Biol. Rev. (2014), 89, pp. 48–67. 48
Behavioural syndromes and social insects:
personality at multiple levels
Jennifer M. Jandt1,∗,†, Sarah Bengston2,†, Noa Pinter-Wollman3, Jonathan N. Pruitt4,
Nigel E. Raine5, Anna Dornhaus2and Andrew Sih6
1Department of Ecology, Evolutionary and Organismal Biology, Iowa State University, Ames, IA 50011, USA
2Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
3BioCircuits Institute, University of California, San Diego, La Jolla, CA 92093-0328, USA
4Department of Biological Science, University of Pittsburgh, Pittsburgh, PA 15260, USA
5School of Biological Sciences, Royal Holloway University of London, Surrey, TW20 0EX, UK
6Department of Environmental Science and Policy, University of California, Davis, CA 95616, USA
Animal personalities or behavioural syndromes are consistent and/or correlated behaviours across two or more
situations within a population. Social insect biologists have measured consistent individual variation in behaviour within
and across colonies for decades. The goal of this review is to illustrate the ways in which both the study of social insects
and of behavioural syndromes has overlapped, and to highlight ways in which both ﬁelds can move forward through the
synergy of knowledge from each. Here we, (i) review work to date on behavioural syndromes (though not always referred
to as such) in social insects, and discuss mechanisms and ﬁtness effects of maintaining individual behavioural variation
within and between colonies; (ii) summarise approaches and principles from studies of behavioural syndromes, such as
trade-offs, feedback, and statistical methods developed speciﬁcally to study behavioural consistencies and correlations,
and discuss how they might be applied speciﬁcally to the study of social insects; (iii) discuss how the study of social
insects can enhance our understanding of behavioural syndromes—research in behavioural syndromes is beginning to
explore the role of sociality in maintaining or developing behavioural types, and work on social insects can provide new
insights in this area; and (iv) suggest future directions for study, with an emphasis on examining behavioural types at
multiple levels of organisation (genes, individuals, colonies, or groups of individuals).
Key words: behavioral syndromes, behavioural types, levels of organisation, behavioural carryover, behavioural
consistency, temperament, repeatability.
I. Introduction ................................................................................................ 49
(1) Deﬁning ‘behavioural syndromes’ ...................................................................... 49
(2) Mechanisms affecting behavioural type ................................................................ 50
(3) Fitness effects of behavioural syndromes ............................................................... 50
II. Social insects and a hierarchy of behavioural types ......................................................... 51
(1) Variation within colonies .............................................................................. 51
(a) Variation in morphological castes .................................................................. 52
(b) Variation in monomorphic species ................................................................. 52
(c) Mechanisms underlying intra-colony variation in behavioural type ................................. 52
(i) Genetics ...................................................................................... 52
(ii ) Physiology .................................................................................... 55
(iii ) Environment ................................................................................. 55
* Address for correspondence (Tel: +520-603-5850; Fax: +515-294-1337; E-mail: firstname.lastname@example.org)
†Authors contributed equally.
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
Behavioural syndromes and social insects 49
(d) Fitness consequences of intra-colony behavioural variation ......................................... 55
(2) Variation among colonies .............................................................................. 56
(a) Mechanisms underlying variation among colonies in behavioural type ............................. 56
(i) Colony genetics ............................................................................... 56
(ii ) Colony composition and emergent behaviour ................................................ 56
(iii ) Colony environment .......................................................................... 57
(b) Fitness consequences of colony behavioural syndromes ............................................. 58
III. Insights from behavioural syndromes for the study of social insects ......................................... 58
(1) Trade-offs .............................................................................................. 58
(2) Feedback ............................................................................................... 58
(3) Statistical methods ..................................................................................... 59
IV. Insights from social insects for behavioural syndromes ..................................................... 59
(1) Group-living might affect behavioural type ............................................................ 59
(2) Mechanisms affecting behavioural type ................................................................ 60
(3) Development of behavioural types across levels of organisation ........................................ 60
V. Future directions ........................................................................................... 60
(1) What are the adaptive reasons for colonies, or groups of individuals, to maintain mixtures of behavioural
types? .................................................................................................. 60
(2) Do colonies differ in their degree of cooperation? ...................................................... 61
(3) How does consistency in behavioural type affect task performance when individuals switch task? ..... 61
VI. Conclusions ................................................................................................ 62
VII. Acknowledgements ......................................................................................... 62
VIII. References .................................................................................................. 62
In recent years, numerous studies have found that animals
exhibit ‘personalities’ or behavioural syndromes—consistent
and/or correlated behaviour across two or more situations
(Gosling, 2001; Dall, Houston & McNamara, 2004; Sih, Bell
& Johnson, 2004a;Sihet al., 2004b;R
eale et al., 2007; Biro &
Stamps, 2008; Sih & Bell, 2008; Dall et al., 2012; Garamszegi
& Herczeg, 2012). For example, although most individuals
alter their level of aggression depending on the ecological
situation (e.g. resource availability or predation risk), some
are consistently more aggressive than others (Riechert &
Hedrick, 1993; Wilson et al., 1994; Sih, Kats & Maurer,
2003; Duckworth, 2006; Bell & Sih, 2007; Johnson & Sih,
2007). Furthermore, aggressive behaviour is often correlated
with bold behaviour or high activity level (Huntingford,
1982; Riechert & Hedrick, 1993; Bell, 2005; Johnson & Sih,
2005). To date, much of the work on behavioural syndromes
has focused on variation in boldness, aggressiveness, or
activity level (R´
eale et al., 2007), referred to here as ‘classical’
Consistent individual differences in behaviour have long
been recognized and studied in several taxa, including
humans, primates, laboratory rodents, and a few domesti-
cated mammals (Gosling, 2001). Intraspeciﬁc differences in
behavioural type have also been described when individuals
differ in morphology. This includes classic stereotypical
ideas on differences in behavioural type between males and
females, and between alternative mating morphs [e.g. larger,
aggressive, territorial males versus smaller, sneaky, satellite
males (Gross & Charnov, 1980)]. Recent studies, however,
have emphasized that individual behavioural differences
also exist in animal taxa that lack phenotypic polymorphism
(Sih et al., 2004b).
Social insects can exhibit behavioural variation at multiple
levels of organisation: between species, colonies, castes,
individuals, and genetic lines (Keller, 1999). Social insect
species have long been known to differ in behavioural type
(e.g. more aggressive species outcompete and may even
displace subordinate species; Davidson, 1998; Holway &
Suarez, 1999). Social insect castes (i.e. reproductive or mor-
phologically distinct individuals) also differ in behavioural
tendencies often associated with their specialized task (e.g.
soldiers are more aggressive than other workers). Thus, social
insect researchers have always considered, and quantiﬁed,
behavioural syndromes. However, until recently, few social
insect studies have investigated differences in behavioral type
among colonies (within a species) or among monomorphic
individuals within a colony (but see Jeanne, 1988). In
addition, few social insect studies have investigated whether
variation in behavioural type carries over across tasks. For
example, in species that exhibit temporal polyethism (work-
ers transition between tasks over time), it would be interesting
to determine whether young nurses (brood-care workers)
with a highly aggressive behavioural type are also more
aggressive as older foragers or more likely to guard the nest.
Such consistency in behavioural type carried over across
task transitions could have implications for colony ﬁtness.
(1) Deﬁning ‘behavioural syndromes’
Behavioural syndromes are deﬁned as consistent individual
differences, within a population, in behaviour within and
across context (Table 1). If an individual differs consistently in
a behaviour (e.g. is consistently more aggressive than others),
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
50 J. M. Jandt and others
Table 1. A comparison of terms used in animal behavior and social insect biology that describe similar phenomena
Animal behaviour terms Social insect biology terms
Individuals within a population exhibit consistency/correlation in
two or more functionally different behaviours
Animal personality Morphological/reproductive caste
Individuals within a population exhibit consistency in a single
Physiological constraints (genetics, morphology, hormones, etc.)
predispose individuals to perform speciﬁc behaviours (e.g.
queens and workers)
Behavioural type Behavioural specialisation
Individual exhibits consistent behaviour across contexts and/or
over time. Repeatability or consistency of the magnitude of
behaviour often observed. This can be a continuous or discrete
Individual exhibits consistent task performance (that is not
necessarily determined by its morphology)
Episodic personality Temporal polyethism
Response to one set of stimuli predicts the response to other sets of
stimuli over a short time scale. Responses are inconsistent over
longer time scales.
In a predictable order, individuals switch among tasks as they
Individuals switch among tasks throughout their lifetime.
Keystone individuals Elite workers/activators
An individual that signiﬁcantly alters the behaviour of other
individuals within the group.
Individuals that stimulate others, perform multiple tasks, or
perform a disproportionate amount of work in the colony.
then that individual has a behavioural type (Table 1), and
the population has a behavioural syndrome (Sih et al., 2004a;
Dingemanse et al., 2010). Recently, Garamszegi & Herczeg
(2012) differentiated animal personalities (‘consistency in
single behaviours’) and behavioural syndromes (consistency
in two or more functionally different behaviours’) (Table 1).
These distinctions are most important when developing
experimental design and performing statistical analyses (see
Section III.3). In either case, to test whether individuals
differ in behaviour in a particular context, it is necessary to
quantify the behaviour of a set of individuals in standardized
conditions, e.g. while foraging or building a nest (R´
et al., 2007). Although most of the recent interest has been
on differences among individuals in behavioural type, one
can also look for consistent differences among populations or
species in behavioural type. Social insects allow for additional
levels of analysis—caste (within colonies) and colony.
(2) Mechanisms affecting behavioural type
A growing literature examines the mechanisms associated
with differences among individuals of a behavioural type.
Numerous studies have quantiﬁed physiological or neu-
roendocrine correlates of behavioural types (Koolhaas et al.,
2007; Biro & Stamps, 2008; Careau et al., 2008; van Oers &
Mueller, 2010). Genetic studies show that behavioural types
typically exhibit low to moderate heritability (i.e. heritability
(H2)=0.2–0.5; van Oers et al., 2005; Penke, Denissen &
Miller, 2007; van Oers & Mueller, 2010), with recent studies
identifying candidate genes, often associated with neuroen-
docrine pathways, that explain some of the variation among
behavioural types (e.g. Ben-Shahar et al., 2002; van Oers &
Mueller, 2010). Genetic effects on behavioural types are also
typically moderated by individual experience. In particular,
early experience can often have strong effects on the devel-
opment of a later behavioural type and associated hormonal
‘stress response’ systems (Stamps & Groothuis, 2010; Del
Giudice, Ellis & Shirtcliff, 2011; Sih, 2011). Many of these
mechanisms have been studied in social insects; however, as
highlighted below, much remains to be discovered.
(3) Fitness effects of behavioural syndromes
Recent behavioural syndrome research has focused on the
ecological and evolutionary relevance of within-population
variation in behavioural type. An individual’s behavioural
type can clearly affect its ﬁtness, typically in context-
dependent ways (Smith & Blumstein, 2008); e.g. in a safe
environment, selection might favour bold individuals that
enjoy high feeding or mating success, but in a dangerous
environment, cautious individuals might be more likely to
survive (Fig. 1A). Notably, if individuals of a particular
behavioural type exhibit limited behavioural plasticity, their
behaviour could be suboptimal in situations that do not ﬁt
their behavioural type well. For example, bolder individuals
can be inappropriately bold when predators are present (Sih
et al., 2003), and aggressive individuals can be inappropriately
aggressive towards mates (Johnson & Sih, 2005), or can
exhibit poor parental care (Duckworth, 2006). Given the
potentially strong effects of behavioural types on ﬁtness,
many studies have asked how variation in behavioural types
is maintained, e.g. via environmental variation in selection
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
Behavioural syndromes and social insects 51
Fig. 1. Concepts that have been borne out in behavioural syndrome (A) and social insect (B) research that could beneﬁt the other
ﬁeld. (A) Behavioural syndromes—trade-offs of behavioural type across ecological context. Trade-offs associated with behavioural
syndromes help us understand why populations maintain correlated behavioural types. For example (i) a bold cricket will be a better
procurer of food, but (ii) a shy cricket will be less likely to be seen and eaten by a predator. (B) Social insects — multiple levels
of selection/organisation. (i) Development of an individual’s behavioural type is affected by internal and external mechanisms. (ii)
Intra-colony composition (variation within and among castes) and development may affect colony behaviour (performance). (iii)
Colony performance may feedback and inﬂuence intra-colony composition. (iv) Inter- and intra-colony interactions can feed back
and affect colony-level behaviour.
pressures (Dingemanse et al., 2004), frequency dependence
(Dall et al., 2004; Pruitt & Riechert, 2009), or condition
dependence (Luttbeg & Sih, 2010). Behavioural syndromes
can also have important ecological implications, e.g. effects
on species interactions, population dynamics, ecological
invasions, etc. (Sih et al., 2012).
II. SOCIAL INSECTS AND A HIERARCHY OF
Social insects are unique in that selection acts on multiple
levels (Fig. 1B; Folse & Roughgarden, 2010) . In a social insect
colony, workers and queens are individual organisms, but the
colony itself can be considered a ‘superorganism’ (H¨
& Wilson, 2009). In general, colonies produce more colonies:
the queen as the primary reproductive resembles a ‘germ cell’,
whereas non-reproductive workers resemble ‘somatic cells’
in that they care for their sisters and queen but do not directly
contribute to the next generation. However, in many species,
workers might also compete with one another and the queen
to lay unfertilized eggs which can develop into reproductive
males. Consistent individual differences (i.e. behavioural
types) are found at both levels of organisation: within a colony
(among workers and queens), and across colonies. Here we
review the current knowledge of individual variation within
and among colonies. We discuss both the mechanisms and
ﬁtness consequences of variation at each of these two levels.
(1) Variation within colonies
Individuals in social insect colonies commonly differ
consistently in behaviour. This is usually interpreted as an
effect of their allocation to specialized roles or ‘tasks’, e.g.
nurses, guards, foragers, etc. Such specialization produces
a division of labour, and is thought to be adaptive at the
colony level (Robinson, 1992; Beshers & Fewell, 2001). When
there is variation in morphology (castes; Table 1), such as
soldiers versus ‘minor’ workers (Wilson, 1976), behavioural
variation might be correlated with caste differences, although
variation could also be found within a caste. The majority
52 J. M. Jandt and others
of social insect species, however, are monomorphic, i.e.
there are no morphological differences between workers
olldobler & Wilson, 1990). Nevertheless, workers that look
the same might vary greatly in their behaviour. In some cases,
these behavioural differences might lead to task groups or
behavioural specialisations (Table 1), and still variation can
be observed within these behavioural groups. Thus, social
insects provide ample opportunities for studying the effects
of morphology and other factors on behavioural syndromes.
(a)Variation in morphological castes
Morphological castes are an important functional ‘grouping’;
variation in morphology often predisposes individuals to
behave in a certain manner or to perform particular
tasks (Oster & Wilson, 1978; H¨
olldobler & Wilson, 1990).
Even in non-insect social groups, individuals often differ in
behavioural tendencies based on morphology (e.g. males and
females; Del Giudice, 2011) or body size (e.g. courting versus
coercive mating tactics in large and small mosquitoﬁsh males;
Hughes, 1985). In social insects, castes are thought to be a
colony-level adaptation (Oster & Wilson, 1978; H¨
& Wilson, 1990): morphologically specialized individuals
are able to perform functions that would otherwise be
inaccessible (e.g. defensive soldier castes in Cephalotes spp.
ants; Powell, 2008).
Within a caste, a range of behavioural variation might
also persist. For example, task preference or efﬁciency can
vary within caste. Within the forager/worker caste of leaf-
cutter ants, as mandibles wear away, the individual can no
longer cut leaves efﬁciently and thus perform the function
to which this particular morphology predisposes it (Schoﬁeld
et al., 2011). This wear not only creates variation within the
caste in terms of cutting efﬁciency, but it also prompts a
switch in task preference to carrying leaves instead of cutting
(Schoﬁeld et al., 2011).
To date there has been little work exploring the extent
to which individuals within a caste vary in other behaviours
(Table 2). For example, are some soldiers more aggressive
than others, and are they also aggressive in other situations
aside from nest defence? While studies have highlighted the
relative importance of castes to colony function (Porter &
Jorgensen, 1981; Powell & Franks, 2006; Powell, 2008), little
has been done to explore the importance of behavioural
variation observed within castes.
(b)Variation in monomorphic species
Variation in behavioural type has also been observed in
species without clear morphological castes. In social insects,
social behavioural types (e.g. foraging, defence, etc.; Table
2) are the most commonly studied. Still, individuals within a
colony could vary in behavioural type along a variety of axes
such as those studied in the classic behavioural syndrome
literature and/or the cognitive ecology literature (Sih & Del
Giudice, 2012; Table 2). For example, Myrmica spp.ant
workers vary not only in the task they are most likely to
perform, but also in general behavioural type: patrollers are
bolder, more aggressive, and more exploratory across various
contexts than nurses or foragers (Chapman et al., 2011).
In social insect research, a lot is known about how individ-
ual workers differ in behaviour in ways that affect their role in
the colony, and how these behaviours correlate with others
across contexts (i.e. behavioural syndromes). A well-studied
case is variation among honey bee (Apis mellifera) foragers.
Some individuals have lower sucrose response thresholds (i.e.
are more likely to respond to less-concentrated nectar), and
are more likely to collect pollen, whereas those with higher
sucrose response thresholds are more likely to collect nectar
while foraging (Page, Erber & Fondrk, 1998; Scheiner,
Erber & Page, 1999; Scheiner, Page & Erber, 2004).
Sucrose response thresholds also correlate with reproductive
development in workers (Amdam & Page, 2010), forager
decision-making (Cakmak et al., 2009), the likelihood
of collecting non-food rewards, such as water or resin
(Simone-Finstrom, Gardner & Spivak, 2010) and learning
ability (Scheiner, 2012). In this sense, the cluster of correlated
behaviours associated with sucrose response threshold is a
broad behavioural syndrome affecting a series of seemingly
unrelated behaviours across a variety of contexts.
We also observe variation in behaviours not directly
corresponding to particular tasks. For example, although
more aggressive workers might be more likely to engage
in colony defence (i.e. more likely to attack non-nestmates:
Crosland, 1990; Modlmeier & Foitzik, 2011), they could
also be inappropriately aggressive to nestmates (van Doorn,
1989; Powell & Tschinkel, 1999; Robson et al., 2000; Foster
et al., 2004; Molina & O’Donnell, 2009).
(c)Mechanisms underlying intra-colony variation in behavioural type
(i)Genetics. Multiple mating by a queen leads to an
increase in within-colony genetic variation (i.e. workers are
less related to one another) that can result in intra-colony
variation in behavioural types (Table 3). In harvester ants
(Pogonomyrmex spp.), genotype could predispose an individual
to develop into a queen or a worker (Volny & Gordon, 2002;
Cahan & Keller, 2003; Schwander, Cahan & Keller, 2007;
Schwander et al., 2010). Genotypic differences in honey
bees might affect individual learning differences (Chandra,
Hosler & Smith, 2000) and foraging preferences (Page et al.,
1998). Genetic factors are also linked to how quickly a honey
bee worker transitions between tasks (Page et al., 1998;
Amdam & Page, 2010). Page, Rueppell & Amdam (2012b)
have summarized many of these genetic effects in terms
of the ‘pollen-hoarding syndrome’, and have shown how
overlapping genetic architecture could provide a mechanism
for behavioural syndromes, both at the individual and
Behavioural variation also readily occurs within colonies
where queens only mate with one male, making all workers
full sisters and intra-colony genetic variation low [e.g. bumble
bees (Jandt & Dornhaus, 2009), rock ants (Dornhaus et al.,
2008), social spiders (Pruitt et al., 2011)]. In these cases, gene
expression difference might underlie behavioural variation
(Table 3). For example, differential expression of the for
Behavioural syndromes and social insects 53
Table 2. Traits in which individual (=Intra-colony) and colony (=Inter-colony) level behavioural variation, i.e. different behavioural
types, have been measured in social insects
Behavioral type Intra-colony-level examples Inter-colony-level examples
Classical Aggression Ants
Chapman et al. (2011), Crosland (1990),
Modlmeier & Foitzik (2011) and Powell &
Pearce et al. (2001)
Cant et al. (2006), Reeve & Nonacs (1997)
Adams et al. (2007)
Buczkowski & Silverman (2006), Crosland
(1990) and Suarez et al. (2002)
Pearce et al. (2001)
Adams et al. (2007)
Chapman et al. (2011) and Modlmeier & Foitzik
Chapman et al. (2011)
Gordon et al. (2011) and Pinter-Wollman
et al. (2012a)
Cognitive Sensory bias/preference Bees
Page et al. (2012b), Spaethe et al. (2007) and
Spaethe & Chittka (2003)
Ings et al. (2009), Raine & Chittka (2005,
2007b) and Raine et al. (2006a)
Latshaw & Smith (2005), Laverty (1994),
Lihoreau et al. (2012b), Molet et al. (2009),
Muller et al. (2010), Page et al. (2012b), Raine &
Chittka (2012), Scheiner et al. (2003) and
Worden et al. (2005)
Chittka et al. (2004), Ings et al. (2009),
Raine & Chittka (2008, 2012) and Raine
et al. (2006a,b)
Speed and accuracy in
Burns & Dyer (2008), Chittka et al. (2003), Dyer &
Chittka (2004) and Kulahci et al. (2008)
Pinter-Wollman et al. (2012a)
Wray & Seeley (2011)
Social Cooperation Ants
Cahan & Fewell (2004)
Pruitt & Riechert (2009)
Robinson et al. (1990)
Pruitt & Riechert (2011)
Pinter-Wollman et al. (2011)
Mattila et al. (2008)
Hygienic behaviour Ants
Diez et al. (2011)
Arathi et al. (2000) and Visscher (1988)
Scharf et al. (2012)
Paleolog (2009) and Wray et al. (2011)
Pinter-Wollman et al. (2012b)
Liang et al. (2012)
Wray & Seeley (2011)
Beverly et al. (2009), Gordon et al. (2005) and
Pinter-Wollman et al. (2012b)
Fewell & Page (1993), Liang et al. (2012),
Lihoreau et al. (2010, 2011, 2012a,b), Muller
et al. (2010), Page et al. (2012b), Raine & Chittka
(2007a), Robinson & Page (1989), Saleh &
Chittka (2007) and Spaethe & Weidenm¨uller
Bengston & Dornhaus (2013), Cole et al.
(2010), Gordon et al. (2011), Gordon et al.
(2013) and Pinter-Wollman et al. (2012a)
Gill et al. (2012), Ings et al. (2006), Page
et al. (2012b), Raine & Chittka (2007b,
2008) and Wray et al. (2011)
Gr¨uter et al. (2012)
Pinter-Wollman et al. (2012a)
Wray et al. (2011)
We divide these into: ‘classical’—those behavioural axes most commonly measured in the behavioural syndrome literature, ‘cognitive’—those most commonly
measured in the psychology/learning literature, and ‘social’—those most commonly measured in the social insect literature. We do not presume this list to
be exhaustive, but instead wish to provide examples for researchers interested in studying behavioural syndromes in social insects.
54 J. M. Jandt and others
Table 3. Mechanisms that affect behavioural variation presented in the behavioural syndrome and social insect literature
Behavioral syndrome literature Social insect literature
Genetic mechanisms Aggression
Kralj-Fiser et al. (2010)
Fairbanks et al. (1999), Jones et al. (2011) and
Kinnally et al. (2006)
Chandra et al. (2000)
Division of labour (general)
Herb et al. (2012), Fewell & Page (1993), Page
et al. (1992), Robinson & Page (1989),
Robinson et al. (1994), Smith et al. (2008) and
Stuart & Page (1991)
Robinson & Page (1988)
Ben-Shahar et al. (2002), Fewell & Page (1993),
Hunt et al. (2007), Ingram et al. (2005), Page
et al. (1998, 2012b), Pankiw et al. (2002),
Robinson & Page (1989), Scheiner et al. (2001)
and Waddington et al. (1998)
Breed et al. (2004), Hunt et al. (2007), Moore
et al. (1987) and Robinson & Page (1988)
Cahan & Keller (2003), Graff et al. (2007), Page
et al. (2012b), Schwander et al. (2007, 2010),
Smith et al. (2008), Volny & Gordon (2002)
and Weiner & Toth (2012)
Physiological mechanisms Aggression
Brown et al. (2003), Bryant & Newton (1994),
Cutts et al. (1998) and Koolhaas et al. (2007)
Careau et al. (2008) and Chappell et al. (2004)
Huntingford et al. (2010)
Careau et al. (2008) and Koolhaas et al. (2007)
Mathot et al. (2009)
Tibbetts & Huang (2010)
Lin et al. (1999)
Division of labour (general)
Blanchard et al. (2000), Dolezal et al. (2012),
Robinson (2009), Robinson & Huang (1998)
and Toth et al. (2009)
Spivak et al. (2003)
Dolezal et al. (2012), Fewell & Page (1993),
Giray et al. (2005), Robinson & Page (1989)
and Seid & Traniello (2006)
Brent et al. (2006), Giray et al. (2005), Page et al.
(2012b) and Smith et al. (2008)
Experiential mechanisms Aggression
Del Giudice et al. (2011) and Niemel¨
Del Giudice et al. (2011), Heifetz & Applebaum
(1995) and Lihoreau et al. (2009)
Del Giudice et al. (2011) and Niemel¨
Lihoreau et al. (2009)
Seeley et al. (1998)
Lin et al. (1999)
Division of labour (general)
Greene & Gordon (2003, 2007), Powell &
Tschinkel (1999), Robinson & Huang (1998)
and Wilson (1985)
Anderson & Ratnieks (1999), Fewell & Page
(1993), Pankiw et al. (2002) and Robinson &
Kamakura (2011) and Suryanarayanan et al.
Mechanisms are not mutually exclusive. Note that each literature has focused on deﬁning mechanisms for very different sets of behavioural
axes: behavioural syndrome research has focused on mechanisms for the classically studied behavioural types whereas social insect literature
has focused on mechanisms for primarily social behavioural types.
Behavioural syndromes and social insects 55
(foraging) gene in honey bees and harvester ants affects
whether an individual will be more likely to engage in brood
care or foraging tasks, irrespective of age (Ben-Shahar et al.,
2002; Ingram, Oefner & Gordon, 2005). Differences in gene
expression might be the result of experience, nutrition, age,
or genotype; and often expression patterns are conserved
across species (e.g. expression of hexamerin storage proteins
often correlates with reproductive caste differentiation: Smith
et al., 2008). Epigenetics, i.e. the effects of DNA methylation,
is a relatively new area of research, and its role on behavioural
type is beginning to be investigated in social insects, both
in terms of reproductive (Weiner & Toth, 2012) and non-
reproductive (Herb et al., 2012) division of labour.
(ii )Physiology. Social insect workers often change their
role or specialisation over the course of their life, referred
to as temporal polyethism (Table 1; Seeley, 1982). In
the behavioural syndrome literature, switching between
behavioural types is referred to as episodic personality
(Table 1; Pronk, Wilson & Harcourt, 2010). In honey bees,
transitions tend to occur in a particular order (Seeley, 1982),
but this is not necessarily the case for all social insects. In some
species, task repertoire (the number of tasks an individual
performs) expands with age (Seid & Traniello, 2006), whereas
in others, the order of task-switching is seemingly random
(Gordon et al., 2005; Jandt, Huang & Dornhaus, 2009).
Often, juvenile hormone (JH) inﬂuences the task an
individual performs (Table 3; Robinson, 1987; Hartfelder,
2000; Giray, Giovanetti & West-Eberhard, 2005; Brent et al.,
2006; Dolezal et al., 2012) (but see Cameron & Robinson,
1990), and in some cases, change in corpulence (fat content)
also correlates with the performance of certain tasks (Table
3; Toth & Robinson, 2005; Robinson, 2009; Robinson
et al., 2009; Daugherty, Toth & Robinson, 2011), but
this is not necessarily true for all social insects (Couvillon
et al., 2011). Research on Polistes dominulus wasps has shown
that JH concentration changes during aggressive encounters
(Tibbetts & Huang, 2010), and so it might be directly related
to an individual’s aggressive behavioural type.
It is indeed possible that temporal polyethism, caused
by physiological change over an individual’s lifetime, might
also be a type of ‘maturation’ or ‘ageing’ syndrome—that is,
several associated traits are ultimately caused by ageing, and
the ageing process could differ among individuals (Dinge-
manse et al., 2010). Therefore, it is important to consider
maturation, as well as unavoidable senescence, as plausible
hypotheses both to explain the evolution of temporal
polyethism and of behavioural syndromes in general.
(iii )Environment. There are a variety of environmental
factors that can inﬂuence behavioural type (Table 3):
abiotic factors (e.g. temperature), ecological environment
(e.g. food availability and/or competition), and social
environment (e.g. interaction rates and communication
signals). Early developmental inﬂuences are often particularly
important. For example, early developmental inﬂuences,
such as larval feeding or maternal effects can lead to size,
reproductive, and in some cases distinct caste differences
(Wheeler, 1986; Winston, 1987; Couvillon & Dornhaus,
2009; Kamakura, 2011; Suryanarayanan et al., 2011a;
Suryanarayanan, Hermanson & Jeanne, 2011b). Thus,
certain individuals that take care of brood could determine
the behavioural types within a colony either through direct
communication (Suryanarayanan & Jeanne, 2008) or by
manipulating the way in which larvae are raised (Pereboom,
Velthuis & Duchateau, 2003; Couvillon & Dornhaus, 2009).
Such manipulations during development will likely have a
strong inﬂuence on the behavioural type of an individual
which might then carry over across contexts or over time
(Bergm¨uller, Sch¨urch & Hamilton, 2010).
In addition to events that happen during development,
the interactions of adult workers (or lack thereof) in a colony
might also determine the behaviour of individuals. Studies
in which individuals performing a certain task are removed
from a colony show that other individuals change which tasks
they perform (Gordon, 1989, 1996; Pinter-Wollman et al.,
2012b, and references therein). Thus, the social environment
is an important factor in determining how individuals behave.
(d)Fitness consequences of intra-colony behavioural variation
Because individuals might not be inﬁnitely ﬂexible, and
because switching between behavioural types (see Table 2 for
examples) can be costly or inefﬁcient, colonies can circumvent
these constraints by maintaining mixtures of individuals with
different behavioural types. For example, if the distribution of
ﬂowering plants changes within a season or even within a day
(O’Neal & Waller, 1984), maintaining a mixture of foragers
that vary along the speed-accuracy behavioural axis could
allow colonies to respond more quickly to environmental
ﬂuctuation (Burns & Dyer, 2008). That is, slower, more
accurate individuals can bring large quantities of food back to
the colony when food abundance is constant, whereas faster,
‘sloppier’ individuals might be more efﬁcient at exploiting
resources in more frequently changing environments (Raine
& Chittka, 2008, 2012; Chittka, Skorupski & Raine, 2009).
A colony containing a mixture of these types might thus
be able to handle different environments despite individual
inﬂexibility or carryover.
In the ant Temnothorax longispinosus and the social spider
Anelosimus studiosus, groups with a mixture of aggression types
tend to have higher ﬁtness than groups with only one type
(Modlmeier & Foitzik, 2011; Pruitt & Riechert, 2011). In
ant colonies, aggressive individuals defend the nest whereas
docile individuals take care of brood. In the spiders, more
aggressive individuals are faster to attack and subdue prey
(leading to an increase in foraging performance), whereas
less aggressive (more docile) individuals promote group
cohesiveness by not escalating aggression during foraging
and/or contest encounters (the absence of docile individuals
can lead to excessive within-group ﬁghting, cannibalism of
colony mates, and group disbandment).
However, maintaining a mixture of relatively inﬂexible
behavioural types could also incur costs to the colony. For
example, aggressive Rhytidoponera confusa ants are not only
more aggressive towards other ants, they are also more likely
to lunge at or bite their own nestmates (Crosland, 1990).
56 J. M. Jandt and others
This suggests a clear trade-off in aggressive behavioural
differences, as well as a limited ﬂexibility in the ability to
‘shut-off’ the aggressive phenotype across contexts.
Not all behaviours are inﬂexible, however. Pearce, Huang
& Breed (2001) showed that although nurse and guard bees
differ in their level of aggressiveness in the summer, these task
groups could not be distinguished in the winter months, sug-
gesting that aggressive behaviour can be somewhat plastic.
Numerous studies have found beneﬁts to maintaining
variation within colonies (Porter & Tschinkel, 1985; Cnaani
& Hefetz, 1994; Page et al., 1995a;Weidenm¨uller, 2004;
Powell & Franks, 2005; Billick & Carter, 2007; Mattila &
Seeley, 2007; Dornhaus, 2008; Powell, 2008; Modlmeier,
Liebmann & Foitzik, 2012; J. M. Jandt & A. Dornhaus, in
preparation), but it is not always clear why exactly variation
(as opposed to all individuals being of one optimal type) is
beneﬁcial. There is a need to develop theory that helps us
to understand under which circumstances we would expect
variation to be a better solution than one stable optimal
type—not only with regards to division of labour, but also
in terms of variation in other behavioural types such as
aggression or exploratory behaviour.
(2) Variation among colonies
The reproductive unit of social insects on which natural
selection acts is the colony. Therefore, consistent differences
among colonies could have important implications
on the success of certain phenotypes over others,
inﬂuencing population structure. Variation among colonies
in a certain behaviour might in itself have important
ecological consequences. For example, colonies of more
aggressive species could out-compete other colonies through
interference competition (Davidson, 1998; Rowles &
O’Dowd, 2007). If colony behaviour is also consistent across
contexts, we might ﬁnd interesting relationships between
the success of a colony in one situation and its success or
failure in another. For example, if there is a relationship
between aggression and exploration, colonies that are both
exploratory and aggressive might be better at invading
new habitat. However, when these two behaviours are not
correlated, exploratory colonies may ﬁnd new habitat, but
be quickly displaced by aggressive colonies (Cote et al., 2010;
Fogarty, Cote & Sih, 2011; Sih et al., 2012).
Aside from work to investigate the heritability of pollen-
foraging behaviour (Page et al., 1995a,b; Page, Fondrk
& Rueppell, 2012a), colony-level behavioural syndromes
have received comparatively little attention. However, the
behavioural repertoires of colonies include traits measured
in classical behavioural syndromes (e.g. aggressiveness),
cognitive behavioural syndromes (e.g. learning ability), and
social behavioural syndromes (e.g. communication: see Table
2). For example, Crosland (1990) showed that colonies of the
ant Rhytidoponera confusa consistently exhibited high or low
levels of aggression towards non-nestmates. This classical
behavioural type of aggression has also been shown to vary
among colonies of the invasive Argentine ants (Suarez et al.,
2002; Buczkowski & Silverman, 2006), a colony trait that
might help to explain the highly invasive success of certain
colonies. Colonies also vary in cognitive behavioural types.
For example, bumble bee colonies vary in their learning
speed and foraging success (Raine et al., 2006b; Raine &
Chittka, 2008, 2012; Ings, Raine & Chittka, 2009; Gill,
Ramos-Rodriguez & Raine, 2012). Colonies also differ in
the degree to which they perform tasks such as foraging,
defence, brood care, or hygienic behaviour. For example,
colonies of harvester ants and honey bees vary in foraging
activity levels (Gordon, 1991; Cole et al., 2010; Gordon
et al., 2011; Wray, Mattila & Seeley, 2011) and in how they
regulate foraging activity (Gordon et al., 2011). Colonies of
honey bees and black harvester ants (Messor andrei) also differ
in defensive response (Wray et al., 2011; Pinter-Wollman,
Gordon & Holmes, 2012a). Furthermore, Africanized honey
bees differ from European honey bees in defensive response
(Collins et al., 1982), as well as a number of other traits related
to the pollen-hoarding syndrome (Pankiw, 2003).
Like workers, colonies also exhibit consistent behavioural
variation across situations. For example, in both honey
bees and black harvester ants, colonies vary consistently
in their response to food and to disturbance, which are
correlated with one another, producing a behavioural
syndrome (Wray et al., 2011; Pinter-Wollman et al., 2012a).
That is, colonies that send out many workers to forage also
send out many workers to defend the nest when disturbed.
These behavioural syndromes might have important ﬁtness
consequences (Wray et al., 2011) and could result from
constraints on colony behaviour. For example, workers
might follow similar local rules in various situations (e.g.
patrolling and foraging; Gordon et al., 2011), and external
features such as nest structure could inﬂuence how a
colony behaves in various situations (Pinter-Wollman, 2012;
Pinter-Wollman et al., 2012a).
(a)Mechanisms underlying variation among colonies in behavioural
(i)Colony genetics. The genetic make-up of a social insect
colony is generally represented by the genotype of the queen
and the number of unrelated males she mates with. The
extent to which workers vary genetically might have an effect
on the behavioural type observed at the colony level (see
Section II.1c). Colonies with greater genetic variation might
achieve better rates of thermoregulatory homeostasis (Jones
et al., 2004; Oldroyd & Fewell, 2007), foraging ability (Page
et al., 1995a; Mattila, Burke & Seeley, 2008), or productivity
and ﬁtness (Mattila & Seeley, 2007). Whether the behavioural
type or genotype of a queen can be used to predict colony
behavioural type has yet to be studied (but see Section
II.2a.iii), although there is evidence that honey bee male
genotype can be used to predict behavioural type in an
offspring colony (Page et al., 2012a).
(ii )Colony composition and emergent behaviour. The
frequency of individual behavioural types in a colony might
affect colony behavioural type and/or colony performance
(Hillesheim, Koeniger & Moritz, 1989; Tsuji, 1994 Paleolog,
2009; Michelena et al., 2010; J. M. Jandt & A. Dornhaus,
Behavioural syndromes and social insects 57
in preparation). Consistent individual differences among
colonies might emerge both from variation in the average
behavioural types of their workers and from the distribution
of worker behavioural types (Pinter-Wollman, 2012). For
example, if ant colonies vary in aggressive behaviour, this
could be caused by the number of highly aggressive ants
present in each colony (Crosland, 1990). That is, there
might be many individuals of an aggressive caste (e.g. high
numbers of soldiers in an aggressive colony), or alternatively
there could be a high frequency of aggressive individuals
within each caste.
Because the collective behaviour of colonies is an
emergent property of individual workers that follow simple,
local rules (Camazine et al., 2001; O’Donnell & Bulova,
2007a; Sumpter, 2010), careful consideration is needed when
measuring colony behaviour. For example, to determine
colony aggression, it is not enough to sample a few workers,
put each in an aggression assay against one other worker
and sum their response to generate a colony aggression level.
A more appropriate test would be to place two colonies in
a situation where they are competing over a scarce resource
(such as food or a nest site). Using entire colonies allows us
to observe colony-level behaviours without the confounding
factor of subsampling heterogeneous colony populations.
That is, the sum of the individual behaviours might not
necessarily represent the behaviour of the whole colony.
The relationship between colony composition and
emergent colony behaviour might be non-linear, i.e. just
a few individuals could signiﬁcantly change the behaviour
of a group or population as a whole (Sih & Watters, 2005;
Sih, Hanser & McHugh, 2009). The queen of a social insect
colony, as the primary reproductive, might be considered a
conspicuous type of keystone (or key) individual (Table 1),
but rarely does she take an active role in inﬂuencing the
behaviour of other workers in the colony in non-reproductive
contexts (Jeanson, 2012). Workers might also take on key roles
in the colony, either as highly active or aggressive individuals
that affect the overall performance of a colony (Paleolog,
2009), or as informed individuals that inﬂuence nest-site
selection decision-making (Couzin et al., 2005). For example,
in honey bees, the presence of only a few aggressive individ-
uals drastically changes the behaviour of the colony, because
the individuals performing the task are a non-random
(more aggressive) subset of the colony (Paleolog, 2009). So,
although there are only a few aggressive individuals, those
are the ones performing the task resulting in an aggressive
colony (Paleolog, 2009). In Anelosimus studiosus spiders, the
presence of only a few aggressive individuals drastically
changes the efﬁciency with which colonies feed, and alters the
nature of a number of species interactions (Pruitt & Ferrari,
2011). In these examples a few aggressive individuals can
create a bias towards the colony becoming highly aggressive.
Key individuals (also referred to as catalysts, perform-
ers, and organisers; Robson & Traniello, 1999) can assume
various roles. As colony behavioural outcomes might be
described in a number of ways (foraging success, fecundity,
activity, etc.), who is recognized as a keystone individual
might differ based on which output is being measured.
Individuals performing keystone roles could increase per-
formance by better facilitating information ﬂow through the
colony (Couzin et al., 2005; Pinter-Wollman et al., 2011), facil-
itate an increase in the rate of activity in other workers (Cao
et al., 2009), motivate nestmates to begin foraging (O’Donnell,
2006; Molet et al., 2008), communicate more avidly with oth-
ers in the colony (Cao et al., 2007), or increase cohesion
within the colony. For example, in honey bee colonies, cer-
tain individuals (i.e. ‘activators’) are more likely to roam the
nest and activate idle nestmates by using vibration signals
(Cao et al., 2009). An interesting next step will be to determine
whether the number or proportion of activators in the nest
can predict overall activity level of the colony. In yet another
type of keystone role, elite workers (or ‘generalist elites’)
perform many tasks (unlike task specialists that tend to focus
on only one task; Table 1), with little or no help from other
workers (Dornhaus, 2008; Pinter-Wollman et al., 2012b). For
example, in Leptothorax allardycei, over 50% of the colony has
been described as inactive—leaving the majority of tasks to
be performed by the remaining workers (Cole, 1986). If this
percentage were to vary, the behavioural type of the colony
might change in the degree to which tasks are performed.
Understanding keystone roles, the types of individuals that
engage in those roles, and the rate of turnover within colonies
is an important issue in any social group (including humans),
and detailed studies can readily be conducted using social
insects, e.g. via removal of diligent workers (Pinter-Wollman
et al., 2012b, and references therein).
(iii )Colony environment. Once a colony is established,
the role of the queen rarely extends beyond functioning
as a reproductive organ. Therefore, in addition to the
difﬁculty of studying queen behaviour in the nest, research
on queens is limited to what they do while founding a
colony (Fewell & Page, 1999; Cahan & Fewell, 2004).
Foundresses (pre-egg-laying reproductive females) vary in
their method of dispersal (founding, swarming, budding,
joining) (Augustin, Santos & Elliot, 2011). For example,
aTemnothorax longispinosus ant foundress can either ﬂy off
and found her own colony (independent foundress) or join
an already established nest (dependent foundress) (Howard,
2006). The level of conspeciﬁc tolerance seen during the
initial nesting phase can also vary. For example, Polistes
dominulus paper wasp foundresses can independently initiate
or co-found colonies, and the number of foundresses can
vary across colonies (Zanette & Field, 2011).
What remains unclear is how variation in queen behaviour
translates into variation in colony behaviour. If queens vary
inherently in traits that affect their habitat selection, this
could have long-term effects on the colony, e.g. bold queens
might found colonies in a densely populated, but high-
quality, location and shy queens might establish further
from other colonies but perhaps in locations with scarcer
resources. This variation in microhabitat could inﬂuence
how early resources for initial brood-rearing are acquired, in
turn, impacting colony behavioural type. Once established,
the on-going role of the queen in the colony can vary. In
58 J. M. Jandt and others
eusocial naked mole rats, Heterocephalus glaber, for example,
queens have been shown to activate lazy workers (Reeve,
1992). If queens vary in their thresholds to tolerate inactive
workers, this might impact the overall activity of the colony.
(b)Fitness consequences of colony behavioural syndromes
A colony’s behavioural type (e.g. in terms of aggressiveness,
defensive response, foraging activity, or undertaking) can
inﬂuence its ﬁtness (in terms of colony productivity or
winter survival; Wray et al., 2011). As a behavioural
syndrome inherently suggests limited behavioural plasticity,
behavioural syndromes are often associated with some kind
of trade-off. Beneﬁcial responses to one stimulus might be
coupled with sub-optimal behaviour in response to others.
These costs might not be apparent until a colony is put
in an alternative context. For example, more aggressive or
exploratory colonies might out-compete other colonies in
areas of limited resources. However in areas with plentiful
resources, excessive or unnecessary contests with other
colonies could result in losses of brood or workers, with
no additional resources gained.
The ﬁtness consequences of behavioural syndromes at
the colony level are difﬁcult to study because of the long
generation time of social insect colonies and the paucity
of studies on their reproductive success. However, indirect
measures of colony success such as growth and foraging
activity might provide some insights about the importance
of behavioural syndromes at the colony level. For example,
Pogonomyrmex barbatus ant colonies vary in how they regulate
their foraging behaviour, which affects how much they forage
on a given day (Gordon, 1991; Gordon et al., 2011) and
potentially how much food the colony can store. Honey
bee colonies bred for better hygienic behaviour (efﬁcient
removal of dead larvae) are less susceptible to disease
(Lapidge, Oldroyd & Spivak, 2002), possibly increasing
overall health. Other research is beginning to show that
connections between colony traits or behavioural types might
have signiﬁcant impact on colony performance and ﬁtness
(Suarez et al., 2002; Buczkowski & Silverman, 2006; Raine &
Chittka, 2008; Paleolog, 2009; Gordon et al., 2011; Wray et al.,
2011; Modlmeier et al., 2012; Pinter-Wollman et al., 2012a).
III. INSIGHTS FROM BEHAVIOURAL
SYNDROMES FOR THE STUDY OF SOCIAL
A common theme in the behavioural syndrome literature is
measuring the beneﬁts or costs of an inﬂexible behavioural
type across contexts. For instance, consistently bold and
aggressive individuals often enjoy increased foraging success
(Sih et al., 2003; Short & Petren, 2008), growth rates
(Biro & Stamps, 2008), and superior performance during
contests (Pruitt & Riechert, 2009), but also suffer increased
susceptibility to predation or parasites (Fig. 1A; Pontier et al.,
1998; Biro et al., 2006). Other trade-offs can be less intuitive,
particularly those involving social interactions. For example,
male western blue birds (Sialia mexicana) exhibit a syndrome
of aggressiveness between nest defence and male-male
competition that ultimately results in decreased ﬁtness.
Highly aggressive males engage in excessive male–male
contests during the breeding season, and consequently fail to
provision nesting females with necessary food. This results in
disrupted incubation patterns, as females must leave the nest
to forage, reducing offspring survival (Duckworth, 2006).
Although recent literature has challenged the potential
of behavioural syndromes to set evolutionary constraints
(Bell, 2005; Dingemanse et al., 2007), a sizeable (and
growing) body of literature continues to document numerous
trade-offs associated with behavioural consistency. It is yet
unclear whether these trade-offs are the result of proximate
constraints such as genetic linkage. Optimality theory
suggests selection should act against limited behavioural
plasticity; however there might be adaptive beneﬁts (Sih et al.,
2004a). For example, limited plasticity prevents animals from
making more costly errors in an unpredictable environment
(Sih, 1992). Conversely, the social insect literature shows
examples of trade-offs being the result of genetic linkage.
For example, the reproductive ground-plan hypothesis
proposes that different levels of pollen-hoarding in honey
bee foragers is the result of evolutionary co-option of the
female reproductive system (Amdam & Page, 2010), and
genetic linkage between foraging behaviour, reproduction
(Graham et al., 2011) and at least two genes (HR46 and
PDK1) has been demonstrated (Wang et al., 2009).
Because consistent traits across different contexts can
produce performance trade-offs, determining the source
and magnitude of these trade-offs is a continuing goal
of behavioural syndromes research. Furthermore, until
recently, colony-level behavioural variation has not received
as much attention as within-colony variation (see Table 2).
It could be useful to examine under what conditions within-
population variation can evolve if trade-offs are present, and
how those conditions match those where variation persists in
populations of non-social animals.
Recent work has addressed how behavioural syndromes are
maintained in a population. Several authors have suggested
that a key mechanism for maintaining consistent differences
in behavioural types is the feedback between the individual’s
behaviour and its state (Luttbeg & Sih, 2010; Wolf &
Weissing, 2010), such as the feedback linking an individual’s
behavioural type and its energy reserves, condition, or social
rank. For example, colonies that are quick to exploit a new
resource could gain an early beneﬁt, but they might also be
easily displaced by a more dominant or aggressive colony
and must then locate a new resource pool. These differences
in strategy might be the result of differing behavioural
types, and are consistently reinforced by the social rank of
a colony. A central premise of this frequency-dependent
selection has been that the mix of behavioural types in social
Behavioural syndromes and social insects 59
groups inﬂuences social dynamics and the ﬁtness of each
behavioural type. Because social dynamics are important in
social insects, understanding how variation in behavioural
types in the colony inﬂuences individual and group outcomes
is an exciting area for future study (Pinter-Wollman, 2012).
(3) Statistical methods
Studies in social insects have illustrated variation in classical,
cognitive, and social behavioural types both within and
among colonies (Table 2). Quantifying various behavioural
types, as well as understanding how variation across
multiple behavioural axes might affect colony ﬁtness are
topics that are beginning to receive attention in the social
insect literature (e.g. see Modlmeier et al., 2012). Scientists
studying social insects can draw on advances in statistical
methods from the general behavioral syndrome literature
for identifying, quantifying, and correlating behavioural
types and syndromes across time and context (Sih et al.,
eale et al., 2007; Garamszegi & Herczeg, 2012).
Recently, statistical approaches have been reviewed to
quantify animal personalities, behavioural syndromes, and
behavioural plasticity (Dingemanse et al., 2010; Dingemanse,
Dochtermann & Nakagawa, 2012; Garamszegi & Herczeg,
2012). We brieﬂy highlight some points here, but refer the
reader to these reviews for detailed analyses of how and
when to use various statistical approaches.
Two key analytical tools for behavioural syndrome
research are principal component analyses (PCAs) and
pairwise correlations. When used together these analyses
provide a convenient way to tackle large data sets where
some combination of variables could predict behavioural
correlations. Factor analyses, structured equation modeling,
generalized linear mixed models, and other statistics have
also been applied to behavioural syndromes research (Bell
& Stamps, 2004; Dingemanse et al., 2010; Garamszegi &
Herczeg, 2012), and these approaches can add to the tool
kit available to social insect biologists. While these statistical
approaches require very large datasets, they help address
the point that variation in behavioural ﬂexibility could be
as vital as differences in mean trait values. Moreover, when
paired with familiar theory on the trade-offs associated
with phenotypic plasticity, these approaches provide us with
clear and testable predictions on when trait ﬂexibility versus
consistency should be favoured.
IV. INSIGHTS FROM SOCIAL INSECTS FOR
(1) Group-living might affect behavioural type
Although many studies of behavioural syndromes have been
conducted on social animals, and many of the commonly
studied behavioural axes are inherently social behaviours
(see Table 2), the social ecology of behavioural types has
not yet received much experimental attention. For example,
how does a mix of behavioural types in a group inﬂuence
individual behaviours [social plasticity (Kurvers et al., 2010)
or group outcomes (Crosland, 1990; Sih & Watters, 2005;
Eldakar et al., 2009; Paleolog, 2009; Pruitt & Riechert,
2011; Sch¨urch, Rothenberger & Heg, 2011)]? Work on
social insects has shown that indirect genetic effects (whether
offspring are raised by the parent or siblings) can inﬂuence
colony phenotype (Linksvayer, 2006). Colonial living can
also result in greater variation in individual experiences,
which can further alter individual behavioural tendencies
(Bergm¨uller et al., 2010; Pruitt et al., 2012). Studies of
social insect colonies have a long history of looking at how
individuals and their behaviours collectively produce group
outcomes (Oster & Wilson, 1978), and there are a variety
of examples where feedback between the individual and the
rest of the group might affect colony behaviour (Fig. 1B;
Crosland, 1990; Beverly et al., 2009; Paleolog, 2009).
Variation in behavioural type within a group could
reduce competitive interactions among group members
(reviewed in Ratnieks & Reeve, 1992; Bergm¨uller et al.,
2010). Furthermore, the spatial organisation of individuals in
a colony might be analogous to niche partitioning measured
in behavioural ecology (Sendova-Franks & Franks, 1995;
Beverly et al., 2009; Jandt & Dornhaus, 2011; Dall et al.,
2012). Recently, social network theory has been employed
to study the development and maintenance of behavioural
types within a social group (Krause, Lusseau & James,
2009; Sih et al., 2009). There are a variety of examples of
the use of network theory to understand how interactions
affect group behaviour in social insects as well (Blonder &
Dornhaus, 2011; Pinter-Wollman et al., 2011). We propose
that a link between models developed on social networks
and on behavioural syndromes could beneﬁt both the study
of social insects and animal behaviour in general.
The study of behavioural syndromes can also beneﬁt from
exploring models that show how division of labour emerges
from feedback mechanisms and interactions among workers,
and models that predict how the interactions of those
workers produce complex patterns and colony behaviour
(Fig. 1B; Camazine, 1991; Theraulaz & Bonabeau, 1995;
Bonabeau, Theraulaz & Deneubourg, 1998; Theraulaz,
Bonabeau & Deneubourg, 1998; Camazine et al., 2001;
O’Donnell & Bulova, 2007b). Social feedbacks can facilitate
the maintenance of multiple behavioural types within
the nest (Gordon, 1989, 1996; Reeve & Nonacs, 1997;
Bergm¨uller et al., 2010). For example, small differences in
response thresholds can lead to stable long-term differences
in behaviour, even among non-social animals (Fewell &
Page, 1999), and the social environment might prevent or
promote transitions among tasks (Gordon, 1989; Amdam
et al., 2005; Gordon et al., 2005). Researchers of behavioural
syndromes are beginning to explore how positive feedback
loops might maintain consistent behavioural types (Luttbeg
& Sih, 2010). These models can guide further study of how
complementary behavioural types in non-social insects can
affect group dynamics, and how these in turn can determine
the behaviour and ﬁtness of individuals.
60 J. M. Jandt and others
(2) Mechanisms affecting behavioural type
A crucial question in behavioural syndrome research is:
what are the mechanisms that affect behaviour? Genetic,
hormonal, and experiential mechanisms that could interact
and predispose an individual to exhibit a particular social
behavioural type have been well studied in social insects
(see Section II.1cand Table 3). Changes in hormone levels
(Robinson, 1987; Giray et al., 2005; Dolezal et al., 2012) and
gene expression (Hunt et al., 2010), often associated with a
change in social environment (Amdam et al., 2005) affect
caste determination and division of labor (Robinson, 1987;
Wheeler, Buck & Evans, 2006; Toth et al., 2009; Amdam
& Page, 2010; Hunt et al., 2010), cooperative behaviour,
in terms of worker egg production (Lin et al., 1999), and
aggressive behaviour (Pearce et al., 2001; Tibbetts & Huang,
2010). For example, genetic linkage between foraging and
reproductive behaviour (Wang et al., 2009) might not only
limit an individual’s behavioural plasticity (or act as a
‘constraint’), but could also have been an adaptive precursor
that allowed solitary ancestors to evolve into social groups
(Amdam et al., 2004; Hunt & Amdam, 2005; Smith et al.,
2008; Toth et al., 2009; Hunt et al., 2010; Page et al., 2012b).
Morphological differences have also been implicated as
a mechanism underlying behavioural syndromes (Sih et al.,
2004b). However, it is often difﬁcult to modify the mor-
phology of an organism to determine which aspects of
an individual’s morphology have the greatest effects on
behaviour. Insect colonies provide a unique system in which
the demography and composition of a colony can be manip-
ulated, i.e. whole task groups or castes can be removed or
proportions adjusted (Porter & Tschinkel, 1985; Cnaani &
Hefetz, 1994; Roux & Korb, 2004; Billick & Carter, 2007; J.
M. Jandt & A. Dornhaus, in preparation). The nest structure
can be considered an extended phenotype of the colony
(Tschinkel, 2004), and changes to this structure, i.e. to nest
morphology, could have an effect on colony-level behaviours
(Pinter-Wollman et al., 2012a). Both colony composition and
nest architecture can be manipulated to determine the rela-
tive role each plays in the maintenance of a behavioural type.
(3) Development of behavioural types across levels
When examining the behavioural type of an individual, its
behaviour is often examined at different stages or in response
to different stimuli (Bell & Stamps, 2004; Briffa, Rundle &
Fryer, 2008; Bell, Hankison & Laskowski, 2009; Biro, Beck-
mann & Stamps, 2010; Dingemanse et al., 2010). It would be
considerably more difﬁcult to monitor the changes of indi-
vidual cells in a vertebrate brain or body to understand how
the parts affect the behavioural type of the individual, but
we concede that these often play a signiﬁcant role. However,
using social insects we can monitor how variation in worker
development [e.g. change in physiology and/or gene expres-
sion patterns (Kocher et al., 2010; Herb et al., 2012)], change
in colony composition (i.e. the development of the superor-
ganism), and feedback between levels of organisation (Kocher
et al., 2010) can affect behavioral type (Fig. 1B). The insight
that can be gained from understanding the biological interac-
tions within a social group and how that translates to colony-
level behaviours can provide important insights to those who
study behavioural syndromes in solitary organisms.
V. FUTURE DIRECTIONS
In the ﬁeld of social insects, it has long been acknowl-
edged that variation among workers might affect colony
ﬁtness by providing a mechanism for division of labour.
Here we have reviewed examples of variation along mul-
tiple behavioural axes both at the colony and individual
levels. While division of labour has long been speculated as
critically important in enhancing colony ﬁtness (Oster & Wil-
son, 1978), the behavioural syndromes approach provides
an alternative method for determining the extent to which
variation in behavioural types within colonies (including, but
not limited to, those associated with caste and division of
labour) and among colonies might affect ﬁtness and ecology.
While we acknowledge there are a variety of ways in which
the behavioural-syndrome approach can be used to create
insightful and important questions, we propose in particular
the following three areas that would beneﬁt from the attention
of eager social-insect/behavioural syndrome enthusiasts.
(1) What are the adaptive reasons for colonies, or
groups of individuals, to maintain mixtures of
As mentioned above (Sections II.1d, and II.2a), many studies
have found beneﬁts to maintaining variation within colonies
(Porter & Tschinkel, 1985; Cnaani & Hefetz, 1994; Page
et al., 1995a;Weidenm¨uller, 2004; Powell & Franks, 2005;
Billick & Carter, 2007; Mattila & Seeley, 2007; Dornhaus,
2008; Powell, 2008; Modlmeier et al., 2012; J. M. Jandt & A.
Dornhaus, in preparation). However, it is not always clear
why exactly variation (as opposed to all individuals being
of one optimal type) is beneﬁcial. Furthermore, these studies
can be expanded to include non-social-insect group-dwelling
species (Sih & Watters, 2005; Eldakar et al., 2009; Pruitt &
Trait complexes could be the product of genetic or
physiological linkage, rather than adaptive combinations
for optimal division of labour. It is possible that mixtures
of behavioural types within a colony (e.g. aggressive or
exploratory types) shaped the way in which task groups
(e.g. guards or patrollers) have evolved. We ﬁnd corre-
lations among multiple physiological factors that affect
the behaviour of individual workers—both within and
between castes—that are not obviously explained by the
requirements of the tasks themselves.
Mixtures of behavioural types within a colony might
affect the ﬂexibility of the colony to react to changing
environmental conditions. For example, colonies could
become more active when environmental conditions are
Behavioural syndromes and social insects 61
favourable (Gordon, 1991; Cole et al., 2010; Pinter-Wollman,
2012). The more variation among workers, the more types
of individuals are available for each ecological condition,
and indeed, high variation among workers increases colony
productivity (Page et al., 1995a;Joneset al., 2004; Mattila
& Seeley, 2007; Oldroyd & Fewell, 2007; Mattila et al.,
2008; Modlmeier & Foitzik, 2011). Differences in colony
ability to respond to changing conditions could be critical in
the modern world of human-induced rapid environmental
change (HIREC; Sih, Ferrari & Harris, 2011), including
changes in climate and habitat, and exposure to novel species
Finally, behavioural variation might persist in a group via
social heterosis (Nonacs & Kapheim, 2007, 2008). Social
heterosis is a mutually beneﬁcial process that occurs when
individuals beneﬁt by associating with genetically dissimilar
individuals. Under such circumstances, groups (or demes) of
mixed genotype outperform monotypic groups and singleton
individuals of any genotype. Potential mechanisms behind
social heterosis include reduced competition among group
constituents, complimentary skill pools, or instances where
individuals are incapable of approximating the optimal
genotype for a population. Importantly, social heterosis is
sufﬁcient in itself to maintain genetic diversity at one or
more loci in the face of genetic drift (Nonacs & Kapheim,
2007, 2008). The predicted outcomes of social heterosis are
high genetic diversity (and heritability) of functional traits
eale & Roff, 2002; Nonacs & Kapheim, 2007), and
a positive association between within-group trait variation
and ﬁtness for group constituents. Both patterns have been
observed in numerous test systems, from microbes (Vos &
Velicer, 2006), to primates (Wooding et al., 2006). In social
insects, social heterosis might be an explanation as to why
unrelated individuals will cooperate with one another during
nest-founding in some species (Tschinkel, 1998; Queller
et al., 2000; Jeanson & Fewell, 2008; Leadbeater et al., 2010;
Zanette & Field, 2011).
(2) Do colonies differ in their degree of cooperation?
A growing ﬁeld in behavioural syndrome research is to
identify the degree to which individuals or groups vary
in cooperativeness. A cooperative behavioural type could
be measured in terms of group cohesion, lack of within-
group conﬂict, short time spent on tasks devoted to self- versus
group-maintenance, and low effort spent on reproduction (or
competing to reproduce). Social insect colonies are generally
assumed to be highly cooperative, yet extreme aggression,
worker reproduction, and over-policing of queen-laid eggs
are a few examples of within-colony non-cooperative
(or cheating) behaviour (Bourke, Have & Franks, 1988;
Schmid-Hempel, 1990; D’Ettorre, Heinze & Ratnieks, 2004;
Wenseleers & Ratnieks, 2006a). Along with the examples
listed above, we might measure colony-level cooperation
based on the proportion of individuals that are inactive, or
regularly refrain from working (Lindauer, 1952; Herbers,
1983; Cole, 1986; Dornhaus et al., 2008; Jandt & Dornhaus,
2009). These inactive individuals might be a reserve set of
workers, or they might be selﬁshly hoarding their fat reserves
and avoiding risky tasks to gain an opportunity to reproduce
(Lindauer, 1952; Michener, 1964; Jandt & Dornhaus, 2011).
While inactive individuals have been identiﬁed in many
social insect species, it is unclear whether the proportion of
‘lazy’ individuals varies across colonies and how that might
affect colony ﬁtness.
An additional method for measuring cooperativeness
is to examine worker policing behaviour—that is, some
workers will regularly inspect the eggs laid in the nest and
will eat those that were not laid by the queen (Ratnieks
& Reeve, 1992; Wenseleers & Ratnieks, 2006b). Some
individuals occasionally ‘make a mistake’ and eat queen eggs
too, although often at a lower rate (D’Ettorre et al., 2004).
Degree of cooperation might be measured by examining
the variation across colonies in the ratio of policing
queen eggs versus worker eggs, and how that might affect
If colonies differ in how cooperative they are, what will
this mean ecologically? Will more cooperative colonies have
an ecological advantage in some environments, whereas
less cooperative colonies have an advantage in others?
Argentine ant colonies that have successfully invaded urban
areas are less aggressive (and, hence, more cooperative)
with conspeciﬁc colonies than those that remain in their
native range (Buczkowski, 2010). That is, colonies interact
and cooperate with one another, and ultimately end up
forming ‘supercolonies’, a phenotype that allows them
aggressively to expand and dominate the areas they colonize
(Holway, 1999; Suarez et al., 1999; Holway & Suarez, 2004;
Buczkowski, 2010). In native areas, on the other hand,
the same species will coexist with a variety of other ant
species, and are less likely to form these supercolonies that
can aggressively out-compete other species for territory.
The theoretical basis for the evolution, maintenance and
consequences of individual variation in cooperation has
been developed in the behavioural syndrome literature
(Bergm¨uller et al., 2010).
(3) How does consistency in behavioural type affect
task performance when individuals switch task?
The extent to which behavioural type persists over time
within an individual, and how this could affect future task
performance, has received little attention. In honey bees,
for example, genetic factors are linked to how quickly
an individual transitions between tasks (Page et al., 1998;
Rueppell et al., 2004; Amdam & Page, 2010). Research on
the honey bee pollen-hoarding syndrome has shown that
this transition time is also linked to learning performance,
and a variety of other behavioural types (Page et al., 2012b).
Incorporating a behavioural-syndromes approach also allows
us to ask whether this variation in transition time correlates
with classical, cognitive, or social behavioural axes (i.e. do
more shy workers take longer to transition between tasks?
Do they vary in the time required to master that new task or
skill set?). Ultimately, this could reveal why individuals vary
62 J. M. Jandt and others
in the time scale over which they become specialised on a
Consistency of behavioural type over time could also
affect division of labour. For example, are individuals
that exhibit high levels of boldness or aggressiveness
as a young nurse more likely to guard when they
are older, whereas those that exhibit high levels of
exploratory behaviour more likely to forage? What role does
senescence, or changes in task based on decreased ability,
play in behavioural syndromes? Do individuals change
behavioural type as they age? Studies using the behavioural-
syndromes approach could be useful when considering
how workers maintain task organisation in a decentralized
(1) There are clearly two ﬁelds of knowledge, the study
of social insects and the study of behavioural syndromes,
working in parallel on complementary ideas, yet until recently
little effort has been invested in bridging these two ﬁelds.
For example, researchers interested in studying behavioural
syndromes of group-living organisms would beneﬁt from the
rich literature in social insects on how social interactions
can affect individual decision-making. On the other hand,
social insect researchers exploring evolutionary causes and
consequences of maintaining behavioural types at multiple
levels of social organisation would beneﬁt from theory
developed in behavioural syndrome research on trade-offs
(Fig. 1A), as well as on statistical methods to analyse these
(2) One of the advantages of studying behavioural
syndromes in social insects is the ability to compare causes
and consequences at multiple levels of social organisation.
Because of the tight interplay between behavioural type
of individuals and groups, it is clear that to understand
behavioural syndromes of social animals it is important
to understand the feedback among the levels of social
organisation (Fig. 1B).
(3) Monitoring the development of an individual’s
behavioural type (i.e. changes of individual cells in a
vertebrate brain or body to understand how the parts affect
the behavioural type of the individual) may be more feasible
using social insects. Here, we can monitor how variation
in worker development (e.g. change in physiology and/or
gene expression patterns), change in colony composition
(i.e. the development of the superorganism), and feedback
between levels of organisation can affect behavioral type.
Furthermore, mechanisms that affect the development of
these types, as well as the ﬁtness effects of maintaining
syndromes—have been measured both within and between
(4) We propose that both ﬁelds take advantage of the
knowledge gleaned from the other to avoid reinventing the
wheel too many times.
All authors wish to acknowledge the International Union
for the Study of Social Insects (IUSSI) international
conference held in Copenhagen, Denmark, August 2010.
The symposium on behavioural syndromes in social insects
provided the fodder for many of the authors to begin the
discussion of bridging the two ﬁelds of behavioural ecology
and social insects in a more formal way. We also wish to thank
the Dornhaus Lab (University of Arizona, U.S.A.) and Toth
Lab (Iowa State University, U.S.A.) for helpful discussions
on manuscript revisions, and are grateful for the thoughtful
suggestions from Dr William Foster and two anonymous
reviewers to improve the manuscript. Funding for travel was
supported by NSF IOS-0841756.
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(Received 28 April 2012; revised 9 April 2013; accepted 17 April 2013; published online 15 May 2013)