Skip to main content Accessibility help

Variation and covariation in strongyle infection in East African shorthorn zebu calves

  • R. CALLABY (a1) (a2) (a3), O. HANOTTE (a4), I. CONRADIE VAN WYK (a5), H. KIARA (a6), P. TOYE (a6), M. N. MBOLE-KARIUKI (a7), A. JENNINGS (a8), S. M. THUMBI (a2), J. A. W. COETZER (a5), B. M. de. C. BRONSVOORT (a9), S. A. KNOTT (a1), M. E. J. WOOLHOUSE (a1) (a2) and L. E. B. KRUUK (a1) (a10)...


Parasite burden varies widely between individuals within a population, and can covary with multiple aspects of individual phenotype. Here we investigate the sources of variation in faecal strongyle eggs counts, and its association with body weight and a suite of haematological measures, in a cohort of indigenous zebu calves in Western Kenya, using relatedness matrices reconstructed from single nucleotide polymorphism (SNP) genotypes. Strongyle egg count was heritable (h 2 = 23·9%, s.e. = 11·8%) and we also found heritability of white blood cell counts (WBC) (h 2 = 27·6%, s.e. = 10·6%). All the traits investigated showed negative phenotypic covariances with strongyle egg count throughout the first year: high worm counts were associated with low values of WBC, red blood cell count, total serum protein and absolute eosinophil count. Furthermore, calf body weight at 1 week old was a significant predictor of strongyle EPG at 16–51 weeks, with smaller calves having a higher strongyle egg count later in life. Our results indicate a genetic basis to strongyle EPG in this population, and also reveal consistently strong negative associations between strongyle infection and other important aspects of the multivariate phenotype.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Variation and covariation in strongyle infection in East African shorthorn zebu calves
      Available formats

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Variation and covariation in strongyle infection in East African shorthorn zebu calves
      Available formats

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Variation and covariation in strongyle infection in East African shorthorn zebu calves
      Available formats


This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (, which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

* Corresponding author. Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, Kings Buildings, West Mains Road, Edinburgh EH9 3JT, UK. E-mail:


Hide All
Aulchenko, Y. S., Ripke, S., Isaacs, A. and Van Duijn, C. M. (2007). GenABEL: an R library for genome-wide association analysis. Bioinformatics 23, 12941296.
Batchelor, N. A., Atkinson, P. M., Gething, P. W., Picozzi, K., Fèvre, E. M., Kakembo, A. S. L. and Welburn, S. C. (2009). Spatial predictions of Rhodesian Human African Trypanosomiasis (Sleeping Sickness) prevalence in Kaberamaido and Dokolo, two newly affected districts of Uganda. PLoS Neglected Tropical Diseases 3, e563.
Beraldi, D., McRae, A. F., Gratten, J., Pilkington, J. G., Slate, J., Visscher, P. M. and Pemberton, J. M. (2007). Quantitative trait loci (QTL) mapping of resistance to strongyles and coccidia in the free-living Soay sheep (Ovis aries). International Journal for Parasitology 37, 121129.
Bérénos, C., Ellis, P. A., Pilkington, J. G. and Pemberton, J. M. (2014). Estimating quantitative genetic parameters in wild populations: a comparison of pedigree and genomic approaches. Molecular Ecology 23, 34343451.
Bishop, S. C. and Stear, M. J. (2001). Inheritance of faecal egg counts during early lactation in Scottish Blackface ewes facing mixed, natural nematode infections. Animal Science 73, 389395.
Bishop, S. C., Bairden, K., McKellar, Q. A., Park, M. and Stear, M. J. (1996). Genetic parameters for faecal egg count following mixed, natural, predominantly Ostertagia circumcincta infection and relationships with live weight in young lambs. Animal Science 63, 423428.
Bricarello, P. A., Zaros, L. G., Coutinho, L. L., Rocha, R. A., Kooyman, F. N. J., De Vries, E., Gonçalves, J. R. S., Lima, L. G., Pires, A. V. and Amarante, A. F. T. (2007). Field study on nematode resistance in Nelore-breed cattle. Veterinary Parasitology 148, 272278.
Bronsvoort, B. d. C., Thumbi, S., Poole, E., Kiara, H., Auguet, O., Handel, I., Jennings, A., Conradie, I., Mbole-Kariuki, M., Toye, P., Hanotte, O., Coetzer, J. and Woolhouse, M. (2013). Design and descriptive epidemiology of the Infectious Diseases of East African Livestock (IDEAL) project, a longitudinal calf cohort study in western Kenya. BMC Veterinary Research 9, 171.
Bryan, R. P. and Kerr, J. D. (1989). The relation between the natural worm burden of steers and the faecal egg count differentiated to species. Veterinary Parasitology 30, 327334.
Clapperton, M., Diack, A., Matika, O., Glass, E., Gladney, C., Mellencamp, M., Hoste, A. and Bishop, S. (2009). Traits associated with innate and adaptive immunity in pigs: heritability and associations with performance under different health status conditions. Genetics Selection Evolution 41, 111.
Clements, M. N., Clutton-Brock, T. H., Guinness, F. E., Pemberton, J. M. and Kruuk, L. E. B. (2011). Variances and covariances of phenological traits in a wild mammal population. Evolution 65, 788801.
Coltman, D. W., Pilkington, J., Kruuk, L. E. B., Wilson, K. and Pemberton, J. M. (2001). Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution 55, 21162125.
Conradie van Wyk, I., Goddard, A., Bronsvoort, B. M. de C., Coetzer, J., Booth, C., Hanotte, O., Jennings, A., Kiara, H., Mashego, P., Muller, C., Pretorius, G., Poole, E., Thumbi, S., Toye, P., Woolhouse, M. and Penzhorn, B. (2012). Hematological profile of East African short-horn zebu calves from birth to 51 weeks of age. Comparative Clinical Pathology 22, 10291036.
Conradie van Wyk, I., Goddard, A., Bronsvoort, B. M. de C., Coetzer, J., Handel, I., Hanotte, O., Jennings, A., Lesosky, M., Kiara, H., Thumbi, S., Toye, P., Woolhouse, M. and Penzhorn, B. (2014). The impact of co-infections on the haematological profile of East African Short-horn Zebu calves. Parasitology 141, 374388.
Crawford, A., Paterson, K., Dodds, K., Diez Tascon, C., Williamson, P., Roberts Thomson, M., Bisset, S., Beattie, A., Greer, G., Green, R., Wheeler, R., Shaw, R., Knowler, K. and McEwan, J. (2006). Discovery of quantitative trait loci for resistance to parasitic nematode infection in sheep: I. Analysis of outcross pedigrees. BMC Genomics 7, 178.
Falconer, D. and Mackay, T. (1996). Introduction to Quantitiative Genetics, 4th Edn. Longman, Harlow.
Garner, C., Tatu, T., Reittie, J. E., Littlewood, T., Darley, J., Cervino, S., Farrall, M., Kelly, P., Spector, T. D. and Thein, S. L. (2000). Genetic influences on F cells and other hematologic variables: a twin heritability study. Blood 95, 342346.
Gilmore, A. R., Gogel, B. J., Cullis, B. R. and Thompson, R. (2006). Asreml User Guide Release 3. VSN International Ltd., Hemel Hempsted.
Goddard, M. E. and Hayes, B. J. (2009). Mapping genes for complex traits in domestic animals and their use in breeding programmes. Nature Reviews Genetics 10, 381391.
Hansen, J. and Perry, B. (1994). The Epidemiology, Diagnosis and Control of Helminth Parasites of Ruminants: A Handbook, 2nd Edn. ILRAD, Nairobi, Kenya.
Hayward, A. D., Wilson, A. J., Pilkington, J. G., Pemberton, J. M. and Kruuk, L. E. B. (2009). Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 276, 34773485.
Hayward, A. D., Pilkington, J. G., Pemberton, J. M. and Kruuk, L. E. B. (2010). Maternal effects and early-life performance are associated with parasite resistance across life in free-living Soay sheep. Parasitology 137, 12611273.
Jain, N. C. (1993). Essentials of Veterinary Hematology. Wiley, Philadelphia.
Kanyari, P. W. N., Kagira, J. M. and Mhoma, J. R. L. (2010). Prevalence of endoparasites in cattle within urban and peri-urban areas of Lake Victoria Basin, Kenya with special reference to zoonotic potential. Scientia Parasitologica 11, 171178.
Kaufmann, J., Dwinger, R. H., Hallebeek, A., van Dijk, B. and Pfister, K. (1992). The interaction of Trypanosoma congolense and Haemonchus contortus infections in trypanotolerant N'Dama cattle. Veterinary Parasitology 43, 157170.
Keyyu, J. D., Kassuku, A. A., Kyvsgaard, N. C. and Willingham, A. L. III (2003). Gastrointestinal nematodes in indigenous zebu cattle under pastoral and nomadic management systems in the lower plain of the Southern Highlands of Tanzania. Veterinary Research Communications 27, 371380.
Kruuk, L. E. B. (2004). Estimating genetic parameters in natural populations using the ‘animal model’. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 359, 873890.
Kruuk, L. E. B. and Hadfield, J. D. (2007). How to separate genetic and environmental causes of similarity between relatives. Journal of Evolutionary Biology 20, 18901903.
Leighton, E. A., Murrell, K. D. and Gasbarre, L. C. (1989). Evidence for genetic-control of nematode egg-shedding rates in calves. Journal of Parasitology 75, 498504.
Lu, Y. P., Zeng, D. Y., Chen, Y. P., Liang, X. J., Xu, J. P., Huang, S. M., Lai, Z. W., Wen, W. R., Von Websky, K. and Hocher, B. (2013). Low birth weight is associated with lower respiratory tract infections in children with hand, foot, and mouth disease. Clinical Laboratory 59, 985992.
Lynch, M. and Walsh, B. (1998). Genetics and analysis of quantitative traits, Sinauer Associates.
Marshall, D. M. (1994). Breed differences and genetic parameters for body composition traits in beef cattle. Journal of Animal Science 72, 27452755.
Matukumalli, L. K., Lawley, C. T., Schnabel, R. D., Taylor, J. F., Allan, M. F., Heaton, M. P., O'Connell, J., Moore, S. S., Smith, T. P. L., Sonstegard, T. S. and Van Tassell, C. P. (2009). Development and characterization of a high density SNP genotyping assay for cattle. Plos One 4, e5350.
Mbole-Kariuki, M. N., Sonstegard, T., Orth, A., Thumbi, S. M., Bronsvoort, B. M. d. C., Kiara, H., Toye, P., Conradie, I., Jennings, A., Coetzer, K., Woolhouse, M. E. J., Hanotte, O. and Tapio, M. (2014). Genome-wide analysis reveals the ancient and recent admixture history of East African Shorthorn Zebu from Western Kenya. Heredity. doi: 10.1038/hdy.2014.31.
Moore, S. L. and Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 20152018.
Murray, G. G., Woolhouse, M. E., Tapio, M., Mbole-Kariuki, M. N., Sonstegard, T. S., Thumbi, S. M., Jennings, A. E., Conradie van Wyk, I., Chase-Topping, M. and Kiara, H. (2013). Genetic susceptibility to infectious disease in East African Shorthorn Zebu: a genome-wide analysis of the effect of heterozygosity and exotic introgression. BMC Evolutionary Biology 13, 246.
Nakagawa, S. and Schielzeth, H. (2010). Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biological Reviews 85, 935956.
Norris, K. and Evans, M. R. (2000). Ecological immunology: life history trade-offs and immune defense in birds. Behavioral Ecology 11, 1926.
Pankow, J. S., Folsom, A. R., Cushman, M., Borecki, I. B., Hopkins, P. N., Eckfeldt, J. H. and Tracy, R. P. (2001). Familial and genetic determinants of systemic markers of inflammation: the NHLBI family heart study. Atherosclerosis 154, 681689.
Pemberton, J. M. (2008). Wild pedigrees: the way forward. Proceedings of the Royal Society B: Biological Sciences 275, 613621.
Perry, B. and Sones, K. (2007). Science for development: poverty reduction though animal health. Science 315, 333334.
Powell, J. E., Visscher, P. M. and Goddard, M. E. (2010). Reconciling the analysis of IBD and IBS in complex trait studies. Nature Reviews Genetics 11, 800805.
Raqib, R., Alam, D. S., Sarker, P., Ahmad, S. M., Ara, G., Yunus, M., Moore, S. E. and Fuchs, G. (2007). Low birth weight is associated with altered immune function in rural Bangladeshi children: a birth cohort study. The American Journal of Clinical Nutrition 85, 845852.
Read, J. S., Clemens, J. D. and Klebanoff, M. A. (1994). Moderate low birth weight and infectious disease mortality during infancy and childhood. American Journal of Epidemiology 140, 721733.
Riggio, V., Matika, O., Pong-Wong, R., Stear, M. J. and Bishop, S. C. (2013). Genome-wide association and regional heritability mapping to identify loci underlying variation in nematode resistance and body weight in Scottish Blackface lambs. Heredity 110, 420429.
Robinson, M. R., Santure, A. W., DeCauwer, I., Sheldon, B. C. and Slate, J. (2013). Partitioning of genetic variation across the genome using multimarker methods in a wild bird population. Molecular Ecology 22, 39633980.
Rowlands, G. J., Mulatu, W., Nagda, S. M., Dolan, R. B. and Dieteren, G. D. M. (1995). Genetic-variation in packed red-cell volume and frequency of parasitemia in East African zebu cattle exposed to drug-resistant trypanosomes. Livestock Production Science 43, 7584.
Stear, M. J., Tierney, T. J., Baldock, F. C., Brown, S. C., Nicholas, F. W. and Rudderh, T. H. (1988). Failure to find an association between class I antigens of the bovine major histocompatibility system and faecal worm egg counts. International Journal for Parasitology 18, 859861.
Stear, M. J., Hetzel, D. J. S., Brown, S. C., Gershwin, L. J., Mackinnon, M. J. and Nicholas, F. W. (1990). The relationships among ecto- and endoparasite levels, class I antigens of the bovine major histocompatibility system, immunoglobulin E levels and weight gain. Veterinary Parasitology 34, 303321.
Stear, M. J., Park, M. and Bishop, S. C. (1996). The key components of resistance to Ostertagia circumcincta in lambs. Parasitology Today 12, 438441.
Thumbi, S., Bronsvoort, M., Kiara, H., Toye, P., Poole, J., Ndila, M., Conradie, I., Jennings, A., Handel, I., Coetzer, J., Steyl, J., Hanotte, O. and Woolhouse, M. (2013 a). Mortality in East African shorthorn zebu cattle under one year: predictors of infectious-disease mortality. BMC Veterinary Research 9, 175.
Thumbi, S. M., Bronsvoort, B. M. d. C., Poole, E. J., Kiara, H., Toye, P., Ndila, M., Conradie, I., Jennings, A., Handel, I. G., Coetzer, J. A., Hanotte, O. and Woolhouse, M. E. (2013 b). Parasite co-infections show synergistic and antagonistic interactions on growth performance of East African zebu cattle under one year. Parasitology 140, 17891798.
Urquhart, G., Armour, J., Duncan, J., Dunn, A. and Jennings, F. (1996). Veterinary Parasitology, 2nd Edn. Blackwell Science Ltd, Oxford.
Vanimisetti, H. B., Andrew, S. L., Zajac, A. M. and Notter, D. R. (2004). Inheritance of faecal egg count and packed cell volume and their relationship with production traits in sheep infected with Haemonchus contortus . Journal of Animal Science 82, 16021611.
Visscher, P. M., Hill, W. G. and Wray, N. R. (2008). Heritability in the genomics era – concepts and misconceptions. Nature Reviews Genetics 9, 255266.
Visscher, P. M., Hemani, G., Vinkhuyzen, A. A. E., Chen, G.-B., Lee, S. H., Wray, N. R., Goddard, M. E. and Yang, J. (2014). Statistical power to detect genetic (co)variance of complex traits using SNP data in unrelated samples. PLoS Genetics 10, e1004269.
Wilson, A. J. (2008). Why h2 does not always equal VA/VP? Journal of Evolutionary Biology 21, 647650.
Wilson, A. J., Pemberton, J. M., Pilkington, J. G., Clutton-Brock, T. H., Coltman, D. W. and Kruuk, L. E. B. (2007). Quantitative genetics of growth and cryptic evolution of body size in an island population. Evolutionary Ecology 21, 337356.
Wymann, M. N., Traore, K., Bonfoh, B., Tembely, S., Tembely, S. and Zinsstag, J. (2008). Gastrointestinal parasite egg excretion in young calves in periurban livestock production in Mali. Research in Veterinary Science 84, 225231.
Yang, J., Benyamin, B., McEvoy, B. P., Gordon, S., Henders, A. K., Nyholt, D. R., Madden, P. A., Heath, A. C., Martin, N. G., Montgomery, G. W., Goddard, M. E. and Visscher, P. M. (2010). Common SNPs explain a large proportion of the heritability for human height. Nature Genetics 42, 565569.
Yang, J., Manolio, T. A., Pasquale, L. R., Boerwinkle, E., Caporaso, N., Cunningham, J. M., de Andrade, M., Feenstra, B., Feingold, E., Hayes, M. G., Hill, W. G., Landi, M. T., Alonso, A., Lettre, G., Lin, P., Ling, H., Lowe, W., Mathias, R. A., Melbye, M., Pugh, E., Cornelis, M. C., Weir, B. S., Goddard, M. E. and Visscher, P. M. (2011). Genome partitioning of genetic variation for complex traits using common SNPs. Nature Genetics 43, 519525.
Zinsstag, J., Ankers, P., Njie, M., Smith, T., Pandey, V. S., Pfister, K. and Tanner, M. (2000). Heritability of gastrointestinal nematode faecal egg counts in West African village N'Dama cattle and its relation to age. Veterinary Parasitology 89, 7178.


Type Description Title
Supplementary materials

Callaby Supplementary Material
Supplementary Material

 Word (92 KB)
92 KB


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed