Natural selection and animal personality

26 Pages·2006·0.25 MB·English

Natural selection and animal personality
NielsJ.Dingemanse1,2) &DenisRéale3)
(1AnimalEcologyGroup,CentreforEvolutionaryandEcologicalStudies,Universityof
Groningen,POBox14,9750AAHaren,TheNetherlands;3CanadianResearchChairein
BehaviouralEcologyandGroupedeRechercheenEcologieComportementaleetAnimale,
DépartementdesSciencesBiologiques,UniversitéduQuébecàMontréal,CP-8888,
SuccursaleCentre-ville,Montréal,Québec,H3C3P,Canada)
(Accepted:1February2005)
Summary
Recentprogresshasbeenmadeonthestudyofpersonalityinanimals,bothfromamecha-
nisticandafunctionalperspective.Whilewestartknowingmoreabouttheproximalmech-
anismsresponsiblefortheconsistentdifferencesinbehaviourbetweenindividualsinapop-
ulation,littleisknownyetabouttherelationshipbetweenthephenotypicdistributionofper-
sonality 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.
Westartbyadescription oftwocasestudiesthathaveexaminedthe roleofnaturalselec-
tiononpersonalitytraitsinthewild(i.e.,thegreattit,Parusmajorandbighornsheep,Ovis
canadensis),andreviewotherstudiesthathavereportedsomelinksbetweenpersonalitytraits
andfitnessindices,inalargevarietyofanimalspecies.Wecontinuebyoutliningbothdirect
approaches(i.e.,measuringcorrelationalselectiononpersonalitytraitcombinations)andin-
directapproaches(i.e.,comparingcorrelationsbetweenpersonalitytraitswithinandbetween
populations) to study suites of correlated traits from an adaptive perspective. This review,
wehope,willbeabletostimulatetheuseofthephenotypicselectionanalysisappliedtothe
studyofselectiononpersonalitytraitsinanimals.
Keywords:personality,behaviouralsyndromes,reproductivesuccess,sexualselection,corre-
lationalselection,geneticconstraints.
Introduction
Behaviouralflexibilityisoftenregardedtobeunlimited,immediate,andre-
versible(Sihetal.,2004a,b),allowingindividualstomaximizetheirfitness
2)Correspondingauthor’se-mailaddress:[email protected]
©KoninklijkeBrillNV,Leiden,2005 Behaviour142,1159-1184
Alsoavailableonline-
1160 Dingemanse&Réale
in the many different environments they encounter during life. Contrary to
this notion of behavioural plasticity as the major adaptive cause of pheno-
typicvariationinbehaviour(Houston&McNamara,1999;Dalletal.,2004;
Neff & Sherman, 2004), animals often show very limited behavioural plas-
ticity(Sihetal.,2004a,b)andcommonlydifferconsistentlyintheirreaction
towardsthesameenvironmentalstimuli(Clark&Ehlinger,1987;Wilsonet
al.,1994;Boissy,1995;Wilson,1998;Gosling,2001;Greenberg&Mettke-
Hofmann, 2001). These individual differences in behaviour are, moreover,
frequently expressed across a wide range of contexts and situations: indi-
vidualscommonlydifferconsistentlyinwholesuitesoffunctionally-distinct
behavioural traits (Sih et al., 2004a, b). For instance, in birds (Verbeek et
al.,1996),rodents(Koolhaasetal.,2001),andfish(Huntingford,1976),an-
imals that are relatively aggressive towards conspecifics are also bolder in
exploringnovelenvironmentsandpredators.Theseindividualdifferencesin
suitesofcorrelatedtraitshavebeennamedbehaviouralsyndromes(Sihetal.,
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 an-
imal personality is poorly understood (Stamps, 1991; Wilson et al., 1994;
Wilson,1998;Dingemanseetal.,2004;Dalletal.,2004;Sihetal.,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
fromthecombinedinfluencesofgeneticandenvironmentalfactors;thefunc-
tional approach how the interaction between phenotypes and their environ-
mentaffectsfitness.Variationinpersonalityhasreceivedconsiderableatten-
tionfromthemechanisticviewpoint;theemergingpatternisthatindividual
differencesinsinglecomponentsofanimalpersonality(e.g.,aggressiveness)
are moderately heritable and relatively stable over the entire life of the in-
dividual (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 underly-
inggeneticcorrelations(Bakker,1994;Bult&Lynch,2000;vanOersetal.,
2004a; Bell, 2005). In contrast, functional approaches towards understand-
ing variation in personality have received far less attention (Réale & Festa-
Bianchet, 2003; Dingemanse et al., 2004; Dall et al., 2004), despite the fact
Naturalselectionandanimalpersonality 1161
thatonlythecombinationofbothapproaches(inthesamestudysystem)will
allowaninformedevaluationofhowbehaviouraltraitsmight(co)evolveun-
derdifferentenvironmentalconditions(Fisher,1930;Endler,1986).
This paper has a three-fold aim. First, we aim to provide an overview of
theavailableliteratureonthefitnessconsequencesofpersonalitytraitsinnat-
ural populations. In doing so, we largely concentrate our discussion on few
studysystemswherebothmechanisticandfunctionalapproacheshavebeen
appliedtounderstandnaturalvariationinpersonality,andwhereselectionon
behavioural phenotypes has been measured in all major life-history stages
andoveranumberofyears;thusprovidingfirstdetaileddescriptionsofhow
andwhennaturalselectionmayoperateonanimalpersonalitytraits.Wefur-
therdiscussexamplesofarangeofstudysystemswhereselectiononanimal
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 hu-
manpersonality,e.g.,susceptibilitytoillness(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).Ourreviewthusfocussesprimarilyonnonhumananimals.
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 (e.g., exploratory behav-
iour 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,
suchstudiescannotprovidefunctionalexplanationsfortheexistenceofani-
malpersonalityperse,asthiswouldrequireinsightinwhyindividualsshow
consistency in their behaviour, either across time, generations, contexts or
situations (Dall et al., 2004; Sih et al., 2004a). We outline both direct and
indirectapproachestostudysuitesofcorrelatedtraitsfromanadaptiveper-
spective.
Our third and last aim is to stimulate the use of the phenotypic selection
approach(Lande&Arnold,1983)whenquantifyingfitnessconsequencesof
animal personality, as this approach produces standardized estimates of the
strength of selection that can directly be compared with those derived from
otherstudiesonthesameorothertypesoftraits(Kingsolveretal.,2001).
1162 Dingemanse&Réale
Naturalselectionandpersonality
Natural selection is measured by the covariance between traits and fitness
(Endler,1986),allowingonetoestimateboththeshape(Brodieetal.,1995)
(i.e.,directional,stabilizing,disruptive)andthestrengthofselection(King-
solver 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
studyingselectiononsuitesofcorrelatedtraits,likelife-historysyndromesor
personalitytraits(Réale&Festa-Bianchet,2003).Whenquantitativegenetic
parametershavealsobeenquantified(i.e.,heritabilityofandgeneticcorrela-
tions between components of personality traits), one can make an informed
evaluationoftheevolutionaryconsequencesoftheimposedselectiveregime
(Falconer & Mackay, 1996; Roff, 1997; Lynch & Walsh, 1998), including
theevolutionofgeneticcorrelationsbetweenbehaviouraltraits(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
twostudyspecies inthe wild,greattit (Parusmajor)andthe bighornsheep
(Ovis canadensis), where both quantitative genetics parameters and fitness
landscapesofanimalpersonalityhavebeenquantifiedsimultaneouslyandin
natural populations, providing a first insight in the evolutionary potential of
personalitytraits.
Fitnessconsequencesofpersonalityingreattits
Individualdifferencesinsuitesofcorrelatedtraits
Laboratory studies on hand-reared great tits showed that individuals dif-
fered in their reaction toward novel or challenging stimuli, comparable to
howrodentsdifferinreactivity(Verbeeketal.,1994;Koolhaasetal.,2001;
Groothuis&Carere,2005).Inthesebirds,speedofexplorationofnovel(lab-
oratory) 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)andscrounging(Marchetti&Drent,2000)duringforaging,andstress
responsiveness (Carere et al., 2001, 2003; Carere & van Oers, 2004). Two
bi-directionalselectionexperiments,thefirstonacombinedscoreforexplo-
ration and boldness (‘early exploratory behaviour’; Drent et al., 2003) and
Naturalselectionandanimalpersonality 1163
the second on risk-taking behaviour (van Oers et al., 2004b), gave realized
heritabilitiesof0.54and0.19respectivelyandevidenceforastronggenetic
correlation(0.84)betweenearlyexploratorybehaviourandrisk-takingunder
laboratory conditions (van Oers et al., 2004a). Repeatabilities (range: 0.27-
0.66; Dingemanse et al., 2002) and narrow-sense heritabilities (0.34±0.13;
Dingemanse et al., 2004) were considerably lower for wild great tits, sug-
gestingthatenvironmentalfactors(i.e.,thosecontrolledforinthelaboratory)
alsoinfluencedexploratorybehaviourinthewild(Riskaetal.,1989;seealso
Carereetal.,2005foradiscussiononenvironmentalsourcesofvariationin
great tits). Alltogether, these quantitative genetics studies showed that great
titsdifferinsuitesof(genetically)correlatedtraits,withtheextremesofthe
trait distribution (ranging from ‘slow’ to ‘fast’ exploratory behaviour) re-
flecting alternative behavioural strategies to cope with novel or challenging
stimuli(Verbeeketal.,1994;Drentetal.,2003;Carereetal.,inpress).Rel-
ativelyhighlevelsofbothadditiveandnonadditivegeneticvarianceinearly
exploratory behaviour of laboratory-bred great tits (van Oers et al., 2004c)
suggesteda history offluctuating selection pressuresin this population (see
vanOersetal.,2005b).
Measuringpersonalityofwildanimals
To quantify selection on avian personality in the wild, large numbers of
wildgreattits(1342individualsbetween1998-2002;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 (Dinge-
manseetal.,2002).Thefollowingmorning,exploratorybehaviourwasmea-
sured 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(Dingemanseetal.,2002).Exploratorybehaviourwasbothrepeat-
able and heritable (see above), and unrelated to age, body condition, or sex
(Dingemanseet al., 2002). Subsequent field studies revealed that the fitness
consequencesofavianpersonalitywerecomplex(Figures1,2).
Fitnessconsequences:adultannualsurvival
Selection as measured by adult annual survival acted on exploratory behav-
iour(basedononetestperindividual),buttheeffectswerealwaysopposite
1164 Dingemanse&Réale
Figure1. Overviewoftheconsequencesofexploratorybehaviourofwildadultgreattits
(Parusmajor)fortwomajorfitnesscomponents(survivalandproductionofrecruits).Arrows
representmeasured(solidlines)orpresumed(brokenlines)directorindirectrelationshipsas
basedonthecorrelationalstudiesdiscussedinthetext.Symbolsindicatetheshapeoflinear
(+: 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
exploratorybehaviourdifferedbetweenyearsorclassesofindividuals,therelationshipshave
beengivenforeachgroupseparately(formoredetailsseeFigure2).Thesedescriptivestudies
suggestedthatfast-exploringadultssurvivedrelativelywellinenvironmentswithintensified
intra-sexualcompetition(ISC),butthattheysurvivedrelativelypoorlywhenISCwasrelaxed,
andthattheoverallshapeofnaturalselectionwasstabilizing.Formoredetailsseethetext.
formalesandfemales,andreversedbetweenyears(Figure2;Dingemanseet
al.,2004).InayearwithmastingofbeechesFagussylvaticus(2000),when
great tits experience relaxed competition for winter food (Perdeck et al.,
2000),andsubsequenthighrecruitmentratesinspring(i.e.,intensifiedcom-
petition 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,
whenslow-exploringadultmalesandfast-exploringadultfemaleshadhigh-
estsurvivalrates.
Naturalselectionandanimalpersonality 1165
Figure 2. Schematic overview of the fitness consequences of exploratory behaviour of
novelenvironments(rangingfrom‘slow’to‘fast’)inwildgreattits(Parusmajor)fortwo
typesofyears(poor[1999/2001]=nobeechmasting;rich[2000]=beechmasting)(Dinge-
manse et al., 2004). The arrows indicate the shape of selection (→ directional selection
favouring fast; ← directional selection favouring slow; →← stabilising; ←→ disruptive)
fortwomainfitnesscomponents,adultannualsurvivalandoffspringrecruitment,Hatched
barsindicatenonsignificanttrends.Formoredetailsseetext.
Temporalvariabilityinenvironmentalconditions
Dingemanse et al. (2004) hypothesized that beech masting affected the
strength of intra-sexual competition but that these effects were always op-
positeforterritorialmalesandfemales(Figures1,2):becausefemaleswere
subordinatetomales(Dingemanse&deGoede,2004),theywerelikelytobe
mostaffectedbycompetitionforwinterfood.Beechmastingthereforemay
resultinrelaxedintra-sexualcompetitionamongfemales,whilecompetition
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
adultssurvivedrelativelywellinyearswithintensifiedintra-sexualcompeti-
tion,andthattheysurvivedrelativelypoorlywhencompetitionwasrelaxed.
Notably, the potential cause for the poor survival of fast-exploring adults
insuchyearshasnotyetbeenidentified.Thisnotionofdifferentialcompeti-
tiveabilitywassupportedbythefindingthatfast-exploringadultsdominated
slow-exploring adults when competing for winter food (Dingemanse & de
Goede, 2004) and that fast-exploring adults bred on the best breeding terri-
1166 Dingemanse&Réale
tories(Bothetal.,2005).Factorsaffectingadultsurvivalaresummarizedin
Figure1.
Between-yearfluctuationinselectiononpersonalitytraitsinthegreattits
is similar to results from other studies on other types of traits (Merilä et al.,
2001).Thisresultindicatesthatselectionstudiesshouldbeperformedonthe
long-termifwewanttounderstandboththeimmediateconsequences(within
a year) and longer term effects (across several generations) of selection on
populations.
Fitnessconsequences:offspringproductionandrecruitment
Slow-exploring females had higher nest success (were more likely to pro-
duceatleastonefledgedoffspring),andproducedlargeroffspringthanfast-
exploring females (Both et al., 2005). Pairs of assortative phenotypes, con-
sisting 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
studyarea(‘offspringrecruitment’)actedonfemale,andtoalesserextenton
male exploratory behaviour and fluctuated between years (Figure 2; Dinge-
manseetal.,2004).Selectiononexploratorybehaviourwasstabilisinginthe
two years without beech masting, but was disruptive in the year with beech
masting.Thepersonalityofboththemaleandthefemaleparentcontributed
to this pattern of disruptive selection, as pairs consisting of assorted part-
ners (i.e., fast-fast or slow-slow pairs) produced most recruits in the beech
cropyear(Dingemanseetal.,2004).Theseassortedpairsalsoproducedoff-
springofhighestbodymass(seeabove),andasbodymassaffectscompeti-
tiveabilityandjuvenilewintersurvivalinyearswithintensecompetitionfor
resources among juveniles (Both et al., 1999), this pattern of disruptive se-
lection probably acted via offspring body massin the yearwith beech crop.
Interestingly, pairs of medium-exploring adults nevertheless produced most
recruits in years without beech crop, suggesting that the higher than aver-
ageoffspringbodymassofassortativepairsonlyincreasedfitnessincertain
years and that other characteristics of the offspring phentoype (e.g., their
exploratorybehaviour,seeFigure1)affectedoffspringrecruitment.
Fitnessconsequences:explainingvariablepatternsinoffspringrecruitment
While these variable patterns in adult survival have now resulted in testable
hypotheses, (i.e., fluctuating and sex-specific survival (Figure 2) reflected
Naturalselectionandanimalpersonality 1167
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 recruit-
ment 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
fromparentstooffspring(e.g.,byaffectingoffspringforagingsuccess;Fig-
ure1).Fieldstudiesshowedthatexploratorybehaviouraffectsbothcompet-
itive ability and settlement decisions of juveniles: fast-exploring juveniles
hadlowestdominancerankswhennonterritorial (Dingemanse&deGoede,
2004)andcametobreedfurtherfromhome(Dingemanseetal.,2003).
Evolutionaryconsequences
Natural selection acted on avian personality, but the direction of selection
variedbetweensexes,age-classesandyearswithdifferentselectiveregimes.
Becauseexploratorybehaviourofwildgreattitsisheritable(seeabove)and
affectscomponentsoffitness,selectiononavianpersonalitycanleadtoevo-
lutionary change (Fisher, 1930; Endler, 1986). While considering that the
response to selection depends both on the frequency with which individ-
uals 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 interme-
diate phenotype had highest offspring recruitment rates in most years, as
mastingofbeechesoccursonlyaboutonceeverythreeyears(Perdecketal.,
2000). Furthermore, the variance in adult survival was lowest for interme-
diate 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(Dingemanseetal.,2004),allowingthemtoproduceoffspringofinter-
mediatephenotypeandincreasetheirlifetimefitness.Notably,disassortative
matingseemedmaladaptivewhenonlyconsideringthatassortativepairshad
highest reproductive success (Both et al., 2005). Temporal variability in se-
lection as observed for this study system can slow down the loss of genetic
variation in avian personality (Sasaki & Ellner, 1997; Burger & Gimelfarb,
2002),butitcannot,however,provideanultimateexplanationforthemain-
tenance of genetic variation in avian personality. Either a balance between
1168 Dingemanse&Réale
mutation,selectionandmigrationinaspatiallyvariableenvironment(Nevo,
1988; Frank & Slatkin, 1990) or frequency-dependent selection (Maynard
Smith, 1982) probably need to be invoked to explain this behavioural di-
versity from an adaptive perspective (Dingemanse et al., 2004; Both et al.,
2005). Similarly, we do yet need to reveal why individual great tits showed
suchlimitedbehaviouralplasticity,asbehaviouralflexibilityseemsadaptive
insuchatemporallyvariableenvironment(Dall,2004).
Fitnessconsequencesofboldnessanddocilityinbighornsheep
Individualdifferencesincorrelatedbehaviours
In a wild Canadian population of bighorn sheep, individuals differed con-
sistently in their willingness to enter corral traps baited with salt (Réale et
al.,2000).Thisbehaviouralvariabilitywasassumedtoreflectindividualdif-
ferences 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
wascapturedinthetrap.Repeatability(betweenyears)andheritabilityesti-
mates 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 7-
point 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
struggledtoescape.Therewasanegative—thoughweak—phenotypiccor-
relationbetweenboldnessanddocility:shyeweswerealsorelativelydocile.
This negative pattern appeared to be caused by the absence of shy, non-
docile ewes. Estimation of quantitative genetics parameters using the ‘ani-
malmodel’(Lynch&Walsh,1998)revealedsignificantheritabilitiesofboth
behavioursaswellasamoderatenegativegeneticcorrelationbetweenthese
behaviours(D.Reale&D.Coltman,unpubl.data).
Fitnessconsequences:reproductivesuccess
Using standard multiple regression techniques to evaluate selection on cor-
relatedcharacters(Lande&Arnold,1983),selectiononeachbehaviourwas
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).
Boldewesreproducedatanearlieragethanshyewes.Similarly,docileewes