- I — Coévolution Hôtes Pathogènes: Caractérisation et Gestion de la Diversité Génétique des deux Partenaires / Co-Evolution Hosts Pathogens: Characterization and Management of Genetic Diversity of Both Partners
- Open access
- Published:
Life-trait evolution of a parasite strongyle nematode in response to host resistance: an experimental approach using Haemonchus contortus in black belly lambs
Évolution des traits de vie des strongles gastro-intestinaux en réponse à la résistance de l’hôte: essai d’une approche expérimental sur un modèle Haemonchus contortus — agneaux “Black Belly”
Genetics Selection Evolution volume 33, Article number: S25 (2001)
Abstract
The selection of resistant sheep in farms could increase the selective pressure during the parasitic phase and this might affect life-traits of the parasite nematodes. Before selecting for host resistance, it is crucial to estimate the potential adaptation of these nematodes to resistant hosts. The objective of this study was to determine the ability of the nematode parasite, Haemonchus contortus, to adapt its life-traits to different resistance states of sheep. The isolates of the nematode Haemonchus contortus were obtained from five locations in Guadeloupe (French West Indies) and a synthetic strain was prepared, which was representative of these isolates on the basis of isoenzymes and morphometric traits. This synthetic strain was reproduced during 10 generations in hosts of marked different resistance status. Primary infected 6-to 8-months old Black Belly ewe lambs, a wellknown to be highly resistant breed to nematode parasites, were used as resistant host. The “susceptible” lambs were obtained by treating with long-acting corticoids to depress the resistance of lambs. The establishment rate of worms and their egg-laying capacities were highly reduced in resistant lambs compared with susceptible ones. It can be assumed that the experimental design of infection apparently mimicked well the differences observed between genotypically resistant and susceptible sheep. To assess the adaptation, resistant, susceptible and naive lambs were infected with the two H. contortus lines, previously reproduced in resistant or susceptible sheep. The hosts were genetically related lambs (monozygotic twin lambs, within-litter brothers) allocated in an experimental plan designed to enhanced the power of the experiment. The use of monozygotic twins did not prove as useful as expected for parasitologi-cal data. There was no significant difference between the life-traits of the two lines. H. contortus did not seem to adapt to the resistance status of the host. Therefore, it was considered that selection for resistant sheep was possible with a limited risk of adaptation of the nematode parasites, although long-term monitoring of nematode adaptation should be scheduled if host selection is planned.
Résumé
L’utilisation d’animaux plus résistants aux strongles gastro-intestinaux dans les nouvelles pratiques d’élevage peut constituer une pression de sélection significative induisant une adaptation des traits de vie des parasites. Il est donc nécessaire, avant d’intégrer le caractère de résistance dans des programmes de sélection, de s’assurer de l’absence d’adaptation du nématode. L’objectif de cette étude était de déterminer si Haemonchus contortus présentait la capacité d’adapter ses traits de vie à des ovins plus resistants. Un isolat synthétique d’Haemonchus contortus a été créé à partir d’isolats de cinq régions de Guadeloupe (French West Indies), en s’assurant de sa bonne representativité sur la base de caractères morphométriques et d’isoenzymes. Cet isolat a ete multiplié durant 10 générations chez des ovins à statut de résistance très différent. Des agnelles primo-infestées âgées de 6–8 mois, de génotype Black Belly connu pour sa resistance aux strongles gastro-intestinaux, ont été utilisées comme hôtes résistants. Des agnelles, immuno-déprimées par injections de corticoïdes retard ont été utilisées comme hôtes sensibles. Le taux d’installation et la production journalière d’SSufs des parasites ont été très fortement diminués par passage chez les hôtes résistants. L’adaptation des deux lignées d’H. contortus a été évaluée par infestation expérimentale de 60 agneaux des deux sexes, répartis en trois groupes: agneaux rendus résistants, agneaux naïfs et agneaux rendus sensibles. Ces animaux, dont neuf couples de jumeaux monozy-gotes, issus de parents génétiquement très proches (pleins frères issus de parents très apparentés, jumeaux monozygotes), ont été répartis dans les groupes afin de max-imiser la probabilitve de mettre en évidence des différences entre lignées. La variabilité entre jumeaux homozygotes n’a pas été significativement diminuée pour les variables parasitaires. Malgré la puissance du dispositif expérimental mis en place, aucune différence dans les traits de vie des deux lignées d’H. contortus n’a pu étre mise en évidence. La sélection d’animaux résistants peut done être engagée sans risque important d’adaptation d’H. contortus dans un premier temps, dans l’attente d’une vérification plus approfondie sur le terrain.
References
Adams D.B., Beth K.J., Immunity acquired by sheep from an experimental infection with Haemonchus contortus, Int. J. Parasitol. 16 (1981) 659–664.
Adams D.B., Developmental arrest of Haemonchus contortus in sheep treated with corticosteroid, Int. J. Parasitol. 12 (1982) 523–529.
Adams D.B., Infection with Haemonchus contortus in sheep and the role of adaptive immunity in selection of the parasite, Int. J. Parasitol. 18 (1988) 1071–1075.
Albers G.A.A., Burgess S.K., Serial passage of Haemonchus contortus in resistant and susceptible sheep, Vet. Parasitol. 28 (1988) 303–306.
Arnold S.J., Wade M.J., On the measurement of natural and sexual selection: applications, Evolution 38 (1984) 720–734.
Aumont G., Gruner L., Hostache G., Comparative resistance of Black Belly vs. INRA401 sheep to Haemonchus contortus, Acta Parasitol. 45 (2000) 221.
Aumont G., Pouillot R., Simon R., Hostache G., Barre N., Varo H., Parasitisme digestif des petits ruminants dans les Antilles frangaises, INRA Prod. Anim. 10 (1997) 79–90.
Aumont G., Barré N., Mandonnet N’Zobadila G., Ouattata L., Vassiliades G., Strongyloses gastro-intestinales des petits ruminants en milieu tropical: résistance génétique et milieu d’infestation. Rapport annuel de l’ATP MIPA 72/94. Résultats de l’année 1996, Unité de Recherches Zootechniques, Guadeloupe, 1997.
Baker R.L., Genetics of disease resistance in small ruminants in Africa, in: Gray G.D., Woolaston R.R., Eaton B.T. (Eds.), Breeding for resistance to infectious diseases in small ruminants, ACIAR, Camberra, 1995, pp. 119–138.
Barger LA., Influence of sex and reproductive status on susceptibility of ruminants to nematode parasitism, Int. J. Parasitol. 23 (1993) 463–469.
Barger I.A., Sutherst R.W., Population biology of host and parasite, in: Gray G.D. Woolaston R.R. (Eds.), Breeding for disease resistance in sheep, Aust. Wool Corp., Melbourne, 1991, pp. 51–56.
Barre N., Amouroux I., Aprelon R., Samut T., Résistance des strongles gastro-intestinaux aux anthelmintiques dans les élevages caprins en Guadeloupe (Antilles françaises), Rev. Élev. Med. Vet. Pays Trop. 50 (1997) 105–110.
Bentounsi B., Cabaret J. Analysis of helminth genetic data: comparative examples with Haemonchus contortus isozymes using exact-tests or resampling procedures, Parasitol. Res. 85 (1999) 855–857.
Berbigier P., Gruner L., Mambrini M., Sophie S.A., Faecal water content and egg survival of goat gastrointestinal strongyles under dry tropical conditions in Guadeloupe, Parasitol. Res. 76 (1990) 379–385.
Chehresa A., Beech R.N., Scott M.E., Life history variation among lines isolated from a laboratory population of Heligmosomoides polygyrus bakeri, Int. J. Parasitol. 27 (1997) 541–555.
Chesné P., Colas G., Cognié Y., Guérin Y., Sévellec C., Lamb production using superovulation, embryo bisection, and transfer, Theriogenology 27 (1987) 751–757.
Clayton D.H., Lee P.L.M., Tomkins D.M., Brodie I.E.D., Reciprocal natural selection on host-parasite phenotypes, Am. Nat. 154 (1999) 261–270.
Coltman D.W., Pilkington J.G., Smith J.A., Pemberton J.M., Parasite-mediated selection against inbred Soay sheep in a free-living, island population, Evolution 53 (1999) 1259–1267.
Courtney C.H., Parker C.F., McClure K.E., Herd R.P., Resistance of exotic and domestic lambs to experimental infection with Haemonchus contortus. Int. J. Parasitol. 15 (1985) 101–109.
Courtney C.H., Parker C.F., McClure K.E., Herd R.P., A comparison of the peri-parturient rise in faecal egg counts of exotic and domestic ewes, Int. J. Parasitol. 14 (1984) 377–381.
Coyne M.J., Smith G., Johnstone C., A study of the mortality and fecundity of Haemonchus contortus in sheep following experimental infections, Int. J. Parasitol. 21 (1991) 847–853.
Dawkins H.J.S., Windon R.G., Eagleson G.K., Eosinophil responses in sheep selected for high and low responsiveness to Trichostrongylus colubriformis, Int. J. Parasitol. 18 (1989) 199–205.
Fabiyi J.P., Production losses and control of helminths in ruminants of tropical regions, Int. J. Parasitol. 17 (1987) 571–578.
Fleming M.W., Selection for a strain of Haemonchus contortus that exhibits peri-parturient egg rise in sheep, J. Parasitol. 79 (1993) 399–402.
Gamble H.R., Zajac A.M., Resistance of St Croix lambs to Haemonchus contortus in experimentally and naturally acquired infection, Vet. Parasitol. 41 (1992) 211–225.
Gasnier N., Cabaret J., Stable and unstable environments influence the genetic diversity of the nematode Teladorsagia circumcincta, a parasite of small ruminants, Parasitol. Res. 84 (1998) 676–681.
Gasnier N., Cabaret J., Moulia C., Allozyme variation between laboratory reared and wild populations of Teladorsagia circumcincta., Int. J. Parasitol. 22 (1992) 581–587.
Gill H.S., Gray G.D., Watson D.L., Husband A.J, Specific antibody responses to Haemonchus contortus in genetically resistant sheep, Parasite Immunol. 15 (1993) 61–67.
Groeneveld E., PEST User’s manual. Institut fur Tierzucht und Tierverhalten, FAL, Neustadt, 1994.
Gruner L., Lantier F., Breeding for resistance to infectious diseases of small ruminants in Europe, in: Breeding for resistance to infectious diseases in small ruminants, Gray G.D., Woolaston R.R., Eaton B.T. (Eds.), Aciar Monograph No. 34 (1995).
Hostache G., Aumont G., Saulai M., Despois P., Depres E., Infection of lambs with two isolates of Haemonchus contortus from the Caribbean, in: Proceedings of the 17th international conference of the WAAVP, Copenhagen, Denmark, C7, 1999, 76.
Hubert J., Kerboeuf D. A new method for culture of larvae used in diagnosis of ruminant gastrointestinal strongylosis: comparison with fecal cultures, Can. J. Comp. Med. 48 (1984) 63–71.
Jacquiet P., Humbert J.F., Comes A.M., Cabaret J., Thiam E., Cheikh D., Ecological, morphological and genetic characterization of sympatric Haemonchus spp. parasites of domestic ruminants in Mauritania, Parasitology 110 (1995) 483–492.
Jorgensen L.T., Leathwick D.M., Charleston W.A.G., Godfrey P.L., Vlassoff A., Sutherland L.A., Variation between hosts in the developmental success of the free-living stages of trichostrongyle infections of sheep, Int. J. Parasitol. 28 (1998) 1347–1352.
Luffau G., Péry P., Charley J. Réponse immunitaire chez les ovins infestés expériment alement par Haemonchus contortus. Étude comparative chez le mâle et chez la femelle, Ann. Rech. Vét. 12 (1981) 173–181.
Mahieu M., Aumont G., Michaux Y., Alexandre G., Archimede H., Boval M., Theriez M., L’association d’ovins et de bovins sur des prairies irriguees en Martinique, INRA Prod. Anim. 10 (1997) 55–65.
Maingi N., Scott M.E., Prichard R.K., Effect of selection pressure for thiabendazole resistance on fitness of Haemonchus contortus in sheep, Parasitology, 100 (1990) 327–335.
Mandonnet N., Aumont G., Fleury J., Gruner L., Bouix J., Vu Tien Khang J., Genetic variability in resistance of Creole goats to natural infection with Tri-chostrongylids in Guadeloupe, Ann. New York Acad. Sci. 791 (1996) 421–431.
Mandonnet N., Aumont G., Fleury J., Gruner L., Bouix J., Vu Tien Khang J., Résistance génétique aux strongles gastro-intestinaux chez les caprins Créoles. Influence de différents environnement tropicaux sur l’expression du potentiel géné-tique de résistance, INRA Prod. Anim. 10 (1997) 91–98.
Matthews D., Brundson R.V., Vlassof A., 1979. Effect of dexamethasone on the ability of sheep to resist re-infection with nematodes, Vet. Parasitol. 5 (1979) 65–75.
Mc Kenna P.B., Morphological evidence of subspeciation in Haemonchus contortus from New-Zealand sheep: the vulval flap formula, N.Z.J. Agric. Res. 14, (1971) 902–914.
Morand S., Life-history traits in parasitic nematodes: a comparative approach for the search of invariants, Funct. Ecol. 10 (1996) 210–218.
Overend D.J., Phillips M.L., Poulton A.L., Foster C.E.D., Anthelmintic resistance in Australian sheep nematode populations, Aust. Vet. J. 71 (1994) 117–121.
Peters A.M., Lively M., The red queen and fluctuating epistasis: a population genetic analysis of antagonistic evolution, Am. Nat. 154 (1999) 393–405.
Piper L.R., Genetic variation in resistance to internal parasites, in: McGuirk B.J. (Ed.), Merino improvement programs in Australia, Aust. Wool Corp. Sydney, 1987, pp. 351–363.
Presson B.L., Gray G.D., Burgess S.K., The effect of immunosuppression with dexamethasone on Haemonchus contortus infections in genetically resistant merino sheep, Parasite Immunol. 10 (1988) 675–680.
SAS/STAT. User’s Guide, Version 6, 4th edn., Vol. 2, Cary, NC, USA, 1998.
Saulai M., Evolution de la fitness de deux lignees d’Haemonchus contortus chez des ovins rendus sensibles ou resist ants en conditions experiment ales, Ph.D. Thesis, Paris XIII University, 1999.
Saulai M., Hostache G., Aumont G., Cabaret J., From isolates to laboratory populations: maintenance of variability in the nematode Haemonchus contortus. Parasites 7 (1999) 31–38.
Shabalina S.A., Yampolsky L.Y., Kondrashov A.S., Rapid decline of fitness in panmictic populations of Drosophila melanogaster maintained under relaxed natural selection, Proc. Nat. Acad. Sci. USA 94 (1997) 13034–13039.
Simon R., Aumont G., Aprelon R., Variations in herbage density of third stage larvae of goats strongyle during dry season in Guadeloupe (F.W.I.), Ann. New York Acad. Sci. 791 (1995) 412–420.
Skorping A., Andrew F.R., Keymer A.E., Life history covariation in intestinal nematodes of mammals, Oikos 60 (1991) 365–372.
Sreter T., Kassai T., Takacs E., The heritability and specificity of responsiveness to infection with Haemonchus contortus in sheep, Int. J. Parasitol. 24 (1994) 871–876.
Stears M.J., Bairden K., Bishop C., Buitkamp J., Duncan J.L., Gettinby G., McKellar Q.A., Park M., Parkins J.J., Reid S.W.J., Strain S., Murray M., The genetic basis of resistance to Ostertagia circumcincta in lambs, Vet. J. 154 (1997) 111–119.
Van Wyk J.A., Malan F.S., Resistance of field strains of Haemonchus contortus to ivermectin, closantel, rafoxanide and the benzimidazoles in South Africa, Vet. Rec. 123 (1988) 226–228.
Watson T.G., Baker R.L., Harvey T.G., Genetic variation in resistance or tolerance to internal nematode parasites in strains of sheep at Rotomahana, Proc. N. Z. Soc. Anim. Prod. 46 (1986) 23–26.
Windon R.G., Genetic control to host responses involved in resistance to gastrointestinal nematodes of sheep, in: Owen J.B., Axford R.F.E. (Eds.), Breeding for disease resistance in farm animals, CAB Int., Wallingford, 1991, pp. 162–186.
Woolaston R.R., Baker R.L., Prospects of breeding small ruminants for resistance to internal parasites, Int. J. Parasitol. 26 (1996) 845–855.
Woolaston R.R., Barger I.A., Piper L.R., Response to helminth infection of sheep selected for resistance to Haemonchus contortus, Int. J. Parasitol. 20 (1990) 1015–1018.
Woolaston R.R., Elwin R.L., Barger I.A., No adaptation of Haemonchus contortus to genetically resistant sheep, Int. J. Parasitol. 22 (1992) 377–380.
Woolaston R.R., Eady S.J., Australian research on genetic resistance to nematode parasites, in: Gray G.D., Woolaston R.R., Eaton B.T. (Eds.), Breeding for resistance to infectious diseases in small ruminants, Camberra ACIAR, 1995, pp. 53–75.
Yazwinski T.A., Goode L., Moncol D.J., Morgan G.W., Linnerud A.C., Haemonchus contortus resistance in straight breed and crossbred Barbados Black belly sheep, J. Anim. Sci. 51 (1980) 279–284.
Yazwinski T.A., Goode L., Moncol D.J., Morgan G.W., Linnerud A.C., Parasite resistance in straight bred and crossbred Barbados Black belly sheep, J. Anim. Sci. 49 (1979) 919–926.
Author information
Authors and Affiliations
Rights and permissions
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
About this article
Cite this article
Saulai, M., Cabaret, J., Hostache, G. et al. Life-trait evolution of a parasite strongyle nematode in response to host resistance: an experimental approach using Haemonchus contortus in black belly lambs. Genet Sel Evol 33 (Suppl 1), S25 (2001). https://doi.org/10.1186/BF03500871
Published:
DOI: https://doi.org/10.1186/BF03500871