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Natural selection and animal personality Niels J. Dingemanse1,2) & Denis Réale3) (1 Animal Ecology Group, Centre for Evolutionary and Ecological Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands; 3 Canadian Research Chaire in Behavioural Ecology and Groupe de Recherche en Ecologie Comportementale et Animale, Département des Sciences Biologiques, Université du Québec à Montréal, CP-8888, Succursale Centre-ville, Montréal, Québec, H3C 3P, Canada) (Accepted: 1 February 2005) Summary Recent progress has been made on the study of personality in animals, both from a mechanistic and a functional perspective. While we start knowing more about the proximal mechanisms responsible for the consistent differences in behaviour between individuals in a population, little is known yet about the relationship between the phenotypic distribution of personality traits, or combinations of traits, and fitness. Here we provide an overview of the available literature on the fitness consequences of personality traits in natural populations. We start by a description of two case studies that have examined the role of natural selection on personality traits in the wild (i.e., the great tit, Parus major and bighorn sheep, Ovis canadensis), and review other studies that have reported some links between personality traits and fitness indices, in a large variety of animal species. We continue by outlining both direct approaches (i.e., measuring correlational selection on personality trait combinations) and indirect approaches (i.e., comparing correlations between personality traits within and between populations) to study suites of correlated traits from an adaptive perspective. This review, we hope, will be able to stimulate the use of the phenotypic selection analysis applied to the study of selection on personality traits in animals. Keywords: personality, behavioural syndromes, reproductive success, sexual selection, correlational selection, genetic constraints. Introduction Behavioural flexibility is often regarded to be unlimited, immediate, and reversible (Sih et al., 2004a, b), allowing individuals to maximize their fitness 2) Corresponding author’s e-mail address: [email protected] © Koninklijke Brill NV, Leiden, 2005 Behaviour 142, 1165-1190 Also available online - 1166 Dingemanse & Réale in the many different environments they encounter during life. Contrary to this notion of behavioural plasticity as the major adaptive cause of phenotypic variation in behaviour (Houston & McNamara, 1999; Dall et al., 2004; Neff & Sherman, 2004), animals often show very limited behavioural plasticity (Sih et al., 2004a, b) and commonly differ consistently in their reaction towards the same environmental stimuli (Clark & Ehlinger, 1987; Wilson et al., 1994; Boissy, 1995; Wilson, 1998; Gosling, 2001; Greenberg & MettkeHofmann, 2001). These individual differences in behaviour are, moreover, frequently expressed across a wide range of contexts and situations: individuals commonly differ consistently in whole suites of functionally-distinct behavioural traits (Sih et al., 2004a, b). For instance, in birds (Verbeek et al., 1996), rodents (Koolhaas et al., 2001), and fish (Huntingford, 1976), animals that are relatively aggressive towards conspecifics are also bolder in exploring novel environments and predators. These individual differences in suites of correlated traits have been named behavioural syndromes (Sih et al., 2004a, b), coping strategies (Koolhaas et al., 2001), temperament (Boissy, 1995; Clarke & Boinski, 1995) or animal personality traits (Buss, 1991; Gosling, 2001). The evolutionary origin and maintenance of phenotypic variation in animal personality is poorly understood (Stamps, 1991; Wilson et al., 1994; Wilson, 1998; Dingemanse et al., 2004; Dall et al., 2004; Sih et al., 2004a). Both mechanistic and functional approaches need to be applied to gain full understanding of why this behavioural variation persists (Stamps, 1991, 2003). The mechanistic approach seeks to evaluate how phenotypes result from the combined influences of genetic and environmental factors; the functional approach how the interaction between phenotypes and their environment affects fitness. Variation in personality has received considerable attention from the mechanistic viewpoint; the emerging pattern is that individual differences in single components of animal personality (e.g., aggressiveness) are moderately heritable and relatively stable over the entire life of the individual (Boissy, 1995; Koolhaas et al., 1999; Bouchard & Loehlin, 2001) and that phenotypic correlations between components of personality (e.g., between aggressiveness and boldness) often originate from strong underlying genetic correlations (Bakker, 1994; Bult & Lynch, 2000; van Oers et al., 2004a; Bell, 2005). In contrast, functional approaches towards understanding variation in personality have received far less attention (Réale & FestaBianchet, 2003; Dingemanse et al., 2004; Dall et al., 2004), despite the fact Natural selection and animal personality 1167 that only the combination of both approaches (in the same study system) will allow an informed evaluation of how behavioural traits might (co)evolve under different environmental conditions (Fisher, 1930; Endler, 1986). This paper has a three-fold aim. First, we aim to provide an overview of the available literature on the fitness consequences of personality traits in natural populations. In doing so, we largely concentrate our discussion on few study systems where both mechanistic and functional approaches have been applied to understand natural variation in personality, and where selection on behavioural phenotypes has been measured in all major life-history stages and over a number of years; thus providing first detailed descriptions of how and when natural selection may operate on animal personality traits. We further discuss examples of a range of study systems where selection on animal personality has been measured incompletely using short-term proxies for fitness only. We emphasize the importance of applying a holistic approach when studying animal personality from an adaptive perspective. Notably, various studies have addressed some (supposed) functional aspect of human personality, e.g., susceptibility to illness (Grossarthmaticek & Eysenck, 1990; Schmitz, 1992) or levels of stress hormones (Bruce et al., 2002), but direct links between personality and fitness have rarely been addressed (but see Eaves et al., 1990; Mealey & Segal, 1993; Wilson, 1994; Nettle et al., 2005). Our review thus focusses primarily on nonhuman animals. To date, the few available naturalistic studies have addressed the functional consequences of animal personality by describing how selection operates on single components of animal personality (e.g., exploratory behaviour of novel environments as a measure of ‘avian personality’ in great tits; Dingemanse et al., 2002). Our second aim is to point out that, ultimately, such studies cannot provide functional explanations for the existence of animal personality per se, as this would require insight in why individuals show consistency in their behaviour, either across time, generations, contexts or situations (Dall et al., 2004; Sih et al., 2004a). We outline both direct and indirect approaches to study suites of correlated traits from an adaptive perspective. Our third and last aim is to stimulate the use of the phenotypic selection approach (Lande & Arnold, 1983) when quantifying fitness consequences of animal personality, as this approach produces standardized estimates of the strength of selection that can directly be compared with those derived from other studies on the same or other types of traits (Kingsolver et al., 2001). 1168 Dingemanse & Réale Natural selection and personality Natural selection is measured by the covariance between traits and fitness (Endler, 1986), allowing one to estimate both the shape (Brodie et al., 1995) (i.e., directional, stabilizing, disruptive) and the strength of selection (Kingsolver et al., 2001), including patterns of selection on correlated characters (Lande, 1979; Lande & Arnold, 1983; Kingsolver et al., 2001) as well as correlational selection (selection for optimal trait combinations; Barton & Turelli, 1991). These estimation models thus provide a suitable method for studying selection on suites of correlated traits, like life-history syndromes or personality traits (Réale & Festa-Bianchet, 2003). When quantitative genetic parameters have also been quantified (i.e., heritability of and genetic correlations between components of personality traits), one can make an informed evaluation of the evolutionary consequences of the imposed selective regime (Falconer & Mackay, 1996; Roff, 1997; Lynch & Walsh, 1998), including the evolution of genetic correlations between behavioural traits (Roff, 1996), i.e., animal personality. Here we discuss the few yet available field studies on the fitness consequences of animal personality, with special reference to two study species in the wild, great tit (Parus major) and the bighorn sheep (Ovis canadensis), where both quantitative genetics parameters and fitness landscapes of animal personality have been quantified simultaneously and in natural populations, providing a first insight in the evolutionary potential of personality traits. Fitness consequences of personality in great tits Individual differences in suites of correlated traits Laboratory studies on hand-reared great tits showed that individuals differed in their reaction toward novel or challenging stimuli, comparable to how rodents differ in reactivity (Verbeek et al., 1994; Koolhaas et al., 2001; Groothuis & Carere, 2005). In these birds, speed of exploration of novel (laboratory) environments is positively correlated with aggressiveness towards conspecifics (Verbeek et al., 1996; Carere et al., in press), boldness towards novel objects (Verbeek et al., 1994), risk-taking (van Oers et al., 2004b, 2005a) and scrounging (Marchetti & Drent, 2000) during foraging, and stress responsiveness (Carere et al., 2001, 2003; Carere & van Oers, 2004). Two bi-directional selection experiments, the first on a combined score for exploration and boldness (‘early exploratory behaviour’; Drent et al., 2003) and Natural selection and animal personality 1169 the second on risk-taking behaviour (van Oers et al., 2004b), gave realized heritabilities of 0.54 and 0.19 respectively and evidence for a strong genetic correlation (0.84) between early exploratory behaviour and risk-taking under laboratory conditions (van Oers et al., 2004a). Repeatabilities (range: 0.270.66; Dingemanse et al., 2002) and narrow-sense heritabilities (0.34±0.13; Dingemanse et al., 2004) were considerably lower for wild great tits, suggesting that environmental factors (i.e., those controlled for in the laboratory) also influenced exploratory behaviour in the wild (Riska et al., 1989; see also Carere et al., 2005 for a discussion on environmental sources of variation in great tits). Alltogether, these quantitative genetics studies showed that great tits differ in suites of (genetically) correlated traits, with the extremes of the trait distribution (ranging from ‘slow’ to ‘fast’ exploratory behaviour) reflecting alternative behavioural strategies to cope with novel or challenging stimuli (Verbeek et al., 1994; Drent et al., 2003; Carere et al., in press). Relatively high levels of both additive and nonadditive genetic variance in early exploratory behaviour of laboratory-bred great tits (van Oers et al., 2004c) suggested a history of fluctuating selection pressures in this population (see van Oers et al., 2005b). Measuring personality of wild animals To quantify selection on avian personality in the wild, large numbers of wild great tits (1342 individuals between 1998-2002; N.J. Dingemanse, pers. comm.) were captured from a nest-box population in the Netherlands and transported to the laboratory where they were housed individually (Dingemanse et al., 2002). The following morning, exploratory behaviour was measured for each bird individually in a sealed room containing five artificial trees (following Verbeek et al., 1994), before the birds were released back in the wild at their individual place of capture. The total number of flights and hops within the first 2 mins were used as an index of their exploratory behaviour (Dingemanse et al., 2002). Exploratory behaviour was both repeatable and heritable (see above), and unrelated to age, body condition, or sex (Dingemanse et al., 2002). Subsequent field studies revealed that the fitness consequences of avian personality were complex (Figures 1, 2). Fitness consequences: adult annual survival Selection as measured by adult annual survival acted on exploratory behaviour (based on one test per individual), but the effects were always opposite 1170 Dingemanse & Réale Figure 1. Overview of the consequences of exploratory behaviour of wild adult great tits (Parus major) for two major fitness components (survival and production of recruits). Arrows represent measured (solid lines) or presumed (broken lines) direct or indirect relationships as based on the correlational studies discussed in the text. Symbols indicate the shape of linear (+: positive; −: negative) and non-linear (s: stabilising selection; d: disruptive selection) relationships. Notably, the relation between exploratory behaviour and offspring mass was variable (denoted ‘v’), as offspring body mass was a function of the interaction between the personality type of the individual and its mate. In cases where the consequences of exploratory behaviour differed between years or classes of individuals, the relationships have been given for each group separately (for more details see Figure 2). These descriptive studies suggested that fast-exploring adults survived relatively well in environments with intensified intra-sexual competition (ISC), but that they survived relatively poorly when ISC was relaxed, and that the overall shape of natural selection was stabilizing. For more details see the text. for males and females, and reversed between years (Figure 2; Dingemanse et al., 2004). In a year with masting of beeches Fagus sylvaticus (2000), when great tits experience relaxed competition for winter food (Perdeck et al., 2000), and subsequent high recruitment rates in spring (i.e., intensified competition for territorial space), fast-exploring adult males and slow-exploring adult females had highest survival. This pattern was reversed in two years (1999, 2001) with little winter food and subsequent low recruitment rates, when slow-exploring adult males and fast-exploring adult females had highest survival rates. Natural selection and animal personality 1171 Figure 2. Schematic overview of the fitness consequences of exploratory behaviour of novel environments (ranging from ‘slow’ to ‘fast’) in wild great tits (Parus major) for two types of years (poor [1999/2001] = no beech masting; rich [2000] = beech masting) (Dingemanse et al., 2004). The arrows indicate the shape of selection (→ directional selection favouring fast; ← directional selection favouring slow; →← stabilising; ←→ disruptive) for two main fitness components, adult annual survival and offspring recruitment, Hatched bars indicate nonsignificant trends. For more details see text. Temporal variability in environmental conditions Dingemanse et al. (2004) hypothesized that beech masting affected the strength of intra-sexual competition but that these effects were always opposite for territorial males and females (Figures 1, 2): because females were subordinate to males (Dingemanse & de Goede, 2004), they were likely to be most affected by competition for winter food. Beech masting therefore may result in relaxed intra-sexual competition among females, while competition is intensified in years without beech mast. As only males defend territories, they are likely to be most affected by competition for territorial space. In years with beech masting, recruitment rates are high (Perdeck et al., 2000), resulting in intensified intra-sexual competition among males (Both et al., 1999), while in non-beech mast years competition is relaxed. The complex patterns in adult survival (Figures 1, 2) may thus reflect that fast-exploring adults survived relatively well in years with intensified intra-sexual competition, and that they survived relatively poorly when competition was relaxed. Notably, the potential cause for the poor survival of fast-exploring adults in such years has not yet been identified. This notion of differential competitive ability was supported by the finding that fast-exploring adults dominated slow-exploring adults when competing for winter food (Dingemanse & de Goede, 2004) and that fast-exploring adults bred on the best breeding terri- 1172 Dingemanse & Réale tories (Both et al., 2005). Factors affecting adult survival are summarized in Figure 1. Between-year fluctuation in selection on personality traits in the great tits is similar to results from other studies on other types of traits (Merilä et al., 2001). This result indicates that selection studies should be performed on the long-term if we want to understand both the immediate consequences (within a year) and longer term effects (across several generations) of selection on populations. Fitness consequences: offspring production and recruitment Slow-exploring females had higher nest success (were more likely to produce at least one fledged offspring), and produced larger offspring than fastexploring females (Both et al., 2005). Pairs of assortative phenotypes, consisting of two slow partners or two fast partners, produced offspring with highest body mass in all years of the study (Both et al., 2005). Selection as measured by the number of these offspring that survived and bred in the study area (‘offspring recruitment’) acted on female, and to a lesser extent on male exploratory behaviour and fluctuated between years (Figure 2; Dingemanse et al., 2004). Selection on exploratory behaviour was stabilising in the two years without beech masting, but was disruptive in the year with beech masting. The personality of both the male and the female parent contributed to this pattern of disruptive selection, as pairs consisting of assorted partners (i.e., fast-fast or slow-slow pairs) produced most recruits in the beech crop year (Dingemanse et al., 2004). These assorted pairs also produced offspring of highest body mass (see above), and as body mass affects competitive ability and juvenile winter survival in years with intense competition for resources among juveniles (Both et al., 1999), this pattern of disruptive selection probably acted via offspring body mass in the year with beech crop. Interestingly, pairs of medium-exploring adults nevertheless produced most recruits in years without beech crop, suggesting that the higher than average offspring body mass of assortative pairs only increased fitness in certain years and that other characteristics of the offspring phentoype (e.g., their exploratory behaviour, see Figure 1) affected offspring recruitment. Fitness consequences: explaining variable patterns in offspring recruitment While these variable patterns in adult survival have now resulted in testable hypotheses, (i.e., fluctuating and sex-specific survival (Figure 2) reflected Natural selection and animal personality 1173 variable selection for competitive ability with sexes; Figure 1), sources of variation in offspring recruitment are not well understood (see question marks in Figure 1). As outlined above, the variance in offspring recruitment partly resulted from variation in parental breeding performance, but primarily in years with beech crop. Offspring recruitment patterns may also have been partly mediated directly via exploratory behaviour inherited from parents to offspring (e.g., by affecting offspring foraging success; Figure 1). Field studies showed that exploratory behaviour affects both competitive ability and settlement decisions of juveniles: fast-exploring juveniles had lowest dominance ranks when nonterritorial (Dingemanse & de Goede, 2004) and came to breed further from home (Dingemanse et al., 2003). Evolutionary consequences Natural selection acted on avian personality, but the direction of selection varied between sexes, age-classes and years with different selective regimes. Because exploratory behaviour of wild great tits is heritable (see above) and affects components of fitness, selection on avian personality can lead to evolutionary change (Fisher, 1930; Endler, 1986). While considering that the response to selection depends both on the frequency with which individuals experience different selective environments as well as the strength of selection in these environments (Figure 1), the overall pattern of selection turned out to be stabilising (Dingemanse et al., 2004): Adults of intermediate phenotype had highest offspring recruitment rates in most years, as masting of beeches occurs only about once every three years (Perdeck et al., 2000). Furthermore, the variance in adult survival was lowest for intermediate phenotypes, resulting in highest overall life expectancy. Taking these long-term fitness consequences into consideration, adult males may have maximized their fitness by means of adaptive mate choice: adult males of extreme phenotype were mated disassortatively with respect to personality type (Dingemanse et al., 2004), allowing them to produce offspring of intermediate phenotype and increase their lifetime fitness. Notably, disassortative mating seemed maladaptive when only considering that assortative pairs had highest reproductive success (Both et al., 2005). Temporal variability in selection as observed for this study system can slow down the loss of genetic variation in avian personality (Sasaki & Ellner, 1997; Burger & Gimelfarb, 2002), but it cannot, however, provide an ultimate explanation for the maintenance of genetic variation in avian personality. Either a balance between 1174 Dingemanse & Réale mutation, selection and migration in a spatially variable environment (Nevo, 1988; Frank & Slatkin, 1990) or frequency-dependent selection (Maynard Smith, 1982) probably need to be invoked to explain this behavioural diversity from an adaptive perspective (Dingemanse et al., 2004; Both et al., 2005). Similarly, we do yet need to reveal why individual great tits showed such limited behavioural plasticity, as behavioural flexibility seems adaptive in such a temporally variable environment (Dall, 2004). Fitness consequences of boldness and docility in bighorn sheep Individual differences in correlated behaviours In a wild Canadian population of bighorn sheep, individuals differed consistently in their willingness to enter corral traps baited with salt (Réale et al., 2000). This behavioural variability was assumed to reflect individual differences in boldness (i.e., willingness to take the risk involved in licking salt), where boldness was measured as the yearly number of times a ewe was captured in the trap. Repeatability (between years) and heritability estimates were 0.36 and 0.21 respectively. Ewes captured in the trap were also compared for their docility during handling: a docility score (based on a 7point scale) was used to measure how much individuals struggled during handling. Docility was highly repeatable both within (r = 0.65-0.66) and between years (r = 0.86); while some ewes were relatively docile, others struggled to escape. There was a negative — though weak — phenotypic correlation between boldness and docility: shy ewes were also relatively docile. This negative pattern appeared to be caused by the absence of shy, nondocile ewes. Estimation of quantitative genetics parameters using the ‘animal model’ (Lynch & Walsh, 1998) revealed significant heritabilities of both behaviours as well as a moderate negative genetic correlation between these behaviours (D. Reale & D. Coltman, unpubl. data). Fitness consequences: reproductive success Using standard multiple regression techniques to evaluate selection on correlated characters (Lande & Arnold, 1983), selection on each behaviour was measured independently of selection on the other (Réale et al., 2000; Réale & Festa-Bianchet, 2003). Selection measured with age at first reproduction as a fitness index acted both on boldness and docility (Réale et al., 2000). Bold ewes reproduced at an earlier age than shy ewes. Similarly, docile ewes Natural selection and animal personality 1175 tended to reproduce at an earlier age than nondocile ewes. Selection measured with weaning success (the number of lambs weaned between first reproduction and the end of the study) as fitness index acted on boldness only, with bold ewes having higher weaning success than shy ewes (Réale et al., 2000). Fitness consequence: adult annual survival Selection measured with adult annual survival as a fitness index acted both on boldness and docility, but the effects differed between years (Réale & Festa-Bianchet, 2003). In the first year of the study, with low predation by cougars Puma concolor, survival was high and unrelated to either age or boldness (docility was not yet measured). In both of the following two years, when predation by cougars was intense, survival rates dropped substantially and selection acted both on age and boldness. These two years, young or bold ewes survived better than old or shy ewes, respectively. In the second year with high predation, when docility was also measured, survival related also to docility and its interaction with age: survival was lowest for ewes that were both young and nondocile. In the fourth year of the study, when predation of cougars was again low, survival was again high and unrelated to either age, boldness, or docility. Evolutionary consequences As both boldness and docility were moderately heritable and genetically correlated (see above), the documented selective pressures acting on these traits could lead to evolutionary change (Fisher, 1930; Endler, 1986). While considering all major fitness components, boldness appeared to be under directional selection favouring bold ewes (Réale et al., 2000; Réale & FestaBianchet, 2003). Bold ewes started reproducing earlier in life, had highest reproductive output, and in years with cougar predation also had higher survival than shy ewes. Docility also appeared to be under directional selection, although the selection gradients were less steep (Réale et al., 2000; Réale & Festa-Bianchet, 2003): docility did not directly affect reproductive output, but docile ewes tended to start reproducing earlier in life than nondocile ewes, and survival selection in years with cougar predation favoured docile individuals among young ewes. As boldness and docility were negatively correlated, directional selection for bold ewes indirectly selects for nondocile 1176 Dingemanse & Réale ewes, and vice versa, directional selection for docile ewes indirectly selects for shy ewes. The negative genetic correlation between boldness and docility is thus likely to act as an evolutionary constraint by preventing both traits from evolving to their independent optimum, at the same time, however, providing a partial explanation for the persistence of genetic variation in both behavioural traits (Mangel & Stamps, 2001). Alternatively, the negative phenotypic and genetic correlations may have resulted from selection acting against ewes that show a combination of both high shyness and low docility. Unfortunately, because of sample size limitation, this study could not estimate correlational selection on boldness and docility in ewes. Fitness studies in other species Several field studies on other species have also shown a link between some personality traits and (usually single components of) fitness, though integrative studies as the ones described above are still rare. Here we give examples of documented naturalistic fitness studies on animal personality in a range of animal taxa. Fitness studies of personality in monkeys Another example illustrating the ecological importance of personality traits is the extensive studies on free-ranging and captive rhesus monkeys (Macaca mulatta). These studies have shown that many behavioural traits are related with the rate of turn-over of a neurotransmitter (serotonin: 5-HT) in the central nervous system, and affect individual fitness (Figure 3). First, cerebrospinal fluid concentration of 5-HIAA and other monoamine concentrations and associated behaviour expressions (e.g., impulsivity, aggressiveness) have been shown to be both repeatable and heritable in this species and other nonhuman primates (Clarke et al., 1995; Higley & Linnoila, 1997; Fairbanks et al., 2004). Young males with low 5-HIAA concentration are less often engaged in grooming and social activities (Mehlman et al., 1995), and more often involved in violent aggressive interactions (Mehlman et al., 1994) with their conspecifics than males with high 5-HIAA concentration. These males were also more often wounded and dispersed at an earlier age (Mehlman et al., 1994, 1995). The same phenomenon has been observed for low 5-HIAA females, which stay in their natal group but can hardly reach a high dominance rank (Higley et al., 1996a). Low 5-HIAA individuals Natural selection and animal personality 1177 Figure 3. Serotonin turn-over, behaviour, and fitness in rhesus monkeys (Macaca mulatta). Serotonin has been measured by the Cerebrospinal Fluid concentration of 5-hydroxyindolacetic acid (5-HIAA), a metabolite of serotonine (5-HT: 5-HydroxyTryptamin). Symbols indicate the shape of the relationship (+: positive; −: negative). For more details see text. also take more life threatening risks, such as leaping from treetop to treetop (Mehlman et al., 1994; Westergaard et al., 2003b). As a result, low 5-HIAA individuals are characterised by premature death (Higley et al., 1996b). CSF 5-HIAA concentration can also affect fitness, through its effects on reproductive behaviour. For example, low 5-HIAA males less often consort with oestrus females and are less often involved in heterosexual mounts and insemination (Mehlman et al., 1997), whereas low 5-HIAA females are more protective mothers and experience a higher rate of foetal and infant loss (Cleveland et al., 2003; Westergaard et al., 2003a). Considering all the evidence for selection favouring high 5-HIAA levels individuals over low level ones, Mehlman et al. (1997) questionned the mechanisms responsible for the maintenance of variation of these traits over time. Here we can provide two possible explanations: First, 5-HIAA concentration may be subject to correlational selection with other traits, which would allow the maintenance of genetic variation for each traits (see also examples on bighorn sheep and humans for a similar line of argumentation). Second, environmental conditions of the free-ranging and/or captive populations may differ strongly from natural environments, resulting in different selection pressures. For example, in a natural environment low 5-HIAA individuals might perform better when 1178 Dingemanse & Réale confronted with predators or when searching for new favourable habitats. This study on rhesus macaques is one of the most complete investigations of the link between a neurotransmitter, behaviour, life history and fitness. Fitness studies of boldness in freshwater fish Personality variation has received considerable attention in freshwater fish, started by a paper of Huntingford (1976) on the aggressiveness-boldness syndrome in three-spined stickleback (Gasterosteus aculeatus). In recent years, various studies have attempted to evaluate functional consequences of personality variation in fish. In Trinidad killifish (Rivulus hartii), individuals that were bold in exploration of novel environments dispersed furthest (for similar findings in other taxa see Dingemanse et al., 2003; Armitage & Van Vuren, 2003; Krakov, 2003) and had larger growth rates (Fraser et al., 2001). Laboratory studies on other species of freshwater fish have found similar results (Magnhagen & Staffan, 2003; Ward et al., 2004; Westerberg et al., 2004) and showed that bold fish grew quicker because of their competitive superiority in direct competition for food (Höjesjö et al., 2002; Ward et al., 2004; Sundström et al., 2004). A recent study on brown trout (Salmo trutta), however, underlined the importance of measuring fitness in various environments that individuals may encounter (Réale & Festa-Bianchet, 2003; Dingemanse et al., 2004), by showing that aggressive individuals had highest growth rates in simple habitats where food could easily be monopolised, but lowest growth rates in spatially complex habitats (Höjesjö et al., 2004). A capture-recapture study on wild brown trout further showed that survivorship did not differ between aggression phenotypes, suggesting that laboratory studies may only provide limited insight in the fitness consequences of animal personality in the wild (Höjesjö et al., 2002). Importantly, the evidence from field studies in other taxa (see above) suggests that different qualitative patterns of selection on personality traits may be shown when selection is measured using different fitness components (Réale & FestaBianchet, 2003; Dingemanse et al., 2004), implying that insight in the overall fitness landscapes of personality traits in fish can probably not be based on a single component of fitness. Fitness studies in captivity Fitness consequences of variation in personality have also been recorded in captivity and may have consequences for the conservation of captive stocks Natural selection and animal personality 1179 (McDougall et al., in press). For instance, a study done on black rhinoceros (Diceros bicornis) in 24 zoos has shown that in captivity females with lower chasing/stereotypy/mouthing behaviour have highest reproductive success (Carlstead et al., 1999). On the other hand, fear, docility, and activity (i.e., patrolling) were not significantly related to reproductive success. The same type of multizoo study has been conducted on 44 cheetahs (Acinonyx jubatus) (Wielebnowshi, 1999). In this study non-breeders were more fearful than breeders, but non-breeders did not differ in their activity or agressiveness from breeders. Studies on farmed fish also strongly suggest that selection can act on personality traits. Farmed stocks, characterized by intense competition for resources and relaxed predation pressure, are often bolder, take greater risks during foraging, and are more aggressive than their wild ancestors (Sundström et al., 2004; for a review see Huntingford & Adams, 2005). Personality and sexual selection Few studies have measured natural selection acting on personality traits, but even fewer have investigated the scope for a link between personality and sexual selection. As far as we know, there are only three studies (all laboratory studies) that examined this link. The first example comes from a study by Godin and Dugatkin (1996) on Trinidadian guppy (Poecilia reticulata), where bright males inspect predators more often than drab males (i.e., they are bolder) and females prefer bold males over shy ones, irrespective of their colour pattern. The second example comes from a study on mate preference in great tits from selection lines for early exploratory behaviour (Groothuis & Carere, 2005). In these birds, adult males of a selection line for ‘fast exploration’ (for details see Drent et al., 2003) showed higher rates of courtship display towards females of the fast-line compared to females of the slow-line; males of the slow-line, however, showed no preference for female personality (Groothuis & Carere, 2005). A third example comes from a recent study on a captive population of zebra finches (Taeniopygia guttata). In these birds, individual females differed in their preference for aggressive males due to nongenetic maternal effects (Forstmeier et al., 2004). Both bird studies show individual differences in preference for personality of sexual partners, highlighting that studies on personality and sexual selection should provide exciting results and therefore deserve more attention. 1180 Dingemanse & Réale Adaptive perspectives to study correlated behaviours Evidence for strong genetic correlations between behavioural traits in laboratory populations of birds (Drent et al., 2003; van Oers et al., 2004a), fish (Bakker & Sevenster, 1989; Bakker, 1994), and rodents (Sluyter et al., 1995; Koolhaas et al., 1999) suggests that behavioural traits are often structured in personality traits because they are controlled by the same hormones (Koolhaas et al., 1999; Ketterson & Nolan, 1999) or genes (Sih et al., 2004a, b). Personality traits have therefore often been proposed to act as evolutionary constraints (Sih et al., 2004a, b), because components of personality might be difficult to decouple (Loeschke, 1987; Ketterson & Nolan, 1999). The reason why whole suites of behavioural traits are often correlated has however, received very limited attention from a functional perspective (Wilson et al., 1994; Coleman & Wilson, 1998; Dall et al., 2004; Sih et al., 2004a; Bell, 2005). From an adaptionist’s viewpoint, correlations between behavioural traits are not necessarily set and if present should reflect adaptation to the environment (Roff, 1996; Wilson, 1998). Notably, all of the fitness studies reviewed in above section of this paper have measured selection acting on single behavioural traits, whereas functional explanations for personality variation (i.e., consistent individual differences in suites of correlated behavioural traits) would require insight in conditions favouring phenotypic (or genetic) correlations among behavioural traits. Here we discuss both direct and indirect approaches to study the adaptive nature of personality per se. Direct approaches: measuring correlational selection The adaptive nature of correlations between behavioural traits can be measured directly by using the phenotypic selection approach (Lande & Arnold, 1983), where fitness is measured as a function of both behaviour x, behaviour y (both measured on each individual) and their interaction (Figure 4). Here x and y could represent the same behaviour at different ontogenic stages, which would allow one to evaluate the adaptive nature of consistent individual differences in a single behavioural trait. X and y could also represent functionally-distinct behaviours, for instance aggressiveness and risk-taking behaviour, which would allow one to evaluate the adaptive nature of phenotypic correlations between traits. Knowledge of the fitness landscape would allow one to evaluate whether an observed association between x and y (i.e., Natural selection and animal personality 1181 Figure 4. Illustration of how multivariate fitness landscapes can help to evaluate whether correlations between behavioural traits would be adaptive. Dots represent all possible behavioural types (large dots have high fitness, small dots have low fitness). We show two behaviours (x and y) that could either represent the same type of trait in different situations (e.g., levels of activity in the absence vs presence of predators) or two functionally distinct traits (e.g., x = aggressiveness and y = risk-taking behaviour); (a) stabilising selection favours a single optimum and correlations between x and y would not be adaptive; (b-d) selection favours a range of behavioural types (i.e., there is more than one phenotype with high fitness), and the ‘ridge’ of high fitness (b-c) indicates that correlational selection favours a positive correlation between x and y. When considering only one behaviour in different situations, dots on the x = y line represent ‘inflexible’ (or stable) phenotypes, i.e., animals that show the same behaviour in both environments, and all other dots represent ‘flexible’ (or plastic) phenotypes. In that case, the fitness landscapes provide information on both adaptive individual differentiation (b-d but not a) and on adaptive behavioural flexibility (a, b, d but not c). For more details see the text. either positive, negative, or absent) is adaptive. For example, imagine a population where x and y are positively correlated. In the case of Figure 4a, selection favours a single optimal phenotype (large dot, scoring low on x and high on y). The observed positive correlation between x and y would thus not be adaptive. In contrast, in the case of positive correlational selection on x and y (as depicted by a ‘ridge’ of high fitness within the landscape; Figures 4b&c), a positive correlation between x and y would be adaptive. When x and y represent the same behaviour in different situations (e.g., activity in the presence vs absence of predators; Sih et al., 2003; Quinn & Creswell, 2005), the fitness landscape provides information not only on the adaptive nature of individual consistency but also on the adaptive nature of behavioural flexibility. For instance, in case 4a behavioural flexibility would be adaptive, as a single flexible phenotype has highest fitness. Situation 4a would thus correspond to what Sih et al. (2004b) have called a behavioural carry-over. Situation 4c illustrates a case where the higher fitness is associated with ‘inflexible’ phenotypes (i.e., selection favors constant behavioural phenotypes in both environments), whereas situation 4b illustrates a case 1182 Dingemanse & Réale of adaptive phenotypic plasticity or flexibility (selection favors an overall decrease in the trait between situation 1 and 2). Notably, if the fitness landscape would look like Figure 4d, selection would favour two distinct behavioural types (as suggested for coping behaviour in rodents; Koolhaas et al., 1999): one inflexible phenotype (upper-right large dot, scoring high on x and y) that does not adjust its behaviour in the different situations, and one flexible phenotype (lower-right large dot, scoring low on x and y) that changes its behaviour in the different situations. We know of only one study that has yet measured correlational selection (Barton & Turelli, 1991; Brodie et al., 1995) on personality traits. In their study on Australian women, Eaves et al. (1990) combined a survey of reproductive success of 1101 postmenopausal females with information on their personality using the Eysenck Personality Questionaire. They showed that the function relating fitness (measured as life time reproductive success) to neuroticism and extraversion was saddle-shaped, with the highest fitness for both the high-extravert/low-neurotic and low-extravert/highneurotic females, intermediate fitness for females that had intermediate scores on both axes, and lowest fitness for low-extravert/low neurotic and high-extravert/high-neurotic females. Their results thus showed that selection favoured a negative correlation between neuroticism and extraversion. We cannot emphasize enough that studies of correlational selection are crucial were we ever to understand personality variation from an adaptive perspective. Indirect approaches: studying correlations within and across populations Comparative approaches provide an alternative way to study the adaptive nature of behavioural correlations. The ‘genetic constraint models’ predict that correlations between traits should always be similar, irrespective of the environmental conditions, and that correlations between traits within populations should be similar to correlations on the population level (Lande, 1979). For instance, the constraint model would predict that if aggressiveness is positively correlated with boldness within populations, populations that are on average more aggressive should also be relatively bold. In its most extreme form (i.e., when the correlated behaviours are influenced by the same genes), the genetic constraint would be absolute. The ‘adaptive divergence models’ on the other hand predict that both correlations within and Natural selection and animal personality 1183 between populations should ultimately be a function of the selective environment (Lande, 1986). For instance, the adaptive divergence model would predict within-population behavioural correlations to be function of the environmental conditions, and would not necessarily predict within and between population correlations to be identical. Notably, even if a genetic correlation is adaptive in the current environment, it would still act as a short-term evolutionary constraint when environmental conditions change. Whereas the predictions of these models have often been tested for morphological traits, few studies have attempted to do the same for behavioural traits (but see Palmer & Dingle, 1986; Riechert & Hedrick, 1993; Bell, 2005). Support for the adaptive divergence model comes from recent work on threespined stickleback, where both phenotypic and genetic correlations between intraspecific aggressiveness and boldness towards predators differed between two populations (Bell, 2005). However, there are circumstances in which both models give the same predictions, particularly when selection favours the same correlation in all environments (Lande, 1979). Positive phenotypic correlations between intraspecific aggressiveness and anti-predator behaviour as documented for each of two populations of a spider (Agelenopsis aperta) (Riechert & Hedrick, 1993), can therefore not readily be interpreted. It should be argued here, that population differentiation in behavioural correlations does not necessarily imply adaptive divergence, and direct approaches are advisable at all times. What could be done next? Two main approaches are available to the study of personality and fitness: the first one is to consider a priori that some personality phenotypes are more fit than others in particular conditions, according to our intuition of the function of personality. This approach runs the risk of providing a ‘just so story’ about the function of personality trait. The second approach (i.e. the one that we strongly recommend) is to provide a scientific test of selection on personality traits, directly by looking at the link between fitness and the phenotypic variation of a personality trait, or of a set of traits, using the methods proposed by quantitative genetics (Lande & Arnold, 1983; Endler, 1986; Brodie et al., 1995; Kingsolver et al., 2001), or indirectly, by comparing correlations between several populations that experience different environments (Lande, 1979, 1986). Indeed, the studies that we reviewed here show 1184 Dingemanse & Réale that it is possible to provide evidence that in many circumstances personality can be subject to natural or sexual selection pressures, and thus illustrate the ecological importance of personality traits. Using this approach we could test adaptive hypotheses (Fairbairn & Reeve, 2001) provided by theoretical models (Dall et al., 2004). In the future, with the increase in the number of estimates on selection gradients (Lande & Arnold, 1983) on personality traits it will be possible to compare the strength of selection on those traits with other behaviour, and with life history or morphological traits (Kingsolver et al., 2001). This approach has another advantage: by questioning the existence, the strength, and the shape, of selection on personality traits we encourage the publication of results showing both evidence or the absence of evidence for selection on these traits, therefore allowing comparisons of selection patterns between personality traits and other types of traits. Until now, we have only been able to review cases where at least a significant relationship between phenotypic variation in one personality trait and fitness has been found. This may overemphasise the ecological importance of personality traits. Several adaptive hypotheses to explain the maintenance of variance of personality traits rely on particular assumptions regarding the selection pressures acting on those traits (e.g., correlational selection, frequencydependent selection, of environmental and temporal heterogeneity; see above). We would like to point out that these selection patterns could only be detected statistically with large sample sizes (Kingsolver et al., 2001), and therefore encourage studies testing the occurrence of selection on personality traits to try to collect data on a minimum of 100 individuals. Multivariate selection analyses, coupled with long term studies of selection in the wild (e.g., populations experiencing different environments; Fairbairn & Reeve, 2001), experimental modification of environmental conditions, and of phenotypic (co)variations (i.e., phenotypic engineering: Sinervo & Denardo, 1996; Ketterson & Nolan, 1999), will allow us to examine the generality of evolutionary mechanisms shaping the distribution of personality traits and their covariation in animals and humans. Acknowledgements Denis Réale was supported by a grant from the Natural Sciences and Engineering Research Council of Canada. 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