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The pace-of-life syndrome (i.e., POLS) hypothesis posits that behavioral and physiological traits mediate the trade-off between current and future reproduction. This hypothesis predicts that life history, behavioral, and physiological traits will covary under clearly defined conditions. Empirical tests are equivocal and suggest that the conditions necessary for the POLS to emerge are not always met. We nuance and expand the POLS hypothesis to consider alternative relationships among behavior, physiology, and life history. These relationships will vary with the nature of predation risk, the challenges posed by resource acquisition, and the energy management strategies of organisms. We also discuss how the plastic response of behavior, physiology, and life history to changes in ecological conditions and variation in resource acquisition among individuals determine our ability to detect a fast-slow pace of life in the first place or associations among these traits. Future empirical studies will provide most insights on the coevolution among behavior, physiology, and life history by investigating these traits both at the genetic and phenotypic levels in varying types of predation regimes and levels of resource abundance. Significance statement We revisit the pace-of-life syndrome hypothesis, suggesting that behaviors involving a risk of death or injury should coevolve with higher metabolic rates, higher fecundity, faster growth, and heightened mortality rates. Empirical support for this hypothesis is mixed. We show how relaxing some of the assumptions underlying the pace-of-life syndrome hypothesis allows us to consider alternative relationships among behavior, physiology, and life history, and why we fail to meet the predictions posed by the pace-of-life syndrome hypothesis in some populations. Our discussion emphasizes the need to re-integrate the role of the species’ natural history, ecological conditions, and phenotypic plasticity in shaping relationships among behavior, physiology, and life history.
Behaviors mediate the trade-off between current and future reproduction through their effects on various components of resources acquisition and risk of predation. Individuals can increase their survival by decreasing the rate of encounter with predators, by decreasing their chances of being detected, by increasing predator detection before an attack, or by improving the probability of escaping or surviving following an attack by a predator, respectively (orange boxes). To acquire resources and fuel their reproduction, individuals must search for, find, and handle food items. In some systems, resource acquisition involves scrounging from or defending food items against conspecifics (green boxes). The behavior most likely to mediate the trade-off between mortality risk and resource acquisition (black arrows and signs) is expected to vary across species depending on their different natural histories and on the relative importance of the various components of predation risk and resource acquisition. For example, we can expect that, in species where survival and resource acquisition depend more strongly on the rate of encounter with a predator and on time spent searching for resources, respectively, active individuals will trade their survival for higher current reproduction. In contrast, in species where survival and resource acquisition depend more strongly on detecting a predator and handling resources, individuals that invest more in reproduction rather than in survival will be less vigilant (but not necessarily more active). Note that some of the behaviors represented here could affect more than one component of predation risk or resource acquisition and that several other trade-offs could shape the evolution of a pace-of-life syndrome
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ORIGINAL ARTICLE
The pace-of-life syndrome revisited: the role of ecological conditions
and natural history on the slow-fast continuum
Pierre-Olivier Montiglio
1,2
&Melanie Dammhahn
1,3
&Gabrielle Dubuc Messier
1,4
&Denis Réale
1
Received: 5 July 2017 / Revised: 1 June 2018 / Accepted: 8 June 2018
#Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
The pace-of-life syndrome (i.e., POLS) hypothesis posits that behavioral and physiological traits mediate the trade-off between
current and future reproduction. This hypothesis predicts that life history, behavioral, and physiological traits will covary under
clearly defined conditions. Empirical tests are equivocal andsuggest thatthe conditions necessary for the POLS to emerge are not
always met. We nuance and expand the POLS hypothesis to consider alternative relationships among behavior, physiology, and
life history. These relationships will vary with the nature of predation risk, the challenges posed by resource acquisition, and the
energy management strategies of organisms. We also discuss how the plastic response of behavior, physiology, and life history to
changes in ecological conditions and variation in resource acquisition among individuals determine our ability to detect a fast-
slow pace of life in the first place or associations among these traits. Future empirical studies will provide most insights on the
coevolution among behavior, physiology, and life history by investigating these traits both at the genetic and phenotypic levels in
varying types of predation regimes and levels of resource abundance.
Significance statement
We revisit the pace-of-life syndrome hypothesis, suggesting that behaviors involving a risk of death or injury should coevolve with
higher metabolic rates, higher fecundity, faster growth, and heightened mortality rates. Empirical support for this hypothesis is
mixed. We show how relaxing some of the assumptions underlying the pace-of-life syndrome hypothesis allows us to consider
alternative relationships among behavior, physiology, and life history, and why we fail to meet the predictions posed by the pace-
of-life syndrome hypothesis in some populations. Our discussion emphasizes theneed to re-integrate the role of the speciesnatural
history, ecological conditions, and phenotypic plasticity in shaping relationships among behavior, physiology, and life history.
Keywords Behavior .Immunity .Life history strategies .Metabolism .Personality .Trait interaction
Introduction
Organisms must decide how much time or energy to invest in
reproduction relative to maintenance and survival (Stearns
1992). Depending on how they negotiate this trade-off, pop-
ulations or species are positioned along a fast-slow life history
continuum. This continuum ranges from organisms that prior-
itize reproduction over survival (i.e., a fast life history) to
those that prioritize survival over reproduction (i.e., a slow
life history, Stearns 1983,1989; Promislow and Harvey
1990). Differences in life history strategies among species or
populations are associated with differences in physiology such
as metabolic rate or stress reactivity (Wikelski and Ricklefs
2001; Ricklefs and Wikelski 2002).
Behavior might play a functional role in the fast-slow life
history continuum and thus covary predictably with life
Communicated by P. T. Niemelä
This article is a contribution to the Topical Collection Pace-of-life syn-
drome: a framework for the adaptive integration ofbehaviour, physiology
and life-history - Guest Editors: Melanie Dammhahn, Niels J.
Dingemanse, Petri T. Niemelä, Denis Réale
*Pierre-Olivier Montiglio
montiglio.pierre-olivier@uqam.ca
1
Département des Sciences Biologiques, Université du Québec à
Montréal, Case Postale 8888, Succursale Centre-ville,
Montreal, QC H3C 3P8, Canada
2
Department of Biology & Redpath Museum, McGill University,
1205 Dr. Penfield Avenue, Montreal, QC H3A 1B1, Canada
3
Animal Ecology, Institute for Biochemistry and Biology, University
of Potsdam, Maulbeerallee 1, 14469 Potsdam, Germany
4
Centre dÉcologie Fonctionnelle et Évolutive (CEFE), CNRS-UMR
5175, 1919 Route de Mende, 34293 Montpellier Cedex 5, France
Behavioral Ecology and Sociobiology (2018) 72:116
https://doi.org/10.1007/s00265-018-2526-2
history traits such as fecundity, survival, or growth (the pace-
of-life syndrome hypothesis, POLS thereafter, Stamps 2007;
Biro and Stamps 2008; Réale et al. 2010). The POLS hypoth-
esis predicts that if some behavioral traits such as high bold-
ness, exploration, aggressiveness, or activity increase acquisi-
tion of resources at an expense of survival, then individuals
expressing these traits should also have a faster life history
(Wolf et al. 2007; Réale et al. 2010). Species, populations,
or individuals with a faster pace of life should also invest less
resources in their immunological defenses (Tieleman et al.
2005;Martinetal.2006). Réale et al. (2010) initially invoked
correlational selection to explain the evolution of such associ-
ations between life history, physiology, and behavior, but
feedbacks between behavior and state could also explain
why we observe these associations at the individual level
(Luttbeg and Sih 2010; Dingemanse and Wolf 2013).
Since the initial publications (Stamps 2007;Biroand
Stamps 2008; Réale et al. 2010), multiple studies have inves-
tigated the relationships between behavior, physiology, and
life history within populations (Dammhahn et al. 2018).
Several of them have examined the relationships between
boldness, exploration, activity, or aggressiveness, and metab-
olism (e.g., Careau et al. 2009,2011; Timonin et al. 2011;
Gifford et al. 2014; Royauté et al. 2015; Binder et al. 2016;
White et al. 2016) or immunological functions (e.g., Niemelä
et al. 2013; Zylberberg et al. 2014; Dosmann et al. 2015).
Others have tested for and quantified the relationships be-
tween behavioral traits and age at maturity (e.g., Réale et al.
2000; Niemelä et al. 2013; Müller and Müller 2015; Urszán et
al. 2015), fecundity (e.g., Réale et al. 2000; Kontiainen et al.
2009; Brommer et al. 2014; Montiglio et al. 2014; Bridger et
al. 2015), survival (e.g., Réale and Festa-Bianchet 2003;Réale
et al. 2009;Bergeronetal.2013), and growth (e.g.,
Hoogenboom et al. 2013; Biro et al. 2014; White et al.
2016). Some studies support the initial predictions made by
the POLS hypothesis in its strict sense, but others have failed
to find such support (reviewed in Royauté et al. 2018,topical
collection on Pace-of-life syndromes).
Studies could fail to support the POLS hypothesis because
they characterize boldness, exploration, or activity with too
diverse methodologies (Royauté et al. 2018, topical collection
on Pace-of-life syndromes). These methodologies could vary
in their sensitivity to detect individual differences, or measure
different aspects of an animals behavior. Alternatively, as-
sumptions made by Wolf et al. (2007) or Réale et al. (2010)
may be too strict to fit all the possible associations between
behavior, physiology, and life history (we refer to these
models as predicting a POLS sensu stricto). Indeed, any trait
improving resources acquisition and current reproduction, at
the expense of survival or future reproduction, could coevolve
with an organisms pace of life. Alternatively, traits such as
exploration, aggressiveness, or activity do not automatically
improve resources acquisition.
Ecological conditions might also lead to varying de-
grees of association between behavior, physiology, and
life history depending on the population studied
(Dammhahn et al. 2018, topical collection on Pace-of-
life syndromes). Hence, we might need to reconsider the
strict definition used in the formulation of the POLS hy-
pothesis to account for the role of ecological conditions.
All these points were discussed in the initial papers (e.g.,
Réale et al. 2010) and in others (Adriaenssens and
Johnsson 2009; Mathot and Dingemanse 2015), but we
still lack a clear framework for predicting whether a syn-
drome should emerge and what relationships between be-
havior, life history, and physiology we should observe.
In this paper, we outline elements of such a frame-
work to explain variation in syndromes across systems
and ecological conditions. Our aim is to switch the focus
from testing whether the POLS structure suggested by
Réale et al. (2010) is observed or not to investigating
how ecological conditions (predation risk, resource ac-
quisition) shape relationships between life history, phys-
iology, and behavior at the genetic and phenotypic
levels. We consider several ways in which we can nu-
ance the predictions on the POLS sensu stricto. We ex-
tend the initial logic underlying the POLS hypothesis
(Stamps 2007;Wolfetal.2007;BiroandStamps2008;
Réale et al. 2010) to consider alternative structures of
relationships among behavior, physiology, and life histo-
ry. We first consider how relaxing the assumptions about
the functional role of behavior and physiology (see Table
1) in supporting the life history of organisms along the
fast-slow continuum generates alternative hypotheses and
predictions on the links among behavior, physiology, and
life history. Second, we consider how phenotypic plastic-
ity of behavior, physiology, and life history could shape
POLS.
Behavior and physiology can have different
roles within the pace-of-life syndrome
The POLS hypothesis assumes that particular behaviors
increase the risk of predation and the acquisition of re-
sources such as food, partners, or territories (Stamps
2007;Wolfetal.2007; Réale et al. 2010). The POLS
hypothesis also assumes that metabolism is the pacemaker
of an organisms pace of life or life history productivity
(Careau et al. 2008; Biro and Stamps 2010; Réale et al.
2010). Relaxing these assumptions allows us to focus on
predicting which behavioral and physiological adaptions
should be favored by a particular set of environmental
conditions. Below we discuss how the role of behavior
and physiology can vary within a POLS exhibited within
a species or population.
116 Page 2 of 9 Behav Ecol Sociobiol (2018) 72:116
Behavior
Several behavioral traits can affect resource acquisition and
the risk of predation (Fig. 1), but their relative importance
varies with the type of interaction between an organism and
its predators (Lima and Dill 1990) and with the characteristics
of the resources consumed. As a result, the type of resources
an organism acquires and the foraging behavior of its preda-
tors can affect which behavioral traits most likely support the
pace of life. For example, when an organisms vulnerability to
predation depends strongly on its ability to avoid encounters
with predators, we expect activity and exploration to covary
with the slow-fast life history continuum (Fig. 1).
Alternatively, when vulnerability to predation depends more
strongly on being detected by predators or increasing chances
of escapes following an attack, then we expect freezing be-
havior or flight initiation distance to covary with the pace of
life (Ydenberg and Dill 1986). Situations where predation risk
can be lowered by increasing the detection of potential pred-
ators by the prey, vigilance, rather than activity or freezing,
should covary with pace of life of organisms (Lima and Dill
1990).
Investigating the relationships between the chances of en-
counter with predators, the probability of being detected by
them, and the probability of detecting predators could also
explain why these traits can be correlated with each other in
some cases and not in others. Furthermore, predators exhibit a
diversity of foraging tactics, from sit-and-wait to active pur-
suit, varying both among individuals and among species
(Schmitz et al. 2004; Pruitt and Ferrari 2011; Miller et al.
2014). Hence, the type of hunting strategy of the predator or
the distribution of food patches in the environment should
affect which behaviors are most likely to be associated with
life history.
The exact constraints placed on resource acquisition can
also affect which behavior covaries with life history.
Activity and exploration are more likely to impact resource
acquisition in organisms foraging on clumped and ephemeral
food sources than in organisms foraging on abundant and
homogeneously distributed resources (Macarthur and Pianka
Table 1 Assumptions at the basis
of the evolution of a pace-of-life
syndrome sensu stricto within
populations and reasons why
these assumptions might not be
met
Assumptions to be tested Reasons why these assumptions may not be met
There is a trade-off between early-life reproduction,
and survival or late-life reproduction.
A large variance in resource acquisition among
individuals can hide the trade-off in the allocation of
resources between early-life and survival or late-life
reproduction.
Plastic responses to environmental changes and
uncontrolled environmental conditions may blur the
detection of the pace-of-life syndrome in a popula-
tion.
A trait associated to the pace of life (i.e., a behavioral
or physiological trait
a
) should play a functional role
for each of the life history traits.
The studied trait does not have any functional role on
either early reproduction or survival.
The studied trait is weakly repeatable, lowering its
association with life history traits or our statistical
power to detect this association.
Strict assumptions about the functional link between
behavior and both survival and reproduction (i.e.,
sensu Wolf et al. 2007; Réale et al. 2010) might not
be met. Relaxing these assumptions (i.e.,
pace-of-life syndrome sensu lato) may permit us to
consider situations in which the direction of the as-
sociation between behavior and life history is con-
trary to what is expected in the POLS hypothesis
sensu stricto.
Although two traits may independently affect
reproduction and survival, they may not be linked
with each other. Therefore,we may not expect that a
behavioral trait may be systematically linked to
metabolism, even though they both affect survival
and reproduction.
Correlational selection should favor some
combinations of behavioral/physiological and life
history traits.
The correlation between traits provides no fitness
benefit but is rather the results of constraints to their
independent expression.
a
Note that these traits need to be repeatable to show consistent links with life history traits. Highly labile traits
cannot be linked to any stable life history strategy. Traits can be repeatablebecause it is heritable ordevelopmen-
tally plastic (i.e., early life conditions or parental effects)
Behav Ecol Sociobiol (2018) 72:116 Page 3 of 9 116
1966;Heads1986;DixonandBaker1987; see also Fraser and
Gilliam 1987). Vigilance or freezing behavior is instead more
likely to covary with the pace of life when organisms rely on
food items requiring long bouts of handling (Krebs 1980;
Lima 1988). Alternatively, aggressiveness might covary with
the pace of life when contest/interference competition is asso-
ciated with resource acquisition (Wolf et al. 2007; Bergmüller
and Taborsky 2010; Montiglio et al. 2013).
Defining the role of behavioral traits in mediating life his-
tory trade-offs allows us to nuance our predictions on the
behaviors that are more likely to covary with the pace of life
of an organism. Considering the ecology of predation risk and
foraging of the individuals can change the predictions one
could derive from the POLS hypothesis. Furthermore, it gen-
erates richer and more specific predictions to on the link be-
tween ecology of species and the type of POLS they exhibit.
Of course, it is also possible that behavior does not mediate
any life history trade-off in some systems. Studies simulta-
neously reporting a clear trade-off between current reproduc-
tion and future reproduction or survival, and no relationship
between life history and behavior, are rare. Such studies would
be the strongest and clearest challenges to the POLS
hypothesis.
Physiology
The original POLS hypothesis posits that metabolism is the
pacemaker of life (Ricklefs and Wikelski 2002). Supporting
this view, individuals with a higher resting metabolic rate also
show the highest daily energy expenditure in many endo-
therms (Careau and Garland 2012). At the within-species lev-
el, individuals with a higher metabolic rate could potentially
afford a faster pace of life, because a higher metabolic rate
allows them to mobilize the energy needed to express a high
level of activity, a fast exploration, or high aggressiveness
(Careau et al. 2008; Biro and Stamps 2010; Réale et al. 2010).
Energy allocation, acquisition, and expenses might be
linked in several different ways (Careau et al. 2008;Careau
and Garland 2012; Mathot and Dingemanse 2015). For exam-
ple, daily energy expenditure can be independent of basal
metabolic rate (i.e., the allocation model, Speakman 1997).
In this case, individuals spending a lot of energy on mainte-
nance (expressed as basal metabolic rate) have less energy
available for energetically costly behaviors. Alternatively, a
greater capacity to produce and mobilize energy (reflected
by basal metabolic rate) could lead to a higher daily energy
expenditure (i.e., the performance model, Speakman 1997). In
this case, behaviors that both increase energy gain and energy
expenditure are predicted to scale positively with basal meta-
bolic rate, because individuals with a fast running metabolic
machinery also have to fuel it and must mobilize more energy
for energetically costly behaviors (Mathot and Dingemanse
2015). Finally, daily energy expenditure and basal metabolic
rate could also be unrelated (independent model) and only
behaviors increasing energy gain might scale positively with
basal metabolic rate (Mathot and Dingemanse 2015). Thus,
predicting the direction of among-individual correlations be-
tween metabolic, behavioral, and life history traits requires a
Fig. 1 Behaviors mediate the trade-off between current and future
reproduction through their effects on various components of resources
acquisition and risk of predation. Individuals can increase their survival
by decreasing the rate of encounter with predators, by decreasing their
chances of being detected, by increasing predator detection before an
attack, or by improving the probability of escaping or surviving
following an attack by a predator, respectively (orange boxes). To
acquire resources and fuel their reproduction, individuals must search
for, find, and handle food items. In some systems, resource acquisition
involves scrounging from or defending food items against conspecifics
(green boxes). The behavior most likely to mediate the trade-off between
mortality risk and resource acquisition (black arrows and signs) is
expected to vary across species depending on their different natural
histories and on the relative importance of the various components of
predation risk and resource acquisition. For example, we can expect
that, in species where survival and resource acquisition depend more
strongly on the rate of encounter with a predator and on time spent
searching for resources, respectively, active individuals will trade their
survival for higher current reproduction. In contrast, in species where
survival and resource acquisition depend more strongly on detecting a
predator and handling resources, individuals that invest more in
reproduction rather than in survival will be less vigilant (but not
necessarily more active). Note that some of the behaviors represented
here could affect more than one component of predation risk or
resource acquisition and that several other trade-offs could shape the
evolution of a pace-of-life syndrome
116 Page 4 of 9 Behav Ecol Sociobiol (2018) 72:116
priori knowledge of the underlying relationships between met-
abolic rate and energy expenditure in a given species (see also
Mathot and Dingemanse 2015).
The relationship between metabolic rate and energy
expenditure could also vary with a speciesnatural histo-
ry. For example, endotherms and ectotherms are likely to
show different relationships between metabolic rate and
energy expenditure, given their fundamental differences
in physiology. Several studies on species of fish demon-
strated that proactive individuals have higher standard
metabolic rates, thereby supporting predictions of the per-
formance model (e.g., Cutts et al. 1998; Lahti et al. 2012).
In contrast, studies on birds and mammals tend to provide
support for the allocation model (e.g., Wiersma and
Verhulst 2005; Vaanholt et al. 2007; but see Careau et
al. 2013). Future comparative research should clarify
whether this is indeed a general pattern and whether the
differential metabolic maintenance costs of these very dif-
ferent ways of life can explain such a pattern.
The relationships between metabolism and pace of life
should not only differ among species as a function of their
energy management strategy but should also vary with the
position of the organism in its life cycle. For example,
endothermic animals can exhibit tremendous reductions
in metabolic rate during some phases of their life cycle
(up to 99% reduction in metabolic rate, e.g., Thomas et al.
1990). The main feature of these strategies is to lower the
running costs of the metabolic engine for short (daily
torpor) or long (hibernation) periods of time by controlled
reduction of body temperature (i.e., heterothermy). Thus,
heterothermy is an important adaptation to fluctuating en-
vironmental conditions and has important life history con-
sequences, such as extended longevity and slow life his-
tories (Turbill et al. 2011). Individuals within species dif-
fer in their energy-saving strategies (Vuarin et al. 2013),
and this affects their survival and reproductive success
(Dammhahn et al. 2017). Analyzing such differences
among individuals can surely help us understand the rela-
tionships between physiology and life history (see also
Glazier 2015).
The pace of life can be apparent or hidden
The previous section detailed how different behaviors and
physiological traits can covary with an organismspaceoflife.
Such a view assumes that there is a life history trade-off and
that populations or species exhibit variation in the position of
their individuals along the fast-slow pace-of-life continuum.
However, the actual fast-slow pace-of-life continuum is not
always present in a population or species. In what follows, we
discuss when individuals should or should not vary over a
fast-slow pace-of-life continuum.
Local ecological conditions can drive or hide life
history trade-offs
Survival and reproduction can covary positively, negative-
ly, or not at all, depending on the variation in resources
acquired among individuals (van Noordwijk and de Jong
1986; Roff and Fairbairn 2007). Failure to detect the pre-
dicted link between behavior and life history could thus
be explained by a failure to detect a fast-slow pace-of-life
continuum in the first place. To fully validate or reject the
assumptions underlying the POLS hypothesis, we need to
study the relationships between life history, physiology,
and behavior over gradients of resource abundance or
predation risk (see Table 1). Yet very few studies have
achieved this level of insights. Changing ecological con-
ditions, for example, yearly fluctuations in predation pres-
sure, could change the role played by some behaviors in
the POLS. In other cases, there may be no clear trade-off
between early and late reproduction (Martin and Festa-
Bianchet 2011;Jablonszkyetal.2018 in press, topical
collection on Pace-of-life syndromes), potentially because
of selection eroding the variation in allocation strategies
within population, thereby making it impossible to detect
a link between behavior, physiology, and life history
(Réale et al. 2009).
Fixed or plastic pace-of-life syndromes?
The POLS hypothesis assumes that the plasticity of be-
havior is constrained by metabolic organs (Biro and
Stamps 2010; see Bijleveld et al. 2014 for an empirical
study challenging this assumption).Yet,temporalorspa-
tial variation in environmental conditions can induce a
change in an individuals morphology, life history, or
behavior (Walther et al. 2002; Réale and Festa-Bianchet
2003; Charmantier et al. 2008;Pfennigetal.2010;
Montiglio et al. 2014; Niemelä and Dingemanse 2017).
Ecological conditions determine our ability to identify a
life history trade-off at the phenotypic level and thus our
ability to detect a link between behavior, physiology,
and life history (Nicolaus et al. 2012; Montiglio et al.
2014).
When environmental variation occurs within at the
same spatial scale as the dispersal of individuals, indi-
viduals are likely to encounter different types of condi-
tions during their life. Selection should favor reversible
plasticity for the traits involved in the POLS (Sultan and
Spencer 2002). Such short-term reversible plastic chang-
es are not considered to be part of the syndrome
(Dingemanse et al. 2012b), but they can hide or affect
the relationships we observe among the traits. We thus
need to account for reversible plastic changes in behavior
and physiology to detect POLS at the population level.
Behav Ecol Sociobiol (2018) 72:116 Page 5 of 9 116
When environmental variation is strong and predictable,
selection should favor developmental (i.e., irreversible) phe-
notypic plasticity (Scheiner 1993;West-Eberhard2003;
Pigliucci 2005;Fitzpatrick2012). In this case, we should ex-
pect the evolution of an integrated developmental plasticity in
the pace of life of an organism (Nicolaus et al. 2012;
Montiglio et al. 2014). Changes in life history trajectory, be-
havior, and physiology may dependon early life conditions or
parental effects (Ellis et al. 2013). The environmental condi-
tions encountered by an organism early in life could be used to
anticipate future conditions and adjust its development ac-
cordingly (i.e., the predictive adaptive response hypothesis;
Gluckman et al. 2005;Monaghan2008) or instead constrain
its ability to cope with future conditions (i.e., the silver spoon
effect; Monaghan 2008). Developmental plasticity compli-
cates our task of detecting an association between the life
history of an organism and its behavior or physiology. For
example, differences in behavior and life history between
three populations of Corsican blue tits (Cyanistes caeruleus)
suggest the existence of a POLS in some years but not in
others (Dubuc Messier et al. 2016). This probably occurs be-
cause of plastic adjustments of both life history and behavior
traits that affect the mean position of each population along
the pace-of-life continuum (Dubuc Messier et al. 2016). It is
thus necessary to compare the traits across populations over
several years to be able to detect potential differences in pace
of life between them.
Finally, when the variation in ecological conditions occurs
at larger spatial scales, selection should favor the evolution of
locally adapted traits (Wang and Bradburd 2014) and thus
maintain some genetic polymorphism for traits along the
POLS (Dubuc Messier et al. 2016; GDM et al. unpublished).
The maintenance of some genetic polymorphism in POLS
traits can alsobe considered through the trade-off between life
history strategies involved in the POLS. The evolution of
plastic POLS traits does not preclude genetic associations be-
tween them (Brommer and Kluen 2012; Fitzpatrick 2012;
Santostefano et al. 2017). The relative importance of fixed
polymorphism and developmental plasticity in generating as-
sociations among traits involved in a syndrome will depend on
the fitness costs of this developmental plasticity, on the
strength of the genetic correlations among traits, and on the
predictability and magnitude of variation in ecological condi-
tions (Scheiner 1993; West-Eberhard 2003; Fitzpatrick 2012).
Conclusion: What should future studies
on the pace-of-life syndrome look like?
We can develop and nuance the initial POLS hypothesis by
considering a wider range of relationships between behavior,
physiology, and life history strategy. These relationships can
also emerge from genetic polymorphism and developmental
plasticity and be obscured by reversible plastic changes in the
traits. While we did not discuss this option extensively, it is
important that we consider the possibility that life history,
physiology, and behavior do not form a syndrome in some
systems. Studying such systems will be useful to illuminate
when we should expect the emergence of a pace-of-life syn-
drome and when we should not.
Future studies on the POLS hypothesis will move for-
ward if they analyze the relationships between life history,
physiology, and behavior over ecological gradients of pre-
dation risk, resource abundance and distribution, or popu-
lation density. This challenging goal will perhaps be
achieved most effectively by long-term studies monitoring
free-ranging individuals over several generations
(Dingemanse et al. 2004;Kontiainenetal.2009; Réale et
al. 2009; Quinn et al. 2011;Montiglioetal.2014;
Jablonszky et al. 2018, topical collection on Pace-of-life
syndromes) or by experiments manipulating ecological
conditions (Mathot et al. 2011,2012;Dingemanseetal.
2012a; Nicolaus et al. 2012a; Guenther and Trillmich
2013). A multivariate quantitative genetic framework and
a reaction norms approach will be key in analyzing such
complex datasets (Robinson et al. 2009; Husby et al. 2010;
Brommer 2013). We are aware that such studies will be
challenging. They will require repeated measurements on
multiple traits across different levels of predation pressure
or resource abundance for several individuals of known
relatedness or pedigree (Nussey et al. 2007; Husby et al.
2010;Brommer2013). Nevertheless, as data on behavioral
traits in long-term study programs are accumulating, this
type of analysis could be soon within reach for a greater
number of study systems (Niemelä and Dingemanse 2017;
for examples, see Santostefano et al. 2017).
Acknowledgements The authors thank all the participants of the two
workshops Towards a general theory of the pace-of-life syndrome,held
in Hannover in 2015 and 2016, for inspiring discussions as well as the
Volkswagen Stiftung (Az. 89905) for generously funding these work-
shops. We thank Jonathan Wright and coauthors for providing us an
unpublished manuscript. Members of DRs laboratory provided construc-
tive comments during the preparation of this manuscript. We also thank
two anonymous reviewers for their comments on the initial version of this
manuscript.
Funding information POM was supported by post-doctoral fellowships
from the Fonds de Recherche Québec: Nature et Technologies (FRQNT)
and the Natural Sciences and Engineering Research Council of Canada
(NSERC). GDM was supported by a FRQNT and a NSERC doctoral
fellowship. MD was supported by a DFG research fellowship (DA
1377/2-1) and DFG return fellowship (DA 1377/2-2). This research
was supported by an NSERC Discovery grant to DR.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict
of interest.
116 Page 6 of 9 Behav Ecol Sociobiol (2018) 72:116
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... Surprisingly, Moirón et al., (2020) had a counter-intuitive finding: risk-taking individuals in the wild lived significantly longer than their shy counterpart, a result that was lost in laboratory experiments. Such discrepancies from the POLS hypothesis can potentially be explained if the testing environment Chapter 1 -General Introduction does not support the correlation of certain relevant behaviours with life-history (Montiglio, Dammhahn, Dubuc Messier, & Réale, 2018) or if the natural and evolutionary history of study models are not favouring the trait association (Royauté et al., 2018). For instance, Moirón et al., (2020) suggest that the lack of resource restriction and predator pressure might explain the lack of relationship observed between risk taking behaviour and mortality in laboratory conditions. ...
... If behavioural syndromes are adaptive and appear as a result of particular ecological pressures, captive testing might hinder our ability to test for the presence of these syndromes (Adriaenssens & Johnsson, 2013). Similarly, if the costs and benefits of resource acquisition are reduced, life-history trade-offs might not be expressed (Montiglio et al., 2018;Royauté et al., 2018). ...
... Despite a large literature on life-history trade-offs and on animal personality, testing the link between these two phenomena has led to equivocal evidence (Montiglio et al., 2018;Royauté et al., 2018). For instance, female wild cavies (Cavia aperea) that explored more in a known captive environment grew faster, in accordance with theoretical predictions. ...
Thesis
In behavioural ecology, interest in the study of animal personality (i.e. consistent individual differences in behaviour across time and/or context) has increased in the last two decades as it is believed to have important ecological and evolutionary consequences. These consequences are especially pronounced when a behaviour that is consistent covaries with other consistent behaviours (i.e. behavioural syndrome) or with life-history traits (i.e. pace-of-life syndrome). So far, studies of behavioural and pace-of-life-syndromes have produced ambiguous outcomes (e.g. hypotheses are sometimes verified and others not), and the prominence of studies on captive animals (i.e. as opposed to wild animals) in the literature may be a reason for inconclusive results as trait covariation has been hypothesized to be environmentally driven. To address this knowledge gap, I investigated the emergence of behavioural and pace-of-life-syndromes in a wild population of juvenile sharks subject to relevant ecological pressures (e.g. predation risk, inter-individual competition). I explored (1) whether a behavioural syndrome existed between two consistent traits (exploration and sociability) and whether the appearance of the syndrome was context dependent, (2) whether a growth-mortality trade-off was mediated by exploration personality and (3) whether personality could predict the foraging habitat of sharks and whether this link was context-dependent. First, I observed a behavioural syndrome between sociability and exploration personality which was inconsistent across years and locations and was dependent on inter-individual competition. Then, I found the association between exploration personality and a growth-mortality trade-off to only be observable in low predation risk. Similarly, I found that exploration personality only predicted wild foraging habitat when predation risk was low. Overall, these results suggest that ecological conditions play a crucial role in the emergence and the shaping of personality and trait association. This thesis offers a possible explanation for the ambiguous results of previous studies and highlights the importance of increasing the focus on wild study systems that are subject to relevant ecological pressures in future animal personality research.
... As discussed by Montiglio, et al. (2018), there are many reasons why research has provided mixed and even contrary evidence for the POLS hypothesis even though it might be valid. One issue is whether behaviors assumed to be indicative of an adaptive "fast" life history strategy really do enhance fitness. ...
... Members of this team had previously proposed that such traits as high boldness, exploration, aggressiveness, and activity are "fast" adaptations (Réale, et al., 2010). They have since concluded that the universality of such trait suites is not supported by research, which should instead focus on how ecological conditions plastically shape fast-slow traits in different ways for different species (Montiglio, et al., 2018). However, LHT-P has generally continued to accept such fast-slow trait suites rather uncritically (Zietsch & Sidari, 2020), without understanding that they were initially presented as suggested research topics rather than as already being research-based (Del Giudice, 2020). ...
... Another common concern, in the special issue as well as the wider literature, is the lack of data on fitness outcomes by which to judge LHT-P hypotheses. Mammalian lab research is typically too far from wild conditions to provide such data, so there are frequent calls for more long-term field studies of animal populations in which individuals of known relatedness are followed from birth until death in sufficient numbers for statistical analyses to indicate the fitness effects of phenotypic responses to early life experiences (Bolund, 2020;Montiglio, et al., 2018;Regan, et al., 2020). ...
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High levels of stress are known to accelerate biological aging in susceptible individuals, often leading to a downward course of ill health and early death. This book-length review explores how and why. It is too long to expect anyone to read the whole thing, but it serves to keep track of my understandings and syntheses (as of May 2022) while delving into literatures on toxic stress, aging, life history, and evolutionary theory. A common theme in these literatures is the connection between early life adversity (ELA) and later ill health and early death. Just about the only evolutionary explanation to be found is that ELA signals infants and children to develop a “live fast, die young” strategy to beat the odds against reproduction in their harsh environments, but this siphons energy from bodily maintenance leading to ill health later in life. However, the “live fast, die young” model has been increasingly questioned based on both theory and research. Even if it is valid in some cases, it must be incomplete because it is based on individual level theoretical reasoning. But humans and most primates live in social groupings that can only exist because individuals give up some degree of autonomy as they cooperate and support each other, especially their close relatives. This review takes the very rare approach of asking what happens if we assess the mass of ELA research through the lenses of inclusive fitness and multilevel selection, which were both developed to explain the puzzle of altruism. Is it possible there’s an altruistic aspect to accelerated biological aging? We arrive at an answer of “yes” in a multilevel model of stress and aging which appears to be particularly unique in simultaneously accounting for (1) inclusive fitness as a universal design principle; (2) the existential imperative to control free-riders (a concept virtually absent in the aging and stress literatures); (3) allometric scaling with body size determining baseline species-specific metabolic rates and lifespans (as reflected in the same lifetime limit in number of heartbeats across all mammal species); (4) social status hierarchies as venues of social selection which imposes distresses and eustresses based on relative current social and prospective fitness values of individuals; and (5) the tendency of high social distress to accelerate biological aging while eustress can maintain or even decelerate it, thereby (6) channeling individuals along diverging reproductive arcs which advantage higher status individuals, but disadvantage and speed the altruistic exit-by-aging of lower status individuals along with identified predatory free-riders.
... insular prey species often fail to recognize or respond adequately to predators; [8,9]) and peculiarities of island birdsongs [10][11][12], whether and how insularity affects other behavioural aspects of animals has received far less attention. This is unfortunate, because behaviour is such an important part of the phenotype, and because many of the drivers of morphological, physiological and life-history evolution on islands are also likely to impinge on behavioural characteristics [13]. ...
Article
Full-text available
Animals on islands typically depart from their mainland relatives in assorted aspects of their biology. Because they seem to occur in concert, and to some extent evolve convergently in disparate taxa, these changes are referred to as the 'island syndrome'. While morphological, physiological and life-history components of the island syndrome have received considerable attention, much less is known about how insularity affects behaviour. In this paper, we argue why changes in personality traits and cognitive abilities can be expected to form part of the island syndrome. We provide an overview of studies that have compared personality traits and cognitive abilities between island and mainland populations, or among islands. Overall, the pickings are remarkably slim. There is evidence that animals on islands tend to be bolder than on the mainland, but effects on other personality traits go either way. The evidence for effects of insularity on cognitive abilities or style is highly circumstantial and very mixed. Finally, we consider the ecological drivers that may induce such changes, and the mechanisms through which they might occur. We conclude that our knowledge of the behavioural and cognitive responses to island environments remains limited, and we encourage behavioural biologists to make more use of these 'natural laboratories for evolution'.
... Alternatively, shy types might compensate for lower food consumption by reducing energy expended for activity or maintenance; these mechanisms need further experimental proof but are in line with results from multigenerational selection line experiments with bank voles (Sadowska et al. 2015). Ultimately, testing among-individual variation in solving the safety-reward tradeoff will require better ecological validation of behaviours (sensu Réale et al. 2007) allowing to identify 'truly risky behaviours' (Moiron et al. 2019), assessing potential compensation mechanisms, and testing the tradeoff under environmental conditions actually imposing predation risk (Montiglio et al. 2018). ...
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Perceived predation risk varies in space and time creating a landscape of fear. This key feature of an animal's environment is classically studied as a species‐specific property. However, individuals differ in how they solve the tradeoff between safety and reward and may, hence, differ consistently and predictively in perceived predation risk across landscapes. To test this hypothesis, we quantified among‐individual differences in boldness and activity and exposed behaviourally phenotyped male bank voles Myodes glareolus individually to two different experimental landscapes of risks in large outdoor enclosures and provided resources as discrete food patches. We manipulated perceived predation risk via vegetation height between 2 and > 30 cm and quantified patch use indirectly via RFID‐logging and giving‐up densities. We statistically disentangled among‐individual differences in microhabitat use from spatially varying perceived risk, i.e. landscape of fear. We found that individuals varied in mean vegetation height of their foraging microhabitats and that this microhabitat selection matched the intrinsic individual differences in perceived risk. As predicted by the patch use model, all individual's perceived higher risks when foraging in lower vegetation. However, individuals differed in their reaction norm slopes of perceived risk to vegetation height, and these differences in slopes were consistent across two different landscapes of risks and resources. We interpret these results as evidence for individual landscapes of fear, which could be predicted by among‐individual differences in activity and boldness. Since perceived predation risk affects when and where to forage, among‐individual differences in fear responses could act as a mode of intraspecific niche complementarity (i.e. individual niche specialization), help explain behavioural type by environment correlations, and will likely have cascading indirect effects on lower trophic levels.
... Potential relationships between metabolic rates and personality traits have received a lot of attention in recent literature (Careau et al. 2008;Biro and Stamps 2010;Réale et al. 2010;Montiglio et al. 2018). Many studies have shown individuals that have higher metabolic rates tend to behave more aggressively and boldly and/or win competitive interactions against conspecifics (Biro and Stamps 2010). ...
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Many animals raise and lower aggressiveness after recent wins and losses, respectively. Individuals that differ in internal/external conditions could also differ in their responsiveness to winning and/or losing experiences. Personality traits have been suggested to have close links with an individual’s responsiveness to environmental stimuli. Whether the responsiveness to winning-losing experiences is related to personality traits, however, remains unclear. Using a mangrove killifish, this study tested the hypothesis that personality traits (aggressiveness and boldness) and responsiveness to winning/losing experiences are linked because of their common associations with competitive ability. We also measured oxygen consumption rates to evaluate the importance of energy supply to the responsiveness. The results showed that aggressiveness, but not boldness or oxygen consumption rate, was associated with competitive ability and affected by winning/losing experiences. The fish’s responsiveness to winning-losing experiences was dependent only on competitive ability, but not aggressiveness or boldness; individuals with better (instead of worse) competitive abilities showed greater decreases in aggressiveness in response to losing experiences. The strong signals from multiple losing experiences together with worse competitors also exhibiting low aggressiveness (floor effects) may have given rise to these unpredicted results. Furthermore, (1) aggressiveness, boldness and oxygen consumption rate were positively correlated both before and after experience treatments and (2) individuals that were bolder or had higher oxygen consumption rates had higher increases in aggressiveness after experience treatments, consistent with the notion that individuals that are able to pay high metabolic costs can afford to behave boldly and aggressively and to raise aggressiveness further. Significance statement To adapt to changing environments, animals often show plasticity in behaviours. Personality traits have been suggested to have close links with responsiveness, such that bolder and more aggressive individuals are less responsive to environmental stimuli. Using a mangrove killifish, our study showed that aggressiveness and boldness did not affect whether or how the fish responded to recent wins or losses. Competitive ability, however, played an important role; better competitors had greater decreases in aggressiveness after losing experiences, contrary to our expectations. These results together with the results of previous studies of the fish suggest that the fish’s responsiveness to winning-losing experiences could be sensitive to its internal conditions, the strength of the stimuli and potential floor/ceiling effects. This study also showed that individuals that are able to pay high metabolic costs are able to behave boldly and aggressively and to raise aggressiveness further.
... Continually shifting environmental conditions can lead to challenges in identifying behavioural patterns and individual personalities, highlighting the importance of long term study [31,36]. Disparate movement behaviours have been observed in spatial ecology studies with links to other personality features [12,17], and in some cases have identified links between movement patterns with life history [13]. ...
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... The pace-of-life syndrome (POLS) hypothesis as an explanation for personality variation (Réale et al., 2010;Dammhahn et al., 2018) has been investigated more widely than the social niche hypothesis, likely because it can be applied to non-social, as well as social, animals (Montiglio et al., 2018;Royauté et al., 2018). POLS predicts that individual behavioural variation is maintained in a population as a result of life-history trade-offs: individuals with a slow paceof-life maximise future reproductive success through minimising risk, whereas individuals with a faster pace-of-life are willing to incur greater risk to increase current reproductive success. ...
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We describe a model for the evolutionary consequences of plasticity in an environmentally heterogeneous metapopulation in which specialists for each of two alternative environments and one plastic type are initially present. The model is similar to that proposed by Moran (1992) but extends her work to two sites. We show that with migration between sites the plastic type is favored over local specialists across a broad range of parameter space. The plastic type may dominate or be fixed even in an environmentally uniform site, and even if the plasticity has imperfect accuracy or bears some cost such that a local specialist has higher fitness in that site, as long as there is some migration between sites with different distributions of environmental states. These results suggest that differences among taxa in dispersal and hence realized migration rates may play a heretofore unrecognized role in their patterns of adaptive population differentiation. Migration relaxes the thresholds for both environmental heterogeneity and accuracy of plastic response above which plasticity is favored. Furthermore, small changes in response accuracy can dramatically and abruptly alter the evolutionary outcome in the metapopulation. A fitness cost to plasticity will substantially reduce the range of conditions in which the plastic type will prevail only if the cost is both large and global rather than environment specific.
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Given fundamental energetic trade-offs among growth, maintenance, and reproduction, individual differences in energy-saving should have consequences for survival and reproductive success. Many endotherms use periodic heterothermy to reduce energy and water requirements and individual variation in heterothermy should have fitness consequences. However, attempts to disentangle individual- and population-level variation in heterothermy are scarce. 2.Here, we quantified patterns of heterothermy of 55 free-ranging eastern chipmunks (Tamias striatus), food-hoarding hibernators. Over five hibernation periods, we obtained a total of 7108 daily individual heterothermy indices (median: 118 per individual). 3.Based on an individual reaction norm approach, we found that the use of heterothermy was repeatable and varied among individuals of the same population under similar environmental conditions. This among-individual variation had consequences for winter survival and reproductive success. Individuals using less heterothermy at the beginning of the winter had decreased survival in resource-rich but not in resource-poor years and higher reproductive success in the subsequent breeding season. 4.These results support the hypothesis that fluctuating selection maintains heterothermic diversity and suggest that individualized eco-physiology can contribute to a more thorough understanding of the evolution of energy-saving strategies in endotherms. This article is protected by copyright. All rights reserved.
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The concept of behavioural syndromes (i.e. correlations between behavioural traits) has provided an important framework for understanding individual variation in animal behaviour and its link to individual variation in physiology and life-history traits. The pace-of-life syndrome concept posits that behavioural, physiological and life-history traits coevolve in response to correlated selection pressures, and therefore predicts a positive correlation between boldness (i.e. exploration and risk taking) and metabolic capacity for locomotor performance in individuals. We tested for a pace-of-life syndrome linking boldness and metabolic capacity for locomotor activity in juvenile bluegill sunfish, Lepomis macrochirus. Individual fish were screened and classified as bold or shy using an established refuge emergence test. Subsequently, the aerobic and anaerobic metabolisms of bold and shy individuals were quantified using respirometry and by measuring the metabolic by-products of white muscle anaerobic glycolysis following exhaustive exercise, respectively. Bold fish demonstrated 25% greater metabolic scope for activity (i.e. aerobic capacity) than shy fish, which was attributable to a 15% greater maximum metabolic rate. However, there was no significant difference in resting metabolic rate or anaerobic energy expenditure (i.e. anaerobic capacity) between bold and shy fish. These results partially support a pace-of-life syndrome linking boldness and aerobic metabolism in juvenile bluegill sunfish, but did not reveal a link between boldness and anaerobic metabolism. Our findings suggest that aerobic and anaerobic capacities may be subject to different selection pressures, and that physiological processes governing maximum anaerobic performance in fishes are independent from behavioural and physiological traits related to boldness.
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This introduction to the topical collection on Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology, and life history provides an overview of conceptual, theoretical, methodological, and empirical progress in research on pace-of-life syndromes (POLSs) over the last decade. The topical collection has two main goals. First, we briefly describe the history of POLS research and provide a refined definition of POLS that is applicable to various key levels of variation (genetic, individual, population, species). Second, we summarise the main lessons learned from current POLS research included in this topical collection. Based on an assessment of the current state of the theoretical foundations and the empirical support of the POLS hypothesis, we propose (i) conceptual refinements of theory, particularly with respect to the role of ecology in the evolution of (sexual dimorphism in) POLS, and (ii) methodological and statistical approaches to the study of POLS at all major levels of variation. This topical collection further holds (iii) key empirical examples demonstrating how POLS structures may be studied in wild populations of (non)human animals, and (iv) a modelling paper predicting POLS under various ecological conditions. Future POLS research will profit from the development of more explicit theoretical models and stringent empirical tests of model assumptions and predictions, increased focus on how ecology shapes (sex-specific) POLS structures at multiple hierarchical levels, and the usage of appropriate statistical tests and study designs.
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Environmental heterogeneity can result in spatial variation in selection pressures that can produce local adaptations. The pace-of-life syndrome hypothesis predicts that habitat-specific selective pressures will favor the coevolution of personality, physiological, and lifehistory phenotypes. Few studies so far have compared these traits simultaneously across different ecological conditions. In this study, we compared 3 personality traits (handling aggression, exploration speed in a novel environment, and nest defense behavior) and 1 physiological trait (heart rate during manual restraint) across 3 Corsican blue tit (Cyanistes caeruleus) populations. These populations are located in contrasting habitats (evergreen vs. deciduous) and are situated in 2 different valleys 25 km apart. Birds from these populations are known to differ in life-history characteristics, with birds from the evergreen habitat displaying a slow pace-of-life, and birds from the deciduous habitat a comparatively faster pace-of-life. We expected personality to differ across populations, in line with the differences in pace-of-life documented for life-history traits. As expected, we found behavioral differences among populations. Despite considerable temporal variation, birds exhibited lower handling aggression in the evergreen populations. Exploration speed and male heart rate also differed across populations, although our results for exploration speed were more consistent with a phenotypic difference between the 2 valleys than between habitats. There were no clear differences in nest defense intensity among populations. Our study emphasizes the role of environmental heterogeneity in shaping population divergence in personality traits at a small spatial scale.