Heterogeneous selection on a heritable temperament trait in a variable environment

Journal of Animal Ecology

Volumn 78, Issue 6, 2009, Pages 1203-1215

  Quinn, John L ^a   Patrick, Samantha C ^a   Bouwhuis, Sandra ^b   Wilkin, Teddy A ^a   Sheldon, Ben C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Environmental heterogeneity; Heritability; Personality; Population density; Selection; Temperament

Indexed keywords

BREEDING SITE; ENVIRONMENTAL GRADIENT; EVOLUTIONARY BIOLOGY; FECUNDITY; GENETIC ANALYSIS; HABITAT QUALITY; HERITABILITY; HETEROGENEITY; INDIVIDUAL VARIATION; MAXIMUM LIKELIHOOD ANALYSIS; PASSERINE; POPULATION DENSITY; REPRODUCTIVE SUCCESS; SELECTION; SURVIVAL;

ANIMAL; ARTICLE; ECOSYSTEM; FEMALE; GENETIC SELECTION; GENETICS; MALE; PHENOTYPE; PHYSIOLOGY; POPULATION DYNAMICS; SEXUAL DEVELOPMENT; SONGBIRD; TEMPERAMENT;

ANIMALS; ECOSYSTEM; FEMALE; MALE; PHENOTYPE; POPULATION DYNAMICS; SELECTION, GENETIC; SEX CHARACTERISTICS; SONGBIRDS; TEMPERAMENT;

ANIMALIA; AVES; PARUS MAJOR; PASSERIFORMES;

EID: 70349920918     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2009.01585.x     Document Type: Article

References (104)

1. Anholt, B.R. Werner, E.E. (1995) Interaction between food availability and predation mortality mediated by adaptive-behavior. Ecology, 76, 2230 2234.
2. Anholt, B.R. Werner, E.E. (1998) Predictable changes in predation mortality as a consequence of changes in food availability and predation risk. Evolutionary Ecology, 12, 729 738.
3. Arnold, S.J. Wade, M.J. (1984a) On the measurement of natural and sexual selection: applications. Evolution, 38, 720 734.
4. Arnold, S.J. Wade, M.J. (1984b) On the measurement of natural and sexual selection: theory. Evolution, 38, 709 719.
5. Arnold, K.E., Ramsay, S.L., Donaldson, C. Adam, A. (2007) Parental prey selection affects risk-taking behaviour and spatial learning in avian offspring. Proceedings of the Royal Society of London. Series B: Biological Sciences, 274, 2563 2569.
6. Arnqvist, G. Henriksson, S. (1997) Sexual cannibalism in the fishing spider and a model for the evolution of sexual cannibalism based on genetic constraints. Evolutionary Ecology, 11, 255 273.
7. Bell, A.M. (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). Journal of Evolutionary Biology, 18, 464 473.
8. Bell, A.M. (2007) Future directions in behavioural syndromes research. Proceedings of the Royal Society of London. Series B: Biological Sciences, 274, 755 761.
9. Betts, M.M. (1955) Food of titmice in oak woodland. Journal of Animal Ecology, 24, 282 323.
10. Biro, P.A. Stamps, J.A. (2008) Are animal personality traits linked to life-history productivity? Trends in Ecology and Evolution, 23, 361 368.
11. Biro, P.A., Abrahams, M.V., Post, J.R. Parkinson, E.A. (2006) Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates. Journal of Animal Ecology, 75, 1165 1171.
12. Biro, P.A., Abrahams, M.V. Post, J.R. (2007) Direct manipulation of behaviour reveals a mechanism for variation in growth and mortality among prey populations. Animal Behaviour, 73, 891 896.
13. Boon, A.K., Reale, D. Boutin, S. (2007) The interaction between personality, offspring fitness and food abundance in North American red squirrels. Ecology Letters, 10, 1094 1104.
14. Both, C., Dingemanse, N.J., Drent, P.J. Tinbergen, J.M. (2005) Pairs of extreme avian personalities have highest reproductive success. Journal of Animal Ecology, 74, 667 674.
15. Brydges, N.M., Colegrave, N., Heathcote, R.J.P. Braithwaite, V.A. (2008a) Habitat stability and predation pressure affect temperament behaviours in populations of three-spined sticklebacks. Journal of Animal Ecology, 77, 229 235.
16. Brydges, N.M., Heathcote, R.J.P. Braithwaite, V.A. (2008b) Habitat stability and predation pressure influence learning and memory in populations of three-spined sticklebacks. Animal Behaviour, 75, 935 942.
17. Carere, C. van Oers, K. (2004) Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress. Physiology and Behavior, 82, 905 912.
18. Carere, C., Welink, D., Drent, P.J., Koolhaas, J.M. Groothuis, T.G.G. (2001) Effect of social defeat in a territorial bird (Parus major) selected for different coping styles. Physiology and Behavior, 73, 427 433.
19. Charmantier, A. Réale, D. (2005) How do misassigned paternities affect the estimation of heritability in the wild? Molecular Ecology, 14, 2839 2850.
20. Charmantier, A., Perrins, C., McCleery, R.H. Sheldon, B.C. (2006) Evolutionary response to selection on clutch size in a long-term study of the mute swan. American Naturalist, 167, 453 465.
21. Charmantier, A., McCleery, R.H., Cole, L.R., Perrins, C., Kruuk, L.E.B. Sheldon, B.C. (2008) Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science, 320, 800 803.
22. Coltman, D.W., Smith, J.A., Bancroft, D.R., Pilkington, J., MacColl, A.D.C., Clutton-Brock, T.H. Pemberton, J.M. (1999) Density-dependent variation in lifetime breeding success and natural and sexual selection in Soay rams. American Naturalist, 154, 730 746.
23. Coltman, D.W., Pilkington, J., Kruuk, L.E.B., Wilson, K. Pemberton, J.M. (2001) Positive genetic correlation between parasite resistance and body size in free-living ungulate population. Evolution, 55, 2116 2125.
24. Daisley, J.N., Bromundt, V., Mostl, E. Kotrschal, K. (2005) Enhanced yolk testosterone influences behavioral phenotype independent of sex in Japanese quail chicks Coturnix japonica. Hormones and Behavior, 47, 185 194.
25. Dall, S.R.X., Houston, A.I. McNamara, J.M. (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecology Letters, 7, 734 739.
26. Dingemanse, N.J. de Goede, P. (2004) The relation between dominance and exploratory behavior is context-dependent in wild great tits. Behavioral Ecology, 15, 1023 1030.
27. Dingemanse, N.J. Réale, D. (2005) Natural selection and animal personality. Behaviour, 142, 1159 1184.
28. Dingemanse, N.J., Both, C., Drent, P.J., van Oers, K. van Noordwijk, A.J. (2002) Repeatability and heritability of exploratory behaviour in great tits from the wild. Animal Behaviour, 64, 929 938.
29. Dingemanse, N.J., Both, C., van Noordwijk, A.J., Rutten, A.L. Drent, P.J. (2003) Natal dispersal and personalities in great tits (Parus major). Proceedings of the Royal Society of London. Series B: Biological Sciences, 270, 741 747.
30. Dingemanse, N.J., Both, C., Drent, P.J. Tinbergen, J.M. (2004) Fitness consequences of avian personalities in a fluctuating environment. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271, 847 852.
31. Dingemanse, N.J., Wright, J., Kazem, A.J.N., Thomas, D.K., Hickling, R. Dawnay, N. (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. Journal of Animal Ecology, 76, 1128 1138.
32. Drent, P.J., van Oers, K. van Noordwijk, A.J. (2003) Realized heritability of personalities in the great tit (Parus major). Proceedings of the Royal Society of London. Series B: Biological Sciences, 270, 45 51.
33. Duckworth, R.A. (2006) Behavioral correlations across breeding contexts provide a mechanism for a cost of aggression. Behavioral Ecology, 17, 1011 1019.
34. Duckworth, R.A. (2008) Adaptive dispersal strategies and the dynamics of a range expansion. American Naturalist, 172, S4 S17.
35. Duckworth, R.A. Badyaev, A.V. (2007) Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proceedings of the National Academy of Sciences of the United States of America, 104, 15017 15022.
36. Eising, C.M. Groothuis, T.G.G. (2003) Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Animal Behaviour, 66, 1027 1034.
37. Endler, J.A. (1986) Natural Selection in the Wild, Princeton University Press, Princeton, NJ.
38. Futuyma, D.J. (1998) Evolutionary Biology, 3rd edn. Sinauer, Sunderland, MA.
39. Garant, D., Kruuk, L.E.B., McCleery, R.H. Sheldon, B.C. (2004) Evolution in a changing environment: a case study with great tit fledging mass. American Naturalist, 164, E115 E129.
40. Giles, N. Huntingford, F.A. (1984) Predation risk and inter-population variation in antipredator behavior in the 3-spined stickleback, Gasterosteus aculeatus L. Animal Behaviour, 32, 264 275.
41. Gilmour, A.R., Gogel, B.J., Cullis, B.R., Welham, S.J. Thompson, R. (2002) ASReml User Guide Release 1.0. VSN International Ltd, Hemel Hempstead, UK.
42. Gosling, S.D. (2001) From mice to men: what can we learn about personality from animal research? Psychological Bulletin, 127, 45 86.
43. Gosling, S.D. John, O.P. (1999) Personality dimensions in nonhuman animals: a cross-species review. Current Directions in Psychological Science, 8, 69 75.
44. Greenwood, P.J., Harvey, P.H. Perrins, C.M. (1978) Inbreeding and dispersal in the great tit. Nature, 271, 52 54.
45. Groothuis, T.G.G. Carere, C. (2005a) Avian personalities: characterization and epigenesis. Neuroscience and Biobehavioral Reviews, 29, 137 150.
46. Groothuis, T.G.G., Muller, W., von Engelhardt, N., Carere, C. Eising, C. (2005b) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuroscience and Biobehavioral Reviews, 29, 329 352.
47. Hadfield, J.D., Nutall, A., Osorio, D. Owens, I.P.F. (2007) Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. Journal of Evolutionary Biology, 20, 549 557.
48. Hill, W.G., Goddard, M.E. Visscher, P.M. (2008) Data and theory point to mainly additive genetic variance for complex traits. Plos Genetics, 4, e/000008.
49. Hojesjo, J., Johnsson, J. Bohlin, T. (2004) Habitat complexity reduces the growth of aggressive and dominant brown trout (Salmo trutta) relative to subordinates. Behavioral Ecology and Sociobiology, 56, 286 289.
50. Huber, H., Kane, N.C., Heschel, M.S., von Wettberg, E.J., Banta, J., Leuck, A.M. Schmitt, J. (2004) Frequency and microenvironmental pattern of selection on plastic shade-avoidance traits in a natural population of Impatiens capensis. American Naturalist, 163, 548 563.
51. Jormalainen, V. Honkanen, T. (2004) Variation in natural selection for growth and phlorotannins in the brown alga Fucus vesiculosus. Journal of Evolutionary Biology, 17, 807 820.
52. Knott, S.A., Sibly, R.M., Smith, R.H. Moller, H. (1995) Maximum-likelihood-estimation of genetic-parameters in life- history studies using the animal-model. Functional Ecology, 9, 122 126.
53. Kruuk, L.E.B. (2004) Estimating genetic parameters in wild populations using the 'animal model'. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 359, 873 890.
54. Kruuk, L.E.B., Slate, J., Pemberton, J.M., Brotherstone, S., Guinness, F. Clutton-Brock, T. (2002) Antler size in red deer: heritability and selection but no evolution. Evolution, 56, 1683 1695.
55. Kruuk, L.E.B., Merila, J. Sheldon, B.C. (2003) When environmental variation short-circuits natural selection. Trends in Ecology and Evolution, 18, 207 209.
56. Lynch, M. Walsh, B. (1998) Genetics and Analysis of Quantitative Traits. Sinauer, Sunderland, MA.
57. Marchetti, C. Drent, P.J. (2000) Individual differences in the use of social information in foraging by captive great tits. Animal Behaviour, 60, 131 140.
58. Martin, J.G.A. Reale, D. (2008) Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. Animal Behaviour, 75, 309 318.
59. Mazer, S.J. Damuth, J. (2001) Nature and causes of variation. Evolutionary Ecology - Concepts and Case Studies (eds C.W. Fox, D.A. Roff D.J. Fairbairn 3 15, Oxford University Press, New York.
60. McAdam, A.G., Boutin, S., Réale, D. Berteaux, D. (2002) Maternal effects and the potential for evolution in a natural population of animals. Evolution, 56, 846 851.
61. McCleery, R.H., Pettifor, R.A., Armbruster, P., Meyer, K., Sheldon, B.C. Perrins, C.M. (2004) Components of variance underlying fitness in a natural population of the Great Tit. American Naturalist, 164, E62 E72.
62. McDonald, D.B., Fitzpatrick, J.W. Woolfenden, G.E. (1996) Actuarial senescence and demographic heterogeneity in the Florida Scrub Jay. Ecology, 77, 2373 2381.
63. McElreath, R. Strimling, P. (2006) How noisy information and individual asymmetries can make 'personality' an adaptation: a simple model. Animal Behaviour, 72, 1135 1139.
64. Merilä, J. Sheldon, B.C. (2001) Avian quantitative genetics. Current Ornithology, 16, 179 255.
65. Milner, J.M., Pemberton, J.M., Brotherstone, S. Albon, S.D. (2000) Estimating variance components and heritabilities in the wild: a case study using the 'animal model' approach. Journal of Evolutionary Biology, 13, 804 813.
66. Morrissey, M.B., Wilson, A.J., Pemberton, J.M. Ferguson, M.M. (2007) A framework for power and sensitivity analyses for quantitative genetic studies of natural populations, and case studies in Soay sheep (Ovis aries). Journal of Evolutionary Biology, 20, 2309 2321.
67. Newton, I. (1998) Population Limitation in Birds. Academic Press, London.
68. van Noordwijk, A.J., McCleery, R.H. Perrins, C.M. (1995) Selection for the timing of great tit (Parus major) breeding in relation to caterpillar growth and temperature. Journal of Animal Ecology, 64, 451 458.
69. van Oers, K., de Jong, G., Drent, P.J. van Noordwijk, A.J. (2004a) A genetic analysis of avian personality traits: correlated, response to artificial selection. Behavior Genetics, 34, 611 619.
70. van Oers, K., Drent, P.J., de Goede, P. van Noordwijk, A.J. (2004b) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271, 65 73.
71. van Oers, K., Drent, P.J., de Jong, G. van Noordwijk, A.J. (2004c) Additive and nonadditive genetic variation in avian personality traits. Heredity, 93, 496 503.
72. van Oers, K., de Jong, G., van Noordwijk, A.J., Kempenaers, B. Drent, P.J. (2005) Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour, 142, 1185 1206.
73. Patrick, S.C. (2008) Individual Personality and Sexual Selection in Great Tits. University of Oxford, Oxford, UK.
74. Pemberton, J.M., Smith, J.A., Coulson, T.N., Marshall, T.C., Slate, J., Paterson, S., Albon, S.D. Clutton-Brock, T.H. (1996) The maintenance of genetic polymorphism in small island populations: Large mammals in the Hebrides. Philosophical Transaction of the Royal Society of London Series B-Biological Sciences, 351, 745 752.
75. Quinn, J.L., Charmantier, A., Garant, D. Sheldon, B.C. (2006) Data depth, data completeness, and their influence on quantitative genetic estimation in two contrasting bird populations. Journal of Evolutionary Biology, 19, 994 1002.
76. Réale, D. Festa-Bianchet, M. (2003) Predator-induced natural selection on temperament in bighorn ewes. Animal Behaviour, 65, 463 470.
77. Reale, D., Festa-Bianchet, M. Jorgenson, J.T. (1999) Heritability of body mass varies with age and season in wild bighorn sheep. Heredity, 83, 526 532.
78. Reale, D., Reader, S.M., Sol, D., McDougall, P.T. Dingemanse, N.J. (2007) Integrating animal temperament within ecology and evolution. Biological Reviews, 82, 291 318.
79. Roff, D.A. (1997) Evolutionary Quantitative Genetics. Chapman and Hall, New York.
80. Sambandan, D., Yamamoto, A., Fanara, J.J., Mackay, T.F.C. Anholt, R.R.H. (2006) Dynamic genetic interactions determine odor-guided behavior in Drosophila melanogaster. Genetics, 174, 1349 1363.
81. Schluter, D. (1988) Estimating the form of natural selection on a quantitative trait. Evolution, 42, 849 861.
82. Sih, A., Kats, L.B. Maurer, E.F. (2003) Behavioural correlations across situations and the evolution of antipredator behaviour in a sunfish-salamander system. Animal Behaviour, 65, 29 44.
83. Sih, A., Bell, A. Johnson, J.C. (2004a) Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology and Evolution, 19, 372 378. (Pubitemid 38800923)
84. Sih, A., Bell, A.M., Johnson, J.C. Ziemba, R.E. (2004b) Behavioral syndromes: an integrative overview. The Quarterly Review of Biology, 79, 241 277.
85. Slater, F.R., Bruce, K.D., Ellis, R.J., Lilley, A.K. Turner, S.L. (2008) Heterogeneous selection in a spatially structured environment affects fitness tradeoffs of plasmid carriage in pseudomonads. Applied and Environmental Microbiology, 74, 3189 3197.
86. Smith, B.R. Blumstein, D.T. (2008) Fitness consequences of personality: a meta-analysis. Behavioral Ecology, 19, 448 455.
87. Stratton, D.A. Bennington, C.C. (1996) Measuring spatial variation in natural selection using randomly-sown seeds of Arabidopsis thaliana. Journal of Evolutionary Biology, 9, 215 228.
88. Stratton, D.A. Bennington, C.C. (1998) Fine-grained spatial and temporal variation in selection does not maintain genetic variation in Erigeron annuus. Evolution, 52, 678 691.
89. Summerville, K.S., Crist, T.O., Kahn, J.K. Gering, J.C. (2003) Community structure of arboreal caterpillars within and among four tree species of the eastern deciduous forest. Ecological Entomology, 28, 747 757.
90. Tufto, J. (2000) The evolution of plasticity and nonplastic spatial and temporal adaptations in the presence of imperfect environmental cues. American Naturalist, 156, 121 130.
91. Van Oers, K., Drent, P.J., Dingemanse, N.J. Kempenaers, B. (2008) Personality is associated with extrapair paternity in great tits, Parus major. Animal Behaviour, 76, 555 563.
92. Verbeek, M.E.M., Drent, P.J. Wiepkema, P.R. (1994) Consistent individual-differences in early exploratory-behavior of male great tits. Animal Behaviour, 48, 1113 1121.
93. Verbeek, M.E., Boone, A. Drent, P.J. (1996) Exploration, agonisitc behaviour and dominance in juvenile great tits. Behaviour, 133, 945 963.
94. VSN International (2005) Genstat, Oxford, UK.
95. Weigensberg, I. Roff, D.A. (1996) Natural heritabilities: can they be reliably estimated in the laboratory? Evolution, 50, 2149 2157.
96. Werner, E.E. Anholt, B.R. (1993) Ecological Consequences of the Trade-Off between Growth and Mortality-Rates Mediated by Foraging Activity. American Naturalist, 142, 242 272.
97. Wilkin, T.A., Garant, D., Gosler, A.G. Sheldon, B.C. (2006) Density effects on life-history traits in a wild population of the great tit Parus major: analyses of long-term data with GIS techniques. Journal of Animal Ecology, 75, 604 615.
98. Wilkin, T.A., Garant, D., Gosler, A.G. Sheldon, B.C. (2007a) Edge effects in the great tit: analyses of long-term data with GIS techniques. Conservation Biology, 21, 1207 1217.
99. Wilkin, T.A., Perrins, C.M. Sheldon, B.C. (2007b) The use of GIS in estimating spatial variation in habitat quality: a case study of lay-date in the Great Tit Parus major. Ibis, 149, 110 118.
100. Wilkin, T.A., King, L.E. Sheldon, B.C. (2009) Habitat quality, nestling diet, and provisioning behaviour in great tits Parus major. Journal of Avian Biology, 40, 135 145.
101. Wilson, D.S. (1998) Adaptive individual differences within single populations. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 353, 199 205.
102. Wilson, A.J. (2008) Why h(2) does not always equal V-A/V-P? Journal of Evolutionary Biology, 21, 647 650.
103. Wilson, A.J., Pemberton, J.M., Pilkington, J.G., Coltman, D.W., Mifsud, D.V., Clutton-Brock, T.H. Kruuk, L.E.B. (2006) Environmental coupling of selection and heritability limits evolution. Plos Biology, 4, 1270 1275.
104. Wolf, M., van Doorn, G.S., Leimar, O. Weissing, F.J. (2007) Life-history trade-offs favour the evolution of animal personalities. Nature, 447, 581 584.