ArticlePDF AvailableLiterature Review

Abstract and Figures

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).
Content may be subject to copyright.
Biol. Rev. (2014), 89, pp. 4867. 48
doi: 10.1111/brv.12042
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 syndromesresearch 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:
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 syndromesconsistent
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’
behavioural types.
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
Behavioural syndrome
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
Task switching
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 analysiscaste (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)=0.20.5; 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 syndromestrade-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).
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
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
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
colony level.
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
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
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 &
Tschinkel (1999)
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)
Exploration Ants
Chapman et al. (2011) and Modlmeier & Foitzik
Boldness/shyness Ants
Chapman et al. (2011)
Proactive/reactive Ants
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)
Learning Bees
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)
Social Spiders
Pruitt & Riechert (2009)
Cahan (2001)
Robinson et al. (1990)
Social Spiders
Pruitt & Riechert (2011)
Communication Ants
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)
House-hunting Ants
Pinter-Wollman et al. (2012b)
Liang et al. (2012)
Wray & Seeley (2011)
Foraging Ants
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)
Defense Bees
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.
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
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)
Hygienic behaviour
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)
Exploratory (activity)
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)
Hygienic behaviour
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¨
aet al.
Exploration (activity)
Del Giudice et al. (2011), Heifetz & Applebaum
(1995) and Lihoreau et al. (2009)
Del Giudice et al. (2011) and Niemel¨
aet al.
Lihoreau et al. (2009)
Exploratory (activity)
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 &
Page (1989)
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.
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
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’ syndromethat 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).
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
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
typenot 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,
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
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 inactiveleaving 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
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
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).
(1) Trade-offs
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 malemale
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.
(2) Feedback
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
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
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.
(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.
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
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
of organisation
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.
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
behavioural types?
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 &
Riechert, 2011).
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 workersboth within and
between castesthat 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
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
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
or contaminants.
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
(Stirling, R´
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 behaviourthat 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
colony fitness.
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
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
62 J. M. Jandt and others
in the time scale over which they become specialised on a
given task.
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
syndromeshave 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.
Adams,E.S.,Atkinson,L.&Bulmer, M. S. (2007). Relatedness, recognition errors,
and colony fusion in the termite Nasutitermes corniger.Behavioral Ecology and Sociobiology
61, 1195– 1201.
K. & Hartfelder, K. (2005). Social reversal of immunosenescence in honey bee
workers. Experimental Gerontology 40, 939– 947.
Amdam,G.V.,Norberg,K.,Fondrk,M.K.&Page, R. E. (2004). Reproductive
ground plan may mediate colony-level selection effects on individual foraging
behavior in honey bees. Proceedings of the National Academy of Sciences of the United States
of America 101, 11350– 11355.
Amdam,G.V.&Page, R. E. J. (2010). The developmental genetics and physiology
of honeybee societies. Animal Behaviour 79, 973 980.
Anderson,C.&Ratnieks, F. L. W. (1999). Worker allocation in insect societies:
coordination of nectar foragers and nectar receivers in honey bee (Apis mellifera)
colonies. Behavioral Ecology and Sociobiology 46, 73– 81.
Arathi,H.S.,Burns,I.&Spivak, M. (2000). Ethology of hygienic behaviour in
the honey bee Apis mellifera L. (Hymenoptera : Apidae): behavioural repertoire of
hygienic bees. Ethology 106, 365– 379.
Augustin, J. O., Santos,J.F.L.&Elliot, S. L. (2011). A behavioral repertoire
of Atta sexdens (Hymenoptera, Formicidae) queens during the claustral founding and
ergonomic stages. Insectes Sociaux 58, 197–206.
Bell, A. M. (2005). Behavioural differences between individuals and two populations
of stickleback (Gasterosteus aculeatus). Journal of Evolutionary Biology 18, 464–473.
Bell,A.M.,Hankison,S.J.&Laskowski, K. L. (2009). The repeatability of
behaviour: a meta-analysis. Animal Behaviour 77, 771 –783.
Bell,A.M.&Sih, A. (2007). Exposure to predation generates personality in
threespined sticklebacks (Gasterosteus aculeatus). Ecology Letters 10, 828 –834.
Bell,A.M.&Stamps, J. A. (2004). Development of behavioural differences between
individuals and populations of sticklebacks, Gasterosteus aculeatus.Animal Behaviour 68,
1339– 1348.
Ben-Shahar,Y.,Robichon,A.,Sokolowski,M.B.&Robinson, G. E. (2002).
Influence of gene action across different time scales on behavior. Science 296,
741– 744.
Bengston,S.E.&Dornhaus, A. (2013). Colony size does not predict foraging
distanceintheantTemnothorax rugatulus: a puzzle for standard scaling models. Insectes
Sociaux 60, 93– 96.
uller,R.,Sch ¨
urch,R.&Hamilton, I. M. (2010). Evolutionary causes and
consequences of consistent individual variation in cooperative behaviour. Philosophical
Transactions of the Royal Society B: Biological Sciences 365, 2751– 2764.
Beshers,S.N.&Fewell, J. H. (2001). Models of division of labor in social insects.
Annual Review of Entomology 46, 413– 440.
Beverly,B.D.,McLendon,H.,Nacu,S.,Holmes,S.&Gordon, D. M. (2009).
How site fidelity leads to individual differences in the foraging activity of harvester
ants. Behavioral Ecology 20, 633– 638.
Billick,I.&Carter, C. (2007). Testing the importance of the distribution of worker
sizes to colony performance in the ant species Formica obscuripes Forel. Insectes Sociaux
54, 113– 117.
Biro,P.A.,Abrahams,M.V.,Post,J.R.&Parkinson, E. A. (2006). Behavioural
trade-offs between growth and mortality explain evolution of submaximal growth
rates. Journal of Animal Ecology 75, 1165– 1171.
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
Behavioural syndromes and social insects 63
Biro,P.A.,Beckmann,C.&Stamps, J. A. (2010). Small within-day increases in
temperature affects boldness and alters personality in coral reef fish. Proceedings of the
Royal Society B: Biological Sciences 277, 71–77.
Biro,P.A.&Stamps, J. A. (2008). Are animal personality traits linked to life-history
productivity? Trends in Ecology & Evolution 23, 361– 368.
Blanchard,G.B.,Orledge,G.M.,Reynolds,S.E.&Franks, N. R. (2000).
Division of labour and seasonality in the ant Leptothorax albipennis: worker corpulence
and its influence on behaviour. Animal Behaviour 59, 723 738.
Blonder,B.&Dornhaus, A. (2011). Time-ordered networks reveal limitations to
information flow in ant colonies. PLoS One 6, e20298.
Bonabeau,E.,Theraulaz,G.&Deneubourg, J.-L. (1998). Fixed response
thresholds and the regulation of division of labor in insect societies. Bulletin of
Mathematical Biology 60,753807.
Bourke,A.F.G.,van der Have,T.M.&Franks,N.R.(1988).Sexratio
determination and worker reproduction in the slave-making ant Harpagoxenus
sublaevis.Behavioral Ecology and Sociobiology 23, 233 –245.
Breed,M.D.,Guzman-Novoa,E.&Hunt, G. J. (2004). Defensive behavior of
honey bees: organization, genetics, and comparisons with other bees. Annual Review
of Entomology 49, 271– 298.
Brent,C.,Peeters,C.,Dietmann,V.,Crewe,R.&Vargo, E. (2006). Hormonal
correlates of reproductive status in the queenless ponerine ant, Streblognathus peetersi.
Journal of Comparative Physiology. A 192, 315– 320.
Briffa,M.,Rundle,S.D.&Fryer,A. (2008). Comparing the strength of behavioural
plasticity and consistency across situations: animal personalities in the hermit crab
Pagurus bernhardus.Proceedings of the Royal Society B: Biological Sciences 275, 1305 –1311.
F. A. (2003). Resting metabolic rate and social status in juvenile giant freshwater
prawns, Macrobrachium rosenbergii.Marine and Freshwater Behaviour and Physiology 36,
Bryant,D.M.&Newton, A. V. (1994). Metabolic costs of dominance in dippers,
Cinclus cinclus.Animal Behaviour 48, 447 –455.
Buczkowski, G. (2010). Extreme life history plasticity and the evolution of invasive
characteristics in a native ant. Biological Invasions 12, 3343–3349.
Buczkowski,G.&Silverman, J. (2006). Geographical variation in Argentine ant
aggression behaviour mediated by environmentally derived nestmate recognition
cues. Animal Behaviour 71, 327 335.
Burns,J.G.&Dyer, A. G. (2008). Diversity of speed-accuracy strategies benefits
social insects. Current Biology 18, R953– R954.
Cahan, S. H. (2001). Cooperation and conflict in ant foundress associations: insights
from geographical variation. Animal Behaviour 61, 819 –825.
Cahan,S.H.&Fewell, J. H. (2004). Division of labor and the evolution of task
sharing in queen associations of the harvester ant Pogonomyrmex californicus.Behavioral
Ecology and Sociobiology 56, 9– 17.
Cahan,S.H.&Keller, L. (2003). Complex hybrid origin of genetic caste
determination in harvester ants. Nature 424, 306– 309.
Barthell,J.F.&Wells, H. (2009). Different solutions by bees to a foraging
problem. Animal Behaviour 77, 1273 1280.
Camazine, S. (1991). Self-organizing pattern formation on the combs of honey bee
colonies. Behavioral Ecology and Sociobiology 28, 61– 76.
Camazine,S.,Deneubourg, J.-L., Franks,N.R.,Sneyd,J.,Theraulaz,G.
&Bonabeau, E. (2001). Self-Organization in Biological Systems. Princeton University
Press, Princeton.
Cameron,S.A.&Robinson, G. E. (1990). Juvenile hormone does not affect division
of labor in bumble bee colonies (Hymenoptera: Apidae). Annals of the Entomological
Society of America 83, 626– 631.
Cant,M.A.,Llop,J.B.&Field, J. (2006). Individual variation in social aggression
and the probability of inheritance: theory and a field test. American Naturalist 167,
837– 852.
(2007). The influence of the vibration signal on worker interactions with the nest
and nest mates in established and newly founded colonies of the honey bee, Apis
mellifera.Insectes Sociaux 54, 144 –149.
(2009). The effect of repeated vibration signals on worker behavior in established
and newly founded colonies of the honey bee, Apis mellifera.Behavioral Ecology and
Sociobiology 63, 521– 529.
Careau,V.,Thomas,D.,Humphries,M.M.&Reale, D. (2008). Energy
metabolism and animal personality. Oikos 117, 641– 653.
Chandra,S.B.C.,Hosler,J.S.&Smith, B. H. (2000). Heritable variation for
latent inhibition and its correlation with reversal learning in honeybees (Apis mellifera).
Journal of Comparative Psychology 114, 86– 97.
Chapman,B.B.,Thain,H.,Coughlin,J.&Hughes, W. O. H. (2011). Behavioural
syndromes at multiple scales in Myrmica ants. Animal Behaviour 82, 391 –397.
Chappell,M.A.,Garland,T.,Rezende,E.L.&Gomes, F. R. (2004). Voluntary
running in deer mice: speed, distance, energy costs and temperature effects. Journal
of Experimental Biology 207, 3839– 3854.
Chittka,L.,Dyer,A.G.,Bock,F.&Dornhaus, A. (2003). Bees trade off foraging
speed for accuracy. Nature 424, 388.
Chittka,L.,Ings,T.C.&Raine, N. E. (2004). Chance and adaptation in the
evolution of island bumblebee behaviour. Population Ecology 46, 243– 251.
Chittka,L.,Skorupski,P.&Raine, N. E. (2009). Speed-accuracy tradeoffs in
animal decision making. Trends in Ecology & Evolution 24, 400– 407.
Cnaani,J.&Hefetz, A. (1994). The effect of workers size frequency distribution on
colony development in Bombus terrestris.Insectes Sociaux 41, 301 –307.
Cole, B. J. (1986). The social behavior of Leptothorax allardycei (Hymenoptera,
Formicidae): time budgets and the evolution of worker reproduction. Behavioral
Ecology and Sociobiology 18, 165– 173.
Cole,B.J.,Smith,A.A.,Huber,Z.J.&Wiernasz, D. C. (2010). The structure of
foraging activity in colonies of the harvester ant, Pogonomyrmex occidentalis.Behavioral
Ecology 21, 337– 342.
defense by Africanized and European honey bees. Science 218, 72– 74.
Cote,J.,Clobert,J.,Brodin,T.,Fogarty,S.&Sih, A. (2010). Personality-
dependent dispersal: characterization, ontogeny and consequences for spatially
structured populations. Philosophical Transactions of the Royal Society B: Biological Sciences
365, 4065– 4076.
Couvillon,M.J.&Dornhaus, A. (2009). Location, location, location: larvae
position inside the nest is correlated with adult body size in worker bumble-bees
(Bombus impatiens). Proceedings of the Royal Society B: Biological Sciences 276, 2411 –2418.
Couvillon,M.J.,Jandt,J.M.,Bonds,J.,Helm,B.R.&Dornhaus, A. (2011).
Percent lipid is associated with body size but not task in the bumble bee Bombus
impatiens.Journal of Comparative Physiology. A, Neuroethology Sensory Neural and Behavioral
Physiology 197, 1097– 1104.
Couzin,I.D.,Krause,J.,Franks,N.R.&Levin, S. A. (2005). Effective leadership
and decision-making in animal groups on the move. Nature 433, 513– 516.
Crosland, M. W. J. (1990). Variation in ant aggression and kin discrimination ability
within and between colonies. Journal of Insect Behavior 3, 359 –379.
Cutts,C.J.,Metcalfe,N.B.&Taylor, A. C. (1998). Aggression and growth
depression in juvenile Atlantic salmon: the consequences of individual variation in
standard metabolic rate. Journal of Fish Biology 52, 1026– 1037.
Dall,S.R.X.,Bell,A.M.,Bolnick,D.I.&Ratnieks, F. L. W. (2012). An
evolutionary ecology of individual differences. Ecology Letters 15, 1189– 1198.
Dall,S.R.X.,Houston,A.I.&McNamara, J. M. (2004). The behavioural ecology
of personality: consistent individual differences from an adaptive perspective. Ecology
Letters 7, 734– 739.
Daugherty,T.H.F.,Toth,A.L.&Robinson, G. E. (2011). Nutrition and division
of labor: effects on foraging and brain gene expression in the paper wasp Polistes
metricus.Molecular Ecology 20, 5337–5347.
Davidson, D. W. (1998). Resource discovery versus resource domination in ants: a
functional mechanism for breaking the trade-off. Ecological Entomology 23, 484– 490.
Del Giudice, M. (2011). Sex differences in romantic attachment: a meta-analysis.
Personality and Social Psychology Bulletin 37, 193– 214.
Del Giudice,M.,Ellis,B.J.&Shirtcliff, E. A. (2011). The Adaptive Calibration
Model of stress responsivity. Neuroscience and Biobehavioral Reviews 35, 1562–1592.
D’Ettorre,P.,Heinze,J.&Ratnieks, F. L. W. (2004). Worker policing by egg
eating in the ponerine ant Pachycondyla inversa.Proceedings of the Royal Society of London.
Series B: Biological Sciences 271, 1427–1434.
Diez,L.,Deneubourg, J.-L., Hoebeke,L.&Detrain, C. (2011). Orientation in
corpse-carrying ants: memory or chemical cues? Animal Behaviour 81, 1171 –1176.
Dingemanse,N.J.,Both,C.,Drent,P.J.&Tinbergen, J. M. (2004). Fitness
consequences of avian personalities in a fluctuating environment. Proceedings of the
Royal Society of London. Series B: Biological Sciences 271, 847–852.
Dingemanse,N.J.,Dochtermann,N.A.&Nakagawa, S. (2012). Defining
behavioural syndromes and the role of ‘syndrome deviation’ in understanding their
evolution. Behavioral Ecology and Sociobiology 66, 1543– 1548.
Dingemanse,N.J.,Kazem,A.J.N.,Reale,D.&Wright, J. (2010). Behavioural
reaction norms: animal personality meets individual plasticity. Trends in Ecology &
Evolution 25, 81– 89.
R. & Dawnay, N. (2007). Behavioural syndromes differ predictably between 12
populations of three-spined stickleback. Journal of Animal Ecology 76, 1128– 1138.
olldobler,B.&Amdam, G. V. (2012). Worker
division of labor and endocrine physiology are associated in the harvester ant,
Pogonomyrmex californicus.The Journal of Experimental Biology 215, 454–460.
van Doorn, A. (1989). Factors influencing dominance behaviour in queenless
bumblebee workers (Bombus terrestris). Physiological Entomology 14, 211–221.
Dornhaus, A. (2008). Specialization does not predict individual efficiency in an ant.
PLoS Biology 6, 2368– 2375.
Dornhaus,A.,Holley,J.A.,Pook,V.G.,Worswick,G.&Franks, N. R. (2008).
Why do not all workers work? Colony size and workload during emigrations in the
ant Temnothorax albipennis.Behavioral Ecology and Sociobiology 63, 43–51.
Duckworth, R. A. (2006). Behavioral correlations across breeding contexts provide
a mechanism for a cost of aggression. Behavioral Ecology 17, 1011– 1019.
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
64 J. M. Jandt and others
Dyer,A.G.&Chittka, L. (2004). Bumblebees (Bombus terrestris) sacrifice foraging
speed to solve difficult colour discrimination tasks. Journal of Comparative Physiology. A,
Neuroethology Sensory Neural and Behavioral Physiology 190, 759– 763.
Eldakar,O.T.,Dlugos,M.J.,Wilcox,R.S.&Wilson, D. S. (2009). Aggressive
mating as a tragedy of the commons in the water strider Aquarius remigis.Behavioral
Ecology and Sociobiology 64,25–33.
J. R. & Mann, J. J. (1999). CSF monoamines, age and impulsivity in wild grivet
monkeys (Cercopithecus aethiops aethiops). Brain, Behavior and Evolution 53, 305 –312.
Fewell,J.H.&Page, R. E. (1993). Genotypic variation in foraging responses to
environmental stimuli by honey bees, Apis mellifera.Experientia 49, 1106–1112.
Fewell,J.H.&Page, R. E. (1999). The emergence of division of labour in forced
associations of normally solitary ant queens. Evolutionary Ecology Research 1,537–548.
Fogarty,S.,Cote,J.&Sih, A. (2011). Social personality polymorphism and the
spread of invasive species: a model. American Naturalist 177, 273 –287.
Folse, H. J. III & Roughgarden, J. (2010). What is an individual organism? A
multilevel selection perspective. The Quarterly Review of Biology 85, 447– 472.
Foster,R.L.,Brunskill,A.,Verdirame,D.&O’Donnell, S. (2004).
Reproductive physiology, dominance interactions, and division of labour among
bumble bee workers. Physiological Entomology 29, 327– 334.
Garamszegi,L.Z.&Herczeg, G. (2012). Behavioural syndromes, syndrome
deviation and the within- and between-individual components of phenotypic
correlations: when reality does not meet statistics. Behavioral Ecology and Sociobiology
66, 1651– 1658.
Gill,R.J.,Ramos-Rodriguez,O.&Raine, N. E. (2012). Combined pesticide
exposure severely affects individual- and colony-level traits in bees. Nature 491,
105– 108.
Giray,T.,Giovanetti,M.&West-Eberhard, M. J. (2005). Juvenile hormone,
reproduction, and worker behavior in the neotropical social wasp Polistes canadensis.
Proceedings of the National Academy of Sciences of the United States of America 102, 3330– 3335.
Gordon, D. M. (1989). Dynamics of task switching in harvester ants. Animal Behaviour
38, 194– 204.
Gordon, D. M. (1991). Behavioral flexibility and the foraging ecology of seed-eating
ants. American Naturalist 138, 379 411.
Gordon, D. M. (1996). The organization of work in social insect colonies. Nature 380,
121– 124.
Gordon,D.M.,Chu,J.,Lillie,A.,Tissot,M.&Pinter, N. (2005). Variation
in the transition from inside to outside work in the red harvester ant Pogonomyrmex
barbatus.Insectes Sociaux 52, 212 –217.
Gordon,D.M.,Dektar,K.N.&Pinter-Wollman, N. (2013). Harvester ant
colony variation in foraging activity and response to humidity. PLoS One in press.
Gordon,D.M.,Guetz,A.,Greene,M.J.&Holmes, S. (2011). Colony variation in
the collective regulation of foraging by harvester ants. Behavioral Ecology 22, 429– 435.
Gosling, S. D. (2001). From mice to men: what can we learn about personality from
animal research? Psychological Bulletin 127,45–86.
Graff,J.,Jemielity,S.,Parker,J.D.,Parker,K.M.&Keller, L. (2007).
Differential gene expression between adult queens and workers in the ant Lasius
niger.Molecular Ecology 16, 675 –683.
Graham,A.,Munday,M.,Kaftanoglu, O., Page,R.,Amdam,G.&Rueppell,
O. (2011). Support for the reproductive ground plan hypothesis of social evolution
and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.).
BMC Evolutionary Biology 11,95.
Greene,M.J.&Gordon, D. M. (2003). Social insects Cuticular hydrocarbons
inform task decisions. Nature 423,32.
Greene,M.J.&Gordon, D. M. (2007). Interaction rate informs harvester ant task
decisions. Behavioral Ecology 18, 451– 455.
Gross,M.R.&Charnov, E. L. (1980). Alternative male life histories in bluegill
sunfish. Proceedings of the National Academy of Sciences of the United States of America: Biological
Sciences 77, 6937– 6940.
(2012). A morphologically specialized soldier caste improves colony defense in a
neotropical eusocial bee. Proceedings of the National Academy of Sciences of the United States
of America 109, 1182– 1186.
Hartfelder, K. (2000). Insect juvenile hormone: from ‘‘status quo’’ to high society.
Brazilian Journal of Medical and Biological Research 33, 157– 177.
Heifetz,Y.&Applebaum, S. W. (1995). Density-dependent physiological phase in
a non-migratory grasshopper Aiolopus thalassinus.Entomologia Experimentalis et Applicata
77, 251– 262.
Herb,B.R.,Wolschin, F., Hansen,K.D.,Aryee,M.J.,Langmead,B.,
Irizarry,R.,Amdam,G.V.&Feinberg, A. P. (2012). Reversible switching
between epigenetic states in honeybee behavioral subcastes. Nature 15, 1371– 1373.
Herbers, J. M. (1983). Social organization in Leptothorax ants: within and between
species patterns. Psyche 90, 361– 386.
Hillesheim,E.,Koeniger,N.&Moritz, R. F. A. (1989). Colony performance
in honeybees (Apis mellifera capensis Esch.) depends on the proportion of subordinate
and dominant workers. Behavioral Ecology and Sociobiology 24,291296.
olldobler,B.&Wilson, E. O. (1990). The Ants. Harvard University Press,
olldobler,B.&Wilson, E. O. (2009). The Superorganism: The Beauty, Elegance, and
Strangeness of Insect Societies. W. W Norton & Company, New York.
Holway, D. A. (1999). Competitive mechanisms underlying the displacement of
native ants by the invasive Argentine ant. Ecology 80, 238– 251.
Holway,D.A.&Suarez, A. V. (1999). Animal behavior: an essential component of
invasion biology. Trends in Ecology & Evolution 14, 328– 330.
Holway,D.A.&Suarez, A. V. (2004). Colony-structure variation and interspecific
competitive ability in the invasive Argentine ant. Oecologia 138, 216– 222.
Howard, K. J. (2006). Three queen morphs with alternative nest-founding behaviors
in the ant, Temnothorax longispinosus.Insectes Sociaux 53, 480 –488.
Hughes, A. L. (1985). Male size, mating success, and mating strategy in the
mosquitofish Gambusia affinis (Poeciliidae). Behavioral Ecology and Sociobiology 17,
271– 278.
Hunt,J.H.&Amdam, G. V. (2005). Bivoltinism as an antecedent to eusociality in
the paper wasp genus Polistes.Science 308, 264–267.
C. E., Rueppell, O., Guzman-Novoa,E.,Arechavaleta-Velasco,M.,
Chandra,S.,Fondrk,M.K.,Beye,M.&Page, R. E. (2007). Behavioral
genomics of honeybee foraging and nest defense. Naturwissenschaften 94, 247– 267.
Hunt,J.H.,Wolschin, F., Henshaw,M.T.,Newman,T.C.,Toth,A.L.&
Amdam, G. V. (2010). Differential gene expression and protein abundance evince
ontogenetic bias toward castes in a primitively eusocial wasp. PLoS One 5, e10674.
Huntingford, F. A. (1982). Do interspecific and intraspecific aggression vary in
relation to predation pressure in sticklebacks. Animal Behaviour 30, 909 916.
Pilarczyk,M.&Kadri, S. (2010). Coping strategies in a strongly schooling fish,
the common carp Cyprinus carpio.Journal of Fish Biology 76, 1576– 1591.
Ingram,K.K.,Oefner,P.&Gordon, D. M. (2005). Task-specific expression of
the foraging gene in harvester ants. Molecular Ecology 14, 813– 818.
Ings,T.C.,Raine,N.E.&Chittka, L. (2009). A population comparison of the
strength and persistence of innate colour preference and learning speed in the
bumblebee Bombus terrestris.Behavioral Ecology and Sociobiology 63, 1207–1218.
Ings,T.C.,Ward,N.L.&Chittka, L. (2006). Can commercially imported bumble
bees out-compete their native conspecifics? Journal of Applied Ecology 43, 940– 948.
Jandt,J.M.&Dornhaus, A. (2009). Spatial organization and division of labour in
the bumblebee Bombus impatiens.Animal Behaviour 77, 641 –651.
Jandt,J.M.&Dornhaus, A. (2011). Competition and cooperation: bumblebee
spatial organization and division of labor may affect worker reproduction late in life.
Behavioral Ecology and Sociobiology 65, 2341– 2349.
Jandt,J.M.,Huang,E.&Dornhaus, A. (2009). Weak specialization of workers
inside a bumble bee (Bombus impatiens)nest.Behavioral Ecology and Sociobiology 63,
1829– 1836.
Jeanne, R. L. (1988). Interindividual Behavioral Variability in Social Insects. Westview Press,
Jeanson, R. (2012). Long-term dynamics in proximity networks in ants. Animal
Behaviour 83, 915– 923.
Jeanson,R.L.&Fewell, J. H. (2008). Influence of the social context on division of
labor in ant foundress associations. Behavioral Ecology 19, 567– 574.
Johnson,J.C.&Sih, A. (2005). Precopulatory sexual cannibalism in fishing spiders
(Dolomedes triton): a role for behavioral syndromes. Behavioral Ecology and Sociobiology 58,
390– 396.
Johnson,J.C.&Sih, A. (2007). Fear, food, sex and parental care: a syndrome of
boldness in the fishing spider, Dolomedes triton.Animal Behaviour 74, 1131 –1138.
Jones,T.C.,Akoury,T.S.,Hauser,C.K.,Neblett, M. F., Linville,B.J.,
Edge,A.A.&Weber, N. O. (2011). Octopamine and serotonin have opposite
effects on antipredator behavior in the orb-weaving spider, Larinioides cornutus.Journal
of Comparative Physiology. A, Neuroethology Sensory Neural and Behavioral Physiology 197,
819– 825.
Jones,J.C.,Myerscough,M.R.,Graham,S.&Oldroyd, B. P. (2004). Honey
bee nest thermoregulation: diversity promotes stability. Science 305, 402– 404.
Kamakura, M. (2011). Royalactin induces queen differentiation in honeybees. Nature
473, 478– 483.
Keller, L. (1999). Levels of Selection in Evolution. Princeton University Press, Princeton.
Kinnally,E.L.,Jensen,H.A.,Ewing,J.H.&French, J. A. (2006). Serotonin
function is associated with behavioral response to a novel conspecific in marmosets.
American Journal of Primatology 68, 812– 824.
Kocher,S.D.,Ayroles,J. F.,Stone,E.A.&Grozinger, C. M. (2010). Individual
variation in pheromone response correlates with reproductive traits and brain gene
expression in worker honey bees. PLoS One 5, e9116.
Koolhaas,J.M.,de Boer, S. F., Buwalda,B.&van Reenen, K. (2007).
Individual variation in coping with stress: a multidimensional approach of ultimate
and proximate mechanisms. Brain, Behavior and Evolution 70, 218– 226.
Kralj-Fiser,S.,Weiss,B.M.&Kotrschal, K. (2010). Behavioural and
physiological correlates of personality in greylag geese (Anser anser). Journal of Ethology
28, 363– 370.
Krause,J.,Lusseau,D.&James, R. (2009). Animal social networks: an introduction.
Behavioral Ecology and Sociobiology 63, 967– 973.
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
Behavioural syndromes and social insects 65
Kulahci,I.G.,Dornhaus,A.&Papaj, D. R. (2008). Multimodal signals enhance
decision making in foraging bumble bees. Proceedings of the Royal Society B: Biological
Sciences 275, 797– 802.
Kurvers,R.,Prins,H.H.T.,van Wieren,S.E.,van Oers,K.,Nolet,B.A.&
Ydenberg, R. C. (2010). The effect of personality on social foraging: shy barnacle
geese scrounge more. Proceedings of the Royal Society B: Biological Sciences 277, 601–608.
Lapidge,K.L.,Oldroyd,B.P.&Spivak, M. (2002). Seven suggestive quantitative
trait loci influence hygienic behavior of honey bees. Naturwissenschaften 89, 565– 568.
Latshaw,J.S.&Smith, B. H. (2005). Heritable variation in learning performance
affects foraging preferences in the honey bee (Apis mellifera). Behavioral Ecology and
Sociobiology 58, 200– 207.
Laverty, T. M. (1994). Bumble bee learning and flower morphology. Animal Behaviour
47, 531– 545.
Leadbeater,E.,Carruthers,J.M.,Green,J.P.,van Heusden,J.&Field,J.
(2010). Unrelated helpers in a primitively eusocial wasp: is helping tailored towards
direct fitness? PLoS One 5, e11997.
&Robinson, G. E. (2012). Molecular determinants of scouting behavior in honey
bees. Science 335, 1225– 1228.
Lihoreau,M.,Brepson,L.&Rivault, C. (2009). The weight of the clan: even in
insects, social isolation can induce a behavioural syndrome. Behavioural Processes 82,
Lihoreau,M.,Chittka,L.,Le Comber,S.C.&Raine, N. E. (2012a). Bees do not
use nearest-neighbour rules for optimization of multi-location routes. Biology Letters
8, 13– 16.
A. D., Osborne,J.L.&Chittka, L. (2012b). Radar tracking and motion-sensitive
cameras on flowers reveal the development of pollinator multi-destination routes
over large spatial scales. PLoS Biology 10, e1001392.
Lihoreau,M.,Chittka,L.&Raine, N. E. (2010). Travel optimization by foraging
bumblebees through readjustments of traplines after discovery of new feeding
locations. American Naturalist 176, 744 757.
Lihoreau,M.,Chittka,L.&Raine, N. E. (2011). Trade-off between travel distance
and prioritization of high-reward sites in traplining bumblebees. Functional Ecology
25, 1284– 1292.
Lin,H.,Winston,M.L.,Haunderland,N.H.&Slessor, K. N. (1999). Influence
of age and population size on ovarian development, and of trophallaxis on ovarian
development and vitellogenin titres of queenless worker honey bee (Hymenoptera:
Apidae). The Canadian Entomologist 131, 695 706.
Lindauer, M. (1952). Ein beitrag zur frage der arbeitsteilung im bienenstaat. Zeitschrift
Fur Vergleichende Physiologie 34, 299–345.
Linksvayer, T. A. (2006). Direct, maternal, and sibsocial genetic effects on individual
and colony traits in an ant. Evolution 60, 2552– 2561.
Luttbeg,B.&Sih, A. (2010). Risk, resources and state- dependent adaptive
behavioural syndromes. Philosophical Transactions of the Royal Society B: Biological Sciences
365, 3977– 3990.
(2009). Testing dynamic variance-sensitive foraging using individual differences in
basal metabolic rates of zebra finches. Oikos 118, 545– 552.
Mattila,H.R.,Burke,K.M.&Seeley, T. D. (2008). Genetic diversity within
honeybee colonies increases signal production by waggle-dancing foragers. Proceedings
of the Royal Society B: Biological Sciences 275, 809–816.
Mattila,H.R.&Seeley, T. D. (2007). Genetic diversity in honey bee colonies
enhances productivity and fitness. Science 317, 362– 364.
Michelena,P.,Jeanson,R.,Deneubourg,J.L.&Sibbald, A. M. (2010).
Personality and collective decision-making in foraging herbivores. Proceedings of the
Royal Society B: Biological Sciences 277, 1093–1099.
Michener, C. (1964). Reproductive efficiency in relation to colony size in
Hymenopterous societies. Insectes Sociaux 11, 317–341.
Modlmeier,A.P.&Foitzik, S. (2011). Productivity increases with variation
in aggression among group members in Temnothorax ants. Behavioral Ecology 22,
1026– 1032.
Modlmeier,A.P.,Liebmann,J.E.&Foitzik, S. (2012). Diverse societies are more
productive: a lesson from ants. Proceedings of the Royal Society B: Biological Sciences 279,
2142– 2150.
Molet,M.,Chittka,L.&Raine, N. E. (2009). How floral odours are learned inside
the bumblebee (Bombus terrestris)nest.Naturwissenschaften 96, 213 –219.
Molet,M.,Chittka,L.,Stelzer,R.J.,Streit,S.&Raine, N. E. (2008). Colony
nutritional status modulates worker responses to foraging recruitment pheromone
in the bumblebee Bombus terrestris.Behavioral Ecology and Sociobiology 62, 1919–1926.
Molina,Y.&O’Donnell, S. (2009). Worker reproductive competition affects
division of labor in a primitively social paperwasp (Polistes instabilis). Insectes Sociaux
56, 14– 20.
Moore,A.J.,Breed,M.D.&Moor, M. J. (1987). The guard honey bee: ontogeny
and behavioural variability of workers performing a specialized task. Animal Behaviour
35, 1159– 1167.
Muller,H.,Grossmann,H.&Chittka, L. (2010). ‘Personality’ in bumblebees:
individual consistency in responses to novel colours? Animal Behaviour 80, 1065 –1074.
a,S.&Kortet, R. (2012). Nymphal
density, behavioral development, and life history in a field cricket. Behavioral Ecology
and Sociobiology 66, 645– 652.
Nonacs,P.&Kapheim, K. M. (2007). Social heterosis and the maintenance of
genetic diversity. Journal of Evolutionary Biology 20, 2253– 2265.
Nonacs,P.&Kapheim, K. M. (2008). Social heterosis and the maintenance of
genetic diversity at the genome level. Journal of Evolutionary Biology 21, 631– 635.
O’Donnell, S. (2006). Polybia wasp biting interactions recruit foragers following
experimental worker removals. Animal Behaviour 71, 709 –715.
O’Donnell,S.&Bulova, S. J. (2007a). Worker connectivity: a review of the design
of worker communication systems and their effects on task performance in insect
societies. Insectes Sociaux 54, 203– 210.
O’Donnell,S.&Bulova, S. J. (2007b). Worker connectivity: a simulation model
of variation in worker communication and its effects on task performance. Insectes
Sociaux 54, 211– 218.
van Oers,K.,de Jong,G.,van Noordwijk,A.J.,Kempenaers,B.&Drent,P.
J. (2005). Contribution of genetics to the study of animal personalities: a review of
case studies. Behaviour 142, 1185– 1206.
van Oers,K.&Mueller, J. C. (2010). Evolutionary genomics of animal personality.
Philosophical Transactions of the Royal Society B: Biological Sciences 365, 3991–4000.
Oldroyd,B.P.&Fewell, J. H. (2007). Genetic diversity promotes homeostasis in
insect colonies. Trends in Ecology & Evolution 22, 408– 413.
O’Neal,R.J.&Waller, G. D. (1984). On the pollen harvest by the honey bee (Apis
mellifera L.) near Tucson, Arizona (1976– 1981). Desert Plants 6, 81– 109.
Oster,G.F.&Wilson, E. O. (1978). Caste and Ecology in the Social Insects. Princeton
University Press, Princeton.
Page,R.E.J.,Erber,J.&Fondrk, M. K. (1998). The effect of genotype on response
thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). Journal
of Comparative Physiology. A 182, 489– 500.
Page,R.E.,Fondrk,M.K.&Rueppell, O. (2012a). Complex pleiotropy
characterizes the pollen hoarding syndrome in honey bees (Apis mellifera L.). Behavioral
Ecology and Sociobiology 66, 1459– 1466.
Page,R.E.,Rueppell,O.&Amdam, G. V. (2012b). Genetics of reproduction and
regulation of honeybee (Apis mellifera L.) social behavior. Annual Review of Genetics 46,
97– 119.
Page,R.E.,Robinson,G.E.,Britton,D.S.&Fondrk, M. K. (1992). Genotypic
variability for rates of behavioral development in worker honeybees (Apis mellifera L).
Behavioral Ecology 3, 173– 180.
Page,R.E.,Robinson,G.E.,Fondrk,M.K.&Nasr, M. E. (1995a). Effects of
worker genotypic diversity on honey bee colony development and behavior (Apis
mellifera L). Behavioral Ecology and Sociobiology 36, 387– 396.
Page,R.E.,Waddington,K.D.,Hunt,G.J.&Fondrk, M. K. (1995b). Genetic
determinants of honey bee foraging behaviour. Animal Behaviour 50, 1617 –1625.
Paleolog, J. (2009). Behavioural characteristics of honey bee (Apis mellifera) colonies
containing mix of workers of divergent behavioural traits. Animal Science Papers and
Reports 27, 237– 248.
Pankiw, T. (2003). Directional change in a suite of foraging behaviors in tropical and
temperate evolved honey bees (Apis mellifera L.). Behavioral Ecology and Sociobiology 54,
458– 464.
Pankiw,T.,Tarpy,D.R.&Page, R. E. (2002). Genotype and rearing environment
affect honeybee perception and foraging behaviour. Animal Behaviour 64, 663 672.
Pearce,A.N.,Huang,Z.Y.&Breed, M. D. (2001). Juvenile hormone and
aggression in honey bees. Journal of Insect Physiology 47, 1243– 1247.
Penke,L.,Denissen,J.J.A.&Miller, G. F. (2007). The evolutionary genetics of
personality. European Journal of Personality 21, 549– 587.
Pereboom,J.J.M.,Velthuis,H.H.W.&Duchateau, M. J. (2003). The
organisation of larval feeding in bumblebees (Hymenoptera, Apidae) and its
significance to caste differentiation. Insectes Sociaux 50, 127– 133.
Pinter-Wollman, N. (2012). Personality in social insects: how does worker
personality determine colony personality? Current Zoology 58, 580– 588.
Pinter-Wollman,N.,Gordon,D.M.&Holmes, S.(2012a). Nest site and weather
affect the personality of harvester ant colonies. Behavioral Ecology 23, 1022– 1029.
(2012b). How is activity distributed among and within tasks in Temnothorax ants?
Behavioral Ecology and Sociobiology 66, 1407– 1420.
(2011). The effect of individual variation on the structure and function of interaction
networks in harvester ants. Journal of the Royal Society, Interface 8, 1562–1573.
Pontier,D.,Fromont,E.,Courchamp, F., Artois,M.&Yoccoz, N. G. (1998).
Retroviruses and sexual size dimorphism in domestic cats (Felis catus L.). Proceedings
of the Royal Society of London. Series B: Biological Sciences 265, 167– 173.
Porter,S.D.&Jorgensen, C. D. (1981). Foragers of the harvester ant, Pogonomyrmex
owyheei: a disposable caste? Behavioral Ecology and Sociobiology 9, 247 –256.
Porter,S.D.&Tschinkel, W. R. (1985). Fire ant polymorphism: the ergonomics
of brood production. Behavioral Ecology and Sociobiology 16, 323– 336.
Powell, S. (2008). Ecological specialization and the evolution of a specialized caste
in Cephalotes ants. Functional Ecology 22, 902– 911.
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
66 J. M. Jandt and others
Powell,S.&Franks, N. R. (2005). Caste evolution and ecology: a special worker
for novel prey. Proceedings of the Royal Society B: Biological Sciences 272, 2173–2180.
Powell,S.&Franks, N. R. (2006). Ecology and the evolution of worker
morphological diversity: a comparative analysis with Eciton army ants. Functional
Ecology 20, 1105– 1114.
Powell,S.&Tschinkel, W. R. (1999). Ritualized conflict in Odontomachus brunneus
and the generation of interaction-based task allocation: a new organizational
mechanism in ants. Animal Behaviour 58, 965 –972.
Pronk,R.,Wilson,D.R.&Harcourt, R. (2010). Video playback demonstrates
episodic personality in the gloomy octopus. Journal of Experimental Biology 213,
1035– 1041.
Pruitt,J.N.&Ferrari, M. C. O. (2011). Intraspecific trait variants determine
the nature of interspecific interactions in a habitat-forming species. Ecology 92,
1902– 1908.
Pruitt,J.N.,Iturralde,G.,Aviles,L.&Riechert, S. E. (2011). Amazonian
social spiders share similar within-colony behavioural variation and behavioural
syndromes. Animal Behaviour 82, 1449 1455.
Pruitt,J.N.,Oufiero,C.E.,Aviles,L.&Riechert, S. E. (2012). Iterative
evolution of increased behavioral variation characterizes the transition to sociality
in spiders and proves advantageous. The American Naturalist 180, 496 –510.
Pruitt,J.N.&Riechert, S. E. (2009). Frequency-dependent success of cheaters
during foraging bouts might limit their spread within colonies of a socially
polymorphic spider. Evolution 63, 2966– 2973.
Pruitt,J.N.&Riechert, S. E. (2011). How within-group behavioural variation
and task efficiency enhance fitness in a social group. Proceedings of the Royal Society B:
Biological Sciences 278, 1209–1215.
Queller,D.C.,Zacchi, F., Cervo,R.,Turillazzi,S.,Henshaw,M.T.,
Santorelli,L.A.&Strassmann, J. E. (2000). Unrelated helpers in a social
insect. Nature 405,784787.
Raine,N.E.&Chittka, L. (2005). Colour preference in relation to the foraging
performance and fitness of the bumblebee Bombus terrestris.Uludag Bee Journal 5,
145– 150.
Raine,N.E.&Chittka, L. (2007a). Pollen foraging: learning a complex motor skill
by bumblebees (Bombus terrestris). Naturwissenschaften 94, 459–464.
Raine,N.E.&Chittka, L. (2007b). The adaptive significance of sensory bias in a
foraging context: floral colour preferences in the bumblebee Bombus terrestris.PLoS
One 2, e556.
Raine,N.E.&Chittka, L. (2008). The correlation of learning speed and natural
foraging success in bumble-bees. Proceedings of the Royal Society B: Biological Sciences 275,
803– 808.
Raine,N.E.&Chittka, L. (2012). No trade-off between learning speed and
associative flexibility in bumblebees: a reversal learning test with multiple colonies.
PLoS One 7, e45096.
Raine,N.E.,Ings,T.C.,Dornhaus,A.,Saleh,N.&Chittka, L. (2006a).
Adaptation, genetic drift, pleiotropy, and history in the evolution of bee foraging
behavior. Advances in the Study of Behavior 36, 305 –354.
Raine,N.E.,Ings,T.C.,Ramos-Rodriguez,O.&Chittka, L. (2006b).
Intercolony variation in learning performance of a wild British bumblebee population
(Hymenoptera: Apidae: Bombus terrestris audax). Entomologia Generalis 28, 241 256.
Ratnieks,F.L.W.&Reeve, H. K. (1992). Conflict in single-queen Hymenopteran
societies: the structure of conflict and processes that reduce conflict in advanced
eusocial species. Journal of Theoretical Biology 158, 33–65.
eale,D.,Reader,S.M.,Sol,D.,McDougall,P.T.&Dingemanse, N. J. (2007).
Integrating animal temperament within ecology and evolution. Biological Reviews 82,
291– 318.
Reeve, H. K. (1992). Queen activation of lazy workers in colonies of the eusocial
naked mole-rat. Nature 358, 147– 149.
Reeve,H.K.&Nonacs, P. (1997). Within-group aggression and the value of group
members: theory and a field test with social wasps. Behavioral Ecology 8, 75– 82.
Riechert,S.E.&Hedrick, A. V. (1993). A test for correlations amongfitness-linked
behavioral traits in the spider Agelenopsis aperta (Araneae, Agelenidae). Animal Behaviour
46, 669– 675.
Robinson, G. E. (1987). Regulation of honey bee age polyethism by juvenile hormone.
Behavioral Ecology and Sociobiology 20, 329– 338.
Robinson, G. E. (1992). Regulation of division of labor in insect societies. Annual
Review of Entomology 37,637665.
Robinson, E. J. H. (2009). Physiology as a caste-defining feature. Insectes Sociaux 56,
Robinson,G.E.&Huang, Z. Y. (1998). Colony integration in honey bees: genetic,
endocrine and social control of division of labor. Apidologie 29, 159– 170.
Robinson,G.E.&Page, R. E. (1988). Genetic determination of guarding and
undertaking in honeybee colonies. Nature 333, 356– 358.
Robinson,G.E.&Page, R. E. (1989). Genetic determination of nectar foraging,
pollen foraging, and nest-site scouting in honey bee colonies. Behavioral Ecology and
Sociobiology 24, 317– 323.
Robinson,G.E.,Page,R.E.&Arensen, N. (1994). Genotypic differences in brood
rearing in honey bee colonies: context-specific? Behavioral Ecology and Sociobiology 34,
125– 137.
Robinson,G.E.,Page,R.E.J.&Fondrk, M. K. (1990). Intracolonial behavioral
variation in worker oviposition, oophagy, and larval care in queenless honey bee
colonies. Behavioral Ecology and Sociobiology 26, 315– 323.
N. (2009). Radio tagging reveals the roles of corpulence, experience and social
information in ant decision making. Behavioral Ecology and Sociobiology 63, 627– 636.
(2000). Social and spatial organisation in colonies of a primitively eusocial wasp,
Ropalidia revolutionalis (de Saussure) (Hymenoptera: Vespidae). Australian Journal of
Entomology 39, 20– 24.
Robson,S.K.&Traniello, J. F. A. (1999). Key individuals and the organisation
of labor in ants. In Information Processing in Social Insects (eds C. Detrain and J. L.
Deneubourg), pp. 239– 260. Birkh¨
auser Verlag, Basel.
Roux,E.A.&Korb, J. (2004). Evolution of eusociality and the soldier caste in
termites: a validation of the intrinsic benefit hypothesis. Journal of Evolutionary Biology
17, 869– 875.
Rowles,A.D.&O’Dowd, D. J. (2007). Interference competition by Argentine ants
displaces native ants: implications for biotic resistance to invasion. Biological Invasions
9, 73– 85.
Rueppell, O., Pankiw,T.,Nielsen,D.I.,Fondrk,M.K.,Beye,M.&Page,
R. E. (2004). The genetic architecture of the behavioral ontogeny of foraging in
honeybee workers. Genetics 167, 1767– 1779.
Saleh,N.&Chittka, L. (2007). Traplining in bumblebees (Bombus impatiens): a
foraging strategy’s ontogeny and the importance of spatial reference memory in
short-range foraging. Oecologia 151, 719– 730.
Scharf,I.,Modlmeier,A.P.,Fries,S.,Tirard,C.&Foitzik, S. (2012).
Characterizing the collective personality of ant societies: aggressive colonies do not
abandon their home. PLoS One 7, e33314.
Scheiner, R. (2012). Birth weight and sucrose responsiveness predict cognitive skills
of honeybee foragers. Animal Behaviour 84, 305 –308.
Scheiner,R.,Barnert,M.&Erber, J. (2003). Variation in water and sucrose
responsiveness during the foraging season affects proboscis extension learning in
honey bees. Apidologie 34, 67– 72.
Scheiner,R.,Erber,J.&Page, R. E. (1999). Tactile learning and the individual
evaluation of the reward in honey bees (Apis mellifera L.). Journal of Comparative
Physiology. A, Sensory Neural and Behavioral Physiology 185, 1– 10.
Scheiner,R.,Page,R.E.&Erber, J. (2001). The effects of genotype, foraging role,
and sucrose responsiveness on the tactile learning performance of honey bees (Apis
mellifera L.). Neurobiology of Learning and Memory 76, 138– 150.
Scheiner,R.,Page,R.E.&Erber,J. (2004). Sucrose responsiveness and behavioral
plasticity in honey bees (Apis mellifera). Apidologie 35, 133–142.
Schmid-Hempel, P. (1990). Reproductive competition and the evolution of work
load in social insects. American Naturalist 135, 501 526.
Schofield,R.,Emmett,K.,Niedbala,J.&Nesson, M. (2011). Leaf-cutter ants
with worn mandibles cut half as fast, spend twice the energy, and tend to carry
instead of cut. Behavioral Ecology and Sociobiology 65, 969– 982.
urch,R.,Rothenberger,S.&Heg, D. (2011). The building-up of social
relationships: behavioural types, social networks and cooperative breeding in a
cichlid. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 4089– 4098.
Schwander,T.,Cahan,S.H.&Keller, L. (2007). Characterization and
distribution of Pogonomyrmex harvester ant lineages with genetic caste determination.
Molecular Ecology 16, 367– 387.
Schwander,T.,Lo,N.,Beekman,M.,Oldroyd,B.P.&Keller, L. (2010).
Nature versus nurture in social insect caste differentiation. Trends in Ecology &
Evolution 25, 275– 282.
Seeley, T. D. (1982). Adaptive significance of the age polyethism schedule in honeybee
colonies. Behavioral Ecology and Sociobiology 11, 287– 293.
Seeley,T.D.,Weidenm ¨
uhnholz, S. (1998). The shaking signal of
the honey bee informs workers to prepare for greater activity. Ethology 104, 10–26.
Seid,M.A.&Traniello, J. F. A. (2006). Age-related repertoire expansion and
division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective
on temporal polyethism and behavioral plasticity in ants. Behavioral Ecology and
Sociobiology 60, 631– 644.
Sendova-Franks,A.B.&Franks, N. R. (1995). Spatial relationships within nests of
the ant Leptothorax unifasciatus (Latr.) and their implications for the division of labor.
Animal Behaviour 50, 121 136.
Short,K.H.&Petren, K. (2008). Boldness underlies foraging success of invasive
Lepidodactylus lugubris geckos in the human landscape. Animal Behaviour 76, 429 –437.
Sih, A. (1992). Prey uncertainty and the balancing of antipredator and feeding needs.
American Naturalist 139, 1052 1069.
Sih, A. (2011). Effects of early stress on behavioral syndromes: an integrated adaptive
perspective. Neuroscience and Biobehavioral Reviews 35, 1452–1465.
Sih,A.&Bell, A. M. (2008). Insights for behavioral ecology from behavioral
syndromes. Advances in the Study of Behavior (Volume 38), pp. 227 281. Elsevier
Academic Press Inc., San Diego.
Sih,A.,Bell,A.&Johnson, J. C. (2004a). Behavioral syndromes: an ecological and
evolutionary overview. Trends in Ecology & Evolution 19, 372– 378.
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
Behavioural syndromes and social insects 67
Sih,A.,Bell,A.,Johnson,J.C.&Ziemba, R. E. (2004b). Behavioral syndromes:
an integrative overview. The Quarterly Review of Biology 79, 241– 277.
Sih,A.,Cote,J.,Evans,M.,Fogarty,S.&Pruitt, J. (2012). Ecological
implications of behavioural syndromes. Ecology Letters 15, 278 –289.
Sih,A.&Del Giudice, M. (2012). Linking behavioural syndromes and cognition:
a behavioural ecology perspective. Philosophical Transactions of the Royal Society B:
Biological Sciences 367, 2762–2772.
Sih,A.,Ferrari,M.C.O.&Harris, D. J. (2011). Evolution and behavioural
responses to human-induced rapid environmental change. Evolutionary Applications 4,
367– 387.
Sih,A.,Hanser,S.F.&McHugh, K. A. (2009). Social network theory: new insights
and issues for behavioral ecologists. Behavioral Ecology and Sociobiology 63, 975– 988.
Sih,A.,Kats,L.B.&Maurer, E. F. (2003). Behavioural correlations across situations
and the evolution of antipredator behaviour in a sunfish-salamander system. Animal
Behaviour 65,29–44.
Sih,A.&Watters, J. V. (2005). The mix matters: behavioural types and group
dynamics in water striders. Behaviour 142, 1423– 1437.
Simone-Finstrom,M.,Gardner,J.&Spivak, M. (2010). Tactile learning in resin
foraging honeybees. Behavioral Ecology and Sociobiology 64, 1609– 1617.
Smith,B.R.&Blumstein, D. T. (2008). Fitness consequences of personality: a
meta-analysis. Behavioral Ecology 19, 448– 455.
Smith,C.R.,Toth,A.L.,Suarez,A.V.&Robinson, G. E. (2008). Genetic and
genomic analyses of the division of labour in insect societies. Nature Reviews Genetics
9, 735– 748.
Spaethe,J.,Brockmann,A.,Halbig,C.&Tautz, J. (2007). Size determines
antennal sensitivity and behavioral threshold to odors in bumblebee workers.
Naturwissenschaften 94, 733– 739.
Spaethe,J.&Chittka, L. (2003). Interindividual variation of eye optics and single
object resolution in bumblebees. Journal of Experimental Biology 206, 3447– 3453.
uller, A. (2002). Size variation and foraging rate in
bumblebees (Bombus terrestris). Insectes Sociaux 49, 142 –146.
Spivak,M.,Masterman,R.,Ross,R.&Mesce, K. A. (2003). Hygienic behavior
in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. Journal of
Neurobiology 55, 341– 354.
Stamps,J.A.&Groothuis, T. G. G. (2010). Developmental perspectives on
personality: implications for ecological and evolutionary studies of individual
differencese. Philosophical Transactions of the Royal Society B: Biological Sciences 365,
4029– 4041.
eale,D.&Roff, D. A. (2002). Selection, structure and the
heritability of behaviour. Journal of Evolutionary Biology 15, 277– 289.
Stuart,R.J.&Page, R. E. (1991). Genetic component to division of labor among
workers of a Leptothoracine ant. Naturwissenschaften 78, 375– 377.
Suarez,A.V.,Holway,D.A.,Liang,D.S.,Tsutsui,N.D.&Case, T. J. (2002).
Spatiotemporal patterns of intraspecific aggression in the invasive Argentine ant.
Animal Behaviour 64, 697 –708.
Suarez,A.V.,Tsutsui,N.D.,Holway,D.A.&Case, T. J. (1999). Behavioral and
genetic differentiation between native and introduced populations of the Argentine
ant. Biological Invasions 1, 43–53.
Sumpter,D.J.T.(2010).Collective Animal Behavior. Princeton University Press,
Suryanarayanan,S.,Hantschel,A.E.,Torres,C.G.&Jeanne, R. L. (2011a).
Changes in the temporal pattern of antennal drumming behavior across the Polistes
fuscatus colony cycle (Hymenoptera, Vespidae). Insectes Sociaux 58, 97 –106.
Suryanarayanan,S.,Hermanson,J.C.&Jeanne, R. L. (2011b). A mechanical
signal biases caste development in a social wasp. Current Biology 21, 231– 235.
Suryanarayanan,S.&Jeanne, R. L. (2008). Antennal drumming, trophallaxis,
and colony development in the social wasp Polistes fuscatus (Hymenoptera: Vespidae).
Ethology 114, 1201– 1209.
Theraulaz,G.&Bonabeau, E. (1995). Modelling the collective building of complex
architectures in social insects with lattice swarms. Journal of Theoretical Biology 177,
381– 400.
Theraulaz,G.,Bonabeau,E.&Deneubourg, J.-L. (1998). Response threshold
reinforcement and division of labour in insect societies. Proceedings of the Royal Society
B265, 327– 332.
Tibbetts,E.A.&Huang, Z. Y. (2010). The challenge hypothesis in an insect:
juvenile hormone increases during reproductive conflict following queen loss in
Polistes wasps. American Naturalist 176,123–130.
(2009). Lipid stores, ovary development, and brain gene expression in Polistes metricus
females. Insectes Sociaux 56, 77–84.
Toth,A.L.&Robinson, G. E. (2005). Worker nutrition and division of labour in
honeybees. Animal Behaviour 69, 427 –435.
Tschinkel, W. (1998). The reproductive biology of fire ant societies. BioScience 48,
593– 605.
Tschinkel, W. R. (2004). The nest architecture of the Florida harvester ant,
Pogonomyrmex badius.Journal of Insect Science 4, 1 19.
Tsuji, K. (1994). Inter-colonial selection for the maintenance of cooperative breeding
in the ant Pristomyrmex pungens: a laboratory experiment. Behavioral Ecology and
Sociobiology 35, 109– 113.
Visscher, P. K. (1988). Undertaker specialists in honey bee colonies. In Interindividual
Behavioral Variability in Social Insects (ed. R. L. Jeanne), pp. 359 –383. Westview Press,
Volny,V.P.&Gordon, D. M. (2002). Genetic basis for queen-worker dimorphism
in a social insect. Proceedings of the National Academy of Sciences of the United States of America
99, 6108– 6111.
Vos,M.&Velicer, G. J. (2006). Genetic population structure of the soil bacterium
Myxococcus xanthus at the centimeter scale. Applied and Environmental Microbiology 72,
3615– 3625.
Waddington,K.D.,Nelson,C.M.&Page, R. E. (1998). Effects of pollen quality
and genotype on the dance of foraging honey bees. Animal Behaviour 56,3539.
Wang,Y.,Amdam,G.V.,Rueppell, O., Wallrichs,M.A.,Fondrk,M.K.,
Kaftanoglu,O.&Page, R. E. Jr. (2009). PDK1 and HR46 gene homologs tie
social behavior to ovary signals. PLoS One 4, e4899.
uller, A. (2004). The control of nest climate in bumblebee (Bombus terrestris)
colonies: interindividual variability and self reinforcement in fanning response.
Behavioral Ecology 15, 120– 128.
Weiner,S.A.&Toth, A. L. (2012). Epigenetics in social insects: a new direction for
understanding the evolution of castes. Genetics Research International 2012,1–11.
Wenseleers,T.&Ratnieks, F. L. W. (2006a). Comparative analysis of worker
reproduction and policing in eusocial hymenoptera supports relatedness theory.
American Naturalist 168, E163 E179.
Wenseleers,T.&Ratnieks, F. L. W. (2006b). Enforced altruism in insect societies.
Nature 444, 50.
Wheeler, D. E. (1986). Developmental and physiological determinants of caste in
social Hymenoptera: evolutionary implications. American Naturalist 128, 13 34.
Wheeler,D.E.,Buck,N.&Evans, J. D. (2006). Expression of insulin pathway
genes during the period of caste determination in the honey bee, Apis mellifera.Insect
Molecular Biology 15, 597– 602.
Wilson, E. O. (1976). Behavioral discretization and number of castes in an ant species.
Behavioral Ecology and Sociobiology 1, 141– 154.
Wilson, E. O. (1985). Between-caste aversion as a basis for division of labor in the
ant Pheidole pubiventris (Hymenoptera: Formicidae). Behavioral Ecology and Sociobiology
17, 35– 37.
Wilson,D.S.,Clark,A.B.,Coleman,K.&Dearstyne, T. (1994). Shyness and
boldness in humans and other animals. Trends in Ecology & Evolution 9, 442–446.
Winston, M. (1987). The Biology of the Honey Bee. Harvard University Press, Cambridge.
Wolf,M.&Weissing, F. J. (2010). An explanatory framework for adaptive personality
differences. Philosophical Transactions of the Royal Society B: Biological Sciences 365,
3959– 3968.
M., Dunn,D.M.,Meyerhof,W.,Weiss,R.B.&Bamshad, M. J. (2006).
Independent evolution of bitter-taste sensitivity in humans and chimpanzees. Nature
440, 930– 934.
Worden,B.D.,Skemp,A.K.&Papaj, D. R. (2005). Learning in two contexts: the
effects of interference and body size in bumblebees. Journal of Experimental Biology
208, 2045– 2053.
Wray,M.K.,Mattila,H.R.&Seeley, T. D. (2011). Collective personalities in
honeybee colonies are linked to colony fitness. Animal Behaviour 81, 559 –568.
Wray,M.K.&Seeley, T. D. (2011). Consistent personality differences in house-
hunting behavior but not decision speed in swarms of honey bees (Apis mellifera).
Behavioral Ecology and Sociobiology 65, 2061– 2070.
Zanette,L.R.S.&Field, J. (2011). Founders versus joiners: group formation in the
paper wasp Polistes dominulus.Animal Behaviour 82, 699 –705.
(Received 28 April 2012; revised 9 April 2013; accepted 17 April 2013; published online 15 May 2013)
Biological Reviews 89 (2014) 48– 67 ©2013 The Authors. Biological Reviews ©2013 Cambridge Philosophical Society
... The structure of a feed-forward loop inherently implies among-individual variation in contact patterns, as each node differs in the number of incoming and outgoing connections (or edges). Insect workers express substantial among-individual variation along a number of behavioural axes that may contribute to the generation of such network structures [15]. For instance, workers vary in the proportion of time that they are actively engaged in tasks: e.g. a minority of workers often carry out the majority of work [16][17][18][19][20], with some workers even appearing to specialize in inactivity [21]. ...
... Our model is not designed to reproduce the dynamics of any specific species. Rather, we seek to evaluate structural and functional consequences of patterns of behavioural variation that are commonly observed across eusocial insects [15,22], with a particular focus on how such variation shapes patterns of physical contact between workers (e.g. antennation), which are central in regulating collective behaviour [2,6,7]. ...
... If negatively correlated, these values are paired such that the agent with the highest value of A also has the lowest value of T, and so on, thus generating a population where more active agents also tend to move in straighter paths. This was done in order to explore whether such a behavioural syndrome [15] may especially contribute to the formation of feed-forward loops, given that active individuals with a greater potential to initiate contact (see Agent interactions, below) would also potentially contact a greater diversity of individuals, due to reduced spatial fidelity. ...
Full-text available
Coordinated responses in eusocial insect colonies arise from worker interaction networks that enable collective processing of ecologically relevant information. Previous studies have detected a structural motif in these networks known as the feed-forward loop, which functions to process information in other biological regulatory networks (e.g. transcriptional networks). However, the processes that generate feed-forward loops among workers and the consequences for information flow within the colony remain largely unexplored. We constructed an agent-based model to investigate how individual variation in activity and movement shaped the production of feed-forward loops in a simulated insect colony. We hypothesized that individual variation along these axes would generate feed-forward loops by driving variation in interaction frequency among workers. We found that among-individual variation in activity drove over-representation of feed-forward loops in the interaction networks by determining the directionality of interactions. However, despite previous work linking feed-forward loops with efficient information transfer, activity variation did not promote faster or more efficient information flow, thus providing no support for the hypothesis that feed-forward loops reflect selection for enhanced collective functioning. Conversely, individual variation in movement trajectory, despite playing no role in generating feed-forward loops, promoted fast and efficient information flow by linking together otherwise unconnected regions of the nest.
... Similarly to vertebrates, certain arthropod taxa have consistent inter-individual behavioural differences (also referred to as animal personality: the temporal variation of the same behavioural trait) (Bell et al. 2009;Réale and Dingemanse 2012). Behavioural consistency (in one behaviour and/or amongst correlated behaviours) might favour individuals and, through them, populations or species in an adaptive manner, depending on the current ecological situation (Dingemanse and Réale 2005;Réale and Dingemanse 2012;Jandt et al. 2014). However, compared with vertebrates, this phenomenon in arthropods has received much less attention. ...
Full-text available
Selection forces often generate sex-specific differences in various traits closely related to fitness. While in adult spiders (Araneae), sexes often differ in colouration, body size, antipredator or foraging behaviour, such sex-related differences are less pronounced amongst immatures. However, sex-specific life-history strategies may also be adaptive for immatures. Thus, we hypothesized that, among spiders, immature individuals show different life-history strategies that are expressed as sex-specific differences in body parameters and behavioural features, and also in their relationships. We used immature individuals of a protandrous jumping spider, Carrhotus xanthogramma, and examined sex-related differences. Results showed that males have higher mass and larger prosoma than females. Males were more active and more risk-tolerant than females. Male activity increased with time, and larger males tended to capture the prey faster than small ones, while females showed no such patterns. However, females reacted to the threatening abiotic stimuli more with the increasing number of test sessions. In both males and females, individuals with better body condition tended to be more risk-averse. Spiders showed no sex-specific differences in inter-individual behavioural consistency and in intra-individual behavioural variation in the measured behavioural traits. Finally, we also found evidence for behavioural syndromes (i.e. correlation between different behaviours), where in males only the activity correlated with the risk-taking behaviour, but in females all the measured behavioural traits were involved. The present study demonstrates that C. xanthogramma sexes follow different life-history strategies even before attaining maturity.
... Simply by performing a task successfully, a worker might increase its propensity to perform the same task in the future through a positive feedback loop (Ravary et al. 2007). Other individual-specific factors, such as behavioral syndromes (personality) or social niche specialization, may shape task specialization, although they have received less attention in social insects than in vertebrates (Bergmüller and Taborsky 2010;Modlmeier et al. 2012;Jandt et al. 2014;Loftus et al. 2021). ...
... Among-individual variation in behaviour has also often been associated with enhanced collective outcomes, including increased foraging rate and colony productivity in honeybees and other social insects (Jandt et al. 2014;Fig O' Shea-Wheller et al. 2021). Network theory offers a variety of metrics that can capture this variation and link it to group-level behaviour (Farine and Whitehead 2015; Table 1). ...
Full-text available
The societies of honeybees (Apis spp.) are microcosms of divided labour where the fitness interests of individuals are so closely aligned that, in some contexts, the colony behaves as an entity in itself. Self-organization at this extraordinary level requires sophisticated communication networks, so it is not surprising that the celebrated waggle dance, by which bees share information about locations outside the hive, evolved here. Yet bees within the colony respond to several other lesser-known signalling systems, including the tremble dance, the stop signal and the shaking signal, whose roles in coordinating worker behaviour are not yet fully understood. Here, we firstly bring together the large but disparate historical body of work that has investigated the “meaning” of such signals for individual bees, before going on to discuss how network-based approaches can show how such signals function as a complex system to control the collective foraging effort of these remarkable social insect societies.
... This pattern means that bolder individuals might play especially important roles in spreading information or disease within groups given their more dispersive social networks. Consequences of individual behavior within a group context have special implications in social and eusocial species as reviewed by Jandt et al. (2014). It is important to note, however, that several empirical papers that have explored the consequences of individual behavior on task specialization and colony success in species of social spiders have been recently retracted (Supplemental Table 1). ...
The study of individual behavioral variation, sometimes called animal personalities or behavioral types, is now a well-established area of research in behavioral ecology and evolution. Considerable theoretical work has developed predictions about its ecological and evolutionary causes and consequences, and studies testing these theories continue to grow. Here, we synthesize the current empirical work to shed light on which theories are well supported and which need further refinement. We find that the major frameworks explaining the existence of individual behavioral variation, the pace-of-life syndrome hypothesis and state-dependent feedbacks models, have mixed support. The consequences of individual behavioral variation are well studied at the individual level but less is known about consequences at higher levels such as among species and communities. The focus of this review is to reevaluate and reestablish the foundation of individual behavioral variation research: What do we know? What questions remain? And where are we going next? Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 53 is November 2022. Please see for revised estimates.