What are the future works in this paper?

( 6 ) The term “ personality ” started to appear independently in behavioral-ecology studies of mam- mals and reptiles as if it expressed a concept that at least seemed easily understood by all, but future studies of animal personality must become more than phenomenological in nature. ( 8 ) Although intraindividual variation and motivation can be seen as “ nuisance ” parameters in studies of performance, they can also become part of a comprehensive study of the relative importance of intra- and interindividual plasticity and consistency in correlations among traits. However, studies that focus on hormone titers alone will likely provide an incomplete picture, as significant variation might be present in other components of neuroendocrine signaling systems, such as concentrations of hormonebinding proteins or the location, type, or abundance of receptors.

What are the contributions in this paper?

The study of phenotypic evolution should be an integrative endeavor that combines different approaches and crosses disciplinary and phylogenetic boundaries to consider complex traits and organisms that historically have been studied in isolation from each other. For example, the study of individual variation recently facilitated the integration of behavior into the concept of a pace-of-life syndrome and effectively linked the field of energetics with research on animal personality. Here, the authors illustrate how studies on the pace-of-life syndrome and the energetics of personality can be integrated within a physiology-performance-behavior-fitness paradigm that includes consideration of ecological context. The authors first introduce key concepts and definitions and then review the rapidly expanding literature on the links between energy metabolism and personality traits commonly studied in nonhuman animals ( activity, exploration, boldness, aggressiveness, sociability ). The authors highlight some empirical literature involving mammals and squamates that demonstrates how emerging fields can develop in rather disparate ways because of historical accidents and/or particularities of different kinds of organisms. The authors then briefly discuss potentially interesting avenues for future conceptual and empirical research in relation to motivation, intraindividual variation, and mechanisms underlying trait correlations. The diversity and design of particular functional systems can be properly understood only from the selective, genetic and historical perspectives that evolution provides ; and the evolutionary processes of selection and adaptation can be truly understood only when the mechanistic bases underlying functional systems are elucidated. The integration of performance traits within the pace-of-life-syndrome concept has the potential to fill a logical gap between the context dependency of selection and how energetics and personality are expected to interrelate.

(Open Access) Performance, Personality, and Energetics: Correlation, Causation, and Mechanism* (2012) | Vincent Careau

Deakin Research Online

This is the published version:

Careau, Vincent and Garland Jr., Theodore 2012, Performance, personality, and energetics:

correlation, causation, and mechanism, Physiological and biochemical zoology, vol. 85, no.

6, November-December, pp. 543-571.

Available from Deakin Research Online:

http://hdl.handle.net/10536/DRO/DU:30056093

Reproduced with the kind permission of the copyright owner.

Performance, Personality, and Energetics: Correlation, Causation, and Mechanism

Author(s): Vincent Careau and Theodore Garland Jr.

Source:

Physiological and Biochemical Zoology,

Vol. 85, No. 6 (November/December 2012), pp.

543-571

Published by: The University of Chicago Press

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543

INVITED PERSPECTIVE

Performance, Personality, and Energetics: Correlation, Causation,

and Mechanism*

* This Invited Perspective is part of the Focused Issue on “Intraspeciﬁc Variation

in Physiology and Behavior.”

†

Corresponding author; e-mail: vcareau@ucr.edu.

Physiological and Biochemical Zoology 85(6):543–571. 2012. 䉷 2012 by The

DOI: 10.1086/666970

Vincent Careau

†

Theodore Garland Jr.

Department of Biology, University of California, Riverside,

California 92521

Accepted 5/27/2012; Electronically Published 10/1/2012

ABSTRACT

The study of phenotypic evolution should be an integrative

endeavor that combines different approaches and crosses dis-

ciplinary and phylogenetic boundaries to consider complex

traits and organisms that historically have been studied in iso-

lation from each other. Analyses of individual variation within

populations can act to bridge studies focused at the levels of

morphology, physiology, biochemistry, organismal perfor-

mance, behavior, and life history. For example, the study of

individual variation recently facilitated the integration of be-

havior into the concept of a pace-of-life syndrome and effec-

tively linked the ﬁeld of energetics with research on animal

personality. Here, we illustrate how studies on the pace-of-life

syndrome and the energetics of personality can be integrated

within a physiology-performance-behavior-ﬁtness paradigm

that includes consideration of ecological context. We ﬁrst in-

troduce key concepts and deﬁnitions and then review the rap-

idly expanding literature on the links between energy metab-

olism and personality traits commonly studied in nonhuman

animals (activity, exploration, boldness, aggressiveness, socia-

bility). We highlight some empirical literature involving mam-

mals and squamates that demonstrates how emerging ﬁelds can

develop in rather disparate ways because of historical accidents

and/or particularities of different kinds of organisms. We then

brieﬂy discuss potentially interesting avenues for future con-

ceptual and empirical research in relation to motivation, in-

traindividual variation, and mechanisms underlying trait cor-

relations. The integration of performance traits within the

pace-of-life-syndrome concept has the potential to ﬁll a logical

gap between the context dependency of selection and how en-

ergetics and personality are expected to interrelate. Studies of

how performance abilities and/or aspects of Darwinian ﬁtness

relate to both metabolic rate and personality traits are partic-

ularly lacking.

It can scarcely be denied that the supreme goal of all

theory is to make the irreducible basic elements as simple

and as few as possible without having to surrender the

adequate representation of a single ... experience. (Ein-

stein 1934, p. 165)

Individual differences are no accident. They are gener-

ated by properties of organisms as fundamental to be-

havioral science and biology as thermodynamic prop-

erties are to physical science. Much research, however,

fails to take them into account. (Hirsch 1963, p. 1436)

Biological reality is so complex that we are very far from

any reasonably mechanistic understanding of evolution-

ary processes. (Felsenstein 1988, p. 468)

The diversity and design of particular functional systems

can be properly understood only from the selective, ge-

netic and historical perspectives that evolution provides;

and the evolutionary processes of selection and adap-

tation can be truly understood only when the mecha-

nistic bases underlying functional systems are elucidated.

(Bennett and Huey 1990, p. 251; citing Arnold 1983)

Introduction

Evolution can be studied in many ways. We can focus on what

happened in the past through phylogenetic analyses of species

and/or population differences, which can be highly informative

even in the absence of information from the fossil record (Nunn

2011; Rezende and Diniz-Filho 2012). We can focus on the

present by studying living populations in order to measure

selection acting in the wild (Endler 1986; Kingsolver and Dia-

mond 2011), perform quantitative genetic analyses (Roff 1997),

and even attempt to identify the genetic and environmental

factors underlying individual variation in traits within popu-

lations (Feder 2007; Visscher et al. 2008; Barrett and Hoekstra

2011). We can also look toward the future by use of selection

experiments and experimental evolution (Garland and Rose

2009).

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544 V. Careau and T. Garland Jr.

Although each of the foregoing approaches has its strengths,

a complete and cohesive understanding of how evolution has

shaped complex phenotypes requires a combination of ap-

proaches (Arnold 1983; Bennett and Huey 1990; Huey and

Kingsolver 1993; Garland and Carter 1994). For example, to

evaluate whether phenotypic differences among populations

and species represent the outcome of adaptive evolution in

response to natural selection, we must understand, at a min-

imum, (1) how different phenotypes perform selectively chal-

lenging tasks under various ecologically relevant conditions, (2)

how different environmental conditions inﬂuence ﬁtness, and

(3) the extent to which phenotypic differences are genetically

based, through the use of common-garden experiments (Rose

and Lauder 1996; Irschick and Garland 2001; Mazer and Da-

muth 2001). In addition, even a clear understanding of steps

1–3 will not accurately predict the response to selection on a

focal phenotypic trait if selection also acts on genetically cor-

related (and perhaps unmeasured) traits (Lande 1979; Lande

and Arnold 1983; Houle 1991; Dochtermann and Roff 2010).

Clearly, the study of evolution should be an integrative enter-

prise that both combines different approaches (Barrett and

Hoekstra 2011) and crosses disciplinary barriers to study phe-

notypic traits that historically have been studied in isolation

from each other.

Irrespective of the method used to study evolution, two facts

are undeniable: individual variation (see table 1 for a glossary

of terms) within populations is omnipresent, and many (if not

most) evolutionarily relevant measurements are made on in-

dividual organisms. Although individual variation is usually

seen as measurement error in comparative analyses of species

differences (Ives et al. 2007), it is the keystone level of analysis

in quantitative genetics and studies of selection in the wild.

Individual variation is most commonly viewed as the raw ma-

terial on which natural selection acts, but it can also be the

result of selection itself, as both natural and sexual selection

sometimes favor the coexistence of alternative morphs or strat-

egies within a population (Wilson et al. 1994; Wilson 1998;

Calsbeek et al. 2002; Dingemanse and Re´ale 2005; Oliveira et

al. 2008; Corl et al. 2010). The study of individual variation

can contribute to our understanding of evolution because it

can be used to (1) determine the magnitude and consistency

of the raw material on which selection can act, (2) measure

selection in action, (3) determine heritabilities and genetic cor-

relations of traits, (4) elucidate the mechanistic bases of higher-

level traits, and (5) identify functional relationships among

traits (Bennett 1987; Pough 1989; Friedman et al. 1992; Garland

and Carter 1994). A renewed focus on individual variation can

provide both challenges to conventional wisdom and tremen-

dous opportunities for physiologists to contribute to evolu-

tionary biology (Williams 2008; see “Mechanisms”).

One main advantage of studying individual variation is that

it has the potential to bridge many gaps in the study of mor-

phology, physiology, behavior, ecology, evolution, and popu-

lation biology (Bennett 1987). Most recently, the study of in-

dividual variation facilitated the integration of behavior into

the pace-of-life-syndrome concept (Re´ale et al. 2010b)and

helped to crystallize study of energetics and personality (Careau

et al. 2008; Biro and Stamps 2010). For example, it is intuitive

to think about a scenario in which differences in boldness can

be generated and maintained within a population, depending

on how performance is affected by metabolic rate (see ﬁg. 5

in Careau et al. 2008). In a high-risk environment (with pred-

ators), the ecologically relevant performance trait for bold in-

dividuals may be sprint speed (to escape predators), whereas

for shy individuals it may be fasting endurance (to survive

longer under protective cover). We therefore believe that further

improvements in these areas of research must consider how

performance relates to both energy metabolism and behavior

and how all three together inﬂuence aspects of Darwinian ﬁt-

ness (see ﬁg. 1).

Objectives

We ﬁrst attempt to integrate performance with concepts related

to the energetics of personality and the more general pace-of-

life syndrome (for deﬁnitions, see table 1). After introducing

the key concepts of performance, personality, and energetics,

we review the rapidly growing literature on the energetics of

personality. To place these recent developments into perspective

and foster the integration of energetics and environmental con-

texts into the physiology-performance-behavior-ﬁtness para-

digm, we also offer a historical overview of the research on

individual variation in nonprimate mammals and squamates.

We consider only these groups because they reﬂect our own

interests and expertise and because the study of individual var-

iation in these groups has a long and surprisingly parallel his-

tory. Finally, we brieﬂy discuss three of the many opportunities

arising from integrative research on individual variation: mo-

tivation, intraindividual variation, and mechanisms.

The Physiology-Performance-Behavior-Fitness Paradigm in

Relation to Energetics and Ecological Context

In an inﬂuential article, Arnold (1983, p. 352) suggested that

“the problem of measuring the selection gradient becomes

manageable if we break it into two parts.” In the laboratory,

we can study how whole-organism performance is related to

underlying variation in morphology, physiology, or biochem-

istry (i.e., quantify the performance gradients). In the ﬁeld, we

can study the associations between performance and Darwinian

ﬁtness or components thereof (i.e., quantify the ﬁtness gradi-

ents). Since Arnold (1983), it has become generally acknowl-

edged that selection acts more directly on performance traits

(e.g., maximum sprint speed, locomotor stamina, fasting en-

durance, milk output) than on lower-level traits that determine

performance abilities (e.g., leg length, muscle-ﬁber type com-

position; e.g., Bennett 1989; Bennett and Huey 1990; Garland

and Carter 1994; Garland and Kelly 2006) and that direct mea-

sures of organismal performance can provide a bridge between

skin-in and skin-out biology.

Arnold (1983, p. 348) used morphology “as a shorthand for

any measurable or countable aspect of structure, physiology or

behavior.” He may have lumped behavior in with other lower-

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Performance, Personality, and Energetics 545

level traits because he mainly had aspects of motivation in

mind. In contrast, Garland and Losos (1994) argued that be-

havior should be at a different level of biological organization

than lower-level or subordinate traits (see ﬁg. 1). In this ex-

panded scheme, behavior is seen as a potential “ﬁlter” (Garland

et al. 1990) between selection and performance capacities (Gar-

land and Carter 1994). For example, an animal confronted with

a particular predator might remain motionless rather than run-

ning away at top speed, which would obviate the selective im-

portance of variation in sprint speed. In addition, animals can

choose microhabitats that affect their performance abilities, as

when a lizard allows its body temperature to fall below the

optimal for sprinting ability or moves onto a substrate that

reduces traction. However, the inclusion of behavior in this

framework remains a matter of considerable discussion (Losos

et al. 2004; Husak 2006; Irschick et al. 2008; Duckworth 2009;

Adriaenssens 2010). Given the proliferation of conceptual stud-

ies on individual variation and empirical research on the phys-

iological underpinnings of behavior, its heritability, and its re-

lationships with Darwinian ﬁtness (Dingemanse and Re´ale

2005; Sih and Bell 2008; Re´ale et al. 2010a), the time is ripe

for further consideration.

The framework we propose in ﬁgure 1 and discuss at length

in its caption is centered on performance and behavior but

includes physiology (used as a shorthand for all lower-level

traits that determine performance capacities), Darwinian ﬁt-

ness, energetics, and environmental context. In an ideal world,

a researcher could gather data at all levels and implement a

path analysis (structural equation model) on the complete di-

agram to test the implied causal relations (e.g., that natural

selection generally acts most directly on behavior and/or en-

ergetics, less on performance abilities, and least directly on

lower-level morphological, physiological, and biochemical

traits). In reality, however, there will always be missing links

(Bennett 1997), as huge effort is needed to obtain (repeated)

measures for all trait categories in multiple environmental con-

texts, which involves using several different techniques and

probably multiple ﬁeld seasons. Moreover, wild animals can be

kept in the laboratory only for short periods of time, as ex-

tended time in captivity may affect their phenotype and/or

incur consequences on their subsequent release (e.g., loss of

territory or food cache), which places additional constraints on

the type and number of measures that can be taken. Therefore,

trade-offs occur involving how many components (physiology,

performance, behavior, and ﬁtness), traits per component (e.g.,

measure one or many behaviors), individuals, and repeated

measurements per individual the researcher wants to consider.

Still, as Bennett (1997, p. 12) noted, “Getting partial answers

may be better than waiting forever to discover the perfect sys-

tem.” In any case, a framework such as that shown in ﬁgure

1 is helpful to guide the design of future studies and to see the

limitations of previous studies that inevitably include fewer than

all possible components (and traits). Long-term, individual-

based studies of a wild population of marked individuals offer

many advantages for studying this framework, presuming that

estimates of lifetime ﬁtness measures can be derived and in-

dividuals can be recaptured to measure different aspects of their

biology (Clutton-Brock and Sheldon 2010).

The framework depicted in ﬁgure 1 has the potential to bring

together researchers with different backgrounds and interests.

Typically, an ecologist would tackle the study of individual var-

iation from the perspective of variation in ecological context

(e.g., population density, food abundance, predation risk). At

the other end of the framework, physiologists would start from

individual variation in biochemical, morphological, and phys-

iological traits. Interestingly, the place where ecologists and

physiologists, starting from their own ends of the framework,

will meet is behavior and/or energetics, making the study of

energetics and behavior pivotal to the entire framework.

Animal Personality

Individual differences in behavior have been of great interest

to psychologists for at least a century (Nettle and Penke 2010),

and it is now generally accepted that human personality (Bou-

chard and Loehlin 2001) includes ﬁve primary factors (extra-

version, openness, conscientiousness, neuroticism, and agree-

ableness), each of which includes a number of subordinate

facets (Digman 1990; Costa and McCrae 1992; Koski 2011). By

using questionnaires to sample these big ﬁve, psychologists have

gained considerable knowledge about human personality and

its ontogeny, heredity, stability in adults, differences between

men and women, and other aspects (Digman 1990; Costa et

al. 2001). Although psychological studies of personality were

mainly restricted to humans (but see Tryon 1942) for the simple

reason that it was difﬁcult to administer a questionnaire to

other species, psychologists have recently renewed their interest

in studying animal personality (Gosling 2001, 2008) and have

started to adopt an evolutionary perspective on human per-

sonality (Nettle 2006; Penke et al. 2007; Nettle and Penke 2010).

Behavioral ecologists also recently became interested in an-

imal personality (Sih et al. 2004a, 2004b; Dingemanse and Re´ale

2005; Re´ale et al. 2007). Re´ale et al. (2010a) highlighted the

different deﬁnitions of animal personality that have emerged

in this ﬁeld. Under the broad deﬁnition of personality, any

repeatable behavior can technically be termed a personality

trait, as repeatability implies that differences among individuals

show at least some statistical consistency (Bell et al. 2009). In

this case, it can be hard to see the advantage of using the word

“personality” instead of “repeatable individual differences in

behavior” other than to save words (or increasing the “sexiness”

of the subject matter). Still, because the substance of science

is intimately related to its expression (Gopen and Swan 1990),

using “personality” as a word encapsulating several others can

help the ﬂow of thoughts and potentially clarify complex con-

cepts. However, if the meaning of animal “personality” varies

substantially among researchers, then it will ultimately hinder

progress. Many important articles on interindividual variation

in behavior published 20–30 yr ago do not contain the word

“personality” (e.g., Bennett 1980; Arnold 1983; Arnold and

Bennett 1984; Garland 1988, 1994b; Boake 1989).

In this review, we emphasize a narrow-sense concept of an-

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Performance, Personality, and Energetics: Correlation, Causation, and Mechanism*

Figures

Citations

Human biochemical genetics

Animal personality and state–behaviour feedbacks: a review and guide for empiricists

Fish bioenergetics: (Fish and Fisheries 13. Series ed. T.J. Pitcher) Malcolm Jobling Chapman and Hall, London, 1994 ISBN 0-412-58090-X, 24.99 Hard cover, acid-free paper, pp. xiv + 309, 31 tables, 61 figures Author, species and subject indexes

Environmental stressors alter relationships between physiology and behaviour.

Variation in the link between oxygen consumption and ATP production, and its relevance for animal performance

References

Introduction to quantitative genetics

The Genetical Theory of Natural Selection

Human biochemical genetics

The Genetical Theory of Natural Selection

Personality structure: emergence of the five-factor model

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