Evolutionary Ecology

, 21:337 | Cite as

Quantitative genetics of growth and cryptic evolution of body size in an island population

  • A. J. WilsonEmail author
  • J. M. Pemberton
  • J. G. Pilkington
  • T. H. Clutton-Brock
  • D. W. Coltman
  • L. E. B. Kruuk
Original Paper


While evolution occurs when selection acts on a heritable trait, empirical studies of natural systems have frequently reported phenotypic stasis under these conditions. We performed quantitative genetic analyses of weight and hindleg length in a free-living population of Soay sheep (Ovis aries) to test whether genetic constraints can explain previously reported stasis in body size despite evidence for strong positive directional selection. Genetic, maternal and environmental covariance structures were estimated across ontogeny using random regression animal models. Heritability increased with age for weight and hindleg length, though both measures of size were highly heritable across ontogeny. Genetic correlations among ages were generally strong and uniformly positive, and the covariance structures were also highly integrated across ontogeny. Consequently, we found no constraint to the evolution of larger size itself. Rather we expect size at all ages to increase in response to positive selection acting at any age. Consistent with expectation, predicted breeding values for age-specific size traits have increased over a twenty-year period, while maternal performance for offspring size has declined. Re-examination of the phenotypic data confirmed that sheep are not getting larger, but also showed that there are significant negative trends in size at all ages. The genetic evolution is therefore cryptic, with the response to selection presumably being masked at the phenotypic level by a plastic response to changing environmental conditions. Density-dependence, coupled with systematically increasing population size, may contribute to declining body size but is insufficient to completely explain it. Our results demonstrate that an increased understanding of the genetic basis of quantitative traits, and of how plasticity and microevolution can occur simultaneously, is necessary for developing predictive models of phenotypic change in nature.


heritability Ovis aries ontogeny cryptic evolytion growth 



We thank the National Trust for Scotland and Scottish Natural Heritage for permission to work on St. Kilda, the Royal Artillery Range (Hebrides) and QinetiQ and Eurest for logistic support. The long-term data collection on St. Kilda has been supported by the Natural Environment Research Council, the Wellcome Trust, the Biotechnology and Biological Sciences Research Council and the Royal Society, through grants to THCB, B.T. Grenfell, M.J. Crawley, T. Coulson, S. Albon, JMP and LEBK. The work described here was funded by a Leverhulme Trust research project grant to LEBK and D.W. Coltman. LEBK is supported by the Royal Society. We also thank the many previous members of the project (including many volunteers) who have collected field data or have contributed genotyping and paternity inference. T. Coulson and two anonymous referees provided useful comments on a previous version of this manuscript.


  1. Arnold SJ (1992) Constraints on phenotypic evolution. Am Nat 140:S85–S107CrossRefPubMedGoogle Scholar
  2. Badyaev AV, Martin TE (2000) Individual variation in growth trajectories: phenotypic and genetic correlations in ontogeny of the house finch (Carpodacus mexicanus). J Evol Biol 13:290–301CrossRefGoogle Scholar
  3. Björklund M (1997) Variation in growth in the blue tit (Parus caeruleus). J Evol Biol 10:139–155CrossRefGoogle Scholar
  4. Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407PubMedCrossRefGoogle Scholar
  5. Blows MW, Hoffman AA (2005) A reassessment of genetic limits to evolutionary change. Ecology 86:1371–1384Google Scholar
  6. Charmantier A, Garant D (2005) Environmental quality and evolutionary potential: lessons from wild populations. Proc R Soc Lond B Bio 272:1415–1425CrossRefGoogle Scholar
  7. Cheverud JM, Leamy LJ, Atchley WR, Rutledge JJ (1983a) Quantitative genetics and the evolution of ontogeny. I. Ontogenetic changes in quantitative genetic variance components in randombred mice. Genet Res 42:65–75CrossRefGoogle Scholar
  8. Cheverud JM, Rutledge JJ, Atchley WR (1983b) Quantitative genetics of development—genetic correlations among age-specific trait values and the evolution of ontogeny. Evolution 37:895–905CrossRefGoogle Scholar
  9. Clutton-Brock TH, Price OF, Albon SD, Jewell PA (1992) Early development and population fluctuations in Soay sheep. J Anim Ecol 61:381–396CrossRefGoogle Scholar
  10. Clutton-Brock TH, Pemberton JM (2004) Soay sheep: Dynamics and selection in an island population. Cambridge University Press, Cambridge, 383ppGoogle Scholar
  11. Coltman DW, Smith JA, Bancroft DR, Pilkington J, MacColl ADC, Clutton-Brock TH, Pemberton JM (1999) Density-dependent variation in lifetime breeding success and natural and sexual selection in Soay rams. Am Nat 154:730–746PubMedCrossRefGoogle Scholar
  12. Coltman DW, Pilkington J, Kruuk LE, Wilson K, Pemberton JM (2001) Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution 55:2116–2125PubMedGoogle Scholar
  13. Coltman DW, O’Donoghue P, Hogg JT, Festa-Bianchet M (2005) Selection and genetic (co)variance in bighorn sheep. Evolution 59:1372–1382PubMedGoogle Scholar
  14. Coulson T, Catchpole EA, Albon SD, Morgan BJT, Pemberton JM, Clutton-Brock TH, Crawley MJ, Grenfell BT (2001) Age, sex, density, winter weather, and population crashes in Soay sheep. Science 292:1528–1531PubMedCrossRefGoogle Scholar
  15. Coulson T, Benton TG, Lundberg P, Dall SRX, Kendall BE, Gaillard J-M (2006) Estimating individual contributions to population growth: evolutionary fitness in ecological time. Proc R Soc Lond B Bio 273:547–556Google Scholar
  16. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman, EssexGoogle Scholar
  17. Fischer TM, Gilmour AR, Van der Werf JHJ (2004) Computing approximate standard errors for genetic parameters derived from random regression models fitted by average information REML. Gen Sel Evol 36:363–369CrossRefGoogle Scholar
  18. Foster J (1964) The evolution of mammals on islands. Nature 202:234–235CrossRefGoogle Scholar
  19. Gaillard JM, Festa-Bianchet M, Delorme D, Jorgenson J (2000) Body mass and individual fitness in female ungulates: bigger is not always better. Proc R Soc Lond Ser B-Biol Sci 267:471–477CrossRefGoogle Scholar
  20. Garant D, Kruuk LEB, McCleery RH, Sheldon BC (2004) Evolution in a changing environment: a case study with great tit fledging mass. Am Nat 164:E115–E129PubMedCrossRefGoogle Scholar
  21. Guinness FE, Clutton-Brock TH, Albon SD (1978) Factors affecting calf mortality in red deer (Cervus elaphus). J Anim Ecol 47:817–832CrossRefGoogle Scholar
  22. Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204PubMedGoogle Scholar
  23. Kirkpatrick M, Lofsvold D, Bulmer M (1990) Analysis of the inheritance, selection and evolution of growth trajectories. Genetics 124:979–993PubMedGoogle Scholar
  24. Kirkpatrick M, Lofsvold D (1992) Measuring selection and constraint in the evolution of growth. Evolution 46:954–971CrossRefGoogle Scholar
  25. Kruuk LEB, Merilä J, Sheldon BC (2001) Phenotypic selection on a heritable size trait revisited. Am Nat 158:557–571CrossRefPubMedGoogle Scholar
  26. Kruuk LEB, Slate J, Pemberton JM, Brotherstone S, Guinness F, Clutton-Brock T (2002) Antler size in red deer: heritability and selection but no evolution. Evolution 56:1683–1695PubMedGoogle Scholar
  27. Kruuk LEB (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Philos T Roy Soc B 359:873–890CrossRefGoogle Scholar
  28. Lomolino M (2005) Body size evolution in insular vertebrates: generality of the island rule. J Biogeogr 32:1683–1699CrossRefGoogle Scholar
  29. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Inc., SunderlandGoogle Scholar
  30. Marshall TC, Slate J, Kruuk LE, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  31. Merilä J, Kruuk LEB, Sheldon BC (2001a) Cryptic evolution in a wild bird population. Nature 412:76–79CrossRefGoogle Scholar
  32. Merilä J, Sheldon BC, Kruuk LEB (2001b) Explaining stasis: microevolutionary studies in natural populations. Genetica 112–113:199–222CrossRefGoogle Scholar
  33. Meyer K (1992) Variance components due to direct and maternal effects for growth traits of Australian beef cattle. Livest Prod Sci 31:179–204CrossRefGoogle Scholar
  34. Meyer K (1998) Estimating covariance functions for longitudinal data using a random regression model. Gen Sel Evol 30:221–240Google Scholar
  35. Milner JM, Albon SD, Illius AW, Pemberton JM, Clutton-Brock TH (1999) Repeated selection of morphometric traits in the Soay sheep on St Kilda. J Anim Ecol 68:472–488CrossRefGoogle Scholar
  36. Milner JM, Pemberton JM, Brotherstone S, Albon SD (2000) Estimating variance components and heritabilities in the wild: a case study using the ‘animal model’ approach. J Evol Biol 13:804–813CrossRefGoogle Scholar
  37. Nussey DH, Clutton-Brock TH, Albon SD, Pemberton JM, Kruuk LEB (2005a) Constraints on plastic responses to climate variation in red deer. Biol Lett 1:457–460CrossRefGoogle Scholar
  38. Nussey DH, Clutton-Brock TH, Elston DA, Albon SD, Kruuk LEB (2005b) Phenotypic plasticity in a maternal trait in red deer. J Anim Ecol 74:387–396CrossRefGoogle Scholar
  39. Nussey DH, Postma E, Gienapp P, Visser ME (2005c) Selection on heritable phenotypic plasticity in a wild bird population. Science 310:304–306CrossRefGoogle Scholar
  40. Overall ADJ, Byrne KA, Pilkington J, Pemberton JM (2005) Heterozygosity, inbreeding and neonatal traits in Soay sheep on St Kilda. Mol Ecol 14:3383–3393PubMedCrossRefGoogle Scholar
  41. Pakkasmaa S, Merilä J, O’Hara RB (2003) Genetic and maternal effect influences on viability of common frog tadpoles under different environmental conditions. Heredity 91:117–124PubMedCrossRefGoogle Scholar
  42. Pease CM, Bull JJ (1988) A critique of methods for measuring life history trade-offs. J Evol Biol 1:293–303CrossRefGoogle Scholar
  43. Postma E (2006) Implications of the difference between true and predicted breeding values for the study of natural selection and micro-evolution. J Evol Biol 19, Doi: 10.1111/j.1420–9101.2005.01007Google Scholar
  44. Ragland GJ, Carter PA (2004) Genetic covariance structure of growth in the salamander Ambystoma macrodactylum. Heredity 92:569–578PubMedCrossRefGoogle Scholar
  45. Réale D, Festa-Bianchet M, Jorgenson JT (1999) Heritability of body mass varies with age and season in wild bighorn sheep. Heredity 83:526–532PubMedCrossRefGoogle Scholar
  46. Réale D, McAdam AG, Boutin S, Berteaux D (2003) Genetic and plastic responses of a northern mammal to climate change. Pro R Soc Lond B 270:591–596CrossRefGoogle Scholar
  47. Schaeffer LR (2004) Application of random regression models in animal breeding. Livest Prod Sci 86:35–45CrossRefGoogle Scholar
  48. Sogard SM (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. B Mar Sci 60:1129–1157Google Scholar
  49. Willham RL (1972) The role of maternal effects in animal breeding: III. Biometrical aspects of maternal effects in animals. J Anim Sci 35:1288–1293PubMedGoogle Scholar
  50. Wilson AJ, Hutchings JA, Ferguson MM (2003) Selective and genetic constraints on the evolution of body size in a stream-dwelling salmonid fish. J Evol Biol 16:584–594PubMedCrossRefGoogle Scholar
  51. Wilson AJ, Coltman DW, Pemberton JM, Overall ADJ, Byrne KA, Kruuk LEB (2005a) Maternal genetic effects set the potential for evolution in a free-living vertebrate population. J Evol Biol 18:405–414CrossRefGoogle Scholar
  52. Wilson AJ, Kruuk LEB, Coltman DW (2005b) Ontogenetic patterns in heritable variation for body size: using random regression models in a wild ungulate population. Am Nat 166:E177–E192CrossRefGoogle Scholar
  53. Wilson AJ, Pilkington JG, Pemberton JM, Coltman DW, Overall ADJ, Byrne KA, Kruuk LEB (2005c) Selection on mothers and offspring: whose phenotype is it and does it matter? Evolution 59:451–463Google Scholar
  54. Wilson AJ, Pemberton JM, Pilkington JG, Coltman DW, Mifsud DV, Clutton-Brock TH, Kruuk LEB (2006) Environmental coupling of selection and heritability limits evolution. PLoS Biol 4(7):e216PubMedCrossRefGoogle Scholar
  55. Wilson AJ, Réale D (2006) Ontogeny of additive and maternal genetic effects: lessons from domestic mammals. Am Nat 167:E23–E38PubMedCrossRefGoogle Scholar
  56. Wolf JB, Brodie ED, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • A. J. Wilson
    • 1
    Email author
  • J. M. Pemberton
    • 1
  • J. G. Pilkington
    • 1
  • T. H. Clutton-Brock
    • 2
  • D. W. Coltman
    • 3
  • L. E. B. Kruuk
    • 1
  1. 1.Institute of Evolutionary BiologyUniversity of EdinburghEdinburghUK
  2. 2.Department of ZoologyUniversity of CambridgeCambridgeUK
  3. 3.Department of Biological SciencesUniversity of AlbertaEdmontonCanada

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