The biology hidden inside residual within-individual phenotypic variation

Biological Reviews

Volumn 90, Issue 3, 2015, Pages 729-743

  Westneat, David F ^a   Wright, Jonathan ^b   Dingemanse, Niels J ^c,d  

^a UNIVERSITY OF KENTUCKY   (United States)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c UNIVERSITY OF MUNICH   (Germany)

^d MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

Author keywords

Bet hedging; Canalization; Gene environment interaction; Phenotypic stability; Plasticity; Reaction norm; Variance sensitivity

Indexed keywords

ENVIRONMENT; GENOTYPE; PHENOTYPE; STATISTICAL MODEL;

ENVIRONMENT; GENOTYPE; MODELS, STATISTICAL; PHENOTYPE;

EID: 84937162204     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/brv.12131     Document Type: Article

References (113)

1. Auld, J. R., Agrawal, A. A. & Relyea, R. A. (2010). Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proceedings of the Royal Society of London B 277, 503-511.
2. Bell, A. M., Hankison, S. L. & Laskowski, K. L. (2009). The repeatability of behaviour: a meta-analysis. Animal Behaviour 77, 771-783.
3. Bergmüller, R. & Taborsky, M. (2010). Animal personality due to social nice specialisation. Trends in Ecology & Evolution 9, 504-511.
4. Biro, P. A. & Adriaenssens, B. (2013). Predictability as a personality trait: consistent differences in intra-individual behavioral variation. The American Naturalist 182, 621-629.
5. Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H. & White, J. S. S. (2009). Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127-135.
6. Breusch, T. S. & Pagan, A. R. (1979). Simple test for heteroscedasticity and random coefficient variation. Econometrica 47, 1287-1294.
7. Briffa, M. (2013). Plastic proteans: reduced predictability in the face of predation risk in hermit crabs. Biology Letters 9, 20130592.
8. Brock, J., Xu, J. Y. & Brooks, K. R. (2011). Individual differences in visual search: relationship to autistic traits, discrimination thresholds, and speed of processing. Perception 40, 739-742.
9. Brommer, J. E., Rattiste, K. & Wilson, A. (2010). The rate of ageing in a long-lived bird is not heritable. Heredity 104, 363-370.
10. Brooke, M. de L., Davies, N. B. & Noble, D. G. (1998). Rapid decline of host defences in response to reduced cuckoo parasitism: behavioural flexibility of reed warblers in a changing world. Proceedings of the Royal Society of London B 265, 1277-1282.
11. Cai, L., Dalal, C. K. & Elowitz, M. B. (2008). Frequency-modulated nuclear localization bursts coordinate gene regulation. Nature 455, 485-490.
12. Cannon, W. B. (1929). Organization for physiological homeostasis. Physiological Reviews 9, 399-431.
13. Caraco, T., Martindale, S. & Whittam, T. S. (1980). An empirical demonstration of risk-sensitive foraging preferences. Animal Behaviour 28, 820-830.
14. Chancellor, R. L. & Isbell, L. A. (2008). Punishment and competition over food in captive rhesus macaques, Macaca mulatta. Animal Behaviour 75, 1939-1947.
15. Changeux, J. P. & Danchin, A. (1976). Selective stabilisation of developing synapses as a mechanism for specification of neuronal networks. Nature 264, 705-712.
16. Charmantier, A. & Garant, D. (2008). Environmental quality and evolutionary potential: lessons from wild populations. Proceedings of the Royal Society of London B 272, 1415-1425.
17. Cipollini, D. (2004). Stretching the limits of plasticity: can a plant defend against both competitors and herbivores? Ecology 85, 28-37.
18. Cleasby, I. R. & Nakagawa, S. (2011). Neglected biological patterns in the residuals. Behavioral Ecology and Sociobiology 65, 2361-2372.
19. Debat, V. & David, P. (2002). Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology & Evolution 16, 555-561.
20. DeWitt, T. J., Sih, A. & Wilson, D. S. (1998). Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution 13, 77-81.
21. Diamond, S. E. & Kingsolver, J. G. (2012). Host plant adaptation and the evolution of thermal reaction norms. Oecologia 169, 353-360.
22. Dingemanse, N. J., Barber, I., Wright, J. & Brommer, J. E. (2012). Quantitative genetics of behavioural reaction norms: genetic correlations between personality and behavioural plasticity vary across stickleback populations. Journal of Evolutionary Biology 25, 485-496.
23. Dingemanse, N. J. & Dochtermann, N. A. (2013). Quantifying individual variation in behaviour: mixed-effect modelling approaches. Journal of Animal Ecology 82, 39-54.
24. Dingemanse, N. J. & Dochtermann, N. A. (2014). Individual behaviour: behavioural ecology meets quantitative genetics. In Quantitative Genetics in the Wild (eds A. Charmantier, D. Garant and L. E. B. Kruuk ), pp. 54-67. Oxford University Press, Oxford.
25. Dingemanse, N. J., Kazem, A. J. N., Réale, D. & Wright, J. (2010). Behavioural reaction norms: animal personality meets individual plasticity. Trends in Ecology & Evolution 25, 81-89.
26. Dingemanse, N. J. & Wolf, M. (2013). Between-individual differences in behavioural plasticity within populations: causes and consequences. Animal Behaviour 85, 1031-1039.
27. Dukas, R. (1998). Constraints on information processing and their effects on behavior. In Cognitive Ecology: The Evolutionary Ecology of Information Processing and Decision-Making (ed. R. Dukas ), pp. 89-128. University of Chicago Press, Chicago.
28. Dutilleul, P. & Potvin, C. (1995). Among-environment heteroscedasticity and genetic autocorrelation: implications for the study of phenotypic plasticity. Genetics 139, 1815-1829.
29. Dworkin, I. (2005). Canalization, cryptic variation, and developmental buffering. In Variation: A Central Concept in Biology (eds B. Halgrimsson and B. K. Hall ), pp. 131-158. Academic Press, New York.
30. Eldar, A. & Elowitz, M. B. (2010). Functional roles for noise in genetic circuits. Nature 467, 167-173.
31. Frank, S. A. (1997). The design of adaptive systems: optimal parameters for variation and selection in learning and development. Journal of Theoretical Biology 184, 31-39.
32. Frank, S. A. & Slatkin, M. (1990). Evolution in a variable environment. The American Naturalist 136, 244-260.
33. Getty, T. (1996). The maintenance of phenotypic plasticity as a signal detection problem. The American Naturalist 148, 378-385.
34. Ghalambor, C. K., Angeloni, L. M. & Carroll, S. P. (2010). Behavior as phenotypic plasticity. In Evolutionary Behavioral Ecology (eds D. F. Westneat and C. W. Fox ), pp. 90-107. Oxford University Press, New York.
35. Gibbon, J. (1977). Scalar expectancy theory and Weber's law in animal timing. Psychology Review 84, 279-325.
36. Gibson, G. & Wagner, G. (2000). Canalization in evolutionary genetics: a stabilizing theory? Bioessays 22, 372-380.
37. Gil, D. (2008). Hormones in avian eggs: physiology, ecology and behavior. Advances in the Study of Behavior 38, 337-398.
38. Gillespie, J. H. (1973). Polymorphism in random environments. Theoretical Population Biology 4, 193-195.
39. Golub, E. S. & Green, D. R. (1991). Immunology: A Synthesis. Second Edition. Sinauer, Sunderland.
40. Gomulkiewicz, R. & Kirkpatrick, M. (1992). Quantitative genetics and the evolution of reaction norms. Evolution 46, 390-411.
41. Hansen, T. F., Carter, A. J. R. & Pélabon, C. (2006). On adaptive accuracy and precision in natural populations. The American Naturalist 168, 168-181.
42. Hill, W. G. & Mulder, H. A. (2010). Genetic analysis of environmental variation. Genetics Research 92, 381-395.
43. Hugie, D. M. (2003). The waiting game: a "battle of waits" between predator and prey. Behavioral Ecology 14, 807-817.
44. Jackson, R. R. & Wilcox, R. S. (1993). Spider flexibly chooses aggressive mimicry signals for different prey by trial and error. Behaviour 127, 21-36.
45. Johnstone, R. A. (2001). Eavesdropping and animal conflict. Proceedings of the National Academy of Sciences of the United States of America 98, 9177-9180.
46. Kagan, M. L., Novoplansky, N. & Sachs, T. (1992). Variable cell lineages from the functional pea epidermis. Annuals of Botany 69, 303-312.
47. Kellner, J. R. & Alford, R. A. (2003). The ontogeny of fluctuating asymmetry. The American Naturalist 161, 931-947.
48. Kingsolver, J. G., Shlichta, J. G., Ragland, G. J. & Massie, K. R. (2006). Thermal reaction norms for caterpillar growth depend on diet. Evolutionary Ecology Research 8, 703-715.
49. Kontiainen, P., Pietiäinen, H., Huttunen, K., Karell, P., Kolunen, H. & Brommer, J. E. (2009). Aggressive ural owl mothers recruit more offspring. Behavioral Ecology 20, 789-796.
50. Kussel, E. & Leibler, S. (2005). Phenotypic diversity, population growth, and information in fluctuating environments. Science 309, 2075-2078.
51. Lee, Y. & Nelder, J. A. (1996). Hierarchical generalized linear models (with discussion). Journal of the Royal Statistical Society B 58, 619-678.
52. Lindholm, A. & Thomas, R. (2000). Differences between populations of reed warblers in defences against brood parasitism. Behaviour 137, 25-42.
53. Losick, R. & Desplan, C. (2008). Stochasticity and cell fate. Science 320, 65-68.
54. Lotem, A., Nakamura, H. & Zahavi, A. (1995). Constraints on egg discrimination and cuckoo-host co-evolution. Animal Behaviour 49, 1185-1209.
55. Lynch, M. & Walsh, B. (1998). Genetics and Analysis of Quantitative Traits. Sinauer Press, Sunderland.
56. Markow, T. A. (1995). Evolutionary ecology and developmental instability. Annual Reviews of Entomology 40, 105-120.
57. Martin, J. G. A., Nussey, D. H., Wilson, A. J. & Réale, D. (2011). Measuring individual differences in reaction norms in field and experimental studies: a power analysis of random regression models. Methods in Ecology and Evolution 2, 362-374.
58. Martin, T. M., Ton, R. & Niklison, A. (2013). Intrinsic versus extrinsic influences on life history expression: metabolism and parentally induced temperature influences on embryo development rate. Ecology Letters 16, 738-745.
59. Mathot, K. J., Wright, J., Kempenaers, B. & Dingemanse, N. J. (2012). Adaptive strategies for managing uncertainty may explain personality-related differences in behavioural plasticity. Oikos 121, 1009-1020.
60. Maynard Smith, J. (1974). Theory of games and the evolution of animal contests. Journal of Theoretical Biology 47, 209-221.
61. Mayr, E. (1963). Animal Species and Evolution. Belknap Press/Harvard University Press, Cambridge.
62. Moczek, A. P., Hunt, J., Emlen, D. J. & Simmons, L. W. (2002). Threshold evolution in exotic populations of a polyphenic beetle. Evolutionary Ecology Research 4, 587-601.
63. Moore, A. J., Brodie, E. D. III & Wolf, J. B. (1997). Interacting phenotypes and the evolutionary process: I. Direct and indirect genetic effects of social interactions. Evolution 51, 1352-1362.
64. Moran, N. A. (1992). The evolutionary maintenance of alternative phenotypes. The American Naturalist 139, 971-989.
65. Müller, M. S., Roelofs, Y., Erikstad, K. E. & Groothuis, T. G. G. (2012). Maternal androgens increase sibling aggression, dominance, and competitive ability in the siblicidal black-legged kittiwake (Rissa tridactyla). PLoS ONE 7(10), e47763 (doi: 10.1371/journal.pone.0047763).
66. Natarajan, D., de Vries, H., Saaltink, D. J., de Boer, S. F. & Koolhaas, J. M. (2009). Delineation of violence from functional aggression in mice: an ethological approach. Behavioral Genetics 39, 73-90.
67. Nesse, R. M. (2001). Evolution and the Capacity for Commitment. Russell Sage Foundation, New York.
68. Nicolaus, M., Brommer, J. E., Ubels, R., Tinbergen, J. M. & Dingemanse, N. J. (2013). Exploring patterns of variation in clutch size-density reaction norms in a wild passerine bird. Journal of Evolutionary Biology 26, 2031-2043.
69. Niemelä, P. T. & Dingemanse, N. J. (2014). Artificial environments and the study of "adaptive" personalities. Trends in Ecology & Evolution 29, 245-247.
70. Nijhout, H. F. & Davidowitz, G. (2003). Developmental perspectives on phenotypic plasticity, canalization, and fluctuating asymmetry. In Developmental Instability: Causes and Consequences (ed. M. Polak ), pp. 3-13. MIT Press, Boston.
71. Nussey, D. H., Wilson, A. J. & Brommer, J. E. (2007). The evolutionary ecology of individual phenotypic plasticity in wild populations. Journal of Evolutionary Biology 20, 831-844.
72. Piché, J., Hutchings, J. A. & Blanchard, W. (2008). Genetic variation in threshold reaction norms for alternative reproductive tactics in male Atlantic salmon, Salmo salar. Proceedings of the Royal Society of London B 275, 1571-1575.
73. Piersma, T. & Drent, J. (2003). Phenotypic flexibility and the evolution of organismal design. Trends in Ecology & Evolution 18, 228-233.
74. Playfair, J. H. L. (1995). Infection and Immunity. Second Edition. Oxford University Press, New York.
75. van de Pol, M. (2012). Quantifying individual variation in reaction norms: how study design affects the accuracy, precision and power of random regression models. Methods in Ecology and Evolution 3, 268-280.
76. Ratikainen, I. I., Wright, J. & Kazem, A. J. N. (2010). Social class influences degree of variance sensitivity in wild Siberian jays. Behavioral Ecology 21, 1067-1072.
77. Reeve, H. K. (1989). The evolution of conspecific acceptance thresholds. The American Naturalist 133, 407-435.
78. Ross, H. E. & Murray, D. J. (1996). E. H. Weber on the Tactile Senses. Second Edition. Erlbaum, Taylor & Francis, Hove.
79. Rothstein, S. I. (1978). Mechanisms of avian egg-recognition: additional evidence for learned components. Animal Behaviour 26, 671-677.
80. Rowe, L., Ludwig, D. & Schluter, D. (1994). Time, condition, and the seasonal decline of avian clutch size. The American Naturalist 143, 698-722.
81. Schaeffer, L. R. (2004). Application of random regression models in animal breeding. Livestock Production Science 86, 35-45.
82. Scheiner, S. M. (2006). Genotype-environment interactions and evolution. In Evolutionary Genetics: Concepts and Case Studies (eds C. W. Fox and J. B. Wolf ), pp. 326-338. Oxford University Press, New York.
83. Schuett, W., Tregenza, T. & Dall, S. R. X. (2010). Sexual selection and animal personality. Biological Reviews 85, 217-246.
84. Shafir, S. (2000). Risk-sensitive foraging: the effect of relative variability. Oikos 88, 663-669.
85. Sherman, P. W., Reeve, H. K. & Pfennig, D. W. (1997). Recognition systems. In Behavioural Ecology: An Evolutioanry Approach. Fourth Edition, (eds J. R. Krebs and N. B. Davies ), pp. 69-96. Blackwell Scientific, Oxford.
86. Simons, A. M. (2011). Modes of response to environmental change and the elusive empirical evidence for bet-hedging. Proceedings of the Royal Society of London B 278, 1601-1609.
87. Smith, H. R., Rowson, M., Basketter, D. A. & McFadden, J. P. (2004). Intra-individual variation of irritant threshold and relationship to trans-epidermal water loss measurement of skin irritation. Contact Dermatitis 51, 26-29.
88. Smyth, G. K. & Verbyla, A. P. (1999). Adjusted likelihood methods for modeling dispersion in generalized linear models. Environmetrics 10, 695-710.
89. Snell-Rood, E. C. (2013). An overview of the evolutionary causes and consequences of behavioural plasticity. Animal Behaviour 85, 1004-1011.
90. Stamps, J. A., Briffa, M. & Biro, P. A. (2012). Unpredictable animals: individual differences in intraindividual variability (IIV). Animal Behaviour 83, 1325-1334.
91. Stamps, J. A. & Groothuis, T. G. G. (2010). Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Philosophical Transactions of the Royal Society B 365, 4029-4041.
92. Stearns, S. C. & Kawecki, T. J. (1994). Fitness sensitivity and the canalization of life-history traits. Evolution 48, 1438-1450.
93. Stephens, D. W. (1981). The logic of risk-sensitive foraging preferences. Animal Behaviour 29, 628-629.
94. Stillwell, R. C., Wallin, W. G., Hitchcock, L. J. & Fox, C. W. (2007). Phenotypic plasticity in a complex world: interactive effects of food and temperature on fitness components of a seed beetle. Oecologia 153, 309-321.
95. Stokke, B. G., Hafstad, I., Rudolfsen, G., Moksnes, A., Møller, A. P., Røskaft, E. & Soler, M. (2008). Predictors of resistance to brood parasitism within and among reed warbler populations. Behavioral Ecology 19, 612-620.
96. Tonsor, S. J., Elnaccash, T. W. & Scheiner, S. M. (2013). Developmental instability is genetically correlated with phenotypic plasticity, constraining heritability, and fitness. Evolution 67, 2923-2935.
97. van Dooren, T. J. M. (2001). Reaction norms with bifurcations shaped by evolution. Proceedings of the Royal Society of London B 268, 279-287.
98. Van Valen, L. (1962). A study of fluctuating asymmetry. Evolution 16, 125-142.
99. Via, S. & Lande, R. (1985). Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39, 505-522.
100. Viswanathan, M. (2005). Measurement Error and Research Design. Sage Publications, Thousand Oaks.
101. Waddington, C. H. (1942). Canalization of development and the inheritance of acquired characters. Nature 150, 563-565.
102. Weinig, C. & Delph, L. F. (2001). Phenotypic plasticity early in life constrains developmental responses later. Evolution 55, 930-936.
103. West-Eberhard, M. J. (2003). Developmental Plasticity and Evolution. Oxford University Press, Oxford.
104. Westneat, D. F., Hatch, M. I., Wetzel, D. P. & Ensminger, A. L. (2011). Individual variation in parental care reaction norms: integration of personality and plasticity. The American Naturalist 178, 652-667.
105. Westneat, D. F., Schofield, M. & Wright, J. (2013). Parental behavior exhibits between-individual variance, plasticity and heterogeneous residual variance. Behavioral Ecology 24, 598-604.
106. Westneat, D. F., Stewart, I. R. K. & Hatch, M. I. (2009). Complex interactions among temporal variables affect the plasticity of clutch size in a multi-brooded bird. Ecology 90, 1162-1174.
107. White, H. (1980). A heteroskedasticity-consistent covariance matrix estimator and a direct test for heteroskedasticity. Econometrica 48, 817-838.
108. Whiten, A. & Byrne, R. W. (1997). Machiavellian Intelligence II. Cambridge University Press, Cambridge.
109. Wiley, R. H. (1994). Errors, exaggeration and deception in animal communication. In Behavioural Mechanisms in Evolutionary Ecology (ed. L. A. Real ), pp. 157-189. University of Chicago Press, Chicago.
110. Wilson, A. J., Réale, D., Clements, M. N., Morrissey, M. M., Postma, E., Walling, C. A., Kruuk, L. E. B. & Nussey, D. H. (2008). An ecologist's guide to the animal model. Journal of Animal Ecology 79, 13-26.
111. Wollerman, L. & Wiley, R. H. (2002). Background noise from a natural chorus alters female discrimination of male calls in a Neotropical frog. Animal Behaviour 63, 15-22.
112. Woltereck, R. (1909). Weitere experimentelle Untersuchungen uber Artveranderung, speziell uber das Wesen quantitativer Artunterschiede bei Daphniden. Versuche Deutsche Zoologishe Geselleschaft 19, 110-172.
113. Ydenberg, R. C. (1994). The behavioral ecology of provisioning in birds. Ecoscience 1, 1-14.