Evolutionary emergence of responsive and unresponsive personalities

Abstract

In many animal species, individuals differ consistently in suites of correlated behaviors, comparable with human personalities. Increasing evidence suggests that one of the fundamental factors structuring personality differences is the responsiveness of individuals to environmental stimuli. Whereas some individuals tend to be highly responsive to such stimuli, others are unresponsive and show routine-like behaviors. Much research has focused on the proximate causes of these differences but little is known about their evolutionary origin. Here, we provide an evolutionary explanation. We develop a simple but general evolutionary model that is based on two key ingredients. First, the benefits of responsiveness are frequency-dependent; that is, being responsive is advantageous when rare but disadvantageous when common. This explains why responsive and unresponsive individuals can coexist within a population. Second, positive-feedback mechanisms reduce the costs of responsiveness; that is, responsiveness is less costly for individuals that have been responsive before. This explains why individuals differ consistently in their responsiveness, across contexts and over time. As a result, natural selection gives rise to stable individual differences in responsiveness. Whereas some individuals respond to environmental stimuli in all kinds of contexts, others consistently neglect such stimuli. Interestingly, such differences induce correlations among all kinds of other traits (e.g., boldness and aggressiveness), thus providing an explanation for environment-specific behavioral syndromes.architecture of behavior ͉ behavioral flexibility ͉ behavioral syndromes ͉ individual differences ͉ reactivity E mpirical findings in Ͼ100 species, ranging from insects to mammals, suggest that personalities are a widespread phenomenon in the animal kingdom (1-9). Individuals differ profoundly from each other in their behavior, and these differences are often consistent over time and extend to various contexts. In birds, fish, and rodents, for example, some individuals are consistently more aggressive than others, and aggressive individuals differ from nonaggressive individuals in many other respects like foraging behavior or the exploration of novel environments (5). From an adaptive point of view, both the coexistence of behavioral types and the consistency of individuals are poorly understood (10, 11).Many researchers believe that a fundamental factor structuring personality differences is the degree to which individual behavior is guided by environmental stimuli (6)(7)(8)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21). Whereas some individuals pay attention to environmental stimuli and quickly adapt their behavior to the prevailing conditions, others show more rigid, routine-like behavior. Such differences in responsiveness (also termed coping style, reactivity, flexibility, plasticity) have been documented in many organisms including birds [e.g., great tits (12), spice finches (13), and zebra finches (14)] and mammals [e.g., rats and mice (7)...

Evolution of learned strategy choice in a frequency-dependent game

“…The prediction that follows from Dubois et al 's model is that a population in which all individuals are able to learn to choose among strategies is unlikely to evolve. These interesting results emphasize the non-trivial nature of learning within a frequency-dependent game and are consistent with recent models of behavioural polymorphism [24]. It is important to note, however, that in Dubois et al the learning process was instantaneous.…”

Melanin-based skin spots reflect stress responsiveness in salmonid fish

“…Correlated behavioural and physiological traits are thought to reflect adaptation to different population densities, the relative frequency of occurrence of similarly or differently behaving individuals, and/or other fluctuating aspects of the environment, including stability and predictability of environmental change (Koolhaas et al 1999;Dingemanse et al 2004;Höjesjö et al 2004;Wolf et al 2008). One important consequence of eumelanin pigment as a visual marker of stress coping style is that it may ease the work of understanding the evolution of correlated traits by providing a convenient and reliable identification of the occurrence of different phenotypes in different environments.…”

Learning in a game context: strategy choice by some keeps learning from evolving in others

“…Their result, however, is attained by a different process from ours. Much as was true in the fighting games, the responsive individuals in Wolf et al's (2008) study decided on settlement strategy on the basis of the assessment of a fixed quantity, the initial difference between the two habitats. They did not then continue to assess as the animals settled in one or the other, and so were not affected by the frequency dependence of the payoffs but only the density dependence that results from accumulation of responsive individuals in the initially better patch.…”

“…Recently, behavioural ecologists have been interested in strong behavioural differences of the type we predict here and have referred to them as syndromes of behavioural plasticity (Sih et al 2004;Dingemanse et al 2009), flexibility (McElreath & Strimling 2006), responsiveness (Wolf et al 2008) or different coping styles (Koolhaas et al 1999). Personality polymorphisms are thought to be maintained as the consequence of strong trade-offs between benefits and costs across ecological contexts, as well as different selective forces acting either at different times during an organism's life history or in different environments exploited by the organism (Wilson 1998;Sih et al 2004).…”