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Genetic growth potential interacts with nutrition on the ability of mice to cope with Heligmosomoides bakeri infection

Published online by Cambridge University Press:  15 June 2009

J. C. COLTHERD ,
L. BÜNGER ,
I. KYRIAZAKIS  and
J. G. M. HOUDIJK
J. C. COLTHERD*
Affiliation:
Animal Health, SAC, West Mains Road, Edinburgh EH9 3JG, UK
L. BÜNGER
Affiliation:
Animal Breeding and Genetics Team, SAC, West Mains Road, Edinburgh EH9 3JG, UK
I. KYRIAZAKIS
Affiliation:
Animal Health, SAC, West Mains Road, Edinburgh EH9 3JG, UK Veterinary Faculty, University of Thessaly, PO Box 199, 43100 Karditsa, Greece
J. G. M. HOUDIJK
Affiliation:
Animal Health, SAC, West Mains Road, Edinburgh EH9 3JG, UK
*
*Corresponding author: Disease Systems Team, SAC, West Mains Road, Edinburgh EH9 3JG, UK. Tel: +44 (0) 131 5353058. Fax: +44 (0) 131 5353121. E-mail: Jennifer.Coltherd@sac.ac.uk
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Summary

Artificial selection for improved productivity may reduce an animal's ability to cope with pathogens. Here, we used Roslin mice, uniquely divergently selected for high (ROH) and low (ROL) body weight, to assess interactive effects of differing growth potential and protein nutrition on host resilience and resistance. In a 2×2×6 factorial design, ROH and ROL mice were either sham-infected or infected with 250 L3Heligmosomoides bakeri and fed diets with 30, 80, 130, 180, 230 and 280 g crude protein per kg. The infected ROL-30 treatment resulted in clinical disease and was discontinued. In the remaining ROL mice, infection and feeding treatments did not affect growth but infection reduced weight gain in ROH-30, ROH-80 and ROH-130 mice. Although infection resulted in temporarily reduced food intake (anorexia) in both mouse lines, mean food intake over the whole experiment was reduced in ROH mice only. ROH mice excreted more worm eggs and had higher worm burdens, with relatively fewer female worms, than ROL mice. However, these resistance traits were not sensitive to dietary protein. These results support the view that selection for high growth may reduce the ability to cope with pathogens, and that improved protein nutrition may to some extent ameliorate this penalty.

Keywords

Heligmosomoides bakeriprotein nutritionanorexiaresilienceresistancegrowth potential
Type
Research Article
Information
Parasitology , Volume 136 , Issue 9 , August 2009 , pp. 1043 - 1055
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Athanasiadou, S., Kyriazakis, I., Jackson, F. and Coop, R. L. (2001). The effects of condensed tannins supplementation of foods with different protein content on parasitism, food intake and performance of sheep infected with Trichostrongylus colubriformis. British Journal of Nutrition 86, 697–706.CrossRefGoogle ScholarPubMed
Bansemir, A. D. and Sukhdeo, M. V. K. (1994). The food resource of adult Heligmosomoides polygyrus in the small-intestine. Journal of Parasitology 80, 24–28.CrossRefGoogle ScholarPubMed
Bansemir, A. D. and Sukhdeo, M. V. K. (1996). Villus length influences habitat selection by Heligmosomoides polygyrus. Parasitology 113, 311–316.CrossRefGoogle ScholarPubMed
Behnke, J. M., Lowe, A., Clifford, S. and Wakelin, D. (2003). Cellular and serological responses in resistant and susceptible mice exposed to repeated infection with Heligmosomoides polygyrus bakeri. Parasite Immunology 25, 333–340.CrossRefGoogle ScholarPubMed
Beilharz, R. G. (1998 a). Environmental limit to genetic change. An alternative theorem of natural selection. Journal of Animal Breeding and Genetics 115, 433–437.CrossRefGoogle Scholar
Beilharz, R. G. (1998 b). The problem of genetic improvement when environments are limiting. Proceedings of the 6th World Congress on Genetics Applied to Livestock Production 26, 81–84.Google Scholar
Beilharz, R. G., Luxford, B. G. and Wilkinson, J. L. (1993). Quantitative genetics and evolution: is our understanding of genetics sufficient to explain evolution? Journal of Animal Breeding and Genetics 110, 161–170.CrossRefGoogle ScholarPubMed
Boulay, M., Scott, M. E., Conly, S. L., Stevenson, M. M. and Koski, K. G. (1998). Dietary protein and zinc restrictions independently modify a Heligmosomoides polygyrus (Nematoda) infection in mice. Parasitology 116, 449–462.CrossRefGoogle ScholarPubMed
Brailsford, T. J. and Mapes, C. J. (1987). Comparisons of Heligmosomoides polygyrus primary infection in protein-deficient and well-nourished mice. Parasitology 95, 311–321.CrossRefGoogle ScholarPubMed
Broughan, J. M. and Wall, R. (2007). Faecal soiling and gastrointestinal helminth infection in lambs. International Journal for Parasitology 37, 1255–1268.CrossRefGoogle ScholarPubMed
Bünger, L., Renne, U. and Buis, R. C. (2001). Body weight limits in mice. In Encyclopedia of Genetics (ed. Reeve, E. C. R.), pp. 337–360. Fitzroy Dearborn Publishers, London and Chicago.Google Scholar
Cable, J., Harris, P. D., Lewis, J. W. and Behnke, J. M. (2006). Molecular evidence that Heligmosomoides polygyrus from laboratory mice and wood mice are separate species. Parasitology 133, 111–122.CrossRefGoogle ScholarPubMed
Christie, M. and Jackson, F. (1982). Specific identification of strongyle eggs in small samples of sheep feces. Research in Veterinary Science 32, 113–117.CrossRefGoogle Scholar
Coop, R. L. and Holmes, P. H. (1996). Nutrition and parasite interaction. International Journal for Parasitology 26, 951–962.CrossRefGoogle ScholarPubMed
Coop, R. L. and Kyriazakis, I. (1999). Nutrition-parasite interaction. Veterinary Parasitology 84, 187–204.CrossRefGoogle ScholarPubMed
Datta, F. U., Nolan, J. V., Rowe, J. B. and Gray, G. D. (1998). Protein supplementation improves the performance of parasitised sheep fed a straw-based diet. International Journal for Parasitology 28, 1269–1278.CrossRefGoogle ScholarPubMed
Dekkers, J. C. M. and Hospital, F. (2002). The use of molecular genetics in the improvement of agricultural populations. Nature Reviews Genetics 3, 22–32.CrossRefGoogle ScholarPubMed
Ehrenford, F. (1954 a). Effects of dietary protein on the relationship between laboratory mice and the nematode Nematospiroides dubius. Journal of Parasitology 40, 486.CrossRefGoogle Scholar
Ehrenford, F. (1954 b). The life cycle of Nematospiroides dubius baylis (Nematoda: Heligmosomidae). Journal of Parasitology 40, 480–481.CrossRefGoogle Scholar
Falconer, D. S. and MacKay, T. F. C. (1996). Introduction to Quantitative Genetics, 4 Edn.Longman Scientific and Technical, Harlow, UK.Google Scholar
Glazier, D. S. (2002). Resource-allocation rules and the heritability of traits. Evolution 56, 1696–1700.Google ScholarPubMed
Goff, W., Johnston, W., Parish, S., Barrington, G., Tuo, W. and Valdez, R. (2001). The age-related immunity in cattle to Babesia bovis infection involves the rapid induction of interleukin-12, interferon-gamma and inducible nitric oxide synthase mRNA expression in the spleen. Parasite Immunology 23, 463–471.CrossRefGoogle ScholarPubMed
Gregory, R. D., Montgomery, S. S. J. and Montgomery, W. I. (1992). Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. Journal of Animal Ecology 61, 749–757.CrossRefGoogle Scholar
Hastings, I. M. and Hill, W. G. (1989). A note on the effect of different selection criteria on carcass composition in mice. Animal Production 48, 229–233.CrossRefGoogle Scholar
Heath, S. C., Bulfield, G., Thompson, R. and Keightley, P. D. (1995). Rates of change of genetic-parameters of body weight in selected mouse lines. Genetical Research 66, 19–25.CrossRefGoogle ScholarPubMed
Houdijk, J. G. M. and Athanasiadou, S. (2003). Direct and indirect effects of host nutrition on ruminant gastrointestinal nematodes. Proceedings of the 4th International Symposium on the Nutrition of Herbivores, Mérida, Mexico, pp. 213–236.Google Scholar
Houdijk, J. G. M. and Bünger, L. (2006). Selection for growth increases the penalty of parasitism on growth performance in mice. Proceedings of the Nutrition Society 65, 68A.Google Scholar
Houdijk, J. G. M. and Bünger, L. (2007). Interactive effects of selection for growth and protein supply on the consequences of gastrointestinal parasitism on growth performance in mice. Proceedings of the British Society of Animal Science, 92.CrossRefGoogle Scholar
Houdijk, J. G. M., Jessop, N. S. and Kyriazakis, I. (2001). Nutrient partitioning between reproductive and immune functions in animals. Proceedings of the Nutrition Society 60, 515–525.CrossRefGoogle ScholarPubMed
Ing, R., Su, Z., Scott, M. E. and Koski, K. G. (2000). Suppress T helper 2 immunity and prolonged survival of the nematode parasite in protein-malnourished mice. Proceedings of the National Academy of Sciences, USA 97, 7078–7083.CrossRefGoogle ScholarPubMed
Iraqi, F., Behnke, J. M., Menge, D. M., Lowe, A., Teale, A. J., Gibson, J. P., Baker, L. R. and Wakelin, D. (2003). Chromosomal regions controlling resistance to gastro-intestinal nematode infections in mice. Mammalian Genome 14, 184–191.CrossRefGoogle ScholarPubMed
Jenkins, S. N. and Behnke, J. M. (1977). Impairment of primary expulsion of Trichuris muris in mice concurrently infected with Nematospiroides dubius. Parasitology 75, 71–78.CrossRefGoogle ScholarPubMed
Keymer, A. and Dobson, A. (1987). The ecology of helminths in populations of small mammals. Mammal Review 17, 105–116.CrossRefGoogle Scholar
Koski, K. G., Su, Z. and Scott, M. (1999). Energy deficits suppress both systemic and gut immunity during infection. Biochemical and Biophysical Research Communications 264, 796–801.CrossRefGoogle ScholarPubMed
Kristan, D. M. (2008). Calorie restriction and susceptibility to intact pathogens. Age 30, 147–156.CrossRefGoogle ScholarPubMed
Kristan, D. M. and Hammond, K. A. (2001). Parasite infection and caloric restriction induce physiological and morphological plasticity. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 281, R502–R510.CrossRefGoogle ScholarPubMed
Kristan, D. M. and Hammond, K. A. (2006). Effects of three simultaneous demands on glucose transport, resting metabolism and morphology of laboratory mice. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 176, 139–151.CrossRefGoogle ScholarPubMed
Kyriazakis, I. (2009). Does food composition affect anorexia during infection? British Journal of Nutrition (in the Press).Google Scholar
Kyriazakis, I., Tolkamp, B. J. and Hutchings, M. R. (1998) Towards a functional explanation for the occurrence of anorexia during parasitic infections. Animal Behaviour 56, 265–274.CrossRefGoogle ScholarPubMed
Kyriazakis, I., Anderson, D. H., Oldham, J. D., Coop, R. L. and Jackson, F. (1996). Long-term subclinical infection with Trichostrongylus colubriformis: Effects on food intake, diet selection and performance of growing lambs. Veterinary Parasitology 61, 297–313.CrossRefGoogle ScholarPubMed
Liu, S. (1966), Genetic influence on resistance of mice to Nematospiroides dubius. Experimental Parasitology 18, 311–319.CrossRefGoogle Scholar
Mercer, J. G., Mitchell, P. I., Moar, K. M., Bisset, A., Geissler, S., Bruce, K. and Chappell, L. H. (2000) Anorexia in rats infected with the nematode, Nippostrongylus brasiliensis: experimental manipulations. Parasitology 120, 641–647.CrossRefGoogle ScholarPubMed
Miller, G., Dunn, G., Reid, T., Ogden, I. and Strachan, N. (2005). Does age acquired immunity confer selective protection to common serotypes of Campylobacter jejuni? BMC Infectious Diseases 5, 66–70.CrossRefGoogle ScholarPubMed
Mitchell, G. and Prowse, S. J. (1979). Three consequences of infection with Nematospiroides dubius in three inbred strains of mice. Journal of Parasitology 65, 820–822.CrossRefGoogle ScholarPubMed
Murray, M. J. and Murray, A. B. (1979). Anorexia of infection as a mechanism of host defense. American Journal of Clinical Nutrition 32, 593–596.CrossRefGoogle ScholarPubMed
NRC (1995) Nutrient Requirements of Laboratory Animals, 4th revised Edn.National Academy Press, Washington D.C., USA.Google Scholar
Rauw, W., Kanis, E., Noordhuizen-Stassen, E. N. and Grommers, F. J. (1998). Undesirable side effects of selection for high production efficiency in farm animals: a review. Livestock Production Science 56, 15–33.CrossRefGoogle Scholar
Sandberg, F. B., Emmans, G. C. and Kyriazakis, I. (2006). A model for predicting feed intake of growing animals during exposure to pathogens. Journal of Animal Science 84, 1552–1566.CrossRefGoogle Scholar
Shi, H. N., Koski, K. G., Stevenson, M. M. and Scott, M. E. (1997). Zinc deficiency and energy restriction modify immune responses in mice during both primary and challenge infection with Heligmosomoides polygyrus (Nematoda). Parasite Immunology 19, 363–373.CrossRefGoogle ScholarPubMed
Slater, A. and Keymer, A. (1988). The influence of protein deficiency on immunity to Heligmosomoides polygyrus (Nematoda) in mice. Parasite Immunology 10, 507–522.CrossRefGoogle ScholarPubMed
Stien, A., Dallimer, M., Irvine, R. J., Halvorsen, O., Langvatn, R., Albon, S. D. and Dallas, J. F. (2005). Sex ratio variation in gastrointestinal nematodes of Svalbard reindeer; density dependence and implications for estimates of species composition. Parasitology 130, 99–107.CrossRefGoogle ScholarPubMed
Tu, T., Koski, K. G., Wykes, L. J. and Scott, M. E. (2007). Re-feeding rapidly restores protection against Heligmosomoides bakeri (Nematoda) in protein-deficient mice. Parasitology 134, 899–909.CrossRefGoogle ScholarPubMed
Vagenas, D., Bishop, S. C. and Kyriazakis, I. (2007). A model to account for the consequences of host nutrition on the outcome of gastrointestinal parasitism in sheep: model evaluation. Parasitology 134, 1279–1289.CrossRefGoogle Scholar
van Houtert, M. and Sykes, A. R. (1996). Implications of nutrition for the ability of ruminants to withstand gastrointestinal nematode infections. International Journal for Parasitology 26, 1151–1167.CrossRefGoogle ScholarPubMed
Wahid, F. N. and Behnke, J. M. (1992). Stimuli for acquired resistance to Heligmosomoides polygyrus from intestinal tissue resident L3 and L4 larvae. International Journal for Parasitology 22, 699–710.CrossRefGoogle ScholarPubMed
Williams, J. L. (2005). The use of marker-assisted selection in animal breeding and biotechnology. Revue Scientifique et Technique-Office International des Epizooties 24, 379–391.CrossRefGoogle ScholarPubMed
Zaralis, K., Tolkamp, B. J., Houdijk, J. G. M., Wylie, A. R. G. and Kyriazakis, I. (2008). Changes in food intake and circulating leptin due to gastrointestinal parasitism in lambs of two breeds. Journal of Animal Science 86, 1891–1903.CrossRefGoogle ScholarPubMed