Heritabilities of IgA and IgE activities against Teladorsagia and Trichostrongylus L3 larval antigens correlated with traits for faecal worm egg count, health and productivity in Merino sheep
Zhongquan Zhao A , Mengzhi Wang B , Shimin Liu C H , Dieter Palmer D , Richard Shaw E , John Karlsson F , Philip E. Vercoe C G , Graeme B. Martin C G and Johan Greeff D
+ Author Affiliations
- Author Affiliations
A College of Animal Science and Technology, Southwest University, Beibei, Chongqing, China.
B College of Animal Science and Technology, Yangzhou University, Wenhui, Yangzhou, China.
C UWA Institute of Agriculture, University of Western Australia, Crawley, WA 6009, Australia.
D Department of Primary Industries and Regional Development Western Australia, South Perth, WA 6151, Australia.
E AgResearch Limited, The Hopkirk Research Institute, Palmerston North, New Zealand.
F BMB 314, Bridgetown, WA 6255, Australia.
G School of Agriculture and Environment, University of Western Australia, Crawley, WA 6009, Australia.
H Corresponding author. Email: shimin.liu@uwa.edu.au
Animal Production Science 59(10) 1792-1802 https://doi.org/10.1071/AN18630
Submitted: 5 October 2018 Accepted: 21 January 2019 Published: 22 February 2019
Abstract
Low faecal worm-egg count (FEC) has been used as a phenotypic trait for breeding sheep for resistance to nematode infection. Application of this trait has resulted in a major reduction in worm-egg output in faeces, but in certain environments some of the resistant sheep develop what is believed to be a hypersensitivity-associated diarrhoea, resulting in soiling of the breech area (dags). To avoid breeding sheep with a propensity to scour, it, therefore, seems logical to combine selection for low FEC with selection for a trait based on the immune response to worm infection. We, therefore, investigated the relationships between immunoglobulin A (IgA) and immunoglobulin E (IgE) activities against L3 larval antigens of Teladorsagia circumcincta and Trichostrongylus colubriformis and measured their inheritance and their genetic relationships with FEC, dag traits and measures of production. Total plasma IgE concentrations were also determined and included in the study. We used 762 progeny from 23 Merino sires selected for resistance to helminths (the ‘Rylington Flock’) and to breech flystrike. Total plasma IgE and IgE activities against T. circumcincta were negatively correlated with liveweight, longissimus dorsi muscle depth, and fleece weight, but positively correlated with severity of dags, softer faeces and back-fat depth. The IgA activity against T. circumcincta was negatively correlated with liveweight and clean fleece weight, but positively correlated with back-fat depth and faecal consistency score. The IgA activity against T. colubriformis was not correlated with any measure, except the breeding value for dags around yearling age. The heritability for the IgA activity against T. circumcincta and T. colubriformis was 0.13 and 0.08 respectively. The heritability for both IgE activity against T. circumcincta and total plasma IgE concentration was 0.39. We conclude that it is feasible to combine FEC and dag traits with an immune trait (in this case, helminth-specific IgE activity and total plasma IgE concentration) and, thus, genetically select sheep for resistance to both helminths and diarrhoea. However, under natural worm-challenge conditions, blood sampling protocols need to developed, on the basis of animal age, season and environment, for optimum estimation of the immune trait and its relationships with other traits.
Additional keywords: diarrhoea, immunoglobulin A, immunoglobulin E, helminth, hypersensitivity.
References
Bachert C, Gevaert P, Holtappels G, Johansson SGO, van Cauwenberge P (2001) Total and specific IgE in nasal polyps is related to local eosinophilic inflammation. The Journal of Allergy and Clinical Immunology 107, 607–614.| Total and specific IgE in nasal polyps is related to local eosinophilic inflammation.Crossref | GoogleScholarGoogle Scholar | 11295647PubMed |
Balic A, Bowles VM, Meeusen EN (2000) The immunobiology of gastrointestinal nematode infections in ruminants. Advances in Parasitology 45, 181–241.
| The immunobiology of gastrointestinal nematode infections in ruminants.Crossref | GoogleScholarGoogle Scholar | 10751941PubMed |
Besier B, Lyon J, McQuade N (1996) Drench resistance: a large economic cost. Journal of Agriculture 2, 60–63.
Burgio G, Lanzavecchia A, Plebani A, Jayakar S, Ugazio A (1980) Ontogeny of secretory immunity: levels of secretory IgA and natural antibodies in saliva. Pediatric Research 14, 1111–1114.
| Ontogeny of secretory immunity: levels of secretory IgA and natural antibodies in saliva.Crossref | GoogleScholarGoogle Scholar | 7008011PubMed |
Coltman D, Wilson K, Pilkington J, Stear M, Pemberton J (2001) A microsatellite polymorphism in the gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally-parasitized population of Soay sheep. Parasitology 122, 571–582.
| A microsatellite polymorphism in the gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally-parasitized population of Soay sheep.Crossref | GoogleScholarGoogle Scholar | 11393831PubMed |
Davies G, Stear M, Benothman M, Abuagob O, Kerr A, Mitchell S, Bishop S (2006) Quantitative trait loci associated with parasitic infection in Scottish blackface sheep. Heredity 96, 252–258.
| Quantitative trait loci associated with parasitic infection in Scottish blackface sheep.Crossref | GoogleScholarGoogle Scholar | 16391549PubMed |
de Cisneros JPJ, Matthews L, Mair C, Stefan T, Stear MJ (2014) The transfer of IgA from mucus to plasma and the implications for diagnosis and control of nematode infections. Parasitology 141, 875–879.
| The transfer of IgA from mucus to plasma and the implications for diagnosis and control of nematode infections.Crossref | GoogleScholarGoogle Scholar |
Douch PGC, Green RS, Risdon PL (1994) Antibody responses of sheep to challenge with Trichostrongylus colubriformis and the effect of dexamethasone treatmen. International Journal for Parasitology 24, 921–928.
| Antibody responses of sheep to challenge with Trichostrongylus colubriformis and the effect of dexamethasone treatmen.Crossref | GoogleScholarGoogle Scholar |
Erb KJ (2007) Helminths, allergic disorders and IgE-mediated immune responses: where do we stand? European Journal of Immunology 37, 1170–1173.
| Helminths, allergic disorders and IgE-mediated immune responses: where do we stand?Crossref | GoogleScholarGoogle Scholar | 17447233PubMed |
Gilmour A, Gogel B, Cullis B, Welham S, Thompson R (2015) ASReml user guide release 4.1 structural specification. (VSN International Ltd: Hemel Hempstead)
Grant AV, Araujo MI, Ponte EV, Oliveira RR, Cruz AA, Barnes KC, Beaty TH (2008) High heritability but uncertain mode of inheritance for total serum IgE level and Schistosoma mansoni infection intensity in a Schistosomiasis-endemic Brazilian population. The Journal of Infectious Diseases 198, 1227–1236.
| High heritability but uncertain mode of inheritance for total serum IgE level and Schistosoma mansoni infection intensity in a Schistosomiasis-endemic Brazilian population.Crossref | GoogleScholarGoogle Scholar | 18717640PubMed |
Greeff J, Karlsson L, Harris J (1995) Heritability of faecal worm egg count at different times of the year in a Mediterranean environment. Proceedings of the Australian Society of Animal Breeding and Genetics 11, 117–121.
Greeff J, Karlsson L, Schlink A (2014) Indicator traits for breech strike in Merino sheep in a Mediterranean environment. Animal Production Science 54, 125–140.
| Indicator traits for breech strike in Merino sheep in a Mediterranean environment.Crossref | GoogleScholarGoogle Scholar |
Hein W, Pernthaner A, Piedrafita D, Meeusen E (2010) Immune mechanisms of resistance to gastrointestinal nematode infections in sheep. Parasite Immunology 32, 541–548.
Jubb T, Shephard R, Webb-Ware J, Fordyce G (2015) ‘Priority list of endemic diseases for the red meat industries.’ No. 2895. (Meat & Livestock Australia: Sydney)
Karlsson L, Greeff J (2005a) Parasite resistant sheep and hypersensitivity diarrhoea. In ‘The 6th international sheep veterinary congress’, Hersonissos, Greece. (Eds GC Fthenakis, QA McKaller) (Hellenic Veterinary Medical Society)
Karlsson L, Greeff J (2005b) ‘Parasite resistant sheep & hypersensitivity diarrhoea, sheep updates.’ (Department of Agriculture and Food WA: WA)
Karlsson L, Greeff J (2007) Selecting sheep for nematode resistance and correlated responses in dags in a winter rainfall environment, genetic improvement: making it happen. In ‘Proceedings of the 17th conference of the Association for the Advancement of Animal Breeding and Genetics’, Armidale, NSW, Australia, 23–26 September 2007. pp. 264–267. (Association for the Advancement of Animal Breeding and Genetics: Armidale, NSW)
Karlsson L, Pollott G, Greeff J, Bell A, Eady S (2004) Relationship between faecal worm egg counts and scouring in Australian Merino sheep. Science Access 1, 100–103.
Kemper K, Palmer D, Liu S, Greeff J, Bishop S, Karlsson L (2010) Reduction of faecal worm egg count, worm numbers and worm fecundity in sheep selected for worm resistance following artificial infection with Teladorsagia circumcincta and Trichostrongylus colubriformis. Veterinary Parasitology 171, 238–246.
| Reduction of faecal worm egg count, worm numbers and worm fecundity in sheep selected for worm resistance following artificial infection with Teladorsagia circumcincta and Trichostrongylus colubriformis.Crossref | GoogleScholarGoogle Scholar | 20471175PubMed |
Larsen JW, Vizard AL, Anderson N (1995) Role of larval nematode infection in lamb diarrhoea. The Veterinary Record 137, 572
| Role of larval nematode infection in lamb diarrhoea.Crossref | GoogleScholarGoogle Scholar | 8644444PubMed |
Larsen J, Anderson N, Vizard A (1999) The pathogenesis and control of diarrhoea and breech soiling in adult Merino sheep. International Journal for Parasitology 29, 893–902.
| The pathogenesis and control of diarrhoea and breech soiling in adult Merino sheep.Crossref | GoogleScholarGoogle Scholar | 10480726PubMed |
Liu S, Smith T, Palmer D, Karlsson L, Besier R, Greeff J (2005) Biochemical differences in Merino sheep selected for resistance against gastro-intestinal nematodes and genetic and nutritional effects on faecal egg count and egg output. Animal Science 81, 149–157.
| Biochemical differences in Merino sheep selected for resistance against gastro-intestinal nematodes and genetic and nutritional effects on faecal egg count and egg output.Crossref | GoogleScholarGoogle Scholar |
McEwan JC, Bisset SA, Morris CA (1997) The selection of sheep for natural resistance to internal parasites. In ‘Sustainable control of internal parasites in ruminates’, animal industries workshop, Lincoln University, New Zealand. Vol. 52. (Ed. G Berrell) pp. 161–182. (Lincoln University: Canterbury, New Zealand)
Meeusen EN (1999) Immunology of helminth infections, with special reference to immunopathology. Veterinary Parasitology 84, 259–273.
| Immunology of helminth infections, with special reference to immunopathology.Crossref | GoogleScholarGoogle Scholar | 10456418PubMed |
Murphy L, Eckersall P, Bishop S, Pettit J, Huntley J, Burchmore R, Stear M (2010) Genetic variation among lambs in peripheral IgE activity against the larval stages of Teladorsagia circumcincta. Parasitology 137, 1249–1260.
| Genetic variation among lambs in peripheral IgE activity against the larval stages of Teladorsagia circumcincta.Crossref | GoogleScholarGoogle Scholar | 20233490PubMed |
Pickering N, Blair H, Hickson R, Johnson P, Dodds K, McEwan J (2015) Estimates of genetic parameters for breech strike and potential indirect indicators in sheep. New Veterinary Journal 63, 98–103.
| Estimates of genetic parameters for breech strike and potential indirect indicators in sheep.Crossref | GoogleScholarGoogle Scholar |
Pollott G, Greeff J (2004) Genetic relationships between faecal egg count and production traits in commercial Merino sheep flocks. Animal Science 79, 21–32.
Pollott GE, Karlsson LJE, Eady S, Greeff JC (2004) Genetic parameters for indicators of host resistance to parasites from weaning to hogget age in Merino sheep. Journal of Animal Science 82, 2852–2864.
Sackett D, Holmes P, Abbott K, Jephcott S, Barber M (2006) Final report: assessing the economic cost of endemic disease on the profitability of Australian beef and sheep production. Meat & Livestock Australia, Sydney.
Shaw R, McNeill M, Gatehouse T, Douch P (1997) Quantification of total sheep IgE concentration using anti-ovine IgE monoclonal antibodies in an enzyme immunoassay. Veterinary Immunology and Immunopathology 57, 253–265.
| Quantification of total sheep IgE concentration using anti-ovine IgE monoclonal antibodies in an enzyme immunoassay.Crossref | GoogleScholarGoogle Scholar | 9261963PubMed |
Shaw R, Morris C, Green R, Wheeler M, Bisset S, Vlassoff A, Douch P (1999) Genetic and phenotypic relationships among Trichostrongylus colubriformis-specific immunoglobulin E, anti-Trichostrongylus colubriformis antibody, immunoglobulin G1, faecal egg count and body weight traits in grazing Romney lambs. Livestock Production Science 58, 25–32.
| Genetic and phenotypic relationships among Trichostrongylus colubriformis-specific immunoglobulin E, anti-Trichostrongylus colubriformis antibody, immunoglobulin G1, faecal egg count and body weight traits in grazing Romney lambs.Crossref | GoogleScholarGoogle Scholar |
Shaw R, Pfeffer A, Bischof R (2009) Ovine IgE and its role in immunological protection and disease. Veterinary Immunology and Immunopathology 132, 31–40.
| Ovine IgE and its role in immunological protection and disease.Crossref | GoogleScholarGoogle Scholar | 19836086PubMed |
Shaw RJ, Morris CA, Wheeler M, Tate M, Sutherland IA (2012) Salivary IgA: a suitable measure of immunity to gastrointestinal nematodes in sheep. Veterinary Parasitology 186, 109–117.
| Salivary IgA: a suitable measure of immunity to gastrointestinal nematodes in sheep.Crossref | GoogleScholarGoogle Scholar | 22153121PubMed |
Shaw RJ, Morris CA, Wheeler M (2013) Genetic and phenotypic relationships between carbohydrate larval antigen (CarLA) IgA, parasite resistance and productivity in serial samples taken from lambs after weaning. International Journal for Parasitology 43, 661–667.
| Genetic and phenotypic relationships between carbohydrate larval antigen (CarLA) IgA, parasite resistance and productivity in serial samples taken from lambs after weaning.Crossref | GoogleScholarGoogle Scholar | 23623806PubMed |
Stear M, Bishop S, Doligalska M, Duncan J, Holmes P, Irvine J, McCririe L, McKellar Q, 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.
| Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta.Crossref | GoogleScholarGoogle Scholar | 8834764PubMed |
Stear MJ, Bairden K, Duncan JL, Holmes PH, McKellar QA, Park M, Strain S, Murray M, Bishop SC, Gettinby G (1997) How hosts control worms. Nature 389, 27
| How hosts control worms.Crossref | GoogleScholarGoogle Scholar | 9288962PubMed |
Stear M, Bairden K, Innocent G, Mitchell S, Strain S, Bishop S (2004) The relationship between IgA activity against 4th-stage larvae and density-dependent effects on the number of 4th-stage larvae of Teladorsagia circumcincta in naturally infected sheep. Parasitology 129, 363–369.
| The relationship between IgA activity against 4th-stage larvae and density-dependent effects on the number of 4th-stage larvae of Teladorsagia circumcincta in naturally infected sheep.Crossref | GoogleScholarGoogle Scholar | 15471011PubMed |
Stear M, Singleton D, Matthews L (2011) An evolutionary perspective on gastrointestinal nematodes of sheep. Journal of Helminthology 85, 113–120.
| An evolutionary perspective on gastrointestinal nematodes of sheep.Crossref | GoogleScholarGoogle Scholar | 24650861PubMed |
Strain S, Bishop S, Henderson N, Kerr A, McKellar Q, Mitchell S, Stear M (2002) The genetic control of IgA activity against Teladorsagia circumcincta and its association with parasite resistance in naturally infected sheep. Parasitology 124, 545–552.
| The genetic control of IgA activity against Teladorsagia circumcincta and its association with parasite resistance in naturally infected sheep.Crossref | GoogleScholarGoogle Scholar | 12049417PubMed |
Williams AR, Palmer DG (2012) Interactions between gastrointestinal nematode parasites and diarrhoea in sheep: pathogenesis and control. Veterinary Journal 192, 279–285.
| Interactions between gastrointestinal nematode parasites and diarrhoea in sheep: pathogenesis and control.Crossref | GoogleScholarGoogle Scholar |
Williams AR, Karlsson L, Palmer D, Vercoe P, Williams I, Greeff J, Emery D (2010) Relationships between faecal dry matter, worm burdens and inflammatory mediators and cells in parasite-resistant Merino rams. Veterinary Parasitology 171, 263–272.
| Relationships between faecal dry matter, worm burdens and inflammatory mediators and cells in parasite-resistant Merino rams.Crossref | GoogleScholarGoogle Scholar | 20430531PubMed |
