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

Max Wolf, G. Sander van Doorn, Olof Leimar, Franz J. Weissing
2007 Nature  
In recent years evidence has been accumulating that personalities are not only found in humans 1 but also in a wide range of other animal species 2-8 . 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 [9] [10] [11] .
more » ... cordingly, many researchers view personalities as resulting from constraints imposed by the architecture of behaviour 7 (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 13 often results in polymorphic populations 14 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 15 . 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 2-8 . The phenomenon of animal personalities is one of the most intriguing challenges to the adaptationist programme in behavioural research. Empirical findings in more than 60 species, ranging from primates to ants, suggest that animal behaviour is much less flexible than previously thought 2-8 . Individuals consistently differ in whole suites of correlated behaviours and these differences are often heritable [16] [17] [18] [19] . At present, the existence of such personalities (also termed behavioural syndromes 20 , coping styles 5 or temperaments 21 ) is puzzling in several respects. First, why do different personality types stably coexist? Second, why is behaviour not more flexible but correlated across contexts and through time? And third, why are the same types of traits correlated in very different taxa 5-7 ? Here we develop an evolutionary model that provides answers to all of these questions. We start with the observation that some of the most prominent personality traits described in the literature can be categorized in terms of risk-taking behaviour. A good example is the correlation between aggressiveness towards conspecifics and boldness towards predators: individuals that risk more in intraspecific fights also risk more when confronted with a predator. This aggression-boldness syndrome has been described for many species 7 , including fish 22,23 , birds 8 and rodents 5 . From life-history theory it is known that individuals should adjust their risk-taking behaviour to their residual reproductive value 13, 15 , that is, their expected future fitness. Individuals with relatively high expectations should be relatively riskaverse, because they have to survive to realize those expectations. By the same reasoning, individuals with relatively low expectations should be relatively risk-prone because they have little to lose. Consequently, whenever individuals differ in their fitness expectations, we should expect stable individual differences and correlated behavioural traits: some individuals are consistently risk-prone whereas others are consistently risk-averse. By means of a simple model we now show that these intuitive arguments do indeed provide an evolutionary explanation for animal personalities. We proceed in three steps. First, we show that the trade-off between current and future reproduction can easily give rise to polymorphic populations in which some individuals put more emphasis on future reproduction than others. Second, we demonstrate that this variation in life-history strategies selects for systematic differences in risk-aversion. Third, we show that these differences in risk-taking behaviour extend to various risky situations and are stable over time, thereby giving rise to animal personalities. Consider the following stylized life history (Fig. 1a) . Individuals live for two years and reproduce at the end of each year. The foraging habitat is heterogeneous with both high-and low-quality resources. Individuals face a trade-off between reproduction in year 1 and reproduction in year 2 that is mediated by exploration behaviour. We characterize the exploration behaviour by the strategic variable x, which ranges from superficial (x~0) to thorough (x~1). Individuals that explore their environment thoroughly have a high probability of obtaining a high-quality resource in year 2. For simplicity, we let this probability correspond to x. Yet, the probability of reproducing in year 1, g(x), decreases with the intensity of exploration. Here we take g(x) 5 (1 2 x) The payoff from feeding on high-or low-quality resources declines with the density of individuals (N high or N low , respectively) competing for such resources. It is given by: for i 5high or low, where a . 0 represents the strength of competition and f high and f low (where f high . f low ) denote the intrinsic benefits of obtaining a high-and a low-quality resource, respectively. At the end of each year, individuals produce a number of offspring that is proportional to the payoff they obtained in that year. To summarize, an individual with exploration intensity x produces g(x)F low offspring at the end of its first year; at the end of its second year it produces F high offspring with probability x and F low offspring with probability 1{x.
doi:10.1038/nature05835 pmid:17538618 fatcat:6dyodi7n35ejhmsxowjckbjoxe