Animal personality and state-behaviour feedbacks: a review and guide for empiricists.

An exciting area in behavioural ecology focuses on understanding why animals exhibit consistent among-individual differences in behaviour (animal personalities). Animal personality has been proposed to emerge as an adaptation to individual differences in state variables, leading to the question of why individuals differ consistently in state. Recent theory emphasizes the role that positive feedbacks between state and behaviour can play in producing consistent among-individual covariance between state and behaviour, hence state-dependent personality. We review the role of feedbacks in recent models of adaptive personalities, and provide guidelines for empirical testing of model assumptions and predictions. We discuss the importance of the mediating effects of ecology on these feedbacks, and provide a roadmap for including state-behaviour feedbacks in behavioural ecology research.

[1]  A. Sih,et al.  Behavioral Syndromes: An Integrative Overview , 2004, The Quarterly Review of Biology.

[2]  J. Stamps,et al.  Are animal personality traits linked to life-history productivity? , 2008, Trends in ecology & evolution.

[3]  Sean A. Rands,et al.  Spontaneous emergence of leaders and followers in foraging pairs , 2003, Nature.

[4]  A. Sih,et al.  Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). , 2007, Ecology letters.

[5]  A. Vainikka,et al.  Parasitism, predation and the evolution of animal personalities. , 2010, Ecology letters.

[6]  D. Réale,et al.  Personality and the emergence of the pace-of-life syndrome concept at the population level , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  Pierre-Olivier Montiglio,et al.  Contaminants as a neglected source of behavioural variation , 2014, Animal Behaviour.

[8]  K. Nishimura,et al.  Predation risk suppresses the positive feedback between size structure and cannibalism. , 2011, The Journal of animal ecology.

[9]  A. J. Moore,et al.  INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS. III. SOCIAL EVOLUTION , 2010, Evolution; international journal of organic evolution.

[10]  Sasha R. X. Dall,et al.  Metabolic Rates Can Drive Individual Differences in Information and Insurance Use under the Risk of Starvation , 2013, The American Naturalist.

[11]  Andrew Sih,et al.  Linking behavioural syndromes and cognition: a behavioural ecology perspective , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

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

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

[15]  J. Krause,et al.  Personality in the context of social networks , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  D. Réale,et al.  Indirect genetic effects and the evolution of aggression in a vertebrate system , 2009, Proceedings of the Royal Society B: Biological Sciences.

[17]  L. Garamszegi,et al.  A meta-analysis of correlated behaviours with implications for behavioural syndromes: mean effect size, publication bias, phylogenetic effects and the role of mediator variables , 2012, Evolutionary Ecology.

[18]  J. Fick,et al.  Dilute Concentrations of a Psychiatric Drug Alter Behavior of Fish from Natural Populations , 2013, Science.

[19]  S. Adamo.  Parasites: evolution’s neurobiologists , 2013, Journal of Experimental Biology.

[20]  R. Mcelreath,et al.  Evolution of animal personalities , 2007, Nature.

[21]  Franz J. Weissing,et al.  Life-history trade-offs favour the evolution of animal personalities , 2007, Nature.

[22]  Kate L. Laskowski,et al.  The repeatability of behaviour: a meta-analysis , 2009, Animal Behaviour.

[23]  Alison M Bell,et al.  An evolutionary ecology of individual differences. , 2012, Ecology letters.

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

[25]  David Raubenheimer,et al.  Modeling Time Series of Animal Behavior by Means of a Latent‐State Model with Feedback , 2008, Biometrics.

[26]  J. Pearce.  Animal Learning and Cognition: An Introduction , 1997 .

[27]  R. Poulin.  Parasite manipulation of host personality and behavioural syndromes , 2013, Journal of Experimental Biology.

[28]  D. Gianola,et al.  Bayesian structural equation models for inferring relationships between phenotypes: a review of methodology, identifiability, and applications. , 2010, Journal of animal breeding and genetics = Zeitschrift fur Tierzuchtung und Zuchtungsbiologie.

[29]  J. Stachowicz,et al.  Behavioral Types of Predator and Prey Jointly Determine Prey Survival: Potential Implications for the Maintenance of Within-Species Behavioral Variation , 2011, The American Naturalist.

[30]  Colin W. Clark,et al.  Antipredator behavior and the asset-protection principle , 1994 .

[31]  I. Neumann.  The advantage of social living: Brain neuropeptides mediate the beneficial consequences of sex and motherhood , 2009, Frontiers in Neuroendocrinology.

[32]  D. Réale,et al.  Energy metabolism and animal personality , 2008 .

[33]  Shinichi Nakagawa,et al.  The consequences of parasitic infections for host behavioural correlations and repeatability , 2010 .

[34]  R. Johnstone,et al.  Social Feedback and the Emergence of Leaders and Followers , 2009, Current Biology.

[35]  A. Vyas,et al.  Toxoplasma gondii infection enhances testicular steroidogenesis in rats , 2013, Molecular ecology.

[36]  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.

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

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

[39]  F. Cézilly,et al.  Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects , 2013, Journal of Experimental Biology.

[40]  J. Koolhaas,et al.  Adolescent social stress does not necessarily lead to a compromised adaptive capacity during adulthood: A study on the consequences of social stress in rats , 2013, Neuroscience.

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

[42]  L. Michael Romero,et al.  The reactive scope model — A new model integrating homeostasis, allostasis, and stress , 2009, Hormones and Behavior.

[43]  J. Rodin,et al.  Insulin levels, hunger, and food intake: an example of feedback loops in body weight regulation. , 1985, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

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

[45]  Theodore Garland,et al.  Performance, Personality, and Energetics: Correlation, Causation, and Mechanism* , 2012, Physiological and Biochemical Zoology.

[46]  T. Stankowich.  When predators become prey: flight decisions in jumping spiders , 2009 .

[47]  D. Slattery,et al.  The Neuropeptide Oxytocin Facilitates Pro-Social Behavior and Prevents Social Avoidance in Rats and Mice , 2011, Neuropsychopharmacology.

[48]  D. Réale,et al.  Social niche specialization under constraints: personality, social interactions and environmental heterogeneity , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[50]  Causes and consequences of contest outcome: aggressiveness, dominance and growth in the sheepshead swordtail, Xiphophorus birchmanni , 2013, Behavioral Ecology and Sociobiology.

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

[52]  Erik Matthysen,et al.  Variation in personality and behavioural plasticity across four populations of the great tit Parus major. , 2012, The Journal of animal ecology.

[53]  J. Stamps,et al.  Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? , 2010, Trends in ecology & evolution.

[54]  Rufus A Johnstone,et al.  Managing uncertainty: information and insurance under the risk of starvation. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[56]  Iain Barber,et al.  Parasitism and the evolutionary ecology of animal personality , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[57]  M. Althaus,et al.  Local oxytocin expression and oxytocin receptor binding in the male rat brain is associated with aggressiveness , 2014, Behavioural Brain Research.

[58]  F. Weissing,et al.  Evolution of animal personalities - Reply , 2007 .

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

[60]  N. Dingemanse,et al.  A method for exploring the structure of behavioural syndromes to allow formal comparison within and between data sets , 2010, Animal Behaviour.

[61]  K. Lafferty,et al.  Comparing mechanisms of host manipulation across host and parasite taxa , 2013, Journal of Experimental Biology.

[62]  Kevin D. Lafferty,et al.  Altered Behavior of Parasitized Killifish Increases Susceptibility to Predation by Bird Final Hosts , 1996 .

[63]  K. Laland,et al.  Cause and Effect in Biology Revisited: Is Mayr's Proximate-ultimate , 2011 .

[64]  J. Wingfield,et al.  The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease , 2005, Neuroscience & Biobehavioral Reviews.

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

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

[67]  Daniel Gianola,et al.  Quantitative Genetic Models for Describing Simultaneous and Recursive Relationships Between Phenotypes This article is dedicated to Arthur B. Chapman, teacher and mentor of numerous animal breeding students and disciple and friend of Sewall Wright. , 2004, Genetics.

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

[69]  T. Fransson,et al.  Impaired predator evasion in fat blackcaps (Sylvia atricapilla) , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[70]  M. Taborsky,et al.  Animal personality due to social niche specialisation. , 2010, Trends in ecology & evolution.

[71]  M. Rosenzweig,et al.  Habitat selection as a source of biological diversity , 1987, Evolutionary Ecology.

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

[73]  Marco Del Giudice,et al.  The Adaptive Calibration Model of stress responsivity , 2011, Neuroscience & Biobehavioral Reviews.

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