Between-individual differences in behavioural plasticity within populations: causes and consequences

Behavioural traits are characterized by their labile expression: behavioural responses can, in principle, be up- and down-regulated in response to moment-to-moment changes in environmental conditions. Evidence is accumulating that individuals from the same population differ in the degree and extent of this form of phenotypic plasticity. We here discuss how such between-individual differences in behavioural plasticity can result from additive and interactive effects of genetic make-up and past environmental conditions, and under which conditions natural selection might favour this form of between-individual variation. We highlight how spatial or temporal variation in the environment, in combination with competition among individuals, can promote adaptive individual differences in plasticity; and we detail how differences in plasticity can emerge as a result of selection pressures induced by social interactions or as a response to between-individual differences in state. We further discuss both ecological and evolutionary consequences of individual differences in plasticity. We outline, for example, how individual differences in plasticity can have knock-on effects on the rate of evolution; and how such differences can enhance the stability and persistence of populations.

[1]  W. Gabriel,et al.  Environmental Tolerance, Heterogeneity, and the Evolution of Reversible Plastic Responses , 2005, The American Naturalist.

[2]  Barbara Taborsky,et al.  Social competence: an evolutionary approach. , 2012, Trends in ecology & evolution.

[3]  Kimberley J. Mathot,et al.  Adaptive strategies for managing uncertainty may explain personality-related differences in behavioural plasticity , 2012 .

[4]  Julie Morand-Ferron,et al.  Learning in a game context: strategy choice by some keeps learning from evolving in others , 2010, Proceedings of the Royal Society B: Biological Sciences.

[5]  Kimberley J. Mathot,et al.  Disentangling the roles of frequency-vs. state-dependence in generating individual differences in behavioural plasticity. , 2011, Ecology letters.

[6]  A. Houston,et al.  Models of adaptive behaviour , 1999 .

[7]  S. Sultan,et al.  The role of developmental plasticity in evolutionary innovation , 2011, Proceedings of the Royal Society B: Biological Sciences.

[8]  D. Falconer,et al.  Introduction to Quantitative Genetics. , 1962 .

[9]  R A Johnstone,et al.  Eavesdropping and animal conflict , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. McNamara,et al.  On the Evolution of Personalities via Frequency-Dependent Selection , 2012, The American Naturalist.

[11]  C. M. Coppens,et al.  Neuroendocrinology of coping styles: Towards understanding the biology of individual variation , 2010, Frontiers in Neuroendocrinology.

[12]  Andrew Sih,et al.  Ecological implications of behavioural syndromes. , 2012, Ecology letters.

[13]  C. Both,et al.  Adjustment to climate change is constrained by arrival date in a long-distance migrant bird , 2001, Nature.

[14]  D. Nussey,et al.  The evolutionary ecology of individual phenotypic plasticity in wild populations , 2007, Journal of evolutionary biology.

[15]  N. Dingemanse,et al.  Quantifying individual variation in behaviour: mixed-effect modelling approaches. , 2013, The Journal of animal ecology.

[16]  Andrew Sih,et al.  Insights for Behavioral Ecology from Behavioral Syndromes. , 2008, Advances in the study of behavior.

[17]  M. Lynch,et al.  Genetics and Analysis of Quantitative Traits , 1996 .

[18]  J. Brommer,et al.  Aggressive Ural owl mothers recruit more offspring , 2009 .

[19]  Franz J Weissing,et al.  On the coevolution of social responsiveness and behavioural consistency , 2011, Proceedings of the Royal Society B: Biological Sciences.

[20]  Samuel M. Scheiner,et al.  Phenotypic plasticity : functional and conceptual approaches , 2004 .

[21]  R. Arlinghaus,et al.  Coexistence of behavioural types in an aquatic top predator: a response to resource limitation? , 2009, Oecologia.

[22]  Charles M. Bishop,et al.  Helping effort increases with relatedness in bell miners, but ‘unrelated’ helpers of both sexes still provide substantial care , 2010, Proceedings of the Royal Society B: Biological Sciences.

[23]  Franz J Weissing,et al.  An explanatory framework for adaptive personality differences , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[24]  N. Dingemanse,et al.  Recent models for adaptive personality differences: a review , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[25]  A. Sih,et al.  Risk, resources and state-dependent adaptive behavioural syndromes , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[26]  Hoffmann,et al.  Heritable variation and evolution under favourable and unfavourable conditions. , 1999, Trends in ecology & evolution.

[27]  D. Sol,et al.  Behavioural adjustments for a life in the city , 2013, Animal Behaviour.

[28]  R. L. Rodríguez,et al.  The evolution and evolutionary consequences of social plasticity in mate preferences , 2013, Animal Behaviour.

[29]  T. Piersma,et al.  Phenotypic flexibility and the evolution of organismal design , 2003 .

[30]  T. Groothuis,et al.  Avian personalities: characterization and epigenesis , 2005, Neuroscience & Biobehavioral Reviews.

[31]  J. Wingfield.  The comparative biology of environmental stress: behavioural endocrinology and variation in ability to cope with novel, changing environments , 2013, Animal Behaviour.

[32]  Andrea Manica,et al.  Evolution of personality differences in leadership , 2011, Proceedings of the National Academy of Sciences.

[33]  Franz J. Weissing,et al.  Evolutionary emergence of responsive and unresponsive personalities , 2008, Proceedings of the National Academy of Sciences.

[34]  Alasdair I. Houston,et al.  Evolution of trust and trustworthiness: social awareness favours personality differences , 2008, Proceedings of the Royal Society B: Biological Sciences.

[35]  R. Dukas.  Effects of learning on evolution: robustness, innovation and speciation , 2013, Animal Behaviour.

[36]  Sasha R. X. Dall,et al.  The behavioural ecology of personality: consistent individual differences from an adaptive perspective , 2004 .

[37]  B. Kempenaers,et al.  Experimental evidence for adaptive personalities in a wild passerine bird , 2012, Proceedings of the Royal Society B: Biological Sciences.

[38]  F. Huntingford,et al.  Coping strategies in a strongly schooling fish, the common carp Cyprinus carpio. , 2010, Journal of fish biology.

[39]  D. Westneat,et al.  Complex interactions among temporal variables affect the plasticity of clutch size in a multi-brooded bird. , 2009, Ecology.

[40]  A. Sih.  Effects of early stress on behavioral syndromes: An integrated adaptive perspective , 2011, Neuroscience & Biobehavioral Reviews.

[41]  A. Agrawal,et al.  Re-evaluating the costs and limits of adaptive phenotypic plasticity , 2010, Proceedings of the Royal Society B: Biological Sciences.

[42]  J. Krebs,et al.  Behavioural Ecology: An Evolutionary Approach , 1978 .

[43]  M. Pigliucci,et al.  Phenotypic Evolution: A Reaction Norm Perspective , 1998 .

[44]  H. de Vries,et al.  Delineation of Violence from Functional Aggression in Mice: An Ethological Approach , 2008, Behavior genetics.

[45]  Massimo Pigliucci,et al.  Evolution of phenotypic plasticity: where are we going now? , 2005, Trends in ecology & evolution.

[46]  M. Kasumovic.  The multidimensional consequences of the juvenile environment: towards an integrative view of the adult phenotype , 2013, Animal Behaviour.

[47]  I Barber,et al.  Quantitative genetics of behavioural reaction norms: genetic correlations between personality and behavioural plasticity vary across stickleback populations , 2012, Journal of evolutionary biology.

[48]  Martijn van de Pol,et al.  Quantifying individual variation in reaction norms: how study design affects the accuracy, precision and power of random regression models , 2012 .

[49]  Ø. Øverli,et al.  Behavioral and Neuroendocrine Correlates of Selection for Stress Responsiveness in Rainbow Trout—a Review1 , 2005, Integrative and comparative biology.

[50]  Hans Slabbekoorn,et al.  Songs of the city: noise-dependent spectral plasticity in the acoustic phenotype of urban birds , 2013, Animal Behaviour.

[51]  Christa Beckmann,et al.  Small within-day increases in temperature affects boldness and alters personality in coral reef fish , 2010, Proceedings of the Royal Society B: Biological Sciences.

[52]  C. Schlichting,et al.  Phenotypic plasticity's impacts on diversification and speciation. , 2010, Trends in ecology & evolution.

[53]  A. Houston,et al.  State-dependent life histories , 1996, Nature.

[54]  S. D. de Boer,et al.  Coping styles in animals: current status in behavior and stress-physiology , 1999, Neuroscience & Biobehavioral Reviews.

[55]  J. Jeschke,et al.  Plastic animals in cages: behavioural flexibility and responses to captivity , 2013, Animal Behaviour.

[56]  A. Sih.  Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview , 2013, Animal Behaviour.

[57]  Franz J Weissing,et al.  Animal personalities: consequences for ecology and evolution. , 2012, Trends in ecology & evolution.

[58]  J. McNamara,et al.  Adaptive between-individual differences in social competence. , 2013, Trends in ecology & evolution.

[59]  Alastair J Wilson,et al.  Exploring plasticity in the wild: laying date–temperature reaction norms in the common gull Larus canus , 2008, Proceedings of the Royal Society B: Biological Sciences.

[60]  J. Gils,et al.  Book Reviews , 2012 .

[61]  Erik Postma,et al.  Selection on Heritable Phenotypic Plasticity in a Wild Bird Population , 2005, Science.

[62]  S. J. Arnold,et al.  THE MEASUREMENT OF SELECTION ON CORRELATED CHARACTERS , 1983, Evolution; international journal of organic evolution.

[63]  J. L. Brooks.  PREDATION AND RELATIVE HELMET SIZE IN CYCLOMORPHIC DAPHNIA. , 1965, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Judy Stamps,et al.  The development of animal personality: relevance, concepts and perspectives , 2010, Biological reviews of the Cambridge Philosophical Society.

[65]  Ian R. Cleasby,et al.  Neglected biological patterns in the residuals , 2011, Behavioral Ecology and Sociobiology.

[66]  S. Foster.  Evolution of behavioural phenotypes: influences of ancestry and expression , 2013, Animal Behaviour.

[67]  C. M. Coppens,et al.  Coping styles and behavioural flexibility: towards underlying mechanisms , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[68]  J. Stamps,et al.  Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[69]  Jonathan Wright,et al.  Parent–offspring conflict and co-adaptation: behavioural ecology meets quantitative genetics , 2008, Proceedings of the Royal Society B: Biological Sciences.

[70]  Barney Luttbeg,et al.  Comparing Alternative Models to Empirical Data: Cognitive Models of Western Scrub‐Jay Foraging Behavior , 2004, The American Naturalist.

[71]  Denis Réale,et al.  Behavioural reaction norms: animal personality meets individual plasticity. , 2010, Trends in ecology & evolution.

[72]  Erik Postma,et al.  An ecologist's guide to the animal model. , 2010, The Journal of animal ecology.

[73]  P. Drent,et al.  Epigenetic effects on personality traits: early food provisioning and sibling competition , 2005 .

[74]  R Gomulkiewicz,et al.  Adaptive phenotypic plasticity: consensus and controversy. , 1995, Trends in ecology & evolution.

[75]  M. West-Eberhard.  Developmental plasticity and evolution , 2003 .

[76]  L. R. Schaeffer,et al.  Application of random regression models in animal breeding , 2004 .

[77]  D. Roff.  Evolutionary Quantitative Genetics , 1997, Springer US.

[78]  Shinichi Nakagawa,et al.  Repeatability for Gaussian and non‐Gaussian data: a practical guide for biologists , 2010, Biological reviews of the Cambridge Philosophical Society.

[79]  D. Wilson,et al.  Costs and limits of phenotypic plasticity. , 1998, Trends in ecology & evolution.

[80]  J. McNamara,et al.  Variation and the response to variation as a basis for successful cooperation , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[81]  David F Westneat,et al.  Individual Variation in Parental Care Reaction Norms: Integration of Personality and Plasticity , 2011, The American Naturalist.

[82]  Molly Schumer,et al.  Genetic accommodation and behavioural evolution: insights from genomic studies , 2013, Animal Behaviour.

[83]  Julien G. A. Martin,et al.  Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus , 2008, Animal Behaviour.

[84]  P. R. Wiepkema,et al.  INDIVIDUAL BEHAVIOURAL CHARACTERISTICS AND DOMINANCE IN AVIARY GROUPS OF GREAT TITS , 1999 .

[85]  Anne Charmantier,et al.  Environmental quality and evolutionary potential: lessons from wild populations , 2005, Proceedings of the Royal Society B: Biological Sciences.

[86]  E. Snell-Rood,et al.  An overview of the evolutionary causes and consequences of behavioural plasticity , 2013, Animal Behaviour.