Download Me and we: the interplay between individual and group behavioral

COIS-49; NO. OF PAGES 9
Available online at www.sciencedirect.com
ScienceDirect
Me and we: the interplay between individual and group
behavioral variation in social collectives
Adria C LeBoeuf1 and Christina M Grozinger2
In social insects, substantial behavioral variation exists
among individuals and across colonies. Here, we discuss the
role of individual variation in shaping behavioral tendencies
of social groups, and highlight gaps in our knowledge about
the role of the social group in modulating individual
behavioral tendencies. We summarize our knowledge of the
genetic mechanisms underpinning these processes, and
describe the use of genomic tools to better understand the
influence of social context on individuals. We discuss rapid
collective phasic transitions, in which a group of individuals
engages in a common novel behavior together, as a
potentially highly informative model system in which to
comprehensively investigate the interplay between individual
and group variation.
Addresses
1
Department of Ecology and Evolution, Center for Integrative Genomics,
University of Lausanne, UNIL-Sorge, Batiment Biophore, CH-1015
Lausanne, Switzerland
2
Department of Entomology, Center for Pollinator Research, Center for
Chemical Ecology, The Pennsylvania State University, 1 Chemical
Ecology Lab, Orchard Road, University Park, PA 16802, USA
Corresponding author: Grozinger, Christina M ([email protected])
Current Opinion in Insect Science 2014, 3:xx–yy
This review comes from a themed issue on Social Insects
extent can and do individuals change their tendencies
depending on their social environment (e.g., the behavioral tendencies of their group)? In this review we will
consider variation on the individual scale, variation on the
group scale, and the interplay between them in social
insects. Furthermore, we discuss the application of molecular and genomic approaches to understand the mechanisms mediating these processes.
Discussions of the effects of individual behavioral variation on group function in social insects have largely
focused on mature colonies and established social groups,
in which individual variation leads to improved division of
labor of colony tasks [4,5,6]. However, the behavior of
social insect colonies changes over time as colonies form,
mature, and eventually die, and the behavioral tendencies
of the individuals may change correspondingly [7].
Furthermore, colonies can undergo rapid collective phasic transitions, such as migrating or swarming, wherein a
large number of individuals, regardless of their current
behavioral or physiological state, engage in a common
behavior simultaneously [8–10]. These rapid collective
phasic transitions thus appear to be a special case of social
behavior, in which the social signals generally override
individual variation. We discuss examples and possible
roles of individual variation in shaping these processes.
Edited by Laurent Keller and Nathalie Stroeymeyt
Variation in behavioral traits of individuals and
groups
http://dx.doi.org/10.1016/j.cois.2014.09.010
2214-5745/# 2014 Elsevier Ltd. All right reserved.
Introduction
Individuals in social insect colonies can vary significantly
in their behavioral tendencies — their propensity to
engage in particular behaviors — and there is mounting
evidence that a great deal of behavioral variation exists
across colonies as well [1,2]. While there have been
many studies examining how group behavior emerges
from individual behavior through self-organization [3],
how individual variation and group variation influence
each other has not been comprehensively considered in
social insects. For example, is the group’s behavior simply
an average of the behavioral tendencies of the individual
group members, or do some individuals disproportionately affect group behavioral tendencies? To what
www.sciencedirect.com
In all animal species, including in social insects, individuals can vary profoundly in their behavioral tendencies
(for excellent recent reviews, see Refs. [1,2]). Behavioral variation often results from differences in response
thresholds to key sensory stimuli, where some individuals
respond rapidly to cues presented at low intensities, while
others require prolonged exposure to high intensities of
these cues before a response is elicited [11,12]. Simple
shifts in sensory sensitivity can result in global shifts in
an organism’s social behavior: for example, honey bee
workers with high response thresholds to queen pheromone are more likely to activate their ovaries and compete with the queen over reproduction [13], less likely to
rear new queens if the queen is lost [14], and exhibit
distinct genome-wide brain gene expression patterns [15]
compared to workers with low response thresholds.
Individual variation in response thresholds can be relatively stable over the lifetime of an individual (if it is due
to genetic variation or early developmental factors) or
change as a result of condition (age, reproductive status,
Current Opinion in Insect Science 2014, 3:1–9
Please cite this article in press as: LeBoeuf AC, Grozinger CM: Me and we: the interplay between individual and group behavioral variation in social collectives, Curr Opin Insect Sci (2014), http://
dx.doi.org/10.1016/j.cois.2014.09.010
COIS-49; NO. OF PAGES 9
2 Social Insects
immune status), experience (including learning), social
interactions, or environmental context (reviewed in Refs.
[1,2]). Few studies have examined whether the same
regulatory neural and genetic mechanisms underlie behavioral differences that are stable between individuals or
plastic throughout an individual’s lifetime, though recent
genomic studies suggest this is likely to be the case [16];
for example, a common set of genes is differentially
expressed between workers from aggressive Africanized
and more docile European honey bee strains (genetic
variation), between aggressive older bees and more docile
younger bees (age-dependent variation), and between
honey bees that are exposed to alarm pheromone or
solvent controls (environmental/social context variation).
Interestingly, expression of a specific subset of these
genes is associated with aggressive behavior in honey
bees, paper wasps, and mice, suggesting that these genes
may mediate aggressive tendencies across species [17].
Many recent studies of individual variation have been
devoted to the analysis and documentation of ‘keystone’
individuals, individuals who have a disproportionately
large, and in some cases, irreplaceable effect on group
dynamics in relation to generic individuals (as defined
and reviewed over many animal species in Ref. [18]). As
noted by Modlmeier et al. [18], in reference to social
insects, the only true fixed, irreplaceable keystone individuals are queens. Workers can occupy keystone roles,
though this is typically temporary and these workers can
be readily replaced by their nestmates [19]. Keystone
workers may be those that have especially low response
thresholds for a specific task-associated signal and thus
respond very rapidly. While there have been several
studies examining the genomic mechanisms distinguishing queens and workers in social insect species (for
examples see Refs. [20–23]), there have been few studies
of the genomic mechanisms that distinguish keystone
workers from their nestmates. A recent study of scout
honey bees (which seek out novel food resources in their
environment and subsequently recruit their nestmates)
demonstrated that these bees have distinct brain gene
expression profiles compared to their non-scout foraging
nestmates [24]. Expression of several genes involved in
biogenic amine signaling differed between the two
groups. Treating colonies with octopamine and glutamate resulted in increased overall scouting behavior,
while treatments with dopamine antagonists inhibited
it. Comparative studies in other model systems will be
necessary to determine if common genes underlie scouting behavior across social insect species. Additionally, it
would be of great interest to determine if common genes
underlie the behavior of different types of keystone
individuals, even if the behaviors of those individuals
are quite distinct. For example, keystone behaviors
could arise from the tuning of molecular activators such
as hormones (discussed in Ref. [13]), biogenic amines
[25], or neuropeptides [26,27].
Current Opinion in Insect Science 2014, 3:1–9
Social insect collectives also exhibit variation in their
group behavioral traits, with three predominant modes
of variation: stable — inter-colony differences that remain
intact over the lifetime of the colony, developmental —
shifting over the course of colony maturation, and phasic — behaviors that vary over short timescales (Figure 1).
We will focus on stable group behavioral variation and
discuss rapid collective phasic transitions in a later
section. Social insect colonies exhibit stable variation
in aggressiveness, foraging choices, queen number
(reviewed in Refs. [1,2]). In many cases, these differences are due to genotypic differences, though the underlying genetic mechanisms have not always been
characterized. Pogonomyrmex barbatus colonies surveyed
over 30 years show heritable behavioral variation in their
foraging choices, with parent and offspring colonies
selecting similar days to forage in terms of the desiccation
threat vs. foraging pay-off [28]. In populations of Apis
mellifera honey bees selected for pollen versus nectar
foraging at the colony level, there are genomic differences
associated with the insulin signaling pathway [29,30]. A
bimodal colony-wide type of variation occurs in the fire
ant Solenopsis invicta, associated with a non-recombining
region encompassing the Gp-9 locus. Whether the
workers accept one or multiple queens in their colony
depends on which Gp-9 alleles are present in the workers
and in the queen [31,32] (Figure 2). Other physiological
traits are also linked with the Gp9 allele: monogyne forms
typically produce larger and more fecund queens, larger
workers, and more alates than do same-sized polygyne
colonies [33].
What is the effect of individual variation on the
social group?
In general, stable, genetic variability across individuals
plays a largely positive role in the performance and fitness
of social groups [4,5], likely through facilitation of
division of labor. Based on differing response thresholds
and spatial location, individuals segregate themselves
amongst different tasks [6,34,35,36,37], with increased
task specialization often leading to increased efficiency
[37,38,39,40]. However, an individual’s behavioral
tendencies can also alter the overall behavioral tendencies
of the group, though effects that can be variable and nonadditive, reflecting the interactions between the individual
and its nestmates.
The type of effect (linear vs. non-linear) that individual
variation has on the group’s behavioral tendencies
depends on the type of behavior, mode of communication
or information transfer, and responsiveness of the group
members (Figure 3). In simple stimulus-response behaviors, individual members shape the group’s behavior in
an additive, linear, manner; for example, several individuals encounter a stimulus (i.e., a corpse) but only a subset
of high-responding individuals responds to that stimulus
(and remove the corpse [41]). In such a case, for a given
www.sciencedirect.com
Please cite this article in press as: LeBoeuf AC, Grozinger CM: Me and we: the interplay between individual and group behavioral variation in social collectives, Curr Opin Insect Sci (2014), http://
dx.doi.org/10.1016/j.cois.2014.09.010
COIS-49; NO. OF PAGES 9
Individual-level and group-level behavioral variation LeBoeuf and Grozinger
3
(c)
% Time out of Nest
Ag
gr
es
siv
en
es
s
Stable Variation
colony A
colony B
Population Density
Age of Individual
small/young
colony
Phasic Variation:
Swarming Honey Bees
Host
Nest
% Time out of Nest
Developmental Variation
New
Nest
(d)
Bivouac
(b)
large/old
colony
Phasic Variation: Locusts
Solitary
(a)
Gregarious
Figure 1
Age of Individual
Population Density
Current Opinion in Insect Science
Schematics demonstrating modes of group-scale variation. (a) A colony can vary in the stable behavioral traits of its component members, here with
thicker lines indicating a larger number of colony members. Timescale: colony lifetime [1,29,70]. (b) Developmental variation can vary the strength of
division of labor over the lifetime of a colony: small colonies require workers to multi-task more, while large colonies can afford greater task
specialization. Timescale: Months to years [37,38,39,40]. (c) Rapid collective phasic transitions between different behavioral states in locusts. Solid
lines correspond to stable states, while dotted lines correspond to unstable transition states, with the gap between the dotted lines indicating the
extent of hysteresis [64]. (d) Rapid collective phasic transitions across stable states in swarming honey bees. Solid lines and point correspond to stable
states, while dotted lines correspond to unstable transition states. When a honey bee colony becomes large and dense (threshold density signified by
the dashed gray line), the honey bees swarm: a subset of the honey bees leave the home nest together, migrate to a temporary location, and form a
bivouac; when a new nest site has been decided upon (decision threshold not pictured in the schematic), the bivouac group then migrates en masse to
the new site. [43,66].
number of corpses, the rate of corpse removal should scale
with the number of low-response-threshold individuals in
the group. In cases of positive feedback loops where a
signal is amplified, such as recruitment, effects of individual variation on the group are by definition non-linear
[42]. The degree of response amplification in recruitment depends on the means of recruitment. Active
recruitment that alters the response thresholds of many
other individuals yields a highly non-linear effect. When a
honey bee recruits other bees to a new food resource with
a waggle dance, she changes the behavior of many others
simultaneously, who after visiting the resource themselves, may recruit more bees with their own waggle
dances [43]. Recruitment methods such as tandem running in ants, where a single ant recruits others one by one,
exert a more mildly non-linear effect on the colony [44].
Non-linear responses can also come about by passive
means through a process called stigmergy, where for
example, bystanders may simply join others that are engaging in a certain behavior [34,45]. Thus, in the absence of a
positive feedback loop, the group’s behavior should reflect
www.sciencedirect.com
the average behavior of the colony members, but if positive
feedback is used, the group’s behavior is predicted to be
driven by that of the most responsive member — which
could correspond to an individual occupying a keystone
role (Figure 3). Note, however, that colony-level behaviors
generally involve a combination of many individual-level
behaviors and are often brought about by different types of
positive and negative feedback.
There are several examples in which social groups of
individuals with mixed behavioral tendencies have been
created and the impacts on the groups’ behavioral
tendencies have been examined. The effect of the Gp-9
non-recombining region on polygyny and monogyny in
fire ants represents a non-linear effect (Figure 2): the
queen-acceptance behavior of an entire monogyne
Gp-9B/Gp-9B colony can be shifted from single-queen
acceptance to multiple-queen acceptance if only 5–10%
of the colony’s workers have the Gp-9b allele [32]. These
experiments suggest that this small proportion of workers
is actively influencing the behavior of the other 90% of
Current Opinion in Insect Science 2014, 3:1–9
Please cite this article in press as: LeBoeuf AC, Grozinger CM: Me and we: the interplay between individual and group behavioral variation in social collectives, Curr Opin Insect Sci (2014), http://
dx.doi.org/10.1016/j.cois.2014.09.010
COIS-49; NO. OF PAGES 9
4 Social Insects
Figure 2
workers
Gp-9B/Gp-9B
individual
threshold percentage for colony-wide behavioral change
proportion of Gp-9B/Gp-9b workers
Gp-9B/Gp-9b
individual
accepted
queen(s)
Monogyne
Monogyne
Polygyne
Polygyne
Gp-9B/Gp-9B
Gp-9B/Gp-9B
Gp-9B/Gp-9b
Gp-9B/Gp-9b
Current Opinion in Insect Science
Polygyny and monogyny in fire ants. Fire ants exhibit a colony level dimorphism controlled by a large non-recombining region encompassing the Gp-9
allele: when the colony is composed of only Gp-9B/Gp-9B (dark red) workers, they will accept only a single queen of their same genotype; if as few as
5% of the colony’s workers are of the Gp-9B/Gp-9b genotype (light red), the colony will accept multiple queens specifically of the Gp-9B/Gp-9b
genotype and will execute any queens with a Gp-9B/Gp-9B genotype [31,32,33,62]. Note that the Gp-9b/Gp-9b genotype is lethal.
workers likely through some highly propagated or volatile
signal. In social spiders, the foraging success of the group
corresponds to the foraging abilities of its most aggressive
members [46]. However, while a group’s ‘boldness’ (the
latency to investigate a possible prey item) correlates most
strongly to the behavior of the boldest individual, it also is
significantly correlated with the average boldness score
across the group [47]. Studies of honey bee colonies
consisting of a mix of defensive and gentle bees indicate
that the guards (which are arguably functioning as keystone
individuals) responded as rapidly as in defensive colonies,
but the number of bees subsequently recruited was intermediate between gentle and defensive colonies [48]. In
mixed colonies of docile European and more aggressive
Africanized honey bees, the Africanized guards attacked a
stimulus first, and subsequent responders were mixed
genotypes [49]. Thus, in this case, the group behavior
reflects both the response thresholds of keystone individuals and recruited individuals.
The signals produced by individuals to influence their
nestmates are regulated by genomic mechanisms, but
these have not been studied comprehensively. In honey
bees, pheromones strongly influence worker behavior,
and there is ample evidence that exposure to specific
pheromones can trigger gene expression changes
Current Opinion in Insect Science 2014, 3:1–9
corresponding to the associated behavioral changes in
recipient bees [16,50,51]. Few studies, however, have
examined which genes actually regulate the production
of pheromones in social insects. A recent study examining
the gene expression patterns in the pheromone-producing mandibular glands of honey bee queens, queenright
workers, queenless reproductive workers and queenless
sterile workers demonstrated that while caste differences
have the strongest influence on gene expression patterns,
social context had a significantly stronger effect than the
reproductive state [52]. Thus, the social context can
influence the expression of genes involved in the production of the social signals that create social context.
What is the effect of the group on the
individual’s behavior?
An individual’s behavior is clearly strongly influenced by
the social cues and signals (such as pheromones) it receives
from other members of its social group [1,53]. On a larger
scale, the overall behavioral tendencies of the group can
impact the behavior of the individual. For example, in
honey bee colonies of 50% mixed aggressive Africanized
and 50% docile European bees, Africanized bees were
more likely to guard than European bees, but there was
no difference in guarding behavior between these two
genotypes in colonies of 25% Africanized, 75% European
www.sciencedirect.com
Please cite this article in press as: LeBoeuf AC, Grozinger CM: Me and we: the interplay between individual and group behavioral variation in social collectives, Curr Opin Insect Sci (2014), http://
dx.doi.org/10.1016/j.cois.2014.09.010
COIS-49; NO. OF PAGES 9
Individual-level and group-level behavioral variation LeBoeuf and Grozinger
5
Figure 3
(a)
Linear
Non-Linear
(b) Linear Effect
CORPSE
Individual
Variation
undertaking
behavior
Non-linear Effect
recruitment
Colony
Phenotype
without interaction,
average personality dominates
foraging
behavior
with interaction, extreme
personalities can dominate
Current Opinion in Insect Science
The effect of individual variation on colony behavioral tendencies. Individual variation can alter the group phenotype either linearly or non-linearly
(a). When the colony behavioral phenotype is an average of the component individual behavioral phenotypes, the mechanism can be assumed to be
linear. Alternately, when the colony behavioral phenotype reflects the most extreme individual(s), the mechanism is likely to be non-linear. This linearity
or non-linearity comes about through the strength and dynamics of the interactions between individuals in the group (b). Namely, when a positivefeedback loop is employed to recruit or amplify a response, more extreme individuals who initiate these responses will have a disproportionately large
effect on the group. Note, however, that colony-level behaviors may reflect a combination of linear and non-linear behaviors.
bees [54]. In cross-fostering experiments with anarchistic
honey bee workers (which activate their ovaries even in
the presence of a queen and brood) and wild-type
workers, anarchistic bees always activated their ovaries
more readily than wild-type workers under any condition, but both types of bees were more likely to activate
their ovaries when housed in an anarchistic colony,
suggesting reduced production of queen and brood
pheromones (which typically inhibit worker reproduction [55]) in anarchistic colonies [56]. In many cases, it is
possible that the behavior of the individual simply
reflects its response thresholds in the context of the
group: for example, a moderately aggressive individual
in the presence of highly aggressive individuals may not
exhibit aggression.
However, several recent studies suggest that the effect of
the social group can go beyond simply ranking individuals
according to their response thresholds. When honey bees
from genotypes displaying low levels of hygienic behavior
(removal of diseased larvae) were caged with bees displaying high levels of hygienic behavior, the low-line bees
actually increased their hygienic activity [57]. This
increased task performance did not appear to be due to
recruitment by the high-line bees, but rather to a more
general effect of the social context. Studies of fanning
behavior in small groups of caged honey bees demonstrated that group size strongly influenced the likelihood
that individual bees would fan (a greater percentage of
bees fan in larger groups) as well as the temperature
threshold at which fanning would be initiated (larger
groups fan at lower thresholds) [58]. Group size also
www.sciencedirect.com
influences information flow through colonies: larger colonies of honey bees with intact dance language were more
efficient at recruiting foragers to new food resources
than smaller colonies [59]. Thus, individual response
thresholds and information flow, both of which shape
group behavior, can change with group size and likely
with other components of group dynamics (for review of
effects of group size see Ref. [60]).
A number of studies on global gene expression patterns
across many social insect species have demonstrated
that social environment often has a greater impact on
global gene expression than an individual’s own reproductive state (in fire ants [61,62], papers wasps [17],
bumble bees [63] and honey bees [52]). Furthermore, in
the case of paired fire ant foundresses which formed
hierarchies with a dominant and subordinate foundress,
switching the dominance rank by switching partners had a
greater impact on gene expression patterns than the rank
itself [61]. In the case of the Gp-9 non-recombining
region in fire ants (Figure 2), when comparing workers
of the same genotype, Gp-9B/Gp-9B, in either the social
context of monogyne colonies (with Gp-9B/Gp-9B queens
and workers) or polygyne colonies (which contain both
Gp-9B/Gp-9b and Gp-9B/Gp-9B workers and multiple
Gp-9B/Gp-9b queens), worker gene expression profiles
reveal a greater effect of the colony’s behavioral phenotype than of the worker’s own genotype [62]. Thus,
genomic expression patterns can represent a sensitive
bioassay for the effects of social context, but the function
of these expression differences and the cues that regulate
them remain to be determined.
Current Opinion in Insect Science 2014, 3:1–9
Please cite this article in press as: LeBoeuf AC, Grozinger CM: Me and we: the interplay between individual and group behavioral variation in social collectives, Curr Opin Insect Sci (2014), http://
dx.doi.org/10.1016/j.cois.2014.09.010
COIS-49; NO. OF PAGES 9
6 Social Insects
The role of individual variation in rapid
collective phasic transitions
Social insect colonies can also exhibit rapid collective
phasic transitions during their lifecycle. In these behaviors, multiple individuals, regardless of their current
activities, are induced to perform a coordinated behavior,
such locusts transitioning from solitary to gregarious
phase [64], ants engaging in mating flights [65], as well
as reproductive colony fission and colony migration in ant,
bee and wasp species [9,10,65,66]. For example, when
honey bee colonies undergo reproductive fission —
‘swarming’ (reviewed in Refs. [43,66]) — thousands of
bees forego their normal behavioral diversity and transition through a series of stereotyped behaviors: exodus of
the swarm from the mother colony, temporary relocation
to a bivouac while scouts search for a new nest site, lift off
of the swarm and finally migration to the new nest site to
establish the new colony. These unified transitions
through a specific series of stereotyped behaviors are
analogous to a dynamical system transitioning through
stable fixed points (Figure 1d).
As in other social behaviors, rapid collective phasic transitions can be brought about by active signaling from
keystone individuals, as in swarming in honey bees
[43,66] or colony migration in some ants [9]. In the
case of honey bees, when colony exodus or swarm liftoff
is imminent, a small subset of individuals (the scouts,
representing 5% of the swarm) use vibration signals,
piping, and/or buzz-running to activate the other individuals in the group and trigger swarm movement. These
scouts also search for and select the new nest site, and
lead the airborne swarm to the new nest by performing
‘streaking’ behavior, in which they fly rapidly in the
direction of the new nest. Thus, a small handful of keystone individuals are responsible for directing the swarm’s
behavior and movement. Interestingly, the same bees that
serve as scouts during swarming serve as scouts for new
foraging resources in established colonies, and thus common genomic and neurophysiological processes likely
drive these behaviors [24]. It is unknown if there is differentiation among the non-scout bees in the swarm: typically,
the young bees in the colony join the swarm and thus they
are likely not particularly variable since they are in the very
early stages of behavioral maturation, but there does
appear to be genetic variation in the likelihood to join a
swarm (reviewed in Ref. [66]). In Temnothorax ants, a group
of individuals initiate scouting and evaluation of new nests,
and then recruit others through tandem running. The
scouts and recruits then physically carry the remaining
ants to the new nest site. Thus, the recruits may exhibit
a phasic transition in their behavioral state, but the
individuals who are simply carried to the new site likely
do not experience any behavioral change. Interestingly,
among the primary scouts there can be significant variation
in their effectiveness to find nest sites and recruit others
to those sites, due to their previous experiences [67].
Current Opinion in Insect Science 2014, 3:1–9
Rapid collective phasic transitions can also be brought
about passively, through an integration of group status by
each individual, which in turn translates to behavioral
change. Colony fission in both honey bees [43,66] and in
Temnothorax ants [68] is correlated with a threshold innest density, a passive measure. In honey bees, increasing
population size and density is thought to limit the distribution of queen pheromones throughout the colony,
triggering the production of new queen rearing which
is the earliest indicator that a colony is preparing to swarm
[43,66]. Within-nest population density in Temnothorax
ants is correlated with polydomy, such that ant colonies
undergoes fission and separate into multiple nests when
population density inside the nest is high [68]. In locusts,
an increase in population density promotes the individual
to transition from the solitary to the gregarious phase [64].
Increasing population density leads to changes in levels of
microRNA-133 in the brain of individual locusts [69].
This microRNA triggers changes in expression of various
genes involved in the dopamine synthesis pathway,
resulting in the dramatic behavioral, physiological, and
morphological changes associated with this behavioral
phase change [64,69]. Shifts between these two phases
are even accompanied by hysteresis (Figure 1c), such that
population densities that triggered the shift to gregarious
phase needed to be greatly reduced to initiate the transition back to solitary phase [64].
Rapid collective phasic transitions represent a special
type of social behavior, in which the group social behavior
temporarily overrides the variation present in individuals,
and thus provides a fascinating system in which to
examine the interplay between individual and grouplevel behavioral variation. For example, unlike stable
social groups, there is low behavioral variation amongst
individuals engaging in these phasic transitions. In these
cases, behavioral diversity might negatively affect group
function, though this remains to be tested. The individuals participating in a rapid collective phasic transition
appear to enter a common behavioral state, suggesting
that pre-existing preferences and tendencies may be
erased, and it is unclear if and how these re-emerge after
the phasic transition is completed, and how this process is
regulated at the genomic and neurophysiological level.
Finally, it remains to be determined what mechanisms
allow the keystone individuals (i.e., the scout bees) to
remain immune to the effects of the social group and able
to maintain their own distinct behavioral repertoires.
Conclusion
Social insects exhibit considerable inter-individual and
inter-colonial variation in behavior, as well as behavioral
shifts that take place over different timescales in both
the individual-scale and colony-scale. Furthermore, the
behavioral tendencies of the individual influence the
tendencies of the group, and vice versa (‘me’ affects
‘we’ and ‘we’ affects ‘me’). However, the relative strength
www.sciencedirect.com
Please cite this article in press as: LeBoeuf AC, Grozinger CM: Me and we: the interplay between individual and group behavioral variation in social collectives, Curr Opin Insect Sci (2014), http://
dx.doi.org/10.1016/j.cois.2014.09.010
COIS-49; NO. OF PAGES 9
Individual-level and group-level behavioral variation LeBoeuf and Grozinger
of these effects has not been broadly considered (for
example, to what extent can the group override the
tendencies of the individual? To what extent are group
behaviors the result of additive or synergistic interactions
among individual group members?). Just as network
motifs such as feedback loops have been extremely helpful in the understanding of genetic and neural circuits
[42], these structures can also inform our experimental
approaches to social networks, where qualitatively different behaviors emerge based on the strength and dynamics
of the component social interactions. While there has
been ample research on the proximate mechanisms mediating individual variation, we have less information about
the genes that underpin the production of social signals
which in turn influence group dynamics, and the genes
that are responsive to social context. Finally, studying the
interactions between the individual and the group during
rapid collective phasic transitions may be particularly
informative. As in stable groups, individuals can influence
the group’s behavior through active or passive mechanisms, but because these individuals will eventually perform the same behavior, the resultant changes are quite
dramatic. While the majority of the studies examining the
interplay between individual and group behavioral
tendencies have used stable groups, social groups themselves are dynamic: the role that individual variation plays
in the functioning of the group under diverse social and
environment conditions is an open area for investigation.
Acknowledgements
We would like to thank Clare Rittschof, Pavan Ramdya, Nathalie
Stroeymeyt and Laurent Keller for helpful discussion and comments on the
manuscript. This work was supported by an NSF-CAREER grant to CMG,
and ACL is supported by the University of Lausanne, the Swiss National
Science Foundation, ERC Starting Independent Grant to Richard Benton
and an ERC Advanced Grant to Laurent Keller.
References
1.
Jandt JM, Bengston S, Pinter-Wollman N, Pruitt JN, Raine NE,
Dornhaus A, Sih A: Behavioural syndromes and social insects:
personality at multiple levels. Biol Rev Camb Philos Soc 2014,
89:48-67.
A comprehensive review of the application of ‘behavioral syndromes and
personalities’ to study of social insects.
2.
Jeanson R, Weidenmüller A: Interindividual variability in social
insects — proximate causes and ultimate consequences. Biol
Rev 2013.
A comprehensive review of the proximate factors regulating individual
behavioral variation in social insects and effects of this variation on social
groups.
3.
Detrain C, Deneubourg JL: Self-organized structures in a
superorganism: do ants ‘behave’ like molecules? Phys Life Rev
2006, 3:162-187.
4.
Mattila HR, Seeley TD: Genetic diversity in honey bee colonies
enhances productivity and fitness. Science 2007, 317:362-364.
5.
Modlmeier AP, Liebmann JE, Foitzik S: Diverse societies are
more productive: a lesson from ants. Proc Biol Sci 2012,
279:2142-2150.
This paper provides further evidence that increased behavioral variation
among individual workers leads to improved colony performance. While
previous studies in honey bees manipulated genetic diversity (e.g.,
inseminated the queen with semen from one versus ten males) in order
www.sciencedirect.com
7
to manipulate behavioral variation within the colony, this study used
naturally occurring colonies of Temnothorax longispinosus ants and
quantified behavioral variation among individuals and correlated this
parameter to colony level traits.
6.
Oldroyd BP, Fewell JH: Genetic diversity promotes
homeostasis in insect colonies. Trends Ecol Evol 2007,
22:408-413.
7.
Evans LJ, Raine NE: Changes in learning and foraging
behaviour within developing bumble bee (Bombus terrestris)
colonies. PLOS ONE 2014:9.
This manuscript explores how the foraging strategies of individual colony
members change during colony growth and maturation.
8.
Sumpter DJT: The principles of collective animal behaviour.
Philos Trans R Soc B Biol Sci 2006, 361:5-22.
9.
Visscher PK: Group decision making in nest-site selection
among social insects. Annu Rev Entomol 2007, 52:255-275.
10. McGlynn TP: The ecology of nest movement in social insects.
Annu Rev Entomol 2012, 57:291-308.
11. Scheiner R, Page RE, Erber J: Review article Sucrose
responsiveness and behavioral plasticity in honey bees
(Apis mellifera). Apidologie 2004, 35:133-142.
12. Arenas A, Giurfa M, Sandoz JC, Hourcade B, Devaud JM,
Farina WM: Early olfactory experience induces structural
changes in the primary olfactory center of an insect brain. Eur J
Neurosci 2012, 35:682-690.
13. Hoover SER, Winston ML, Oldroyd BP: Retinue attraction and
ovary activation: responses of wild type and anarchistic honey
bees (Apis mellifera) to queen and brood pheromones. Behav
Ecol Sociobiol 2005, 59:278-284.
14. Pankiw T: Queen rearing by high and low queen mandibular
pheromone responding worker honey bees (Apis mellifera L.).
Can Entomol 1997, 129:679-690.
15. Kocher SD, Ayroles JF, Stone EA, Grozinger CM: Individual
variation in pheromone response correlates with reproductive
traits and brain gene expression in worker honey bees. PLoS
ONE 2010, 5:e9116.
16. Alaux C, Sinha S, Hasadsri L, Hunt GJ, Guzmán-Novoa E,
DeGrandi-Hoffman G, Uribe-Rubio JL, Southey BR, RodriguezZas S, Robinson GE: Honey bee aggression supports a link
between gene regulation and behavioral evolution. Proc Natl
Acad Sci U S A 2009, 106:15400-15405.
17. Toth AL, Tooker JF, Radhakrishnan S, Minard R, Henshaw MT,
Grozinger CM: Shared genes related to aggression, rather than
chemical communication, are associated with reproductive
dominance in paper wasps (Polistes metricus). BMC Genomics
2014, 15:75.
In a genome-wide analysis of gene expression patterns in paper wasps,
the authors demonstrate that environment (either season or group composition) is a greater contributor to brain gene expression patterns than
caste or physiological state, indicating that environmental factors can
potentially override individual variation.
18. Modlmeier AP, Keiser CN, Watters JV, Sih A, Pruitt JN: The
keystone individual concept: an ecological and evolutionary
overview. Anim Behav 2014, 89:53-62.
Comprehensive and clarifying review on the keystone individual concept.
19. Tenczar P, Lutz CC, Rao VD, Goldenfeld N, Robinson GE:
Automated monitoring reveals extreme interindividual
variation and plasticity in honeybee foraging activity levels.
Anim Behav 2014, 95:41-48.
20. Ferreira PG, Patalano S, Chauhan R, Ffrench-Constant R,
Gabaldón T, Guigó R, Sumner S, Gabaldon T, Guigo R:
Transcriptome analyses of primitively eusocial wasps
reveal novel insights into the evolution of sociality and
the origin of alternative phenotypes. Genome Biol 2013,
14:R20.
21. Grozinger CM, Fan Y, Hoover SER, Winston ML: Genome-wide
analysis reveals differences in brain gene expression patterns
associated with caste and reproductive status in honey bees
(Apis mellifera). Mol Ecol 2007, 16:4837-4848.
Current Opinion in Insect Science 2014, 3:1–9
Please cite this article in press as: LeBoeuf AC, Grozinger CM: Me and we: the interplay between individual and group behavioral variation in social collectives, Curr Opin Insect Sci (2014), http://
dx.doi.org/10.1016/j.cois.2014.09.010
COIS-49; NO. OF PAGES 9
8 Social Insects
22. Gräff J, Jemielity S, Parker JD, Parker KM, Keller L: Differential
gene expression between adult queens and workers in the ant
Lasius niger. Mol Ecol 2007, 16:675-683.
40. Holbrook CT, Barden PM, Fewell JH: Division of labor increases
with colony size in the harvester ant Pogonomyrmex
californicus. Behav Ecol 2011, 22:960-966.
23. Bonasio R, Li Q, Lian J, Mutti NS, Jin L, Zhao H, Zhang P, Wen P,
Xiang H, Ding Y et al.: Genome-wide and caste-specific DNA
methylomes of the ants camponotus floridanus and
harpegnathos saltator. Curr Biol 2012, 22:1755-1764.
41. Sun Q, Zhou X: Corpse management in social insects. Int J Biol
Sci 2013, 9:313-321.
24. Liang ZS, Nguyen T, Mattila HR, Rodriguez-Zas SL, Seeley TD,
Robinson GE: Molecular determinants of scouting behavior in
honey bees. Science 2012, 335:1225-1228.
25. Muscedere ML, Johnson N, Gillis BC, Kamhi JF, Traniello JF:
Serotonin modulates worker responsiveness to trail
pheromone in the ant Pheidole dentata. J Comp Physiol A
Neuroethol Sens Neural Behav Physiol 2012, 198:219-227.
26. Brockmann A, Annangudi SP, Richmond TA, Ament SA, Xie F,
Southey BR, Rodriguez-Zas SR, Robinson GE, Sweedler JV:
Quantitative peptidomics reveal brain peptide signatures of
behavior. Proc Natl Acad Sci U S A 2009, 106:2383-2388.
27. Galizia CG, Kreissl S: Honeybee neurobiology and behavior. In
Honeybee neurobiology and behavior. Edited by Galizia CG,
Eisenhardt D, Giurfa M. Netherlands: Springer; 2012:211-226.
28. Gordon DM: The rewards of restraint in the collective
regulation of foraging by harvester ant colonies. Nature 2013,
498:91-93.
29. Page RE, Rueppell O, Amdam GV: Genetics of reproduction and
regulation of honeybee (Apis mellifera L.) social behavior.
Annu Rev Genet 2012, 46:97-119.
Provides excellent overview of the mechanisms regulating worker foraging strategies in honey bees and how these shape colony-level traits.
Furthermore, the review highlights the role of common mechanisms
underlying behavioral variation across multiple timescales.
30. Linksvayer TA, Fondrk MK, Page RE: Honeybee social regulatory
networks are shaped by colony-level selection. Am Nat 2009,
173:E99-E107.
31. Wang J, Wurm Y, Nipitwattanaphon M, Riba-Grognuz O, Huang Y
C, Shoemaker D, Keller L: A Y-like social chromosome causes
alternative colony organization in fire ants. Nature 2013,
493:664-668.
The authors describe the large genetic polymorphism underlying a major
difference in fire ant colony phenotype. It is worth considering what other
colony-wide differences might have such a genetic element underpinning
them.
32. Ross KG, Keller L: Experimental conversion of colony social
organization by manipulation of worker genotype composition
in fire ants (Solenopsis invicta). Behav Ecol Sociobiol 2002,
51:287-295.
33. Ross K, Keller L: Ecology and evolution of social organization:
insights from fire ants and other highly eusocial insects. Annu
Rev Ecol Syst 1995, 26:631-656.
34. Richardson TO, Christensen K, Franks NR, Jensen HJ, SendovaFranks AB: Ants in a labyrinth: a statistical mechanics
approach to the division of labour. PLoS ONE 2011, 6:e18416.
35. Mersch DP, Crespi A, Keller L: Tracking individuals shows
spatial fidelity is a key regulator of ant social organization.
Science 2013, 340:1090-1093.
36. Sendova-Franks AB, Hayward RK, Wulf B, Klimek T, James R,
Planqué R, Britton NF, Franks NR: Emergency networking:
famine relief in ant colonies. Anim Behav 2010, 79:473-485.
37. Goldsby HJ, Dornhaus A, Kerr B, Ofria C: Task-switching costs
promote the evolution of division of labor and shifts in
individuality. Proc Natl Acad Sci U S A 2012, 109:13686-13691.
A computational modeling and in silico evolution approach to determining
the costs of task switching in division of labor.
38. Jeanson R, Fewell JH, Gorelick R, Bertram SM: Emergence of
increased division of labor as a function of group size. Behav
Ecol Sociobiol 2007, 62:289-298.
39. Flanagan TP, Letendre K, Burnside WR, Fricke GM, Moses ME:
Quantifying the effect of colony size and food distribution on
harvester. Ant Foraging 2012, 7:1-9.
Current Opinion in Insect Science 2014, 3:1–9
42. Alon U: An introduction to systems biology: design principles of
biological circuits. 2007.
An excellent introduction to biological circuit and network analysis.
43. Seeley TD: Honeybee democracy. Princeton University Press;
2010.
44. Shaffer Z, Sasaki T, Pratt SC: Linear recruitment leads to
allocation and flexibility in collective foraging by ants. Anim
Behav 2013, 86:967-975.
This study combines theory and experiment to analyze different types of
positive feedback through recruitment.
45. Arganda S, Pérez-Escudero A, de Polavieja GG: A common rule
for decision making in animal collectives across species. Proc
Natl Acad Sci U S A 2012, 109:20508-20513.
A modeling study working with decision-making data from a range of
biological organisms.
46. Pruitt JN, Riechert SE: How within-group behavioural variation
and task efficiency enhance fitness in a social group. Proc Biol
Sci 2011, 278:1209-1215.
47. Pruitt JN, Grinsted L, Settepani V: Linking levels of personality:
personalities of the ‘average’ and ‘most extreme’ group
members predict colony-level personality. Anim Behav 2013,
86:391-399.
This study demonstrates how the personality traits of the individuals
shape the personality of the group, and specifically examines the relative
effects of extreme vs average individuals.
48. Paleolog J: Behavioural characteristics of honey bee
(Apis mellifera) colonies containing mix of workers of
divergent behavioural traits. Anim Sci Pap Rep 2009,
27:237-248.
49. Guzman-Novoa et al.: Genotypic effects of honey bee (Apis
mellifera) defensive behavior at the individual and colony
levels: the relationship of guarding, pursuing and stinging.
Apidologie 2004, 35:15-24.
50. Grozinger CM, Sharabash NM, Whitfield CW, Robinson GE:
Pheromone-mediated gene expression in the honey bee brain.
Proc Natl Acad Sci U S A 2003, 100 Suppl.:14519-14525.
51. Alaux C, Le Conte Y, Adams HA, Rodriguez-Zas S, Grozinger CM,
Sinha S, Robinson GE: Regulation of brain gene expression in
honey bees by brood pheromone. Genes Brain Behav 2009,
8:309-319.
52. Malka O, Niño EL, Grozinger CM, Hefetz A: Genomic analysis of
the interactions between social environment and social
communication systems in honey bees (Apis mellifera). Insect
Biochem Mol Biol 2014, 47:36-45.
This analysis of global gene expression patterns in pheromone-producing
glands in honey bees which demonstrate that social status (presence of
absence of a queen) plays a much greater role in regulating gene
expression patterns than ovary activation state, indicating that environmental factors can potentially override individual variation.
53. Janis I: Victims of groupthink: a psychological study of foreignpolicy decisions and fiascoes. Mifflin: Houghton; 1972, .
54. Hunt GJ, Guzmán-Novoa E, Uribe-Rubio JL, Prieto-Merlos D:
Genotype–environment interactions in honeybee guarding
behaviour. Anim Behav 2003, 66:459-467.
55. Le Conte Y, Hefetz A: Primer pheromones in social
hymenoptera. Annu Rev Entomol 2008, 53:523-542.
56. Barron AB, Oldroyd BP: Social regulation of ovary activation in
‘anarchistic’ honey-bees (Apis mellifera). Behav Ecol Sociobiol
2001, 49:214-219.
57. Gempe T, Stach S, Bienefeld K, Beye M: Mixing of honeybees
with different genotypes affects individual worker behavior
and transcription of genes in the neuronal substrate. PLoS
ONE 2012:7.
www.sciencedirect.com
Please cite this article in press as: LeBoeuf AC, Grozinger CM: Me and we: the interplay between individual and group behavioral variation in social collectives, Curr Opin Insect Sci (2014), http://
dx.doi.org/10.1016/j.cois.2014.09.010
COIS-49; NO. OF PAGES 9
Individual-level and group-level behavioral variation LeBoeuf and Grozinger
58. Cook CN, Breed MD: Social context influences the initiation
and threshold of thermoregulatory behaviour in honeybees.
Anim Behav 2013, 86:323-329.
59. Donaldson-Matasci MC, DeGrandi-Hoffman G, Dornhaus A:
Bigger is better: honeybee colonies as distributed
information-gathering systems. Anim Behav 2013, 85:585-592.
60. Dornhaus A, Powell S, Bengston S: Group size and its effects on
collective organization. Annu Rev Entomol 2012, 57:123-141.
61. Manfredini F, Riba-Grognuz O, Wurm Y, Keller L, Shoemaker D,
Grozinger CM: Sociogenomics of cooperation and conflict
during colony founding in the fire ant Solenopsis invicta. PLOS
Genet 2013, 9:e1003633.
This study examined global gene expression patterns in ant queens which
founded colonies either individually or in pairs. Expression patterns were
regulated primarily by social context (e.g., queens founding singly versus
with a co-foundress, or co-foundresses that switched versus maintained
dominance rank) than an individual’s own social rank/reproductive status.
62. Wang J, Ross KG, Keller L: Genome-wide expression patterns
and the genetic architecture of a fundamental social trait.
PLoS Genet 2008:4.
63. Amsalem E, Malka O, Grozinger C, Hefetz A: Exploring the role of
juvenile hormone and vitellogenin in reproduction and social
behavior in bumble bees. BMC Evol Biol 2014, 14:45.
This study demonstrated that expression levels of an egg-yolk protein,
vitellogenin, are regulated by social interactions rather than an individual’s
ovary activation levels, demonstating that social factors can potentially
override individual variation arising from physiological differences, and
the function of vitellogenin may have been co-opted during the evolution
of sociality.
www.sciencedirect.com
9
64. Guttal V, Romanczuk P, Simpson SJ, Sword GA, Couzin ID:
Cannibalism can drive the evolution of behavioural
phase polyphenism in locusts. Ecol Lett 2012,
15:1158-1166.
65. Peeters C, Ito F: Colony dispersal and the evolution of queen
morphology in social Hymenoptera. Annu Rev Entomol 2001,
46:601-630.
66. Grozinger CM, Richards J, Mattila HR:: From molecules
to societies: mechanisms regulating swarming
behavior in honey bees (Apis spp.). Apidologie 2013,
45:327-346.
67. Stroeymeyt N, Franks NR, Giurfa M:: Knowledgeable
individuals lead collective decisions in ants. J Exp Biol 2011,
214:3046-3054.
68. Cao TT: High social density increases foraging and scouting
rates and induces polydomy in Temnothorax ants. Behav Ecol
Sociobiol 2013, 67:1799-1807.
69. Yang M, Wei Y, Jiang F, Wang Y, Guo X, He J, Kang L:
MicroRNA-133 inhibits behavioral aggregation by
controlling dopamine synthesis in locusts.
PLoS Genet 2014, 10:e1004206.
Excellent study elucidating a causal factor in how locusts detect population density changes and then enact the physiological and morphological
changes associated with the shift to gregarious phase.
70. Scharf I, Modlmeier AP, Fries S, Tirard C, Foitzik S: Characterizing
the collective personality of ant societies: aggressive colonies
do not abandon their home. PLoS ONE 2012, 7:e33314.
Current Opinion in Insect Science 2014, 3:1–9
Please cite this article in press as: LeBoeuf AC, Grozinger CM: Me and we: the interplay between individual and group behavioral variation in social collectives, Curr Opin Insect Sci (2014), http://
dx.doi.org/10.1016/j.cois.2014.09.010