Natural selection and animal personalitybehav.zoology.unibe.ch/sysuif/uploads/files/esh/pdf_online/ws/Dinge... · Natural selection and animal personality 1163 the second on risk-taking

Natural selection and animal personality

Niels J Dingemanse12) amp Denis Reacuteale3)

(1 Animal Ecology Group Centre for Evolutionary and Ecological Studies University ofGroningen PO Box 14 9750 AA Haren The Netherlands 3 Canadian Research Chaire inBehavioural Ecology and Groupe de Recherche en Ecologie Comportementale et Animale

Deacutepartement des Sciences Biologiques Universiteacute du Queacutebec agrave Montreacuteal CP-8888Succursale Centre-ville Montreacuteal Queacutebec H3C 3P Canada)

(Accepted 1 February 2005)

Summary

Recent progress has been made on the study of personality in animals both from a mecha-nistic and a functional perspective While we start knowing more about the proximal mech-anisms responsible for the consistent differences in behaviour between individuals in a pop-ulation little is known yet about the relationship between the phenotypic distribution of per-sonality traits or combinations of traits and fitness Here we provide an overview of theavailable literature on the fitness consequences of personality traits in natural populationsWe start by a description of two case studies that have examined the role of natural selec-tion on personality traits in the wild (ie the great tit Parus major and bighorn sheep Oviscanadensis) and review other studies that have reported some links between personality traitsand fitness indices in a large variety of animal species We continue by outlining both directapproaches (ie measuring correlational selection on personality trait combinations) and in-direct approaches (ie comparing correlations between personality traits within and betweenpopulations) to study suites of correlated traits from an adaptive perspective This reviewwe hope will be able to stimulate the use of the phenotypic selection analysis applied to thestudy of selection on personality traits in animals

Keywords personality behavioural syndromes reproductive success sexual selection corre-lational selection genetic constraints

Introduction

Behavioural flexibility is often regarded to be unlimited immediate and re-versible (Sih et al 2004a b) allowing individuals to maximize their fitness

2) Corresponding authorrsquos e-mail address njdingemanserugnl

copy Koninklijke Brill NV Leiden 2005 Behaviour 142 1159-1184Also available online -

1160 Dingemanse amp Reacuteale

in the many different environments they encounter during life Contrary tothis notion of behavioural plasticity as the major adaptive cause of pheno-typic variation in behaviour (Houston amp McNamara 1999 Dall et al 2004Neff amp Sherman 2004) animals often show very limited behavioural plas-ticity (Sih et al 2004a b) and commonly differ consistently in their reactiontowards the same environmental stimuli (Clark amp Ehlinger 1987 Wilson etal 1994 Boissy 1995 Wilson 1998 Gosling 2001 Greenberg amp Mettke-Hofmann 2001) These individual differences in behaviour are moreoverfrequently expressed across a wide range of contexts and situations indi-viduals commonly differ consistently in whole suites of functionally-distinctbehavioural traits (Sih et al 2004a b) For instance in birds (Verbeek etal 1996) rodents (Koolhaas et al 2001) and fish (Huntingford 1976) an-imals that are relatively aggressive towards conspecifics are also bolder inexploring novel environments and predators These individual differences insuites of correlated traits have been named behavioural syndromes (Sih et al2004a b) coping strategies (Koolhaas et al 2001) temperament (Boissy1995 Clarke amp Boinski 1995) or animal personality traits (Buss 1991Gosling 2001)

The evolutionary origin and maintenance of phenotypic variation in an-imal personality is poorly understood (Stamps 1991 Wilson et al 1994Wilson 1998 Dingemanse et al 2004 Dall et al 2004 Sih et al 2004a)Both mechanistic and functional approaches need to be applied to gain fullunderstanding of why this behavioural variation persists (Stamps 19912003) The mechanistic approach seeks to evaluate how phenotypes resultfrom the combined influences of genetic and environmental factors the func-tional approach how the interaction between phenotypes and their environ-ment affects fitness Variation in personality has received considerable atten-tion from the mechanistic viewpoint the emerging pattern is that individualdifferences in single components of animal personality (eg aggressiveness)are moderately heritable and relatively stable over the entire life of the in-dividual (Boissy 1995 Koolhaas et al 1999 Bouchard amp Loehlin 2001)and that phenotypic correlations between components of personality (egbetween aggressiveness and boldness) often originate from strong underly-ing genetic correlations (Bakker 1994 Bult amp Lynch 2000 van Oers et al2004a Bell 2005) In contrast functional approaches towards understand-ing variation in personality have received far less attention (Reacuteale amp Festa-Bianchet 2003 Dingemanse et al 2004 Dall et al 2004) despite the fact

Natural selection and animal personality 1161

that only the combination of both approaches (in the same study system) willallow an informed evaluation of how behavioural traits might (co)evolve un-der different environmental conditions (Fisher 1930 Endler 1986)

This paper has a three-fold aim First we aim to provide an overview ofthe available literature on the fitness consequences of personality traits in nat-ural populations In doing so we largely concentrate our discussion on fewstudy systems where both mechanistic and functional approaches have beenapplied to understand natural variation in personality and where selection onbehavioural phenotypes has been measured in all major life-history stagesand over a number of years thus providing first detailed descriptions of howand when natural selection may operate on animal personality traits We fur-ther discuss examples of a range of study systems where selection on animalpersonality has been measured incompletely using short-term proxies forfitness only We emphasize the importance of applying a holistic approachwhen studying animal personality from an adaptive perspective Notablyvarious studies have addressed some (supposed) functional aspect of hu-man personality eg susceptibility to illness (Grossarthmaticek amp Eysenck1990 Schmitz 1992) or levels of stress hormones (Bruce et al 2002) butdirect links between personality and fitness have rarely been addressed (butsee Eaves et al 1990 Mealey amp Segal 1993 Wilson 1994 Nettle et al2005) Our review thus focusses primarily on nonhuman animals

To date the few available naturalistic studies have addressed the func-tional consequences of animal personality by describing how selection op-erates on single components of animal personality (eg exploratory behav-iour of novel environments as a measure of lsquoavian personalityrsquo in great titsDingemanse et al 2002) Our second aim is to point out that ultimatelysuch studies cannot provide functional explanations for the existence of ani-mal personality per se as this would require insight in why individuals showconsistency in their behaviour either across time generations contexts orsituations (Dall et al 2004 Sih et al 2004a) We outline both direct andindirect approaches to study suites of correlated traits from an adaptive per-spective

Our third and last aim is to stimulate the use of the phenotypic selectionapproach (Lande amp Arnold 1983) when quantifying fitness consequences ofanimal personality as this approach produces standardized estimates of thestrength of selection that can directly be compared with those derived fromother studies on the same or other types of traits (Kingsolver et al 2001)


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)(ie directional stabilizing disruptive) and the strength of selection (King-solver et al 2001) including patterns of selection on correlated characters(Lande 1979 Lande amp Arnold 1983 Kingsolver et al 2001) as well ascorrelational selection (selection for optimal trait combinations Barton ampTurelli 1991) These estimation models thus provide a suitable method forstudying selection on suites of correlated traits like life-history syndromes orpersonality traits (Reacuteale amp Festa-Bianchet 2003) When quantitative geneticparameters have also been quantified (ie heritability of and genetic correla-tions between components of personality traits) one can make an informedevaluation of the evolutionary consequences of the imposed selective regime(Falconer amp Mackay 1996 Roff 1997 Lynch amp Walsh 1998) includingthe evolution of genetic correlations between behavioural traits (Roff 1996)ie animal personality Here we discuss the few yet available field studieson the fitness consequences of animal personality with special reference totwo study species in the wild great tit (Parus major) and the bighorn sheep(Ovis canadensis) where both quantitative genetics parameters and fitnesslandscapes of animal personality have been quantified simultaneously and innatural populations providing a first insight in the evolutionary potential ofpersonality 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 dif-fered in their reaction toward novel or challenging stimuli comparable tohow rodents differ in reactivity (Verbeek et al 1994 Koolhaas et al 2001Groothuis amp Carere 2005) In these birds speed of exploration of novel (lab-oratory) environments is positively correlated with aggressiveness towardsconspecifics (Verbeek et al 1996 Carere et al in press) boldness towardsnovel objects (Verbeek et al 1994) risk-taking (van Oers et al 2004b2005a) and scrounging (Marchetti amp Drent 2000) during foraging and stressresponsiveness (Carere et al 2001 2003 Carere amp van Oers 2004) Twobi-directional selection experiments the first on a combined score for explo-ration and boldness (lsquoearly exploratory behaviourrsquo Drent et al 2003) and


the second on risk-taking behaviour (van Oers et al 2004b) gave realizedheritabilities of 054 and 019 respectively and evidence for a strong geneticcorrelation (084) between early exploratory behaviour and risk-taking underlaboratory conditions (van Oers et al 2004a) Repeatabilities (range 027-066 Dingemanse et al 2002) and narrow-sense heritabilities (034plusmn013Dingemanse et al 2004) were considerably lower for wild great tits sug-gesting that environmental factors (ie those controlled for in the laboratory)also influenced exploratory behaviour in the wild (Riska et al 1989 see alsoCarere et al 2005 for a discussion on environmental sources of variation ingreat tits) Alltogether these quantitative genetics studies showed that greattits differ in suites of (genetically) correlated traits with the extremes of thetrait distribution (ranging from lsquoslowrsquo to lsquofastrsquo exploratory behaviour) re-flecting alternative behavioural strategies to cope with novel or challengingstimuli (Verbeek et al 1994 Drent et al 2003 Carere et al in press) Rel-atively high levels of both additive and nonadditive genetic variance in earlyexploratory behaviour of laboratory-bred great tits (van Oers et al 2004c)suggested a history of fluctuating selection pressures in this population (seevan Oers et al 2005b)

Measuring personality of wild animals

To quantify selection on avian personality in the wild large numbers ofwild great tits (1342 individuals between 1998-2002 NJ Dingemanse perscomm) were captured from a nest-box population in the Netherlands andtransported to the laboratory where they were housed individually (Dinge-manse et al 2002) The following morning exploratory behaviour was mea-sured for each bird individually in a sealed room containing five artificialtrees (following Verbeek et al 1994) before the birds were released backin the wild at their individual place of capture The total number of flightsand hops within the first 2 mins were used as an index of their exploratorybehaviour (Dingemanse et al 2002) Exploratory behaviour was both repeat-able and heritable (see above) and unrelated to age body condition or sex(Dingemanse et al 2002) Subsequent field studies revealed that the fitnessconsequences of avian personality were complex (Figures 1 2)

Fitness consequences adult annual survival

Selection as measured by adult annual survival acted on exploratory behav-iour (based on one test per individual) but the effects were always opposite


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) Arrowsrepresent measured (solid lines) or presumed (broken lines) direct or indirect relationships asbased on the correlational studies discussed in the text Symbols indicate the shape of linear(+ positive minus negative) and non-linear (s stabilising selection d disruptive selection)relationships Notably the relation between exploratory behaviour and offspring mass wasvariable (denoted lsquovrsquo) as offspring body mass was a function of the interaction betweenthe personality type of the individual and its mate In cases where the consequences ofexploratory behaviour differed between years or classes of individuals the relationships havebeen given for each group separately (for more details see Figure 2) These descriptive studiessuggested that fast-exploring adults survived relatively well in environments with intensifiedintra-sexual competition (ISC) but that they survived relatively poorly when ISC was relaxedand 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 etal 2004) In a year with masting of beeches Fagus sylvaticus (2000) whengreat tits experience relaxed competition for winter food (Perdeck et al2000) and subsequent high recruitment rates in spring (ie intensified com-petition for territorial space) fast-exploring adult males and slow-exploringadult females had highest survival This pattern was reversed in two years(1999 2001) with little winter food and subsequent low recruitment rateswhen slow-exploring adult males and fast-exploring adult females had high-est survival rates


Figure 2 Schematic overview of the fitness consequences of exploratory behaviour ofnovel environments (ranging from lsquoslowrsquo to lsquofastrsquo) in wild great tits (Parus major) for twotypes of years (poor [19992001] = no beech masting rich [2000] = beech masting) (Dinge-manse et al 2004) The arrows indicate the shape of selection (rarr directional selectionfavouring fast larr directional selection favouring slow rarrlarr stabilising larrrarr 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 thestrength of intra-sexual competition but that these effects were always op-posite for territorial males and females (Figures 1 2) because females weresubordinate to males (Dingemanse amp de Goede 2004) they were likely to bemost affected by competition for winter food Beech masting therefore mayresult in relaxed intra-sexual competition among females while competitionis intensified in years without beech mast As only males defend territoriesthey are likely to be most affected by competition for territorial space Inyears with beech masting recruitment rates are high (Perdeck et al 2000)resulting in intensified intra-sexual competition among males (Both et al1999) while in non-beech mast years competition is relaxed The complexpatterns in adult survival (Figures 1 2) may thus reflect that fast-exploringadults survived relatively well in years with intensified intra-sexual competi-tion and that they survived relatively poorly when competition was relaxedNotably the potential cause for the poor survival of fast-exploring adultsin such years has not yet been identified This notion of differential competi-tive ability was supported by the finding that fast-exploring adults dominatedslow-exploring adults when competing for winter food (Dingemanse amp deGoede 2004) and that fast-exploring adults bred on the best breeding terri-


tories (Both et al 2005) Factors affecting adult survival are summarized inFigure 1

Between-year fluctuation in selection on personality traits in the great titsis similar to results from other studies on other types of traits (Merilauml et al2001) This result indicates that selection studies should be performed on thelong-term if we want to understand both the immediate consequences (withina year) and longer term effects (across several generations) of selection onpopulations

Fitness consequences offspring production and recruitment

Slow-exploring females had higher nest success (were more likely to pro-duce at least one fledged offspring) and produced larger offspring than fast-exploring females (Both et al 2005) Pairs of assortative phenotypes con-sisting of two slow partners or two fast partners produced offspring withhighest body mass in all years of the study (Both et al 2005) Selectionas measured by the number of these offspring that survived and bred in thestudy area (lsquooffspring recruitmentrsquo) acted on female and to a lesser extent onmale exploratory behaviour and fluctuated between years (Figure 2 Dinge-manse et al 2004) Selection on exploratory behaviour was stabilising in thetwo years without beech masting but was disruptive in the year with beechmasting The personality of both the male and the female parent contributedto this pattern of disruptive selection as pairs consisting of assorted part-ners (ie fast-fast or slow-slow pairs) produced most recruits in the beechcrop year (Dingemanse et al 2004) These assorted pairs also produced off-spring of highest body mass (see above) and as body mass affects competi-tive ability and juvenile winter survival in years with intense competition forresources among juveniles (Both et al 1999) this pattern of disruptive se-lection probably acted via offspring body mass in the year with beech cropInterestingly pairs of medium-exploring adults nevertheless produced mostrecruits in years without beech crop suggesting that the higher than aver-age offspring body mass of assortative pairs only increased fitness in certainyears and that other characteristics of the offspring phentoype (eg theirexploratory 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 testablehypotheses (ie fluctuating and sex-specific survival (Figure 2) reflected


variable selection for competitive ability with sexes Figure 1) sources ofvariation in offspring recruitment are not well understood (see questionmarks in Figure 1) As outlined above the variance in offspring recruit-ment partly resulted from variation in parental breeding performance butprimarily in years with beech crop Offspring recruitment patterns mayalso have been partly mediated directly via exploratory behaviour inheritedfrom parents to offspring (eg by affecting offspring foraging success Fig-ure 1) Field studies showed that exploratory behaviour affects both compet-itive ability and settlement decisions of juveniles fast-exploring juvenileshad lowest dominance ranks when nonterritorial (Dingemanse amp de Goede2004) and came to breed further from home (Dingemanse et al 2003)

Evolutionary consequences

Natural selection acted on avian personality but the direction of selectionvaried between sexes age-classes and years with different selective regimesBecause exploratory behaviour of wild great tits is heritable (see above) andaffects components of fitness selection on avian personality can lead to evo-lutionary change (Fisher 1930 Endler 1986) While considering that theresponse to selection depends both on the frequency with which individ-uals experience different selective environments as well as the strength ofselection in these environments (Figure 1) the overall pattern of selectionturned out to be stabilising (Dingemanse et al 2004) Adults of interme-diate phenotype had highest offspring recruitment rates in most years asmasting of beeches occurs only about once every three years (Perdeck et al2000) Furthermore the variance in adult survival was lowest for interme-diate phenotypes resulting in highest overall life expectancy Taking theselong-term fitness consequences into consideration adult males may havemaximized their fitness by means of adaptive mate choice adult males ofextreme phenotype were mated disassortatively with respect to personalitytype (Dingemanse et al 2004) allowing them to produce offspring of inter-mediate phenotype and increase their lifetime fitness Notably disassortativemating seemed maladaptive when only considering that assortative pairs hadhighest reproductive success (Both et al 2005) Temporal variability in se-lection as observed for this study system can slow down the loss of geneticvariation in avian personality (Sasaki amp Ellner 1997 Burger amp Gimelfarb2002) but it cannot however provide an ultimate explanation for the main-tenance of genetic variation in avian personality Either a balance between


mutation selection and migration in a spatially variable environment (Nevo1988 Frank amp Slatkin 1990) or frequency-dependent selection (MaynardSmith 1982) probably need to be invoked to explain this behavioural di-versity from an adaptive perspective (Dingemanse et al 2004 Both et al2005) Similarly we do yet need to reveal why individual great tits showedsuch limited behavioural plasticity as behavioural flexibility seems adaptivein 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 con-sistently in their willingness to enter corral traps baited with salt (Reacuteale etal 2000) This behavioural variability was assumed to reflect individual dif-ferences in boldness (ie willingness to take the risk involved in lickingsalt) where boldness was measured as the yearly number of times a ewewas captured in the trap Repeatability (between years) and heritability esti-mates were 036 and 021 respectively Ewes captured in the trap were alsocompared for their docility during handling a docility score (based on a 7-point scale) was used to measure how much individuals struggled duringhandling Docility was highly repeatable both within (r = 065-066) andbetween years (r = 086) while some ewes were relatively docile othersstruggled to escape There was a negative mdash though weak mdash phenotypic cor-relation between boldness and docility shy ewes were also relatively docileThis negative pattern appeared to be caused by the absence of shy non-docile ewes Estimation of quantitative genetics parameters using the lsquoani-mal modelrsquo (Lynch amp Walsh 1998) revealed significant heritabilities of bothbehaviours as well as a moderate negative genetic correlation between thesebehaviours (D Reale amp D Coltman unpubl data)

Fitness consequences reproductive success

Using standard multiple regression techniques to evaluate selection on cor-related characters (Lande amp Arnold 1983) selection on each behaviour wasmeasured independently of selection on the other (Reacuteale et al 2000 Reacutealeamp Festa-Bianchet 2003) Selection measured with age at first reproductionas a fitness index acted both on boldness and docility (Reacuteale et al 2000)Bold ewes reproduced at an earlier age than shy ewes Similarly docile ewes


tended to reproduce at an earlier age than nondocile ewes Selection mea-sured with weaning success (the number of lambs weaned between first re-production and the end of the study) as fitness index acted on boldness onlywith bold ewes having higher weaning success than shy ewes (Reacuteale et al2000)

Fitness consequence adult annual survival

Selection measured with adult annual survival as a fitness index acted bothon boldness and docility but the effects differed between years (Reacuteale ampFesta-Bianchet 2003) In the first year of the study with low predation bycougars Puma concolor survival was high and unrelated to either age orboldness (docility was not yet measured) In both of the following two yearswhen predation by cougars was intense survival rates dropped substantiallyand selection acted both on age and boldness These two years young orbold ewes survived better than old or shy ewes respectively In the secondyear with high predation when docility was also measured survival relatedalso to docility and its interaction with age survival was lowest for ewesthat were both young and nondocile In the fourth year of the study whenpredation of cougars was again low survival was again high and unrelated toeither age boldness or docility


As both boldness and docility were moderately heritable and genetically cor-related (see above) the documented selective pressures acting on these traitscould lead to evolutionary change (Fisher 1930 Endler 1986) While con-sidering all major fitness components boldness appeared to be under di-rectional selection favouring bold ewes (Reacuteale et al 2000 Reacuteale amp Festa-Bianchet 2003) Bold ewes started reproducing earlier in life had highestreproductive output and in years with cougar predation also had higher sur-vival than shy ewes Docility also appeared to be under directional selectionalthough the selection gradients were less steep (Reacuteale et al 2000 Reacutealeamp Festa-Bianchet 2003) docility did not directly affect reproductive out-put but docile ewes tended to start reproducing earlier in life than nondocileewes and survival selection in years with cougar predation favoured docileindividuals among young ewes As boldness and docility were negativelycorrelated directional selection for bold ewes indirectly selects for nondocile


ewes and vice versa directional selection for docile ewes indirectly selectsfor shy ewes The negative genetic correlation between boldness and docilityis thus likely to act as an evolutionary constraint by preventing both traitsfrom evolving to their independent optimum at the same time howeverproviding a partial explanation for the persistence of genetic variation inboth behavioural traits (Mangel amp Stamps 2001) Alternatively the nega-tive phenotypic and genetic correlations may have resulted from selectionacting against ewes that show a combination of both high shyness and lowdocility Unfortunately because of sample size limitation this study couldnot 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 somepersonality traits and (usually single components of) fitness though integra-tive studies as the ones described above are still rare Here we give examplesof documented naturalistic fitness studies on animal personality in a range ofanimal taxa

Fitness studies of personality in monkeys

Another example illustrating the ecological importance of personality traitsis the extensive studies on free-ranging and captive rhesus monkeys (Macacamulatta) These studies have shown that many behavioural traits are re-lated with the rate of turn-over of a neurotransmitter (serotonin 5-HT) inthe central nervous system and affect individual fitness (Figure 3) Firstcerebrospinal fluid concentration of 5-HIAA and other monoamine concen-trations and associated behaviour expressions (eg impulsivity aggressive-ness) have been shown to be both repeatable and heritable in this speciesand other nonhuman primates (Clarke et al 1995 Higley amp Linnoila 1997Fairbanks et al 2004) Young males with low 5-HIAA concentration areless often engaged in grooming and social activities (Mehlman et al 1995)and more often involved in violent aggressive interactions (Mehlman et al1994) with their conspecifics than males with high 5-HIAA concentrationThese males were also more often wounded and dispersed at an earlier age(Mehlman et al 1994 1995) The same phenomenon has been observedfor low 5-HIAA females which stay in their natal group but can hardlyreach a high dominance rank (Higley et al 1996a) Low 5-HIAA individuals


Figure 3 Serotonin turn-over behaviour and fitness in rhesus monkeys (Macaca mu-latta) Serotonin has been measured by the Cerebrospinal Fluid concentration of 5-hydroxy-indolacetic acid (5-HIAA) a metabolite of serotonine (5-HT 5-HydroxyTryptamin) Sym-bols indicate the shape of the relationship (+ positive minus 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-HIAAindividuals are characterised by premature death (Higley et al 1996b) CSF5-HIAA concentration can also affect fitness through its effects on repro-ductive behaviour For example low 5-HIAA males less often consort withoestrus females and are less often involved in heterosexual mounts and in-semination (Mehlman et al 1997) whereas low 5-HIAA females are moreprotective mothers and experience a higher rate of foetal and infant loss(Cleveland et al 2003 Westergaard et al 2003a) Considering all the evi-dence for selection favouring high 5-HIAA levels individuals over low levelones Mehlman et al (1997) questionned the mechanisms responsible for themaintenance of variation of these traits over time Here we can provide twopossible explanations First 5-HIAA concentration may be subject to cor-relational selection with other traits which would allow the maintenance ofgenetic variation for each traits (see also examples on bighorn sheep and hu-mans for a similar line of argumentation) Second environmental conditionsof the free-ranging andor captive populations may differ strongly from nat-ural environments resulting in different selection pressures For example ina natural environment low 5-HIAA individuals might perform better when


confronted with predators or when searching for new favourable habitatsThis study on rhesus macaques is one of the most complete investigations ofthe link between a neurotransmitter behaviour life history and fitness

Fitness studies of boldness in freshwater fish

Personality variation has received considerable attention in freshwater fishstarted by a paper of Huntingford (1976) on the aggressiveness-boldness syn-drome in three-spined stickleback (Gasterosteus aculeatus) In recent yearsvarious studies have attempted to evaluate functional consequences of per-sonality variation in fish In Trinidad killifish (Rivulus hartii) individualsthat were bold in exploration of novel environments dispersed furthest (forsimilar findings in other taxa see Dingemanse et al 2003 Armitage amp VanVuren 2003 Krakov 2003) and had larger growth rates (Fraser et al 2001)Laboratory studies on other species of freshwater fish have found similarresults (Magnhagen amp Staffan 2003 Ward et al 2004 Westerberg et al2004) and showed that bold fish grew quicker because of their competitivesuperiority in direct competition for food (Houmljesjouml et al 2002 Ward et al2004 Sundstroumlm et al 2004) A recent study on brown trout (Salmo trutta)however underlined the importance of measuring fitness in various envi-ronments that individuals may encounter (Reacuteale amp Festa-Bianchet 2003Dingemanse et al 2004) by showing that aggressive individuals had high-est growth rates in simple habitats where food could easily be monopolisedbut lowest growth rates in spatially complex habitats (Houmljesjouml et al 2004)A capture-recapture study on wild brown trout further showed that survivor-ship did not differ between aggression phenotypes suggesting that labora-tory studies may only provide limited insight in the fitness consequences ofanimal personality in the wild (Houmljesjouml et al 2002) Importantly the ev-idence from field studies in other taxa (see above) suggests that differentqualitative patterns of selection on personality traits may be shown whenselection is measured using different fitness components (Reacuteale amp Festa-Bianchet 2003 Dingemanse et al 2004) implying that insight in the over-all fitness landscapes of personality traits in fish can probably not be basedon a single component of fitness

Fitness studies in captivity

Fitness consequences of variation in personality have also been recorded incaptivity and may have consequences for the conservation of captive stocks


(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 lowerchasingstereotypymouthing behaviour have highest reproductive success(Carlstead et al 1999) On the other hand fear docility and activity (iepatrolling) were not significantly related to reproductive success The sametype of multizoo study has been conducted on 44 cheetahs (Acinonyx ju-batus) (Wielebnowshi 1999) In this study non-breeders were more fearfulthan breeders but non-breeders did not differ in their activity or agressive-ness from breeders Studies on farmed fish also strongly suggest that selec-tion can act on personality traits Farmed stocks characterized by intensecompetition for resources and relaxed predation pressure are often boldertake greater risks during foraging and are more aggressive than their wildancestors (Sundstroumlm et al 2004 for a review see Huntingford amp Adams2005)

Personality and sexual selection

Few studies have measured natural selection acting on personality traits buteven fewer have investigated the scope for a link between personality andsexual selection As far as we know there are only three studies (all lab-oratory studies) that examined this link The first example comes from astudy by Godin and Dugatkin (1996) on Trinidadian guppy (Poecilia reticu-lata) where bright males inspect predators more often than drab males (iethey are bolder) and females prefer bold males over shy ones irrespectiveof their colour pattern The second example comes from a study on matepreference in great tits from selection lines for early exploratory behaviour(Groothuis amp Carere 2005) In these birds adult males of a selection linefor lsquofast explorationrsquo (for details see Drent et al 2003) showed higher ratesof courtship display towards females of the fast-line compared to females ofthe slow-line males of the slow-line however showed no preference for fe-male personality (Groothuis amp Carere 2005) A third example comes from arecent study on a captive population of zebra finches (Taeniopygia guttata)In these birds individual females differed in their preference for aggressivemales due to nongenetic maternal effects (Forstmeier et al 2004) Both birdstudies show individual differences in preference for personality of sexualpartners highlighting that studies on personality and sexual selection shouldprovide exciting results and therefore deserve more attention


Adaptive perspectives to study correlated behaviours

Evidence for strong genetic correlations between behavioural traits in labo-ratory populations of birds (Drent et al 2003 van Oers et al 2004a) fish(Bakker amp Sevenster 1989 Bakker 1994) and rodents (Sluyter et al 1995Koolhaas et al 1999) suggests that behavioural traits are often structured inpersonality traits because they are controlled by the same hormones (Kool-haas et al 1999 Ketterson amp Nolan 1999) or genes (Sih et al 2004a b)Personality traits have therefore often been proposed to act as evolutionaryconstraints (Sih et al 2004a b) because components of personality mightbe difficult to decouple (Loeschke 1987 Ketterson amp Nolan 1999) Thereason why whole suites of behavioural traits are often correlated has how-ever received very limited attention from a functional perspective (Wilsonet al 1994 Coleman amp Wilson 1998 Dall et al 2004 Sih et al 2004aBell 2005) From an adaptionistrsquos viewpoint correlations between behav-ioural traits are not necessarily set and if present should reflect adaptation tothe environment (Roff 1996 Wilson 1998) Notably all of the fitness stud-ies reviewed in above section of this paper have measured selection actingon single behavioural traits whereas functional explanations for personalityvariation (ie consistent individual differences in suites of correlated be-havioural traits) would require insight in conditions favouring phenotypic(or genetic) correlations among behavioural traits Here we discuss both di-rect and indirect approaches to study the adaptive nature of personality perse

Direct approaches measuring correlational selection

The adaptive nature of correlations between behavioural traits can be mea-sured directly by using the phenotypic selection approach (Lande amp Arnold1983) where fitness is measured as a function of both behaviour x behavioury (both measured on each individual) and their interaction (Figure 4) Herex and y could represent the same behaviour at different ontogenic stageswhich would allow one to evaluate the adaptive nature of consistent indi-vidual differences in a single behavioural trait X and y could also representfunctionally-distinct behaviours for instance aggressiveness and risk-takingbehaviour which would allow one to evaluate the adaptive nature of pheno-typic correlations between traits Knowledge of the fitness landscape wouldallow one to evaluate whether an observed association between x and y (ie


Figure 4 Illustration of how multivariate fitness landscapes can help to evaluate whethercorrelations between behavioural traits would be adaptive Dots represent all possible behav-ioural types (large dots have high fitness small dots have low fitness) We show two behav-iours (x and y) that could either represent the same type of trait in different situations (eglevels of activity in the absence vs presence of predators) or two functionally distinct traits(eg x = aggressiveness and y = risk-taking behaviour) (a) stabilising selection favoursa single optimum and correlations between x and y would not be adaptive (b-d) selectionfavours a range of behavioural types (ie there is more than one phenotype with high fit-ness) and the lsquoridgersquo of high fitness (b-c) indicates that correlational selection favours apositive correlation between x and y When considering only one behaviour in different situ-ations dots on the x = y line represent lsquoinflexiblersquo (or stable) phenotypes ie animals thatshow the same behaviour in both environments and all other dots represent lsquoflexiblersquo (orplastic) phenotypes In that case the fitness landscapes provide information on both adaptiveindividual 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 pop-ulation where x and y are positively correlated In the case of Figure 4aselection favours a single optimal phenotype (large dot scoring low on x andhigh on y) The observed positive correlation between x and y would thusnot be adaptive In contrast in the case of positive correlational selection onx and y (as depicted by a lsquoridgersquo of high fitness within the landscape Figures4bampc) a positive correlation between x and y would be adaptive

When x and y represent the same behaviour in different situations (egactivity in the presence vs absence of predators Sih et al 2003 Quinn ampCreswell 2005) the fitness landscape provides information not only on theadaptive nature of individual consistency but also on the adaptive nature ofbehavioural flexibility For instance in case 4a behavioural flexibility wouldbe adaptive as a single flexible phenotype has highest fitness Situation 4awould thus correspond to what Sih et al (2004b) have called a behaviouralcarry-over Situation 4c illustrates a case where the higher fitness is associ-ated with lsquoinflexiblersquo phenotypes (ie selection favors constant behaviouralphenotypes in both environments) whereas situation 4b illustrates a case


of adaptive phenotypic plasticity or flexibility (selection favors an overall de-crease in the trait between situation 1 and 2) Notably if the fitness landscapewould look like Figure 4d selection would favour two distinct behaviouraltypes (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 flexiblephenotype (lower-right large dot scoring low on x and y) that changes itsbehaviour in the different situations

We know of only one study that has yet measured correlational selec-tion (Barton amp Turelli 1991 Brodie et al 1995) on personality traits Intheir study on Australian women Eaves et al (1990) combined a survey ofreproductive success of 1101 postmenopausal females with information ontheir personality using the Eysenck Personality Questionaire They showedthat the function relating fitness (measured as life time reproductive suc-cess) to neuroticism and extraversion was saddle-shaped with the high-est fitness for both the high-extravertlow-neurotic and low-extraverthigh-neurotic females intermediate fitness for females that had intermediatescores on both axes and lowest fitness for low-extravertlow neurotic andhigh-extraverthigh-neurotic females Their results thus showed that selec-tion favoured a negative correlation between neuroticism and extraversionWe cannot emphasize enough that studies of correlational selection are cru-cial were we ever to understand personality variation from an adaptive per-spective

Indirect approaches studying correlations within and across populations

Comparative approaches provide an alternative way to study the adaptivenature of behavioural correlations The lsquogenetic constraint modelsrsquo predictthat correlations between traits should always be similar irrespective of theenvironmental conditions and that correlations between traits within pop-ulations should be similar to correlations on the population level (Lande1979) For instance the constraint model would predict that if aggressive-ness is positively correlated with boldness within populations populationsthat are on average more aggressive should also be relatively bold In itsmost extreme form (ie when the correlated behaviours are influenced bythe same genes) the genetic constraint would be absolute The lsquoadaptive di-vergence modelsrsquo on the other hand predict that both correlations within and


between populations should ultimately be a function of the selective envi-ronment (Lande 1986) For instance the adaptive divergence model wouldpredict within-population behavioural correlations to be function of the envi-ronmental conditions and would not necessarily predict within and betweenpopulation correlations to be identical Notably even if a genetic correla-tion is adaptive in the current environment it would still act as a short-termevolutionary constraint when environmental conditions change Whereas thepredictions of these models have often been tested for morphological traitsfew studies have attempted to do the same for behavioural traits (but seePalmer amp Dingle 1986 Riechert amp Hedrick 1993 Bell 2005) Supportfor the adaptive divergence model comes from recent work on threespinedstickleback where both phenotypic and genetic correlations between in-traspecific aggressiveness and boldness towards predators differed betweentwo populations (Bell 2005) However there are circumstances in whichboth models give the same predictions particularly when selection favoursthe same correlation in all environments (Lande 1979) Positive phenotypiccorrelations between intraspecific aggressiveness and anti-predator behav-iour as documented for each of two populations of a spider (Agelenopsisaperta) (Riechert amp Hedrick 1993) can therefore not readily be interpretedIt should be argued here that population differentiation in behavioural corre-lations does not necessarily imply adaptive divergence and direct approachesare advisable at all times

What could be done next

Two main approaches are available to the study of personality and fitnessthe first one is to consider a priori that some personality phenotypes aremore fit than others in particular conditions according to our intuition of thefunction of personality This approach runs the risk of providing a lsquojust sostoryrsquo about the function of personality trait The second approach (ie theone that we strongly recommend) is to provide a scientific test of selectionon personality traits directly by looking at the link between fitness and thephenotypic variation of a personality trait or of a set of traits using the meth-ods proposed by quantitative genetics (Lande amp Arnold 1983 Endler 1986Brodie et al 1995 Kingsolver et al 2001) or indirectly by comparingcorrelations between several populations that experience different environ-ments (Lande 1979 1986) Indeed the studies that we reviewed here show


that it is possible to provide evidence that in many circumstances personal-ity can be subject to natural or sexual selection pressures and thus illustratethe ecological importance of personality traits Using this approach we couldtest adaptive hypotheses (Fairbairn amp Reeve 2001) provided by theoreticalmodels (Dall et al 2004) In the future with the increase in the numberof estimates on selection gradients (Lande amp Arnold 1983) on personalitytraits it will be possible to compare the strength of selection on those traitswith other behaviour and with life history or morphological traits (King-solver et al 2001) This approach has another advantage by questioning theexistence the strength and the shape of selection on personality traits weencourage the publication of results showing both evidence or the absenceof evidence for selection on these traits therefore allowing comparisons ofselection patterns between personality traits and other types of traits Untilnow we have only been able to review cases where at least a significant rela-tionship between phenotypic variation in one personality trait and fitness hasbeen found This may overemphasise the ecological importance of personal-ity traits

Several adaptive hypotheses to explain the maintenance of variance ofpersonality traits rely on particular assumptions regarding the selectionpressures acting on those traits (eg correlational selection frequency-dependent selection of environmental and temporal heterogeneity see above)We would like to point out that these selection patterns could only be de-tected statistically with large sample sizes (Kingsolver et al 2001) andtherefore encourage studies testing the occurrence of selection on personal-ity traits to try to collect data on a minimum of 100 individuals Multivariateselection analyses coupled with long term studies of selection in the wild(eg populations experiencing different environments Fairbairn amp Reeve2001) experimental modification of environmental conditions and of pheno-typic (co)variations (ie phenotypic engineering Sinervo amp Denardo 1996Ketterson amp Nolan 1999) will allow us to examine the generality of evo-lutionary mechanisms shaping the distribution of personality traits and theircovariation in animals and humans

Acknowledgements

Denis Reacuteale was supported by a grant from the Natural Sciences and Engineering ResearchCouncil of Canada We are grateful to Marco Festa-Bianchet Jon Jorgenson and others who


have collected field data over the years at Ram Mountain and to Christiaan Both ClaudioCarere Piet Drent Piet de Goede Ton Groothuis Kees van Oers Arie van Noordwijk JoostTinbergen and others who helped collecting data on avian personalities in the wild and AlisonBell Felicity Huntingford Charlotte Hemelrijk Ani Kazem Andy Sih and Jon Wright forinspiring discussions

References

Armitage KB amp Van Vuren DH (2003) Individual differences and reproductive successin yellow-bellied marmots mdash Ethol Ecol Evol 15 207-233

Bakker TCM (1994) Genetic correlations and the control of behavior exemplified byaggressiveness in sticklebacks mdash Adv Study Behav 23 135-171

Bakker TCM amp Sevenster P (1989) Changes in the sexual tendency accompagnyingselection for aggressiveness in the three-spined stickleback Gasterosteus aculeatus Lmdash J Fish Biol 34 233-243

Barton NH amp Turelli M (1991) Natural and sexual selection on many loci mdash Genetics127 229-255

Bell AM (2005) Behavioral differences between individuals and two populations of stick-leback (Gasterosteus aculeatus) mdash J Evol Biol 18 464-473

Boissy A (1995) Fear and fearfulness in animals mdash Q Rev Biol 70 165-191Both C Dingemanse NJ Drent PJ amp Tinbergen JM (2005) Pairs of extreme avian

personality have highest reproductive success mdash J Anim Ecol 74 667-674Both C Visser ME amp Verboven N (1999) Density dependent recruitment rates in great

tits the importance of being heavier mdash Proc R Soc Lond B 266 465-469Bouchard TJ amp Loehlin JC (2001) Genes evolution and personality mdash Behav Gen 31

243-273Brodie ED Moore AJ amp Janzen FJ (1995) Visualizing and quantifying natural selec-

tion mdash Trends Ecol Evol 10 313-318Bruce J Davis EP amp Gunnar MR (2002) Individual differences in childrenrsquos cortisol

response to the beginning of a new school year mdash Psychoneuroendocr 27 635-650Bult A amp Lynch CB (2000) Breaking through artificial selection limits of an adaptive

behavior in mice and the consequences for correlated responses mdash Behav Genet 30193-206

Burger R amp Gimelfarb A (2002) Fluctuating environments and the role of mutation inmaintaining quantitative genetic variation mdash Genet Res 80 31-46

Buss DM (1991) Evolutionary personality psychology mdash Annu Rev Psychol 42 459-491

Carere C Drent PJ Koolhaas JM amp Groothuis TGG (2005) Epigenetic effects onpersonality traits early food provisioning and sibling competition mdash Behaviour 1421335-1361

Carere C Drent PJ Privitera L Koolhaas JM amp Groothuis TGG (in press) Person-alities in great tits Parus major Stability and consistency mdash Anim Behav

Carere C Groothuis TGG Moestl E Daan S amp Koolhaas JM (2003) Fecal corti-costeroids in a territorial bird selected for different personalities daily rhythm and theresponse to social stress mdash Horm Behav 43 540-548


Carere C amp van Oers K (2004) Shy and bold great tits (Parus major) body temperatureand breath rate in response to handling stress mdash Physiol Behav 82 905-912

Carere C Welink D Drent PJ Koolhaas JM amp Groothuis TGG (2001) Effect ofsocial defeat in a territorial bird (Parus major) selected for different coping styles mdashPhysiol Behav 73 427-433

Carlstead K Mellen J amp Kleiman DG (1999) Black rhinoceros (Diceros bicornis) in USzoos I Individual behavior profiles and their relationship to breeding success mdash ZooBiol 18 17-34

Clark AB amp Ehlinger TJ (1987) Pattern and adaptation in individual behavioral differ-ences mdash In Perspectives in ethology (Bateson PPG amp Klopfer PH eds) PlenumNew York p 1-47

Clarke AS amp Boinski S (1995) Temperament in nonhuman-primates mdash Am J Primotol37 103-125

Clarke AS Kammerer CM Georgre KP Kupfer DJ Mckinney WT Spence MAamp Kraemer GW (1995) Evidence for heritability of biogenic amine levels in thecerebrospinal fluid of rhesus monkeys mdash Biol Psychiatry 38 572-577

Cleveland A Westergaard GC Trenkle MK amp Higley JD (2003) Physiological pre-dictors of reproductive outcome and mother-infant behaviors in captive rhesus macaquefemales (Macaca mulatta) mdash Neuropsychopharmacol 29 109-910

Coleman K amp Wilson DS (1998) Shyness and boldness in pumpkinseed sunfish individ-ual differences are context specific mdash Anim Behav 56 927-936

Dall SRX (2004) Behavioural biology fortune favours bold and shy personalities mdashCurrent Biology 14 R470-R472

Dall SRX Houston AI amp McNamara JM (2004) The behavioural ecology of person-ality consistent individual differences from an adaptive perspective mdash Ecol Lett 7734-739

Dingemanse NJ Both C Drent PJ van Oers K amp van Noordwijk AJ (2002) Repeata-bility and heritability of exploratory behaviour in great tits from the wild mdash AnimBehav 64 929-937

Dingemanse NJ Both C Drent PJ amp Tinbergen JM (2004) Fitness consequences ofavian personalities in a fluctuating environment mdash Proc R Soc Lond B 271 847-852

Dingemanse NJ Both C van Noordwijk AJ Rutten AL amp Drent PJ (2003) Nataldispersal and personalities in great tits (Parus major) mdash Proc R Soc Lond B 270741-747

Dingemanse NJ amp de Goede P (2004) The relation between dominance and exploratorybehavior is context-dependent in wild great tits mdash Behav Ecol 15 1023-1030

Drent PJ van Oers K amp van Noordwijk AJ (2003) Realized heritability of personalitiesin the great tit (Parus major) mdash Proc R Soc Lond B 270 45-51

Eaves LJ Martin NG Heath AC amp Hewitt JK (1990) Personality and reproductivefitness mdash Behav Genet 20 563-568

Endler JA (1986) Natural selection in the wild mdash Princeton University Press PrincetonNJ

Fairbairn DJ amp Reeve JP (2001) Natural selection mdash In Evolutionary ecology conceptsand case studies (Fox CW Roff D amp Fairbairn DJ eds) Oxford University PressOxford 29-43

Fairbanks LA Newman TK Bailey JN Jorgensen MJ Breidenthal SE OphoffRA Comuzzie AG Martin LJ amp Rogers J (2004) Genetic contributions to socialimpulsivity and aggressiveness in vervet monkeys mdash Biol Psychiatry 55 642-647


Falconer DS amp Mackay TFC (1996) Introduction to quantitative genetics mdash LongmanNew York

Fisher RA (1930) The genetical theory of natural selection mdash Oxford University PressOxford

Forstmeier W Coltman DW amp Birkhead TR (2004) Maternal effects influence the sexualbehaviour of sons and daughters in the zebra finch mdash Evolution 58 121-130

Frank SA amp Slatkin M (1990) Evolution in a variable environment mdash Am Nat 136244-260

Fraser DF Gilliam JF Daley MJ Le AN amp Skalski GT (2001) Explaining leptokur-tic movement distributions intrapopulation variation in boldness and exploration mdashAm Nat 158 124-135

Godin JJG amp Dugatkin LA (1996) Female mating preference for bold males in theguppy Phoecilia reticulata mdash Proc Natl Acad Sci USA 93 10262-10267

Gosling SD (2001) From mice to men what can we learn about personality from animalresearch mdash Psychol Bull 127 45-86

Greenberg R amp Mettke-Hofmann C (2001) Ecological aspects of neophobia and neophiliain birds mdash Curr Ornithol 16 119-178

Groothuis TGG amp Carere C (2005) Avian personalities characterization and epigenesismdash Neurosci Biobehav Rev 29 137-150

Grossarthmaticek R amp Eysenck HJ (1990) Personality stress and disease mdash descriptionand validation of a new inventory mdash Psychol Rep 66 355-373

Higley JD King ST Hasert MF Champoux M Suomi SJ amp Linnoila M (1996a)Stability of interindividual differences in serotonin function and its relationship to se-vere aggression and competent social behavior in rhesus macaque females mdash Neu-ropsychopharmacol 14 67-76

Higley JD amp Linnoila M (1997) Low central nervous system serotonergic activity is trait-like and correlates with impulsive behaviour A nonhuman primate model investigatinggenetic and environmental influences on neurotransmission mdash Ann NY Acad Sci886 39-56

Higley JD Mehlman PT Higley SB Fernald B Vickers J Lindelle SG Taub DMSuomi SJ amp Linnoila M (1996b) Excessive mortality in young free-ranging malenonhuman primates with low cerebrospinal fluid 5-hydroxyindoleacetic acid concentra-tions mdash Arch Gen Psychiat 53 537-543

Houmljesjouml J Johnsson J amp Bohlin T (2004) Habitat complexity reduces the growth ofaggressive and dominant brown trout (Salmo trutta) relative to subordinates mdash BehavEcol Sociobiol 56 286-289

Houmljesjouml J Johnsson JI amp Bohlin T (2002) Can laboratory studies on dominance predictfitness of young brown trout in the wild mdash Behav Ecol Sociobiol 52 102-108

Houston AI and McNamara JM (1999) Models of adaptive behaviour mdash CambridgeUniversity Press Cambridge

Huntingford FA (1976) The relationship between anti-predator behaviour and aggressionamong conspecifics in the three-spined stickleback Gasterosteus aculeatus mdash AnimBehav 24 245-260

Huntingford FA amp Adams CE (2005) Behavioural syndromes in farmed fish implica-tions for production and welfare mdash Behaviour 142 1207-1221

Ketterson ED amp Nolan V Jr (1999) Adaptation exaptation and constraint a hormonalperspective mdash Am Nat 154 S4-S25


Kingsolver JG Hoekstra HE Hoekstra JM Berrigan D Vignieri SN Hill CEHoang A Gilbert P amp Beerli P (2001) The strength of phenotypic selection innatural populations mdash Am Nat 157 245-261

Koolhaas JM de Boer SF Buwalda B van der Vegt BJ Carere C amp Groothuis TGG(2001) How and why coping systems vary among individuals mdash In Welfare in animalsincluding humans (Broom DM ed) Dahlem University Press Dahlem p 197-209

Koolhaas JM Korte SM de Boer SF van der Vegt BJ van Reenen CG Hopster Hde Jong IC Ruis MAW amp Blokhuis HJ (1999) Coping styles in animals currentstatus in behavior and stress-physiology mdash Neurosci Biobehav Rev 23 925-935

Krakov S (2003) Motivational and heritable determinants of dispersal latency in wild malehouse mice (Mus musculus musculus) mdash Ethology 109 671-689

Lande R (1979) Quantitative genetics analysis of multivariate evolution applied tobrainbody size allometry mdash Evolution 33 402-416

Lande R (1986) The dynamics of peak shifts and the patterns of morphological evolutionmdash Paleobiology 12 343-354

Lande R amp Arnold SJ (1983) The measurement of selection on correlated characters mdashEvolution 37 1210-1226

Loeschke V (1987) Genetic constraints on adaptive evolution mdash Springer Verlag BerlinLynch M amp Walsh B (1998) Genetics and analysis of quantitative traits mdash Sinauer Asso-

ciates Sunderland MAMagnhagen C amp Staffan F (2003) Social learning in young-of-the-year perch encountering

a novel food type mdash J Fish Biol 63 824-829Mangel M amp Stamps JA (2001) Trade-offs between growth and mortality and the main-

tenance of individual varation in growth mdash Evol Ecol Res 3 538-593Marchetti C amp Drent PJ (2000) Individual differences in the use of social information in

foraging by captive great tits mdash Anim Behav 60 131-140Maynard Smith J (1982) Evolution and the theory of games mdash Cambridge University

Press CambridgeMcDougall PT Reacuteale D Sol D amp Reader S (in press) Wildlife conservation and ani-

mal temperament causes and consequences of evolutionary change for captive reintro-duced and wild populations ndash Anim Conserv

Mealey L amp Segal NL (1993) Heritable and environmental variables affect reproduction-related behaviors but not ultimate reproductive success mdash Pers Indiv Differ 14 783-794

Mehlman PT Higley JD Faucher I Lilly AA Taub DM Vickers J Suomi SJamp Linnoila M (1994) Low CSF 5-HIAA concentrations and severe aggression andimpaired impulse control in nonhuman primates mdash Am J Psychiat 151 1485-1491

Mehlman PT Higley JD Faucher I Lilly AA Taub DM Vickers J Suomi SJ ampLinnoila M (1995) Correlation of CSF 5-HIAA concentration with sociality and thetiming of emigration in free-ranging primates mdash Am J Psychiat 152 907-913

Mehlman PT Higley JD Fernald BJ Sallee FR Suomi SJ amp Linnoila M (1997)CSF 5-HIAA testosterone and sociosexual behaviors in free-ranging male rhesusmacaques in the mating season mdash Psychiat Res 72 89-102

Merilauml J Sheldon BC amp Kruuk LEB (2001) Explaining statis microevolutionary stud-ies in natural populations mdash Genetica 112-113 199-222

Neff BD amp Sherman PW (2004) Behavioral syndromes versus Darwinian algorithms mdashTrends Ecol Evol 19 621-622


Netlle D (2005) An evolutionary approach to the extra version continuum mdash Evol HumanBehav 26 363-373

Nevo E (1988) Genetic diversity in nature ndash patterns and theory mdash Evol Biol 23 217-246van Oers K de Jong G Drent PJ amp van Noordwijk AJ (2004a) A genetic analysis of

avian personality traits correlated response to artificial selection mdash Behav Genet 34611-619

van Oers K Drent PJ de Goede P amp van Noordwijk AJ (2004b) Repeatability andheritability of risk-taking behaviour in relation to avian personalies mdash Proc R SocLond B 271 65-71

van Oers K Drent PJ de Jong G amp van Noordwijk AJ (2004c) Additive and nonaddi-tive genetic variation in avian personality traits mdash Heredity 93 496-503

van Oers K Klunder M amp Drent PJ (2005a) Context dependence of personalities risk-taking behavior in a social and non-social context mdash Behav Ecol 16 716-723

van Oers K de Jong G van Noordwijk AJ Kempenaers B amp Drent PJ (2005b)Contribution of genetics to the study of animal personalities a review of case studiesmdash Behaviour 142 1191-1212

Palmer JO amp Dingle H (1986) Direct and correlated responses to selection among life-history traits in milkweed bugs (Oncopeltus fasciatus) mdash Evolution 40 767-777

Perdeck AC Visser ME amp Balen JHv (2000) Great tit Parus major survival and thebeech-crop cycle mdash Ardea 88 99-106

Quinn JL amp Creswell W (2005) Personality anti-predation behaviour and behaviouralplasticity in the chaffinch Fringilla coelebs mdash Behaviour 142 1389-1408

Reacuteale D amp Festa-Bianchet M (2003) Predator-induced natural selection on temperamentin bighorn ewes mdash Anim Behav 65 463-470

Reacuteale D Gallant BY Leblanc M amp Festa-Bianchet M (2000) Consistency of tempera-ment in bighorn ewes and correlates with behaviour and life history mdash Anim Behav60 589-597

Riechert SE amp Hedrick AV (1993) A test of correlations among fitness-related behav-ioural traits in the spider Agelenopsis aperta (Aranea Agelinadae) mdash Anim Behav46 669-675

Riska B Prout T amp Turelli M (1989) Laboratory estimates of heritabilities and geneticcorrelations in nature mdash Genetics 123 865-871

Roff DA (1996) The evolution of genetic correlations an analysis of patterns mdash Evolution50 1392-1403

Roff DA (1997) Evolutionary quantitative genetics mdash Chapman and Hall New YorkSasaki A amp Ellner S (1997) Quantitative genetic variance maintained by fluctuating selec-

tion with overlapping generations variance components and covariances mdash Evolution51 682-696

Schmitz PG (1992) Personality stress-reactions and disease mdash Pers Indiv Differ 13683-691

Sih A Bell A amp Johnson JC (2004a) Behavioral syndromes an ecological and evolu-tionary overview mdash Trends Ecol Evol 19 372-378

Sih A Bell AM Johnson JC amp Ziemba RE (2004b) Behavioural syndromes anintegrative overview mdash Q Rev Biol 79 241-277

Sih A Kats LB amp Maurer EF (2003) Behavioural correlations across situations andthe evolution of ineffective antipredator behaviour in a sunfish-salamander system mdashAnim Behav 65 29-44


Sinervo B amp Denardo DF (1996) Costs of reproduction in the wild path analysis of naturalselection and experimental tests of causation mdash Evolution 50 1299-1313

Sluyter F Bult C Lynch GA van Oortmerssen GA amp Koolhaas JM (1995) A com-parison between house mouse lines selected for attack latency or nest-building Evi-dence for a genetic basis of alternative behavioral strategies mdash Behav Genet 25 247-252

Stamps J (2003) Behavioural processes affecting development Tinbergenrsquos fourth questioncomes of age mdash Anim Behav 66 1-13

Stamps JA (1991) Why evolutionary issues are reviving interest in proximate behavioralmechanisms mdash Am Zool 31 338-348

Sundstroumlm LF Petersson E Houmljesjouml J Johnsson JI amp Jarvi T (2004) Hatchery selec-tion promotes boldness in newly hatched brown trout (Salmo trutta) implications fordominance mdash Behav Ecol 15 192-198

Verbeek MEM Boon A amp Drent PJ (1996) Exploration aggressive behaviour anddominance in pair-wise confrontations of juvenile male great tits mdash Behaviour 133945-963

Verbeek MEM Drent PJ amp Wiepkema PR (1994) Consistent individual differences inearly exploratory behaviour of male great tits mdash Anim Behav 48 1113-1121

Ward AJW Thomas P Hart PJB amp Krause J (2004) Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus) mdash Behav Ecol Sociobiol 55 561-568

Westerberg M Staffan F amp Magnhagen C (2004) Influence of predation risk on individualcompetitive ability and growth in Eurasian perch Perca fluviatilis mdash Anim Behav 67273-279

Westergaard GC Cleveland A Trenkle MK Lussier ID amp Higley JD (2003a) CSF5-HIAA concentration as an early screening tool for predicting significant life historyoutcomes in female specific-pathogen-free (SPF) rhesus macaques (Macaca mulatta)mdash J Med Primatol 32 95-104

Westergaard GC Suomi SJ Chavanne TJ Houser L Hurley A Cleveland A SnoyPJ amp Higley JD (2003b) Physiological correlates of aggression and impulsivity infree-ranging female primates mdash Neuropsychopharmacol 28 1045-1055

Wielebnowshi NC (1999) Behavioral differences as predictor of breeding status in captivecheetahs mdash Zoo Biol 18 335-349

Wilson DS (1994) Adaptive genetic-variation and human evolutionary psychology mdashEthol Sociobiol 15 219-235

Wilson DS (1998) Adaptive individual differences within single populations mdash PhilTrans R Soc Lond B 353 199-205

Wilson DS Clark AB Coleman K amp Dearstyne T (1994) Shyness and boldness inhumans and other animals mdash Trends Ecol Evol 9 442-446


in the many different environments they encounter during life Contrary tothis notion of behavioural plasticity as the major adaptive cause of pheno-typic variation in behaviour (Houston amp McNamara 1999 Dall et al 2004Neff amp Sherman 2004) animals often show very limited behavioural plas-ticity (Sih et al 2004a b) and commonly differ consistently in their reactiontowards the same environmental stimuli (Clark amp Ehlinger 1987 Wilson etal 1994 Boissy 1995 Wilson 1998 Gosling 2001 Greenberg amp Mettke-Hofmann 2001) These individual differences in behaviour are moreoverfrequently expressed across a wide range of contexts and situations indi-viduals commonly differ consistently in whole suites of functionally-distinctbehavioural traits (Sih et al 2004a b) For instance in birds (Verbeek etal 1996) rodents (Koolhaas et al 2001) and fish (Huntingford 1976) an-imals that are relatively aggressive towards conspecifics are also bolder inexploring novel environments and predators These individual differences insuites of correlated traits have been named behavioural syndromes (Sih et al2004a b) coping strategies (Koolhaas et al 2001) temperament (Boissy1995 Clarke amp Boinski 1995) or animal personality traits (Buss 1991Gosling 2001)

The evolutionary origin and maintenance of phenotypic variation in an-imal personality is poorly understood (Stamps 1991 Wilson et al 1994Wilson 1998 Dingemanse et al 2004 Dall et al 2004 Sih et al 2004a)Both mechanistic and functional approaches need to be applied to gain fullunderstanding of why this behavioural variation persists (Stamps 19912003) The mechanistic approach seeks to evaluate how phenotypes resultfrom the combined influences of genetic and environmental factors the func-tional approach how the interaction between phenotypes and their environ-ment affects fitness Variation in personality has received considerable atten-tion from the mechanistic viewpoint the emerging pattern is that individualdifferences in single components of animal personality (eg aggressiveness)are moderately heritable and relatively stable over the entire life of the in-dividual (Boissy 1995 Koolhaas et al 1999 Bouchard amp Loehlin 2001)and that phenotypic correlations between components of personality (egbetween aggressiveness and boldness) often originate from strong underly-ing genetic correlations (Bakker 1994 Bult amp Lynch 2000 van Oers et al2004a Bell 2005) In contrast functional approaches towards understand-ing variation in personality have received far less attention (Reacuteale amp Festa-Bianchet 2003 Dingemanse et al 2004 Dall et al 2004) despite the fact


























































text


































Acknowledgements




References














































































































































































text


































Acknowledgements




References









































































































































































text


































Acknowledgements




References



































































































































































text


































Acknowledgements




References





























































































































































text


































Acknowledgements




References


























































































































































text


































Acknowledgements




References





















































































































































text


































Acknowledgements




References














































































































































text


































Acknowledgements




References










































































































































text


































Acknowledgements




References



































































































































text


































Acknowledgements




References





























































































































text


































Acknowledgements




References























































































































text


































Acknowledgements




References





















































































































































Acknowledgements




References















































































































































Acknowledgements




References











































































































































Acknowledgements




References






































































































































Acknowledgements




References

































































































































Acknowledgements




References




























































































































Acknowledgements




References
























































































































Acknowledgements




References























































































































References
























































































































































































































































































































































































































Documents

Natural selection and animal personalitybehav.zoology.unibe.ch/sysuif/uploads/files/esh/pdf_online/ws/Dinge... · Natural selection and animal personality 1163 the second on risk-taking