Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal

Journal of Evolutionary Biology

Volumn 24, Issue 8, 2011, Pages 1664-1676

  Hayward, Adam D ^a   Wilson, A J ^a   Pilkington, J G ^a   Clutton Brock, T H ^b   Pemberton, J M ^a   Kruuk, L E B ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Faecal egg count; Parasite burden; Soay sheep; Strongyles; Teladorsagia; Trichostrongylus

Indexed keywords

DATA SET; EGG; FITNESS; HOST-PARASITE INTERACTION; IMMUNITY; LIFE HISTORY TRAIT; MORTALITY; NATURAL SELECTION; PARASITE INFESTATION; PARASITIC DISEASE; SHEEP; WILD POPULATION;

AGE; ANIMAL; ANIMAL DISEASE; ARTICLE; BODY SIZE; FECES; FEMALE; GENETIC SELECTION; GENETICS; GENOTYPE; IMMUNOLOGY; INNATE IMMUNITY; MALE; PARASITOLOGY; PHENOTYPE; REPRODUCTION; SEX DIFFERENCE; SHEEP; SHEEP DISEASE; TRICHOSTRONGYLOSIS;

AGE FACTORS; ANIMALS; BODY SIZE; FECES; FEMALE; GENOTYPE; IMMUNITY, INNATE; MALE; PHENOTYPE; REPRODUCTION; SELECTION, GENETIC; SEX FACTORS; SHEEP DISEASES; SHEEP, DOMESTIC; TRICHOSTRONGYLOSIS;

MAMMALIA; OVIS ARIES; STRONGYLES; TELADORSAGIA; TRICHOSTRONGYLUS;

EID: 79960204618     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02300.x     Document Type: Article

References (75)

1. Beraldi, D., McRae, A.F., Gratten, J., Pilkington, J.G., Slate, J., Visscher, P.M. et al. 2007. Quantitative trait loci (QTL) mapping of resistance to strongyles and coccidea in the free-living Soay sheep (Ovis aries). Int. J. Parasitol. 37: 121-129.
2. Bonneaud, C., Mazuc, J., Chastel, O., Westerdahl, H. & Sorci, G. 2004. Terminal investment induced by immune challenge and fitness traits associated with major histocompatibility complex in the house sparrow. Evolution 58: 2823-2830.
3. Brommer, J.E., Wilson, A.J. & Gustafsson, L. 2007. Exploring the genetics of aging in a wild passerine bird. Am. Nat. 170: 643-650.
4. Clutton-Brock, T.H. & Pemberton, J.M. 2004. Individuals and populations. In: Soay Sheep: Dynamics and Selection in an Island Population (T.H. Clutton-Brock & J.M. Pemberton, eds), pp. 1-16. Cambridge University Press, Cambridge.
5. Clutton-Brock, T.H., Price, O.F., Albon, S.D. & Jewell, P.A. 1991. Persistent instability and population regulation in Soay sheep. J. Anim. Ecol. 60: 593-608.
6. Clutton-Brock, T.H., Price, O.F., Albon, S.D. & Jewell, P.A. 1992. Early development and population fluctuations in Soay sheep. J. Anim. Ecol. 61: 381-396.
7. Clutton-Brock, T.H., Stevenson, I.R., Marrow, P., Maccoll, A.D.C., Houston, A.I. & McNamara, J.M. 1996. Population fluctuations, reproductive costs and life-history tactics in female Soay sheep. J. Anim. Ecol. 65: 675-689.
8. Clutton-Brock, T.H., Pemberton, J.M., Coulson, T., Stevenson, I.R. & Maccoll, A.D.C. 2004. The sheep of St. Kilda. In: Soay Sheep: Dynamics and Selection in an Island Population (T.H. Clutton-Brock & J.M. Pemberton, eds), pp. 17-51. Cambridge University Press, Cambridge.
9. Cockburn, A., Osmond, H.L. & Double, M.C. 2008. Swingin' in the rain: condition dependence and sexual selection in a capricious world. Proc. R. Soc. Lond. B Biol. Sci. 275: 605-612.
10. Colditz, I.G. 2008. Six costs of immunity to gastrointestinal nematode infections. Parasit. Immunol. 30: 63-70.
11. Coltman, D.W., Smith, J.A., Bancroft, D.R., Pilkington, J., Maccoll, A.D.C., Clutton-Brock, T.H. et al. 1999. Density-dependent variation in lifetime breeding success and natural and sexual selection in Soay rams. Am. Nat. 154: 730-746.
12. Coltman, D.W., Pilkington, J.G., Kruuk, L.E.B., Wilson, K. & Pemberton, J.M. 2001a. Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution 55: 2116-2125.
13. Coltman, D.W., Wilson, K., Pilkington, J.G., Stear, M.J. & Pemberton, J.M. 2001b. 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.
14. Coulson, T., Catchpole, E.A., Albon, S.D., Morgan, B.J.T., Pemberton, J.M., Clutton-Brock, T.H. et al. 2001. Age, sex, density, winter weather, and population crashes in Soay sheep. Science 292: 1528-1531.
15. Coulson, T., Benton, T.G., Lundberg, P., Dall, S.R.X., Kendall, B.E. & Gaillard, J.M. 2006. Estimating individual contributions to population growth: evolutionary fitness in ecological time. Proc. R. Soc. Lond. B Biol. Sci. 273: 547-555.
16. Cox, F.E.G. 2001. Concomitant infections, parasites and immune response. Parasitology 122: S23-S38.
17. Craig, B.H., Pilkington, J.G. & Pemberton, J.M. 2006. Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology 133: 485-496.
18. Craig, B.H., Tempest, L.J., Pilkington, J.G. & Pemberton, J.M. 2008. Metazoan-protozoan parasite co-infections and host body weight in St Kilda Soay sheep. Parasitology 135: 433-441.
19. Craig, B.H., Jones, O.R., Pilkington, J.G. & Pemberton, J.M. 2009. Re-establishment of nematode infra-community and host survivorship in wild Soay sheep following anthelmintic treatment. Vet. Parasitol. 161: 47-52.
20. Devevey, G. & Christe, P. 2009. Flea infestation reduces the life span of the common vole. Parasitology 136: 1351-1355.
21. Engen, S., Lande, R., Saether, B.-E. & Dobson, F.S. 2009. Reproductive value and the stochastic demography of age-structured populations. Am. Nat. 174: 795-804.
22. Gatongi, P.M., Scott, M.E., Ranjan, S., Gathuma, J.M., Munyua, W.K., Cheruiyot, H. et al. 1997. Effects of three nematode anthelmintic treatment regimes on flock performance of sheep and goats under extensive management in semi-arid Kenya. Vet. Parasitol. 68: 323-336.
23. Graham, A.L., Hayward, A.D., Watt, K.A., Pilkington, J.G., Pemberton, J.M. & Nussey, D.H. 2010. Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330: 662-665.
24. Grenfell, B.T., Wilson, K., Isham, V.S., Boyd, H.E.G. & Dietz, K. 1995. Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode-ruminant interactions as a case study. Parasitology 111: S135-S151.
25. Gruner, L., Bouix, J. & Brunel, J.C. 2004. High genetic correlation between resistance to Haemonchus contortus and to Trichostrongylus colubriformis in INRA 401 sheep. Vet. Parasitol. 119: 51-58.
26. Gulland, F.M.D. 1991. The role of parasites in the population dynamics of Soay sheep on St. Kilda. PhD thesis, University of Cambridge.
27. Gulland, F.M.D. 1992. The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology 105: 493-503.
28. Gulland, F.M.D., Albon, S.D., Pemberton, J.M., Moorcroft, P.R. & Clutton-Brock, T.H. 1993. Parasite-associated polymorphism in a cyclic ungulate population. Proc. R. Soc. Lond. B Biol. Sci. 254: 7-13.
29. Gustafsson, L. 1987. Interspecific competition lowers fitness in collared flycatchers Ficedula albicollis: an experimental demonstration. Ecology 68: 291-296.
30. Gustafsson, L., Nordling, D., Andersson, M.S., Sheldon, B.C. & Qvarnstrom, A. 1994. Infectious diseases, reproductive effort, and the cost of reproduction in birds. Philos. Trans. R. Soc. Lond. B Biol. Sci. 346: 323-331.
31. Hadfield, J.D., Richardson, D.S. & Burke, T. 2006. Towards unbiased parentage assignment: combining genetic, behavioural and spatial data in a Bayesian framework. Mol. Ecol. 15: 3715-3730.
32. Hayward, A.D., Wilson, A.J., Pilkington, J.G., Pemberton, J.M. & Kruuk, L.E.B. 2009. Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proc. R. Soc. Lond. B Biol. Sci. 276: 3477-3485.
33. Hughes, J., Albon, S.D., Irvine, R.J. & Woodin, S. 2009. Is there a cost of parasites to caribou? Parasitology 136: 253-265.
34. Hutchings, M.R., Milner, J.M., Gordon, I.J., Kyriazakis, I. & Jackson, F. 2002. Grazing decisions of Soay sheep, Ovis aries, on St Kilda: a consequence of parasite distribution? Oikos 96: 235-244.
35. Jones, O.R., Crawley, M.J., Pilkington, J.G. & Pemberton, J.M. 2005. Predictors of early survival in Soay sheep: cohort-, maternal-, and individual-level variation. Proc. R. Soc. Lond. B Biol. Sci. 272: 2619-2625.
36. Jones, O.R., Gaillard, J.-M., Tujalpurkar, S., Alho, J.S., Armitage, K.B., Becker, P.H. et al. 2008. Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecol. Lett. 11: 664-673.
37. Kingsolver, J.G., Hoekstra, H.E., Hoekstra, J.M., Berrigan, D., Vignieri, S.N., Hill, C. et al. 2001. The strength of phenotypic selection in natural populations. Am. Nat. 157: 245-261.
38. Knowles, S.C.L., Palinauskas, V. & Sheldon, B.C. 2010. Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. J. Evol. Biol. 23: 557-569.
39. Lande, R. 1982. A quantitative genetic theory of life history evolution. Ecology 63: 607-615.
40. Lande, R. & Arnold, S.J. 1983. The measurement of selection on correlated characters. Evolution 37: 1210-1226.
41. M.A.F.F. 1986. Manual of Veterinary Parasitological Laboratory Techniques, 3rd edn. H.M.S.O., London.
42. Mills, S.C., Grapputo, A., Jokinen, I., Koskela, E., Mappes, T. & Poikonen, T. 2010. Fitness trade-offs mediated by immunosuppression costs in a small mammal. Evolution 64: 166-179.
43. Milner, J.M., Albon, S.D., Illius, A.W., Pemberton, J.M. & Clutton-Brock, T.H. 1999. Repeated selection of morphometric traits in the Soay sheep on St Kilda. J. Anim. Ecol. 68: 472-488.
44. Mitchell-Olds, T. & Shaw, R.G. 1987. Regression analysis of natural selection: statistical inference and biological interpretation. Evolution 41: 1149-1161.
45. van Oosterhout, C., Mohammed, R.S., Hansen, H., Archard, G.A., McMullan, M., Weese, D.J. et al. 2007. Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). Int. J. Parasitol. 37: 805-812.
46. Parejo, D. & Silva, N. 2009. Immunity and fitness in a wild population of Eurasian kestrels Falco tinnunculus. Naturwissenschaften 96: 1193-1202.
47. Paterson, S., Wilson, K. & Pemberton, J.M. 1998. Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proc. Natl Acad. Sci. USA 95: 3714-3719.
48. Pelletier, F., Clutton-Brock, T.H., Pemberton, J.M., Tuljapurkar, S. & Coulson, T. 2007. The evolutionary demography of ecological change: linking trait variation and population growth. Science 315: 1571-1574.
49. Pemberton, J.M., Coltman, D.W., Smith, J.A. & Pilkington, J.G. 1999. Molecular analysis of a promiscuous, fluctuating mating system. Biol. J. Linn. Soc. 68: 289-301.
50. Phillips, P.C. & Arnold, S.J. 1989. Visualizing multivariate selection. Evolution 43: 1209-1222.
51. Poulin, R. 2007. The Evolutionary Ecology of Parasites, 2nd edn. Princeton University Press, Princeton, NJ.
52. Price, T. & Schluter, D. 1991. On the low heritability of life-history traits. Evolution 45: 853-861.
53. Price, T.D., Grant, P.R., Gibbs, H.L. & Boag, P.T. 1984. Recurrent patterns of natural selection in a population of Darwin's finches. Nature 309: 787-789.
54. Raberg, L. & Stjernman, M. 2003. Natural selection on immune responsiveness in blue tits Parus caeruleus. Evolution 57: 1670-1678.
55. Rausher, M.D. 1992. The measurement of selection on quantitative traits: biases due to environmental covariances between traits and fitness. Evolution 46: 616-626.
56. Robinson, M.R., Pilkington, J.G., Clutton-Brock, T.H., Pemberton, J.M. & Kruuk, L.E.B. 2006. Live fast, die young: trade-offs between fitness components and sexually antagonistic selection on weaponry in Soay sheep. Evolution 60: 2168-2181.
57. Robinson, M.R., Pilkington, J.G., Clutton-Brock, T.H., Pemberton, J.M. & Kruuk, L.E.B. 2008. Environmental heterogeneity generates fluctuating selection on a secondary sexual trait. Curr. Biol. 18: 751-757.
58. Robinson, M.R., Wilson, A.J., Pilkington, J.G., Clutton-Brock, T.H., Pemberton, J.M. & Kruuk, L.E.B. 2009. The impact of environmental heterogeneity on genetic architecture in a wild population of Soay sheep. Genetics 181: 1639-1648.
59. Rowe, L. & Houle, D. 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. Lond. B Biol. Sci. 263: 1415-1421.
60. Sayers, G. & Sweeney, T. 2005. Gastrointestinal nematode infection in sheep? A review of the alternatives to anthelmintics in parasite control. Anim. Health Res. Rev. 6: 159-171.
61. Smith, W.D., Jackson, F., Jackson, E. & Williams, J. 1985. Age immunity to Ostertagia circumcincta: comparison of the local immune responses of 4 1/2- and 10-month-old lambs. J. Comp. Pathol. 95: 235-245.
62. Stear, M.J., Bishop, S.C., Doligalska, M., Duncan, J.L., Holmes, P.H., Irvine, J. et al. 1995. Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunol. 17: 643-652.
63. Stear, M.J., Bairden, K., Duncan, J.L., Holmes, P.H., McKellar, Q.A., Park, M. et al. 1997. How hosts control worms. Nature 389: 27.
64. Stear, M.J., Boag, B., Cattadori, I. & Murphy, L. 2009. Genetic variation in resistance to mixed, predominantly Teladorsagia circumcincta nematode infections of sheep: from heritabilities to gene identification. Parasite Immunol. 31: 274-282.
65. Stjernman, M., Raberg, L. & Nilsson, J.-A. 2008. Maximum host survival at intermediate parasite infection intensities. PLoS ONE 3: e2463.
66. Tempest, L.J. 2005. Parasites and the cost of reproduction in Soay sheep. PhD thesis, University of Stirling.
67. Thomson, E.F., Gruner, L., Bahhady, F., Orita, G., Termanini, A., Ferdawi, A.K. et al. 2000. Effects of gastro-intestinal and lungworm nematode infections on ewe productivity in farm flocks under variable rainfall conditions in Syria. Livest. Prod. Sci. 63: 65-75.
68. Velando, A., Drummond, H. & Torres, R. 2006. Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis. Proc. R. Soc. Lond. B Biol. Sci. 273: 1443-1448.
69. Verhulst, S. 1998. Multiple breeding in the great tit, II. The costs of rearing a second clutch. Funct. Ecol. 12: 132-140.
70. Viney, M.E., Riley, E.M. & Buchanan, K.L. 2005. Optimal immune responses: immunocompetence revisited. Trends Ecol. Evol. 20: 665-669.
71. Waller, P.J. & Thomas, R.J. 1981. The natural regulation of Trichostrongylus spp. populations in young grazing sheep. Vet. Parasitol. 9: 47-55.
72. Wilson, K., Grenfell, B.T., Pilkington, J.G., Boyd, H.E.G. & Gulland, F.M.D. 2004. Parasites and their impact. In: Soay Sheep: Dynamics and Selection in an Island Population (T.H. Clutton-Brock & J.M. Pemberton, eds), pp. 17-51. Cambridge University Press, Cambridge.
73. Wilson, A.J., Pemberton, J.M., Pilkington, J.G., Coltman, D.W., Mifsud, D.V., Clutton-Brock, T.H. et al. 2006. Environmental coupling of selection and heritability limits evolution. PLoS Biol. 4: 1270-1275.
74. Wilson, A.J., Pemberton, J.M., Pilkington, J.G., Clutton-Brock, T.H. & Kruuk, L.E.B. 2009. Trading offspring size for number in a variable environment: selection on reproductive investment in female Soay sheep. J. Anim. Ecol. 78: 354-364.
75. Woolaston, R.R. 1992. Selection of Merino sheep for increased and decreased resistance to Haemonchus contortus- peri-parturient effects on fecal egg counts. Int. J. Parasitol. 22: 947-953.