A genome scan for QTL affecting resistance to haemonchus contortus in sheep

Journal of Animal Science

Volumn 90, Issue 13, 2012, Pages 4690-4705

  Salle G ^a,b   Jacquiet, P ^b   Gruner, L ^c   Cortet, J ^c   Sauve C ^c   Prevot F ^b   Grisez, C ^b   Bergeaud, J P ^b   Schibler, L ^a   Tircazes, A ^a   Francois D ^a   Pery, C ^a   Bouvier, F ^a   Thouly, J C ^a   Brunel, J C ^a   Legarra, A ^a   Elsen, J M ^a   Bouix, J ^a   Rupp, R ^a   Moreno, C R ^a  

^a CEMAGREF   (France)

^b IHAP   (France)

^c UR1282   (France)

Author keywords

Haemonchus contortus; Linkage disilibrium; Quantitative trait loci; Resistance; Sheep

Indexed keywords

MICROSATELLITE DNA;

ANIMAL; ANIMAL DISEASE; ARTICLE; BLOOD ANALYSIS; BREEDING; CROSS BREEDING; DISEASE RESISTANCE; DNA MICROARRAY; FEMALE; FRANCE; GENETIC MARKER; GENETICS; GENOTYPING TECHNIQUE; HAEMONCHOSIS; HAEMONCHUS; HEMATOCRIT; IMMUNOLOGY; ISOLATION AND PURIFICATION; MALE; PARASITE IDENTIFICATION; PARASITE LOAD; PARASITOLOGY; QUANTITATIVE TRAIT LOCUS; SHEEP; SHEEP DISEASE; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BLOOD CHEMICAL ANALYSIS; BREEDING; CROSSES, GENETIC; DISEASE RESISTANCE; FEMALE; FRANCE; GENETIC MARKERS; GENOTYPING TECHNIQUES; HAEMONCHIASIS; HAEMONCHUS; HEMATOCRIT; MALE; MICROSATELLITE REPEATS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARASITE EGG COUNT; PARASITE LOAD; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SHEEP; SHEEP DISEASES;

EID: 84882667245     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2012-5121     Document Type: Article

References (54)

1. Amarante, A. F. T., P. A. Bricarello, R. A. Rocha, and S. M. Gennari. 2004. Resistance of Santa Ines, Suffolk and Ilede France sheep to naturally acquired gastrointestinal nematode infections. Vet. Parasitol. 120:91-106.
2. Archibald, A. L., N. E. Cockett, B. P. Dalrymple, T. Faraut, J. W. Kijas, J. F. Maddox, J. C. McEwan, V. Hutton Oddy, H. W. Raadsma, C. Wade, J. Wang, W. Wang, and X. Xun. 2010. The sheep genome reference sequence: A work in progress. Anim. Genet. 41:449-453.
3. Aumont, G., L. Gruner, and G. Hostache. 2003. Comparison of the resistance to sympatric and allopatric isolates of Haemonchus contortus of Black Belly sheep in Guadeloupe (FWI) and of INRA 401 sheep in France. Vet. Parasitol. 116:139-150.
4. Beavis, W. D. 1994. The power and deceit of QTL experiments: Lessons from comparative QTL studies. Pages 250-256 in The Proceedings of the Forty-Ninth Annual Corn & Sorghum Industry Research Conference. American Seed Trade Assoc., Washington, DC.
5. Beh, K. J., D. J. Hulme, M. J. Callaghan, Z. Leish, I. Lenane, R. G. Windon, and J. F. Maddox. 2002. A genome scan for quantitative trait loci affecting resistance to Trichostrongylus colubriformis in sheep. Animal Genetics 33:97-106.
6. Beraldi, D., A. F. McRae, J. Gratten, J. G. Pilkington, J. Slate, P. M. Visscher, and J. M. Pemberton. 2007. Quantitative trait loci (QTL) mapping of resistance to strongyles and coccidia in the free-living Soay sheep (Ovis aries). Int. J. Parasitol. 37:121-129.
7. Bishop, S. C., and C. A. Morris. 2007. Genetics of disease resistance in sheep and goats. Small Ruminant Res. 70:48-59.
8. Bovenhuis, H., and R. J. Spelman. 2000. Selective genotyping to detect quantitative trait loci for multiple traits in outbred populations. J. Dairy Sci. 83:173-180.
9. Cezar, A. S., G. Toscan, G. Camillo, L. A. Sangioni, H. O. Ribas, and F. S. Vogel. 2010. Multiple resistance of gastrointestinal nematodes to nine different drugs in a sheep flock in southern Brazil. Vet. Parasitol. 173:157-160.
10. Churchill, G. A., and R. W. Doerge. 1994. Empirical threshold values for quantitative trait mapping. Genetics 138:963-971.
11. Cole, J. B., P. M. VanRaden, J. R. O'Connell, C. P. Van Tassell, T. S. Sonstegard, R. D. Schnabel, J. F. Taylor, and G. R. Wiggans. 2009. Distribution and location of genetic effects for dairy traits. J Dairy Sci. 92:2931-2946.
12. Coop, R. L., W. D. Smith, K. W. Angus, R. B. Graham, S. E. Wright, and F. Jackson. 1985. Effect of Ostertagia ostertagi on lamb performance and cross resistance to O. circumcincta. Res. Vet. Sci. 39:200-206.
13. Courtney, C. H., C. F. Parker, K. E. McClure, and R. P. Herd. 1985. Resistance of nonlambing exotic and domestic ewes to naturally acquired gastrointestinal nematodes. Int. J. Parasitol. 15:239-243.
14. Crawford, A. M., K. A. Paterson, K. G. Dodds, C. Diez Tascon, P. A. Williamson, M. Roberts Thomson, S. A. Bisset, A. E. Beattie, G. J. Greer, R. S. Green, R. Wheeler, R. J. Shaw, K. Knowler, J. C. McEwan. 2006. Discovery of quantitative trait loci for resistance to parasitic nematode infection in sheep: I. Analysis of outcross pedigrees. BMC Genomics 7:178.
15. Darvasi, A., A. Weinreb, V. Minke, J. I. Weller, and M. Soller. 1993. Detecting marker-QTL linkage and estimating QTL gene effect and map location using a saturated genetic map. Genetics 134:943-951.
16. Davies, G., M. J. Stear, M. Benothman, O. Abuagob, A. Kerr, S. Mitchell, and S. C. Bishop. 2006. Quantitative trait loci associated with parasitic infection in Scottish blackface sheep. Heredity 96:252-258.
17. Dominik, S., P. W. Hunt, J. McNally, A. Murrell, A. Hall, and I. W. Purvis. 2010. Detection of quantitative trait loci for internal parasite resistance in sheep. I. Linkage analysis in a Romney × Merino sheep backcross population. Parasitology 137:1275-1282.
18. Dorny, P., and J. Vercruysse. 1998. Evaluation of a micro method for the routine determination of serum pepsinogen in cattle. Res. Vet. Sci. 65:259-262.
19. Elsen, J. M., B. Mangin, B. Goffinet, D. Boichard, and P. Le Roy. 1999. Alternative models for QTL detection in livestock. I. General introduction. Genet. Sel. Evol. 31:213.
20. Good, B., J. P. Hanrahan, B. A. Crowley, and G. Mulcahy. 2006. Texel sheep are more resistant to natural nematode challenge than Suffolk sheep based on faecal egg count and nematode burden. Vet. Parasitol. 136:317-327.
21. Green, P., K. Falls, and S. Crooks. 1990. Documentation for CRI-MAP. v. 2.4. Washington Univ. School of Medicine, St. Louis, MO.
22. Gutierrez-Gil, B., J. Perez, L. Alvarez, M. Martinez-Valladares, L. F. de la Fuente, Y. Bayon, A. Meana, F. San Primitivo, F. A. Rojo-Vazquez, and J. J. Arranz. 2009. Quantitative trait loci for resistance to trichostrongylid infection in Spanish Churra sheep. Genet. Sel. Evol. 41:46.
23. Hayes, B., and M. E. Goddard. 2001. The distribution of the effects of genes affecting quantitative traits in livestock. Genet. Sel. Evol. 33:209-229.
24. Hill, W. G., and A. Robertson. 1968. Linkage disequilibrium in finite populations. Theor. Appl. Genet. 38:226-231.
25. Hoglund, J., K. Gustafsson, B. L. Ljungstrom, A. Engstrom, A. Don-nan and P. Skuce. 2009. Anthelmintic resistance in Swedish sheep flocks based on a comparison of the results from the faecal egg count reduction test and resistant allele frequencies of the beta-tubulin gene. Vet Parasitol. 161:60-68.
26. Howell, S. B., J. M. Burke, J. E. Miller, T. H. Terrill, E. Valencia, M. J. Williams, L. H. Williamson, A. M. Zajac, and R. M. Kaplan. 2008. Prevalence of anthelmintic resistance on sheep and goat farms in the southeastern United States. J. Am. Vet. Med. Assoc. 233:1913-1919.
27. Kemper, K. E., D. L. Emery, S. C. Bishop, H. Oddy, B. J. Hayes, S. Dominik, J. M. Henshall, and M. E. Goddard. 2011. The distribution of SNP marker effects for faecal worm egg count in sheep, and the feasibility of using these markers to predict genetic merit for resistance to worm infections. Genet Res. 93:203-219.
28. Knott, S. A., L. Marklund, C. S. Haley, K. Andersson, W. Davies, H. Ellegren, M. Fredholm, I. Hansson, B. Hoyheim, K. Lundström, M. Moller, and L. Andersson. 1998. Multiple marker mapping of quantitative trait loci in a cross between outbred wild boar and large white pigs. Genetics 149:1069-1080.
29. Lacroux, C., T. H. Nguyen, O. Andreoletti, F. Prevot, C. Grisez, J. P. Ber-geaud, L. Gruner, J. C. Brunel, D. Francois, P. Dorchies, P. Jacqui-et. 2006. Haemonchus contortus (Nematoda: Trichostrongylidae) infection in lambs elicits an unequivocal Th2 immune response. Vet. Res. 37:607-622.
30. Lander, E. S., and D. Botstein. 1989. Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185-199.
31. Lander, E., and L. Kruglyak. 1995. Genetic dissection of complex traits: Guidelines for interpreting and reporting linkage results. Nat Genet. 11:241-247.
32. Legarra, A., and R. L. Fernando. 2009. Linear models for joint association and linkage QTL mapping. Genet. Sel. Evol. 41:43.
33. Lynch, M., and B. Walsh. 1998. Genetics Analysis of Quantitative Traits. Sinauer Associates, Sunderland, MA.
34. Mandonnet, N., M. Bachand, M. Mahieu, R. Arquet, F. Baudron, L. Abi-nne-Molza, H. Varo, and G. Aumont. 2005. Impact on productivity of peri-parturient rise in fecal egg counts in Creole goats in the humid tropics. Vet. Parasitol. 134:249-259.
35. Mandonnet, N., V. Ducrocq, R. Arquet, and G. Aumont. 2003. Mortality of Creole kids during infection with gastrointestinal strongyles: A survival analysis. J. Anim. Sci. 81:2401-2408.
36. Marshall, K., J. F. Maddox, S. H. Lee, Y. Zhang, L. Kahn, H.-U. Graser, C. Gondro, S. W. Walkden-Brown, and J. H. J. van der Werf. 2009. Genetic mapping of quantitative trait loci for resistance to Haemonchus contortus in sheep. Anim. Genet. 40:262-272.
37. Matika, O., R. Pong-Wong, J. A. Wooliams, and S. C. Bishop. 2011. Confirmation of two quantitative trait loci regions for nematode resistance in commercial British terminal sire breeds. Animal 5:1149-1156.
38. McRae, A. F., J. C. McEwan, K. G. Dodds, T. Wilson, A. M. Crawford, and J. Slate. 2002. Linkage disequilibrium in domestic sheep. Genetics 160:1113-1122.
39. Meadows, J. R., E. K. Chan, and J. W. Kijas. 2008. Linkage disequilibrium compared between fi ve populations of domestic sheep. BMC Genet. 9:61.
40. Meeusen, E. N., and A. Balic. 2000. Do eosinophils have a role in the killing of helminth parasites? Parasitol. Today 16:95-101.
41. Melchinger, A. E., H. F. Utz, and C. C. Schön. 1998. Quantitative trait locus (QTL) mapping using different testers and independent population samples in maize reveals low power of QTL detection and large bias in estimates of QTL effects. Genetics 149:383-403.
42. Meuwissen, T. H. E., and M. E. Goddard. 2007. Multipoint identity-by-descent prediction using dense markers to map quantitative trait loci and estimate effective population size. Genetics 176:2551-2560.
43. Ooijen, J. 1992. Accuracy of mapping quantitative trait loci in autogamous species. Theor. Appl. Genet. 84:803-811.
44. Pérez-Enciso, M., and L. Varona. 2000. Quantitative trait loci mapping in F2 crosses between outbred lines. Genetics 155:391-405.
45. Piepho, H. P. 2001. A quick method for computing approximate thresholds for quantitative trait loci detection. Genetics 157:425-432.
46. Raynaud, J. P. 1970. Etude de l'effi cacité d'une technique de coproscopie quantitative pour le diagnostic de routine et le contrôle des infestations parasitaires des bovins, ovins, équins et porcins. Ann. Parasitol. 45:321-342.
47. de Roos, A. P., B. J. Hayes, R. J. Spelman, and M. E. Goddard. 2008. Linkage disequilibrium and persistence of phase in Holstein-Friesian, Jersey and Angus cattle. Genetics 179:1503-1512.
48. Sargison, N. D., F. Jackson, D. J. Bartley, D. J. Wilson, L. J. Stenhouse, and C. D. Penny. 2007. Observations on the emergence of multiple anthelmintic resistance in sheep flocks in the south-east of Scotland. Vet. Parasitol. 145:65-76.
49. Simpson, H. V. 2000. Pathophysiology of abomasal parasitism: is the host or parasite responsible? Vet J. 160:177-191.
50. Stear, M. J., M. Parkand, S. C. Bishop. 1996. The key components of resistance to Ostertagia circumcincta in lambs. Parasitol. Today 12:438-441.
51. Terefe, G., C. Lacroux, O. Andreoletti, C. Grisez, F. Prevot, J. P. Berge-aud, J. Penicaud, V. Rouillon, L. Gruner, J. C. Brunel, A. Legarra, J. M. Elsen, J. Bouix, R. Rupp, and C. R. Moreno. 2007. Immune response to Haemonchus contortus infection in susceptible (INRA 401) and resistant (Barbados Black Belly) breeds of lambs. Parasite Immunol. 29:415-424.
52. Terefe, G., C. Lacroux, F. Prévot, C. Grisez, J. P. Bergeaud, C. Bleuart, P. Dorchies, G. Foucras, and P. Jacquiet. 2009. Eosinophils in Hae-monchus contortus-infected resistant and susceptible breeds of sheep: Abomasal tissue recruitment and in vitro functional state. Vet. Parasitol. 165:161-164.
53. Traversa, D., B. Paoletti, D. Otranto, and J. Miller. 2007. First report of multiple drug resistance in trichostrongyles affecting sheep under field conditions in Italy. Parasitol Res. 101:1713-1716.
54. Yazwinski, T. A., L. Goode, D. J. Moncol, G. W. Morgan, and A. C. Lin-nerud. 1980. Haemonchus contortus resistance in straightbred and crossbred Barbados Blackbelly sheep. J Anim. Sci. 51:279-284.