Max Wolf

Life-history trade-offs favour the evolution of animal personalities

In recent years evidence has been accumulating that personalities are not only found in humans but also in a wide range of other animal species. Individuals differ consistently in their behavioural tendencies and the behaviour in one context is correlated with the behaviour in multiple other contexts. From an adaptive perspective, the evolution of animal personalities is still a mystery, because a more flexible structure of behaviour should provide a selective advantage. Accordingly, many researchers view personalities as resulting from constraints imposed by the architecture of behaviour (but see ref. 12). In contrast, we show here that animal personalities can be given an adaptive explanation. Our argument is based on the insight that the trade-off between current and future reproduction often results in polymorphic populations in which some individuals put more emphasis on future fitness returns than others. Life-history theory predicts that such differences in fitness expectations should result in systematic differences in risk-taking behaviour. Individuals with high future expectations (who have much to lose) should be more risk-averse than individuals with low expectations. This applies to all kinds of risky situations, so individuals should consistently differ in their behaviour. By means of an evolutionary model we demonstrate that this basic principle results in the evolution of animal personalities. It simultaneously explains the coexistence of behavioural types, the consistency of behaviour through time and the structure of behavioural correlations across contexts. Moreover, it explains the common finding that explorative behaviour and risk-related traits like boldness and aggressiveness are common characteristics of animal personalities.

Animal personalities: consequences for ecology and evolution

Personality differences are a widespread phenomenon throughout the animal kingdom. Past research has focused on the characterization of such differences and a quest for their proximate and ultimate causation. However, the consequences of these differences for ecology and evolution received much less attention. Here, we strive to fill this gap by providing a comprehensive inventory of the potential implications of personality differences, ranging from population growth and persistence to species interactions and community dynamics, and covering issues such as social evolution, the speed of evolution, evolvability, and speciation. The emerging picture strongly suggests that personality differences matter for ecological and evolutionary processes (and their interaction) and, thus, should be considered a key dimension of ecologically and evolutionarily relevant intraspecific variation.

Evolutionary emergence of responsive and unresponsive personalities

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.

Recent models for adaptive personality differences: a review

In this paper we review recent models that provide adaptive explanations for animal personalities: individual differences in behaviour (or suites of correlated behaviours) that are consistent over time or contexts. We start by briefly discussing patterns of variation in behaviour that have been documented in natural populations. In the main part of the paper we discuss models for personality differences that (i) explain animal personalities as adaptive behavioural responses to differences in state, (ii) investigate how feedbacks between state and behaviour can stabilize initial differences among individuals and (iii) provide adaptive explanations for animal personalities that are not based on state differences. Throughout, we focus on two basic questions. First, what is the basic conceptual idea underlying the model? Second, what are the key assumptions and predictions of the model? We conclude by discussing empirical features of personalities that have not yet been addressed by formal modelling. While this paper is primarily intended to guide empiricists through current adaptive theory, thereby stimulating empirical tests of these models, we hope it also inspires theoreticians to address aspects of personalities that have received little attention up to now.

An explanatory framework for adaptive personality differences

We develop a conceptual framework for the understanding of animal personalities in terms of adaptive evolution. We focus on two basic questions. First, why do behavioural types exhibit limited behavioural plasticity, that is, behavioural correlations both across contexts and over time? Second, how can multiple behavioural types coexist within a single population? We emphasize differences in ‘state’ among individuals in combination with state-dependent behaviour. Some states are inherently stable and individual differences in such states can explain stable differences in suites of behaviour if it is adaptive to make behaviour in various contexts dependent on such states. Behavioural stability and cross-context correlations in behaviour are more difficult to explain if individual states are potentially more variable. In such cases stable personalities can result from state-dependent behaviour if state and behaviour mutually reinforce each other by feedback mechanisms. We discuss various evolutionary mechanisms for the maintenance of variation (in states and/or behaviour), including frequency-dependent selection, spatial variation with incomplete matching between habitat and phenotype, bet-hedging in a temporally fluctuating environment, and non-equilibrium dynamics. Although state differences are important, we also discuss how social conventions and social signalling can give rise to adaptive personality differences in the absence of state differences.

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.

On the coevolution of social responsiveness and behavioural consistency

Recent research focuses on animal personalities, that is individual differences in behaviour that are consistent across contexts and over time. From an adaptive perspective, such limited behavioural plasticity is surprising, since a more flexible structure of behaviour should provide a selective advantage. Here, we argue that consistency can be advantageous because it makes individuals predictable. Predictability, however, can only be advantageous if at least some individuals in the population respond to individual differences. Consequently, the evolution of consistency and responsiveness are mutually dependent. We present a general analysis of this coevolutionary feedback for scenarios that can be represented as matrix games with two pure strategies (e.g. hawk-dove game, snowdrift game). We first show that responsive strategies are favoured whenever some individual differences are present in the population (e.g. due to mutation and drift). We then show that the presence of responsive individuals can trigger a coevolutionary process between responsiveness and consistency that gives rise to populations in which responsive individuals coexist with unresponsive individuals who show high levels of adaptive consistency in their behaviour. Next to providing an adaptive explanation for consistency, our results also link two key features associated with personalities, individual differences in responsiveness and behavioural consistency.

The evolutionary and ecological consequences of animal social networks: emerging issues

The first generation of research on animal social networks was primarily aimed at introducing the concept of social networks to the fields of animal behaviour and behavioural ecology. More recently, a diverse body of evidence has shown that social fine structure matters on a broader scale than initially expected, affecting many key ecological and evolutionary processes. Here, we review this development. We discuss the effects of social network structure on evolutionary dynamics (genetic drift, fixation probabilities, and frequency-dependent selection) and social evolution (cooperation and between-individual behavioural differences). We discuss how social network structure can affect important coevolutionary processes (host-pathogen interactions and mutualisms) and population stability. We also discuss the potentially important, but poorly studied, role of social network structure on dispersal and invasion. Throughout, we highlight important areas for future research.

On the Evolution of Personalities via Frequency-Dependent Selection

Personality differences can be found in a wide range of species across the animal kingdom, but why natural selection gave rise to such differences remains an open question. Frequency-dependent selection is a potent mechanism explaining variation; it does not explain, however, the other two key features associated with personalities, consistency and correlations. Using the hawk-dove game and a frequency-dependent foraging game as examples, we here show that this changes fundamentally whenever one takes into account the physiological architecture underlying behavior (e.g., metabolism). We find that the inclusion of physiology changes the evolutionary predictions concerning consistency and correlations: while selection gives rise to inconsistent individuals and stochastically fluctuating behavioral correlations in scenarios that neglect physiology, we find high levels of behavioral consistency and tight and stable trait correlations in scenarios that incorporate physiology. The coevolution of behavioral and physiological traits also gives rise to adaptive physiological differences that are systematically associated with behavioral differences. As well as providing a framework for understanding behavioral consistency and behavioral correlations, our work thus also provides an explanation for systematic physiological differences within populations, a phenomenon that appears to exist in a wide range of species but that, up to now, has been poorly understood.

Why personality differences matter for social functioning and social structure

We outline three main ways how personality differences can affect social functioning and social structure. By highlighting the broad and significant consequences that personality differences can have for social processes, our article might serve as a starting point for a research focus that aims at a systematic understanding of these consequences.