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Maternal effects and early-life performance are associated with parasite resistance across life in free-living Soay sheep

Published online by Cambridge University Press:  17 March 2010

A. D. HAYWARD ,
J. G. PILKINGTON ,
J. M. PEMBERTON  and
L. E. B. KRUUK
A. D. HAYWARD*
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland
J. G. PILKINGTON
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland
J. M. PEMBERTON
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland
L. E. B. KRUUK
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland
*
*Corresponding author: Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland. Tel: +44 (0) 131 650 5440. Fax: +44 (0) 131 650 6564. E-mail: adam.hayward@ed.ac.uk
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Summary

Maternal effects occur when the maternal phenotype influences that of the offspring in addition to the effects of maternal genes, and may have a considerable influence on offspring parasite resistance. These effects, and the effects of early levels of reproduction and parasite resistance, may persist into later life and even influence ageing rates. Here we analyse a 20-year longitudinal data set collected on a free-living population of Soay sheep, to investigate the associations between a suite of maternal phenotypic traits and early-life performance on measures of parasite resistance across life. Our results show that maternal effects are important in determining offspring parasite resistance, since lambs born as twins and those born to the youngest and oldest mothers show higher parasite burdens. We show that the association between parasite resistance and natal litter size persists into adulthood. We also show that age-specific changes in parasite resistance in males are associated with natal litter size, and that age-specific changes in females are influenced by early-life levels of reproduction and parasite infection. These results add to the growing evidence that conditions experienced by individuals during development can have a profound influence on immediate and late-life performance and may even influence ageing.

Keywords

maternal effectsSoay sheepparasite resistancestrongylesfaecal egg countsearly-life performance
Type
Research Article
Information
Parasitology , Volume 137 , Issue 8 , July 2010 , pp. 1261 - 1273
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Bishop, S. C., Birden, 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, 423–428.CrossRefGoogle Scholar
Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H. and White, J. S. (2009). Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24, 127–135. doi:10.1016/j.tree.2008.10.008.CrossRefGoogle ScholarPubMed
Carlier, Y. and Truyens, C. (1995) Influences of maternal infection on offspring resistance towards parasites. Parasitology Today 11, 94–99.CrossRefGoogle ScholarPubMed
Christley, R. M., Morgan, K. L., Parkin, T. D. H. and French, N. P. (2003). Factors related to the risk of neonatal mortality, birth-weight and serum immunoglobulin concentration in lambs in the UK. Preventive Veterinary Medicine 57, 209–226. doi:10.1016/S0167-5877(02)00235-0.CrossRefGoogle Scholar
Clutton-Brock, T. H. (2004). The causes and consequences of instability. In Soay Sheep (ed. Clutton-Brock, T. H. and Pemberton, J. M.), pp. 276–310. Cambridge University Press, Cambridge, UK.Google Scholar
Clutton-Brock, T. H., Grenfell, B. T., Coulson, T., MacColl, A. D. C., Illius, A. W., Coltman, D. W., Pilkington, J. G., Smith, J. G. and Pemberton, J. M. (1999). Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53, 1259–1267.Google Scholar
Clutton-Brock, T. H. and Pemberton, J. M. (2004). Individuals and Populations. In Soay Sheep (ed. Clutton-Brock, T. H. and Pemberton, J. M.), pp. 1–16. Cambridge University Press, Cambridge, UK.Google Scholar
Clutton-Brock, T. H., Price, O. F., Albon, S. D. and Jewell, P. A. (1992). Early development and population fluctuations in Soay sheep. Journal of Animal Ecology 61, 381–396.CrossRefGoogle Scholar
Clutton-Brock, T. H., Stevenson, I. R., Marrow, P., MacColl, A. D. C., Houston, A. I. and McNamara, J. M. (1996). Population fluctuations, reproductive costs and life-history tactics in female Soay sheep. Journal of Animal Ecology 65, 675–689.CrossRefGoogle Scholar
Coltman, D. W., Pilkington, J. G., Kruuk, L. E. B., Wilson, K. and Pemberton, J. M. (2001 a). Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution 55, 2116–2125. doi: 10.1554/0014-3820(2001)055[2116:PGCBPR]2.0.CO;2.Google Scholar
Coltman, D. W., Pilkington, J. G., Smith, J. A. and Pemberton, J. M. (1999). Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53, 1259–1267.Google Scholar
Coltman, D. W., Wilson, K., Pilkington, J. G., Stear, M. J. and Pemberton, J. M. (2001 b). 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. doi: 10.1017/S0031182001007570.Google Scholar
Coulson, T., Albon, S., Pilkington, J. G. and Clutton-Brock, T. H. (1999). Small-scale spatial dynamics in a fluctuating ungulate population. Journal of Animal Ecology 68, 658–671. doi: 10.1046/j.1365-2656.1999.00298.x.CrossRefGoogle Scholar
Craig, B. H., Jones, O. R., Pilkington, J. G. and Pemberton, J. M. (2009). Re-establishment of nematode infra-community and host survivorship in wild Soay sheep following anthelmintic treatment. Veterinary Parasitology 161, 47–52. doi: 10.1016/j.vetpar.2008.11.027.CrossRefGoogle ScholarPubMed
Craig, B. H., Pilkington, J. G. and Pemberton, J. M. (2006). Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology 133, 485–496. doi: 10.1017/S0031182006000618.CrossRefGoogle Scholar
Craig, B. H., Tempest, L. J., Pilkington, J. G. and Pemberton, J. M. (2008). Metazoan-protozoan parasite co-infections and host body weight in St Kilda Soay sheep. Parasitology 135, 433–441. doi: 10.1017/S0031182008004137.CrossRefGoogle ScholarPubMed
Dwyer, C. M. and Morgan, C. A. (2006). Maintenance of body temperature in the neonatal lamb: Effects of breed, birth weight, and litter size. Journal of Animal Science 84, 1093–1101.Google Scholar
Gabriël, S., Geldhof, P., Phiri, I. K., Cornillie, P., Goddeeris, B. M. and Vercruysse, J. (2005). Placental transfer of immunoglobulins in cattle infected with Schistosoma mattheei. Veterinary Immunology and Immunopathology 104, 265–272. doi:10.1016/j.vetimm.2004.12.010.CrossRefGoogle ScholarPubMed
Grindstaff, J. L., Brodie, E. D. III and Ketterson, E. D. (2003). Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proceedings of the Royal Society of London, B 270, 2309–2319. doi: 10.1098/rspb.2003.2485.CrossRefGoogle ScholarPubMed
Gruver, A. L., Hudson, L. L. and Sempowski, G. D. (2007). Immunosenescence of ageing. Journal of Pathology 211, 144–156. doi: 10.1002/path.2104.CrossRefGoogle ScholarPubMed
Gulland, F. M. D. (1992) The role of nematode parasites in Soay sheep (Ovies aries L.) mortality during a population crash. Parasitology 105, 493–503.Google Scholar
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. Proceedings of the Royal Society of London, B 276, 3477–3485. doi: 10.1098/rspb.2009.0906.Google Scholar
Henderson, N. G. and Stear, M. J. (2006). Eosinophil and IgA responses in sheeo infected with Teladorsagia circumcincta. Veterinary Immunology and Immunopathology 112, 62–66. doi:10.1016/j.vetimm.2006.03.012.CrossRefGoogle Scholar
Iposu, S. O., McAnulty, R. W., Greer, A. W., Xie, H. L., Green, R. S., Stankiewicz, M. and Sykes, A. R. (2008). Does suckling offer protection to the lamb against Teladorsagia circumcincta infection? Veterinary Parasitology 153, 294–301. doi:10.1016/j.vetpar.2008.01.034.CrossRefGoogle Scholar
Jones, O. R., Crawley, M. J., Pilkington, J. G. and Pemberton, J. M. (2005). Predictors of early survival in Soay sheep: cohort-, maternal-, and individual-level variation. Proceedings of the Royal Society of London, B 272, 2619–2625. 10.1098/rspb.2005.3267.Google ScholarPubMed
Lindstrom, J. (1999). Early development and fitness in birds and mammals. Trends in Ecology and Evolution 14, 343–348. doi: 10.1016/S0169-5347(99)01639-0.CrossRefGoogle ScholarPubMed
Lindstrom, J., Coulson, T., Kruuk, L., Forchhammer, M. C., Coltman, D. W. and Clutton-Brock, T. H. (2002). Sex-ratio variation in Soay sheep. Behavioural Ecology and Sociobiology 53, 25–30. doi: 10.1007/s00265-002-0545-4.Google Scholar
Lochmillar, R. L. and Deerenberg, C. (2000). Tradeoffs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98. doi: 10.1034/j.1600-0706.2000.880110.x.CrossRefGoogle Scholar
Marshall, D. J. and Uller, T. (2007). When is a maternal effect adaptive? Oikos 116, 1957–1963. doi: 10.1111/j.2007.0030-1299.16203.x.CrossRefGoogle Scholar
Nowak, R. and Poindron, P. (2006). From birth to colostrum: early steps leading to lamb survival. Reproduction Nutrition Development 46, 431–446. doi: 10.1051/rnd:2006023.CrossRefGoogle ScholarPubMed
Nussey, D. H., Coulson, T., Festa-Bianchet, M. and Gaillard, J.-M. (2008). Measuring senescence in wild animal populations: towards a longitudinal approach. Functional Ecology 22, 393–406. doi: 10.1111/j.1365-2435.2008.01408.x.CrossRefGoogle Scholar
Nussey, D. H., Kruuk, L. E. B., Donald, A., Fowlie, M. and Clutton-Brock, T. H. (2006). The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecology Letters 9, 1342–1350. doi: 10.1111/j.1461-0248.2006.00989.x.CrossRefGoogle ScholarPubMed
Nussey, D. H., Kruuk, L. E. B., Morris, A. and Clutton-Brock, T. H. (2007). Environmental conditions in early life influence ageing rates in a wild population of red deer. Current Biology 17, r1000–r1001. doi: 10.1016/j.cub.2007.10.005.Google Scholar
Pfeffer, A., Shaw, R. J., Green, R. S. and Phegan, M. D. (2005). The transfer of maternal IgE and other immunoglobulins specific for Trichostrongylus colubriformis larval excretory/secretory product to the neonatal lamb. Veterinary Immunology and Immunopathology 108, 315–323. doi:10.1016/j.vetimm.2005.06.004.CrossRefGoogle Scholar
Pinheiro, J. C. and Bates, D. M. (2000). Mixed-effects Models in S and S-PLUS. Springer, New York, USA.CrossRefGoogle Scholar
Rasanen, K. and Kruuk, L. E. B. (2007). Maternal effects and evolution at ecological time-scales. Functional Ecology 21, 408–421. doi: 10.1111/j.1365-2435.2007.01246.x.CrossRefGoogle Scholar
Reid, J. M., Arcese, P., Keller, L. F. and Hasselquist, D. (2006). Long-term maternal effect on offspring immune response in song sparrows Melospiza melodia. Biology Letters 2, 573–576. doi: 10.1098/rsbl.2006.0544.Google Scholar
Robinson, M. R., Wilson, A. J., Pilkington, J. G., Clutton-Brock, T. H., Pemberton, J. M. and Kruuk, L. E. B. (2009). The impact of environmental heterogeneity on genetic architecture in a wild population of Soay sheep. Genetics 181, 1639–1648. doi: 10.1534/genetics.108.086801.CrossRefGoogle Scholar
Schall, R. (1991). Estimation in generalized linear models with random effects. Biometrika 78, 719–727. doi: 10.1093/biomet/78.4.719.CrossRefGoogle Scholar
Stear, M. J., Bishop, S. C., Henderson, N. G. and Scott, I. (2003). A key mechanism of pathogenesis in sheep infected with the nematode Teladorsagia circumcincta. Animal Health Research Reviews 4, 45–52. doi: 10.1079/AHRR200351.CrossRefGoogle ScholarPubMed
Stear, M. J., Boag, B., Cattadori, I. and Murphy, L. (2009). Genetic variation in resistance to mixed, predominantly Teladorsagia circumcincta nematode infections of sheep: from heritabilities to gene identification. Parasite Immunology 31, 274–282. doi: 10.1111/j.1365-3024.2009.01105.x.Google Scholar
Stevenson, I. R., Marrow, P., Preston, B. T., Pemberton, J. M. and Wilson, K. (2004). Adaptive reproductive strategies. In Soay Sheep (ed. Clutton-Brock, T. H. and Pemberton, J. M.), pp. 243–275. Cambridge University Press, Cambridge, UK.Google Scholar
Tavecchia, G., Coulson, T., Morgan, B. J. T., Pemberton, J. M., Pilkington, J. G., Gulland, F. M. D. and Clutton-Brock, T. H. (2005). Predictors of reproductive cost in female Soay sheep. Journal of Animal Ecology 74, 201–213. doi: 10.1111/j.1365-2656.2005.00916.x.CrossRefGoogle Scholar
Theodorou, G., Fragou, S., Chronopoulou, R., Kominakis, A., Rogdakis, E. and Politis, I. (2007). Study of immune parameters in three Greek dairy sheep breeds during the periparturient period. Journal of Dairy Science 90, 5567–5571. doi: 10.3168/jds.2007-0247.Google Scholar
Wilson, A. J., Kruuk, L. E. B. and Coltman, D. W. (2005 b). Ontogenetic patterns in heritable variation for body size: using random regression models in a wild ungulate population. American Naturalist 166, E177–E192. doi: 10.1086/497441.CrossRefGoogle Scholar
Wilson, A. J., Pilkington, J. G., Pemberton, J. M., Coltman, D. W., Overall, A. D. J., Byrne, K. A. and Kruuk, L. E. B. (2005 a). Selection on mothers and offspring: whose phenotype is it and does it matter? Evolution 59, 451–463. doi: 10.1554/04-480.Google ScholarPubMed
Wilson, K., Grenfell, B. T., Pilkington, J. G., Boyd, H. E. G. and Gulland, F. M. D. (2004). Parasites and their impact. In Soay Sheep (ed. Clutton-Brock, T. H. and Pemberton, J. M.), pp. 113–165. Cambridge University Press, Cambridge, UK.Google Scholar