. (1999) The curvilinear relationship between worm length and fecundity of Teladorsagia circumcincta. International Journal for Parasitology 29, 777–780.Google Scholar
Stear, M.J. & Wakelin, D. (1998) Genetic resistance to parasitic infection. Revue Scientifique et Technique de l'Office International des Epizooties 17, 143–153.Google Scholar
Stear, M.J., Bishop, S.C., Doligalska, M., Duncan, J.L., Holmes, P.H., Irvine, J., McCririe, L., McKellar, Q.A., Sinski, E. & Murray, M. (1995) Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology 17, 643–652.Google Scholar
Stear, M.J., Bairden, K., Bishop, S.C., Buitkamp, J., Duncan, J.L., Gettinby, G., McKellar, Q.A., Park, M., Parkins, J.J., Reid, S.W.J., Strain, S.A.J. & Murray, M. (1997a) The genetic basis of resistance to Ostertagia circumcincta in lambs. The Veterinary Journal 154, 111–119.Google Scholar
Stear, M.J., Bairden, K., Duncan, J.L., Holmes, P.H., McKellar, Q.A., Park, M., Strain, S.A.J., Murray, M., Bishop, S.C. & Gettinby, G. (1997b) How hosts control worms. Nature 389, 27.Google Scholar
Stear, M.J., Bairden, K., Bishop, S.C., Gettinby, G., McKellar, Q.A., Park, M., Strain, S.A.J. & Wallace, D.S. (1998) The processes influencing the distribution of parasitic nematodes among naturally infected lambs. Parasitology 117, 165–171.Google Scholar
Stear, M.J., Strain, S.A.J. & Bishop, S.C. (1999a) How lambs control infection with Ostertagia circumcincta. Veterinary Immunology and Immunopathology 72, 213–218.Google Scholar
Stear, M.J., Strain, S.A.J. & Bishop, S.C. (1999b) Mechanisms underlying resistance to nematode infection. International Journal for Parasitology 29, 51–56.Google Scholar
Stear, M.J., Bishop, S.C., Mallard, B. & Raadsma, H.W. (2001) The sustainability, feasibility and desirability of breeding livestock for disease resistance. Research in Veterinary Science 71, 1–7.Google Scholar
Stear, M.J., Bishop, S.C., Henderson, N.G. & Scott, I. (2003) A key mechanism of pathogenesis in sheep infected with the nematode Teladorsagia circumcincta. Animal Health Research Reviews 4, 45–52.Google Scholar
Stear, M.J., Doligalska, M. & Donskow-Schmelter, K. (2007) Alternatives to anthelmintics for the control of nematodes in livestock. Parasitology 134, 139–151.Google Scholar
Stear, M.J., Fitton, L.A., Innocent, G.T., Murphy, L., Rennie, K. & Matthews, L. (2008) The dynamic influence of genetic variation on the susceptibility of sheep to gastrointestinal nematode infection. Journal of the Royal Society Interface 4, 767–776.Google Scholar
Stear, M.J., Boag, B., Cattadori, I.M. & Murphy, L. (2009) Genetic variation in resistance to mixed, predominantly Teladorsagia circumcincta nematode infections of sheep – from heritabilities to gene identification. Parasite Immunology 31, 274–282.CrossRefGoogle ScholarPubMed
Stebbins, G.L. (1981) Coevolution of grasses and herbivores. Annals of the Missouri Botanical Garden 68, 75–86.Google Scholar
Strain, S.A.J., Bishop, S.C., Henderson, N.G., Kerr, A., McKellar, Q.A., Mitchell, S. & Stear, M.J. (2002) The genetic control of IgA activity against Teladorsagia circumcincta and its association with parasite resistance in naturally infected sheep. Parasitology 124, 545–552.Google Scholar
Woolaston, R.R. & Windon, R.G. (2001) Selection of sheep for response to Trichostrongylus colubriformis larvae: genetic parameters. Animal Science 73, 41–48.Google Scholar
Woolaston, R.R., Barger, I.A. & Piper, L.R. (1990) Response to helminth infection of sheep selected for resistance to Haemonchus contortus. International Journal for Parasitology 20, 1015–1018.Google Scholar
Yazwinski, T.A., Goode, L., Moncol, D.J., Morgan, G.W. & Linnerud, A.C. (1979) Parasite resistance in straightbred and crossbred Barbados Blackbelly sheep. Journal of Animal Science 49, 919–926.Google Scholar
Yazwinski, T.A., Goode, L., Moncol, D.J., Morgan, G.W. & Linnerud, A.C. (1981) Haemonchus contortus resistance in straightbred and crossbred Barbados Blackbelly sheep. Journal of Animal Science 51, 279–284.Google Scholar