Temperaments and behavioural syndromes in non-human animals

Jean-François Le Galliard CNRS, University Pierre & Marie Curie, France

Concepts and methods

From behaviour to life histories

Behavioural variation mediates variation in habitat use and exploration growth and survival strategies mating strategies social interactions including competition & cooperation interspecific interactions

Obvious importance for life-history variation growth-survival trade-offs : activity behaviour density-dependence : aggressiveness / sociability reproductive effort vs. mating success : aggressiveness habitat use : exploration behaviour

From behaviour to life histories

Réale, D., Reader, S. M., Sol, D., McDougall, P. T., & Dingemanse, N. J. (2007) Biol. Rev. 82, 291-318.

Advantages of behavioural flexibility Behavioural variation vs “classical” phenotypic plasticity flexible (of the order of msec. or sec.) relatively cost-free (unlimited flexibility) integrates multiple sources of information reversible but sensitive to past experience (learning)

Main features of behavioural flexibility controlled by the neuro-endocrine system extremely sensitive to external factors (cues or stimuli) optimised to promote efficient responses optimised to allow efficient information transfer

Behavioral flexibility = adaptive flexibility The animal as a well-designed “behavioral machine”

Adaptive behavioural flexibility http://www.herpnet.net/Iowa-Herpetology/amphibians/frogs_toads/plainsSpadefootToad.html

Pfennig, D. W., Reeve, H. K., & Sherman, P. W. (1993) Anim. Behav. 46, 87-94.

Individual and population variation

Population mean Population response

Individual mean Individual response

Sih, A., Bell, A., & Johnson, J. C. (2004) Trends in Ecology and Evolution 19, 372-377.

Sources of variation among individuals Sampling variation measurement error (supposedly high for behavioural traits

Extrinsic factors experimental conditions : microclimate, day hour, season, etc environmental conditions : biotic and other abiotic experienced during and before behavioural tests, possibly mediated by intrinsic factors

Intrinsic factors genetic make up internal factors such as age, sex, developmental stage, but also condition, size, immune capacities, etc

A B

A B Behavioral variation

Behavioral variation

Behavioral variation

Behavioral variation

Behavioral variation

Behavioral variation

Individual and population variation

A B

A B

A B

A B

Individual and population variation

http://aquafish.free.fr/database/fish.php3?Fish=Poecilia%20Reticulata

Magellan, K. & Magurran, A. E. (2007) Animal Behaviour 74, 1545-1550.

When this individual variation gets a name Defined and reviewed in Réale et al. (2007) Biol. Rev. 82, 291-318.

Temperament / personality / individuality (Réale et al. 2007) differences in behaviour are consistent across time and / or contexts

Personality (restrictive, Gosling 1999) all those characters and qualities of individuals that account for consistent differences in thinking, feeling and behaving

Coping style (Koolhaas et al. 1999)

Inconsistency Randomness Consistency Personality

A

B

Behavioral variation

Behavioral variation

a coherent set of behavioural and physiological stress responses which is consistent over time and which is characteristic to a certain group of individuals

A

B

Structure in individual variation Territorial behavior in various stages and contexts in sticklebacks Dart at a facing position Toward and away movement

Biting attempt Movement of spines

Huntingford, F. A. (1976) Anim. Behav. 24, 245-260.

Structure in individual variation

G = intraspecific competition P = competition with another stickleback species N = newt

Consistency of territorial behaviors across stages and treatments

Huntingford, F. A. (1976) Anim. Behav. 24, 245-260.

Structure in individual variation Consistence of PCA factors (from all behaviors) across treatments

Huntingford, F. A. (1976) Anim. Behav. 24, 245-260.

Structure in individual variation Tests of boldness (against predators) and exploration Continuous record during 15 mins Movement, position, etc Two major axis “precaution-curiosity” “boldness-timidity” (audace)

Continuous record during few mins Movements, swimming Two novel tanks = weeded / bare tanks Two major axis “activity” “timidity-boldness”

Huntingford, F. A. (1976) Anim. Behav. 24, 245-260.

Structure in individual variation Comparison of response to predators, exploration and intruders

bold for a predator and a novel environment

shy for a predator and a novel environment

Huntingford, F. A. (1976) Anim. Behav. 24, 245-260.

Structure in individual variation : conclusion Behaviors in the three-spine sticklebacks are very consistent across contexts and across stages correlated changes in aggressiveness during reproductive cycle correlated changes in aggressiveness among intruders

Personality involves several “dimensions” territoriality : a temperament of curiosity and aggressiveness predation : a behavior of curiosity and boldness exploration : predation : a behavior of activity and boldness Some behaviors / temperaments are correlated boldness against predators and boldness against novel environment boldness against novel environments and aggression boldness against predators and aggression

Huntingford, F. A. (1976) Anim. Behav. 24, 245-260.

Behavioural syndromes

“Behavioral syndrome: a suite of correlated behaviors reflecting between-individual consistency in behavior across multiple (two or more) situations.” “Situation: a given set of conditions at one point in time. Different situations could involve different levels along an environmental gradient (e.g. different levels of predation risk) or different sets of conditions across time (e.g. the breeding season versus the non-breeding season).” Sih, A., Bell, A., & Johnson, J. C. (2004) Trends in Ecology and Evolution 19, 372-377. Bell, A. M. (2007) Proceedings of the Royal Society B-Biological Sciences 274, 755-761.

Temperaments and behavioural syndromes in context The Big Five

Personality dimensions in humans

Dominance

Gosling, S. D. & John, O. P. (1999) Curr Direc Psych Sci 8, 69-75. Gosling, S. D. (2001) Physiological Bulletin 127, 45-86.

Personality and ecology: some (clear) jargon Five potential categories defined by Réale et al. (2007) shyness-boldness: an individual’s reaction to any risky but not new situations = risk-taking behavior, docility, tameness and fearfulness exploration-avoidance : an individual’s reaction to a new situation = sometimes called boldness, neophobia activity: the general level of activity of an individual = sometimes boldness and exploration aggressiveness: an individual’s agonistic reaction towards conspecifics sociability: an individual’s reaction to the presence of conspecifics (excluding aggressive behavior) = sometimes shyness, avoidance (in solitary species)

Réale, D., Reader, S. M., Sol, D., McDougall, P. T., & Dingemanse, N. J. (2007) Biol. Rev. 82, 291-318.

Personality and ecology: a workable definition of temperament traits ?

Réale, D., Reader, S. M., Sol, D., McDougall, P. T., & Dingemanse, N. J. (2007) Biol. Rev. 82, 291-318.

Linking temperaments with the FFM ? Emotionality / coping Aggression Sociability Exploration

Gosling, S. D. & John, O. P. (1999) Curr Direc Psych Sci 8, 69-75.

Activity

Ecological tests of temperaments: boldness

Time 1

Time 2

Time 3

van Oers et al. (2004) Proceedings of the Royal Society of London Series B-Biological Sciences 271, 65-73.

Ecological tests of temperaments: boldness

Between-year repeatability r = 0.26 +/- 0.07

van Oers et al. (2004) Proceedings of the Royal Society of London Series B-Biological Sciences 271, 65-73.

Ecological tests of temperaments: boldness Consistency in ratings: P < 0.01-0.04

Correlation across contexts: r = 0.08, P = 0.50

Behavioral differences (tested before ratings) Novel object (stick)

Novel food source

Response category (rating) Shy = escape immediately Intermediate = escape after introd but above 5 cm Bold = espace below 5 cm

Coleman, K. & Wilson, D. S. (1998) Animal Behaviour 56, 927-936.

Ecological tests of temperaments: exploration

Day 1 “novel environment” Exploration: minimal time to visit 5 trees (or a similar measure!) Activity : several measures

Additional measures of behavior 1. Feeding behavior Reaction to a change in food location after habituation 2. “Boldness” Reaction to a novel object on a tree

Verbeek, M. E. M., Drent, P. J., & Wiepkema, P. R. (1994) Anim. Behav. 48, 1113-1121. Dingemanse et al. (2002) Animal Behaviour 64, 929-938.

Ecological tests of temperaments: exploration Arrival time varies between 40 sec and 10 mins

Verbeek, M. E. M., Drent, P. J., & Wiepkema, P. R. (1994) Anim. Behav. 48, 1113-1121.

Ecological tests of temperaments: exploration

Measure of repeatability (here from a fixed effect model) Intraclass correlation coefficient: r = V_between / (V_within + V_between)

Dingemanse et al. (2002) Animal Behaviour 64, 929-938.

Exploration in tits : one or two dimensions? Fast (superficial) exploration

Boldness

Strong habit strength

Fast (superficial) exploration

Verbeek, M. E. M., Drent, P. J., & Wiepkema, P. R. (1994) Anim. Behav. 48, 1113-1121.

Ecological tests of temperaments: sociability Field observation of social interactions between individuals Focal sampling Amicable: greetings and allogrooming Agonistic: avoid, chase and flee

http://www.u.arizona.edu/~rad3/index.html

Mirror image stimulation (15 mins)

Svendsen, G. E. & Armitage, K. B. (1973) Ecology 54, 623-627. Armitage, K. B. (1986) Ecology 67, 1186-1193.

Spent most time in from half of the cage

Ecological tests of temperaments: sociability

Engages in no activity close to the mirror

Makes nose contact with the mirror

Armitage, K. B. (1986) Ecology 67, 1186-1193.

Ecological tests of temperaments: activity

Introduction in a “novel environment” Boldness : measure of time to emerge from refuge Activity : measure of % time spent moving after emergence Exploration : measure of total volume explored

Cote et al. (2010) Proc London B

Ecological tests of temperaments: aggression http://www.u.arizona.edu/~rad3/index.html

Measurement of nest defense Trait rating at various breeding stages s ow d l l a ir sw ueb e e bl ch Tr ale efin M ous H

Duckworth, R. A. (2006) Behavioral Ecology 17, 1011-1019.

Tr

ee

ws llo a sw

Ecological tests of temperaments: aggression http://www.u.arizona.edu/~rad3/index.html

Duckworth, R. A. (2006) Behavioral Ecology 17, 1011-1019.

Ecological tests of temperaments: aggression http://www.u.arizona.edu/~rad3/index.html

b = -0.37, P = 0.41 Nestling period

b = -0.86, P < 0.01 Incubation period

Aggressiveness towards conspecific males

Duckworth, R. A. (2006) Behavioral Ecology 17, 1011-1019.

Synthesis A variety of traits exhibit significant consistency

Consistency across time suggests stable individual differences due to strong genetic effects, canalization of developmental trajectories and/or poor environmental effects Consistency across contexts suggests carry-over effects of behavioural traits measured in one ecological setting (feeding) on the same behavioral trait measured in another setting (territorial defense) Correlation between traits (syndromes) are often detected aggressive and boldness syndrome activity and exploration syndrome exploration and pro-active syndrome aggressiveness and parental care

To what extent does behavioural variation reflects temperaments ? Measure of repeatability from all published studies (759 estimates) Intraclass correlation coefficient: r = V_between / (V_within + V_between)

Grand mean: r = 0.37 [0.36, 0.38] Strong variation between contexts Some effects of study duration when excluding two outliers

< 1 year

> 1 year

Bell et al. (2009) Animal Behaviour 77, 771-783.

Not all behavioural traits are consistent! Test with fishes from two different populations Activity in an unfamiliar environment Aggressiveness towards a conspecific Boldness under predation risks Summarized in a PCA for each behavior and age class

es nil e v Ju

137 days

bSu

s ult d a

210 days

s ult d A

322 days

Bell, A. M., and J. A. Stamps. 2004. Animal Behaviour 68:1339-1348.

Fitness consequences & emergence of personality traits

Alternative views on temperaments and syndromes These processes reflect constraints At a mechanistic level : e.g. developmental, neural and hormonal mechanisms involved in behavioural variation within and between contexts [high T levels associated with territorial aggression also increases sexual aggression / activity levels, etc]. At a genetic level : pleiotropic effects of genetic variation in the developmental, neural and hormonal mechanisms involved in behavioral variation. Functional and evolutionary constraints on adaptive behavioral flexibility

These processes reflect adaptations Developmental canalization of behavioral variation, consistency of behavioral differences or syndromes may be beneficial : strong costs of canalization or flexibility selection against temporal and individual variation in behavioral traits that are most important for fitness and less costly to canalize social (frequency-dependent) selection for persistent differences in behaviors: being predictable can increase fitness in social encounters, state dependent behaviors, dominance hierarchies,

Dall, S. R. X., Houston, A. I., & McNamara, J. M. (2004) Ecology Letters 7, 734-739. Sih, A., Bell, A., & Johnson, J. C. (2004) Trends in Ecology and Evolution 19, 372-377.

Example of social interactions that can lead to stable differences Assumptions Pairs of active or inactive foragers Active foraging much more safe in pairs and birds observe each other Dynamic reserves associated with foraging / resting activities Threshold reserves for foraging

Dall, S. R. X., Houston, A. I., & McNamara, J. M. (2004) Ecology Letters 7, 734-739.

Maintenance of stable behavioural differences by life history trade offs Assumptions Two years life cycle with birthplace in a low-quality habitat Exploration (x) increases the chance to settle in high-quality habitats Exploration decreases the probability to breeding during the first year Fecundity is density-dependent in each habitat with larger baseline fecundity in HQ habitats Life history trade off between breeding at age 1 and dispersing/reproducing in a good habitat at age 2 Trade off mediated by exploration Density-dependent selection

Wolf, M., van Doorn, G. S., Leimar, O., & Weissing, F. J. (2007) Nature 447, 581-584.

Maintenance of stable behavioural differences by life history trade offs Assumptions Animals confronted to several risky situations (games) between year 1 and year 2 Foraging with a predator : boldness (bold-shy anti-predator game) = mortality cost but fitness rewards Confrontation to a competitor : aggressiveness (haw-dove game) = fighting cost but fitness rewards

Wolf, M., van Doorn, G. S., Leimar, O., & Weissing, F. J. (2007) Nature 447, 581-584.

Field tests of fitness effects of exploration Very complex effects on survival and fecundity in each sex ! Adult survival (sex of adult)

Fecundity * offspring survival (sex of parent)

Opposite selection between sexes

Opposite selection in each sex and between this year and the poor years

Opposite selection between sexes

Poor = low winter food Dingemanse et al. (2004) Proceedings of the Royal Society of London Series B-Biological Sciences 271, 847-852.

Field tests of fitness effects of exploration

A posteriori explanation Males compete for territories: they benefit from exploration/aggressiveness for territory acquisition in spring Females compete for resources and are subordinate: they benefit from exploration in winter Rich years are associated with poor winter competition for food relaxing competition on females exploration capacity (and costs are detected) Poor years are associated with low territory competition relaxing competition on males exploration capacity (and costs are detected)

Dingemanse et al. (2004) Proceedings of the Royal Society of London Series B-Biological Sciences 271, 847-852.

Field tests of fitness effects of boldness statesymbolsusa.org weblogs.cltv.com

Quantification of temperament Boldness : trappability of females Docility : score at each capture of females

Detection of selection during high predation years Predators select less bolder individuals ! Predators select less docile & younger individuals !

Réale, D. & Festa-Bianchet, M. (2003) Animal Behaviour 65, 463-470.

So what ?

Variable selection on temperaments fluctuating environments sexual and age differences Helps explain the maintenance of variation per se

Does not explain why individuals are consistent !

Meta-analysis of fitness effects Overview of 31 studies quantifying temperaments and fitness correlates Quantification of the Pearson’s product moment correlation coefficient between boldness/aggression/exploration and survival/reproductive success

Antagonistic reproductive and natural selection on boldness Positive natural selection on exploration Positive reproductive and natural selection on aggression

Smith, B. R. & Blumstein, D. T. (2008) Behavioral Ecology 19, 448-455.

Fitness landscape

Survival

Exploration / boldness

Boldness and life-history trade-offs

Growth and reproduction

Exploration / boldness Stamps, J. A. (2007) Ecology Letters 10, 355-363.