Leading Edge

Review

Ecology and Evolution

of Communication in Social Insects
Sara Diana Leonhardt,1,4 Florian Menzel,2,4 Volker Nehring,3,4 and Thomas Schmitt1,*
1Department of Animal Ecology and Tropical Biology, University of Würzburg, 97074 Würzburg, Germany
2Evolutionary Biology, Institute of Zoology, University of Mainz, 55128 Mainz, Germany
3Department of Evolutionary Biology and Animal Ecology, University of Freiburg, 79104 Freiburg, Germany
4Co-first authors

*Correspondence: thomas.schmitt@uni-wuerzburg.de
http://dx.doi.org/10.1016/j.cell.2016.01.035

Insect life strategies comprise all levels of sociality from solitary to eusocial, in which individuals
form persistent groups and divide labor. With increasing social complexity, the need to communi-
cate a greater diversity of messages arose to coordinate division of labor, group cohesion, and
concerted actions. Here we summarize the knowledge on prominent messages in social insects
that inform about reproduction, group membership, resource locations, and threats and discuss
potential evolutionary trajectories of each message in the context of social complexity.

Introduction uals start to detect substances emitted by other individuals. At

Communication in social insects has fascinated scientists for
centuries. One of the most famous examples is the dance lan-
guage of honeybees. Karl von Frisch showed that honeybees
dance in order to inform their nestmates about the location of
resources (von Frisch, 1967), a breakthrough for which he was
granted the Nobel Prize in 1973. Since then, our understanding
of the topics and mechanisms of communication in social in-
sects has significantly advanced for a wide variety of species.
Insects show all levels of social organization, from solitary spe-
cies where conspecific individuals rarely meet to eusocial spe-
cies with large, persistent colonies, where groups of individuals
(‘‘castes’’) perform different tasks (division of labor). The evolu-
tion of sociality in insects can be compared by analogy to other
major evolutionary transitions, such as the evolution of multicel-
lularity. For example, the division of labor in eusocial insects re-
sembles the diversification of cells that take over specific tasks in
a multicellular organism. Just as somatic cells are disposable
and reproduction is restricted to germline cells, there is division
of labor between social insect workers and royals (Boomsma,
2013). And just like separate organs communicate using hor-
mones, individuals in insect societies use pheromones as mes-
sengers. The diversity of information, i.e., the number of different
messages that become encoded by signals, increases with the
complexity of social organization.
In this Review, we give an overview of the current knowledge
on intraspecific communication in social insects, defined as the
transfer between individuals of information that is either mutually
beneficial or beneficial for one and neutral for the other partici-
pant. We provide insights into the evolution of the messages
used by social insects and discuss how their diversity increased
with the evolution of social complexity.
Evolution of Communication with Sociality
The oldest mode of communication is the transfer of chemicals
(Wyatt, 2014). Chemical communication evolves when individ-
that stage the chemicals effectively become ’’cues.’’ Cues are
informative traits of individuals that are unintentionally presented
by an emitter and used by a receiver to infer information about
the emitter (Figure 1). When receivers respond and emitters
benefit from the receivers’ responses, emitters evolve more
sophisticated and reliable ‘‘signals,’’ i.e., co-evolved traits in-
tended to transfer information; this is defined as ‘‘true com-
munication’’ (Figure 1) (Dusenbery, 1992). However, information
provided by a sender can also be aimed at manipulating the
receiver to its disadvantage (e.g., predators attracting prey by
mimicking prey signals) or be exploited by a second receiver to
the sender’s disadvantage (e.g., by parasites to locate hosts)
(Steiger et al., 2011), rendering a precise definition of communi-
cation elusive.
Subsequently, in the animal kingdom signaling modes beyond
chemicals evolved, including acoustic/vibrational, visual, and
tactile communication. In insects, chemical cues and signals
(pheromones) still dominate, although all other modes of
communication occur (Bradbury and Vehrencamp, 2011; Wyatt,
2014) (Figure 2).
Both solitary and social insects communicate. In strictly
solitary insects, communication is largely restricted to sexual
context and involves signals that attract and inform mating part-
ners, frequently with a multitude of signals transferred between
mating partners during courtship. The most prominent and wide-
spread examples for such signals are sex pheromones (single
substances or blends of chemicals) (Wyatt, 2014), which are
largely species and sex specific to ensure mating with an appro-
priate partner. Sexual signals can also be visual, acoustic/vibra-
tional, or tactile or involve multiple communication modes, e.g.,
chemical and tactile/visual signals such as those used for mating
in Drosophila melanogaster (Bontonou and Wicker-Thomas,
2014). Mating signals can also bear information on kinship so in-
dividuals can recognize each other’s relatedness and avoid
inbreeding (Lihoreau et al., 2007).

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Figure 1. Proposed Stages in the Evolution of Chemical Communi-
cation in Insects
Ancestrally, chemicals are unintentionally emitted by an individual (emitter)
and not detected by any other individual. If another individual (receiver) evolves
the capability to perceive the unintentionally emitted chemical and benefits
from the transferred information, the chemical becomes a cue. If there is
additional advantage to the emitter from receiving reciprocal information, the
emitter becomes a sender and the cue a signal, and this can be considered
‘‘true communication.’’ Adapted from Wyatt (2014), with image by Ivan Hino-
josa (www.flickr.com/photos/ivan_hinojosa).
As insects evolved higher levels of sociality, the information
they needed to exchange between group members diversified
to include division of labor, collaborative resource utilization,
and collective defensive actions (Figures 3 and 4). This trend is
reflected in the diversity of chemical signals required to maintain
eusocial insect colonies (Box 1). However, it is important to note
that increased message diversity does not necessarily correlate
with increased complexity of the signals themselves (Kather and
Martin 2015). Indeed, signals used in solitary insects are in some
cases more complex in terms of composition than some signals
used in social insects, and pheromone signals in social insects
most likely evolved from systems regulating more basal behav-
iors in solitary insects (Blum, 1969) (Figure 5). For example,
although kin recognition is important for solitary insects to
avoid inbreeding, in insects with brood-care, kin recognition is
expected to play an even more important role to prevent parents
from feeding or protecting someone else’s offspring. However,
kin recognition has rarely been shown (Linsenmair, 1987).
Instead, most species seem to employ rules of thumb whenever
simpler cues suffice. Illustrating this point, parents of the subso-
cial burying beetle Nicrophorus vespilloides (Figure 4A) cannot
discriminate between their own and artificially introduced larvae
1278 Cell 164, March 10, 2016 ª2016 Elsevier Inc.
but accept all brood that is of the right age (calculated from time
of egg laying) (Steiger, 2015).
Signals such as aggregation pheromones that help individuals
to find each other, dispersion pheromones that disassemble
groups (Heifetz et al., 1998), alarm signals, and recruitment
signals that guide group members to resources are important
tools for supporting insect societies. Group gathering can be
accomplished by species-specific long-range aggregation pher-
omones that attract both sexes of a species (Figure 4B). Here,
the most prominent and best studied examples are insect pest
species, e.g., gregarious bark beetles, which use species-spe-
cific aggregation pheromones to overcome a tree’s defense in
a concerted action (Byers, 1989).
In the most derived insect societies, reproduction is monopo-
lized by one (or few) individual(s) (‘‘queens’’/’’kings’’), whereas
the others (‘‘workers’’) perform foraging, nest maintenance,
and nursing duties (eusociality; Figure 4D).
Below we highlight four types of messages typically used in
eusocial insect colonies: queen signals (which organize repro-
ductive division of labor), nestmate recognition (which ensures
group cohesion), recruitment, and alarm signals (both of which
organize concerted group actions). We discuss evolutionary
trajectories of each message in the context of social complexity
and finally suggest future directions to better understand the
evolution of communication in insect societies.
Queen Signaling
Signals produced by queens in eusocial colonies indicate the
queen’s presence and/or fertility to workers who then abandon
their own reproduction and help with rearing siblings (Keller
and Nonacs, 1993) (Figure 4D). Workers can further use this in-
formation to control each other’s reproduction by for instance
destroying eggs laid by other workers (egg policing: Ratnieks,
1988; Ratnieks and Reeve, 1992). When a colony loses its queen
or the queen loses fertility, the queen signal diminishes and non-
sterile workers can start laying eggs themselves (Keller and Non-
acs, 1993). Consequently, communicating the presence and
fertility of a queen reinforces reproductive division of labor and
benefits the social organization within colonies.
Signals Used
In species with small colonies (<100 individuals), queen signals
can comprise aggressive queen-worker interactions and even vi-
sual signals in addition to chemical signals (Tannure-Nascimento
et al., 2008). In contrast, large colonies (several 100 individuals)
typically rely entirely on chemical signals, the so-called queen
pheromones (Hölldobler and Wilson, 1990; Keller and Nonacs,
1993). In very large colonies (>1,000 individuals), information
about the queen’s presence and fertility is further communicated
indirectly, e.g., through messenger workers who spread the
queen pheromone in the colony (e.g., in the honeybee: Naumann
et al., 1991) or through a specific chemical signature on queen-
laid eggs (Endler et al., 2004).
Queen pheromones are likely present in most eusocial insect
species and are thought to be located on the queen’s cuticle
(Monnin, 2006; Oi et al., 2015). Different species appear to use
different (albeit partly structurally related) compounds as queen
pheromones (Kocher and Grozinger, 2011; Oi et al., 2015).
However, only a few studies experimentally demonstrated that
Figure 2. Types of Social Organization and Communication Modes Employed by Major Clades in the Insecta
Triangle = solitary insects: no evidence of social behavior other than inter- and intrasexual; circle = communal insects: gregarious, aggregate/form groups;
diamond = subsocial insects: perform brood care; star = (primitively) eusocial. Communication typically takes place between sexes (e.g., courtship, mating),
among the same sex (e.g., dominance, territorial marking), among groups (e.g., aggregation, nestmate recognition, trail following, alarm), or among family
members (e.g., begging, kin recognition) and can comprise the following modes: ear = acoustic or vibrational, nose = chemical, eye = visual, hand = tactile.
Phylogeny based on Misof et al. (2014). Communication modes used by each taxon were assessed by a key word search with Google Scholar. We
first entered the Latin taxon name or common taxon name and ‘‘communication’’ or (more specifically) ‘‘visual,’’ ‘‘acoustic,’’ ‘‘vibrational,’’ ‘‘tactile,’’ or
‘‘chemical’’ communication.’’ For taxa with many hits, the search was further refined by adding ‘‘intersexual’’ or ‘‘intrasexual’’ (or ‘‘among or between
individuals/sexes/males/females/males and females’’) or ‘‘among or between groups.’’ In doing so, we most likely biased the graph toward more thoroughly
studied taxa (such as Diptera or Hymenoptera), whereas communication modes present in less well-studied taxa (e.g., Zygentoma) may have been
underestimated.

putative queen pheromones actually inhibited reproductive ac-
tivity in workers (Kocher and Grozinger, 2011). For example,
queens of the black garden ant (Lasius niger) produce large
amounts of a methyl-branched hydrocarbon in both their own
and the chemical profile of their eggs, which inhibits worker
aggression and ovarian activity (Holman et al., 2010). Queens
of the red imported fire ant (Solenopsis invicta) produce several
compounds (two pyrones and a terpene), which inhibit reproduc-
tive activity in virgin queens and reinforce helping behavior in
workers (Kocher and Grozinger, 2011). Similarly, an ester and
an alcohol from secondary queens and queen-laid eggs of the
termite Reticulitermes speratus attract workers and inhibit differ-
entiation of new queens (Matsuura et al., 2010).
Beyond doubt, queen pheromones have been most inten-
sively studied in the European honeybee Apis mellifera, wherein
the queen mandibular pheromone (QMP) represents the most
complex queen pheromone or pheromone cocktail examined
so far. It comprises at least nine components (five fatty acid de-
rivatives, two alcohols, and two phenolics) (Keeling et al., 2003)
that regulate worker ovarian activity, inhibit rearing of new
queens and juvenile hormone synthesis in workers, delay the
transition from nursing to foraging, attract workers and males,
and coordinate swarming (Le Conte and Hefetz, 2008; Kocher
and Grozinger, 2011). Thus, QMP can act as both a sex phero-
mone and a social coordinator.
In other insects, various hydrocarbons are positively corre-
lated with ovarian activity and therefore candidates for queen
pheromones, e.g., in paper wasps (Polistes dominulus, Sledge
et al., 2004), termites (Cryptotermes secundus, Weil et al.,
2009), and ants (Pachycondyla inversa, D’Ettorre et al., 2004;
several Lasius species, Holman et al., 2013).
Evolutionary Trajectories
In many eusocial insect species, queen pheromones seem to be
represented by specific cuticular hydrocarbons (CHCs, Box 2)
that increase or decrease in parallel with fertility and ovarian
activity (Monnin, 2006) or with the hormonal changes underlying

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Figure 3. Levels of Sociality and Evolution of Increasing Social
Complexity in Insects
In solitary insects, individuals hardly interact except for random encounters
and for mating (e.g., many dipteran species); in subsocial insects, either males
or females or both remain with their brood (e.g., burying beetles of the genus
Nicrophorus); in communal or gregarious insects, individuals of both sexes
aggregate either periodically or permanently for, e.g., better predator defense
(e.g., tent caterpillars Hyphantria cunea) or to overcome plant defenses
and more efficiently exploit resources (e.g., tent caterpillars of the genus
Malacosoma and the moth family Lasiocampidae, bark beetles, Scolytinae);
in eusocial insects, individuals perform periodic (in the case of primitive
eusociality) or permanent (in the case of the most derived eusociality) family
groups with at least two overlapping generations, division of labor, and
cooperative brood care (e.g., several bee and wasp species, all ant and termite
species).
reproductive activity (Oi et al., 2015). Evidence from multiple
species further indicates that changes in cuticular profiles are
associated not only with fertility but also with a female’s mating
status, and that males prefer chemical profiles of unmated over
mated females (Thomas, 2011). Thus, queen pheromones may
have evolved from compounds that are produced at the onset
of ovarian activity in solitary insects and, e.g., signal successful
mating to males (Caliari Oliveira et al., 2015; Oi et al., 2015;
Figure 5). However, there are no comprehensive comparative
studies of compounds that signal fertility in solitary and social
species, which would be needed to test this hypothesis (Kocher
and Grozinger, 2011).
1280 Cell 164, March 10, 2016 ª2016 Elsevier Inc.
Figure 4. Social Interactions in Insects
(A) A female of the burying beetle Nicrophorus vespilloides feeds its larvae.
(B) Firebugs (Pyrrhocoris apterus) aggregate.
(C) A forager of the stingless bee Trigona recursa lays a scent mark.
(D) A royal chamber of the West African termite Macrotermes bellicosus. The
queen (white) is surrounded by the substantially smaller king (black, below the
queen) and workers.
(E) Three Crematogaster modiglianii workers from the same colony fight a
non-nestmate (center).
(F) Two Wasmannia auropunctata workers antennate to sense each other‘s
recognition cues.
(G) Two nestmate workers of Polyrhachis ypsilon ants perform trophallaxis to
exchange food and cuticular hydrocarbons.
Photo credit: H. Bellmann (A), S. Leonhardt (B), S. Jarau (C), J. Korb (D),
F. Menzel (E and G), and A. Wild (F).
Recent studies suggest that wasps, ants, and some bees all
use structurally related hydrocarbons as queen pheromones,
which likely evolved from conserved signals of solitary ancestors
(Oi et al., 2015; Van Oystaeyen et al., 2014). CHCs associated
with fertility are further similar among several lower termites,
suggesting that the use of CHCs as queen pheromones either
is common to most (if not all) insects or has convergently evolved
in many insect species (Hoffmann et al., 2014; Weil et al., 2009).
However, this hypothesis was derived primarily from potential
queen pheromones that were found to be correlated with repro-
ductive activity but were not necessarily tested for their physio-
logical or behavioral activity. Given the structural diversity of
the few queen pheromones that have hitherto been function-
ally confirmed (see above), queen pheromones may not be as
conserved as suggested by Oi et al. (2015) and Van Oystaeyen
et al. (2014).
Manipulation or Honest Signal?
Most recent reviews on queen pheromones agree that they
represent an honest signal that indicates the presence and/
or fertility of a dominant, reproductively active female, rather
than a manipulative cue of mothers to coerce daughters into
involuntary helping (e.g., Kocher and Grozinger, 2011;
Oi et al., 2015; Ratnieks and Wenseleers, 2008, Keller and
Nonacs 1993). However, Kocher and Grozinger (2011) further
suggest that the honeybee QMP might represent a control
 Box 1. Communication Contexts in Insects and Modes and Sig-
nals Involved: A Non-exhaustive List
d Mating (in solitary and all social insects): Individuals attract the
opposite sex over a distance, recognize their own species, and
choose between mating partners (e.g., sex pheromones, acoustic
signals such as chirping).
d Brood care (in brood-caring and eusocial insects): Offspring
signals hunger or other needs (e.g., pheromones, tapping).
d Concerted action (in gregarious and eusocial insects): Group
members warn each other of potential danger (e.g., alarm
pheromones or drumming) and inform others about where to find
resources (e.g., trail pheromones, tandem running, waggle dance).
d Division of labor (in eusocial insects): Queens specialize in
reproduction and signal their presence and fertility to others
(e.g., queen pheromones); workers take over specific duties
(e.g., nursing, entrance guarding, or foraging) and can signal their
task to other workers (e.g., task-specific cuticular profiles).
d Group cohesion (in eusocial insects): To keep resources safe from
outsiders, group members must be able to discriminate group
members from non-members (nestmate recognition).
system because one of its components (HVA) acts
as dopamine antagonist in workers and inhibits their ovarian
activity. Moreover, not all workers equally respond to QMP,
which might indicate a counter-strategy by workers to escape
the queen’s influence under a queen-worker arms race
scenario. In turn, Van Oystaeyen et al. (2014) argue that, under
such a scenario, queen pheromones should evolve quickly
and be composed of rather complex blends. They found no
evidence for such a rapid evolution of queen pheromones
but strong evidence in several bee species for workers
regulating production according to their own interests,
and therefore they argue against queen control in social
insects in general and honeybees in particular (Oi et al.,
2015). Hence, without more studies on actual functional
properties of putative queen pheromones across a wide(r)
range of species, the debate on signal honesty remains unre-
solved.
Chemical Complexity and Diversification
Because the precise components of queen pheromones are
unknown for most insect species, we can only speculate on
whether they became more complex (i.e., consisting of
numerous compounds) and/or specific (i.e., consisting of only
one or few compounds) over evolutionary time. If queen phero-
mones are evolutionarily conserved, as suggested by Van
Oystaeyen et al. (2014), there should be little or no increase in
pheromone complexity. Alternatively, signal complexity could
increase if queen pheromones serve more than one function
(Van Oystaeyen et al., 2014). For example, in the honeybee
genus Apis, major components of queen mandibular pheromone
(the carboxylic acids) appear to be conserved across workers
and queens of different species, whereas the less abundant phe-
nolics have only been found in derived cavity-nesting species
(Abrol, 2013). Signal complexity could further increase as a
consequence of an arms race between queen manipulation
and workers evolving counter-strategies to escape the manipu-
lation (Kocher and Grozinger, 2011) or to avoid social parasitism
(Martin et al., 2011).
Nestmate Recognition
If an insect colony is to survive, its members must discriminate
nestmates from non-nestmates, only allowing the former to enter
the nest. This discrimination is crucial to prevent non-members
of the colony from exploiting a nest’s resources, which would
result in the breakdown of the insect colony, as known for hon-
eybee colonies invaded by cape honeybees (Wenseleers et al.,
2011). To discriminate nestmates from non-nestmates, social in-
sects need colony-specific recognition cues and mechanisms to
perceive and evaluate these cues, followed by either acceptance
or rejection (d’Ettorre and Lenoir, 2010).
Recognition Cues
In species with small colonies, nestmates may recognize each
other individually. This is known in ants using chemical cues
(van Zweden and d’Ettorre, 2010) and especially common in pa-
per wasps (Vespidae: Polistes), where nestmates recognize
each other based on visual cues of their faces (Sheehan and Tib-
betts, 2008). However, virtually all other social insects do not
recognize their nestmates individually but rely on colony-specific
chemical cues. These cues typically consist of CHCs (Martin
et al., 2008; van Zweden and d’Ettorre, 2010).
Perception of the Profile and Behavioral Response
When two individuals meet, they touch each other with their
antennae and sense each other’s recognition cues (Figure 4F).
If the perceived cues are unfamiliar and/or differ from nestmate
cues, the individuals will respond aggressively (Figure 4E) (van
Zweden and d’Ettorre, 2010). The decision to attack or accept
always embodies two sources of error: erroneously rejecting
nestmates and erroneously accepting non-nestmates. Colonies
trade off the costs of the two errors against each other
and adjust the trade-off according to the frequency of intruders
(D’Ettorre et al., 2004; Couvillon et al., 2008; Fürst et al., 2012).
Generally, false acceptance of non-nestmates occurs in various
species, whereas false rejection of nestmates is very rare
(Johnson et al., 2011). Honeybee guards, for instance, adjust
their acceptance threshold depending on nectar availability:
when nectar is scarce, the costs of accepting non-nestmates
that steal nectar from the colony are higher. Hence, the guards
reduce their acceptance threshold at the cost of erroneously
rejecting nestmates (Couvillon et al., 2008; Downs and Rat-
nieks, 2000).
Evolutionary Trajectories
The nestmate recognition system probably evolved from kin
recognition. Ancestral insect colonies only consisted of close
relatives (Hughes et al., 2008), where individuals with similar
CHC cues were likely to be kin. However, many derived euso-
cial insect species have multiple nests and have more complex
colony structures with multiple queens or multiple fathers (if the
queen mated several times), reducing worker relatedness. Low
genetic relatedness could in theory result in the evolution of
nepotism, wherein multiple family lines within a colony compete
for resources. Nepotism seems however to be rare or absent in
eusocial insects (DeHeer and Ross, 1997; but see Hannonen
and Sundström, 2003), which is surprising given that, in several
species, CHCs bear honest information on kinship, thus
enabling nepotism (Helanterä and d’Ettorre, 2015; Nehring
et al., 2011). However, in other species, CHCs lack kinship in-
formation, which may have evolved to counteract nepotism
Cell 164, March 10, 2016 ª2016 Elsevier Inc. 1281

(Wong et al., 2014). Similarly, the CHC profiles of facultative
polygynous ant species seem to bear nestmate information
but no kinship signal (Helanterä et al., 2011; Martin et al.,
2009). The transition from kin to nestmate recognition was
further facilitated by environmentally induced variation in CHC
composition, e.g., through food, gut microbes, or nest-site ma-
terial. Thus, even related individuals carry different recognition
cues if their environments differ (d’Ettorre and Lenoir, 2010).
In ants, individuals of the same colony therefore continuously
exchange their CHCs through allogrooming (i.e., acquiring
CHCs from a nestmate by licking) and trophallaxis (i.e.,
mouth-to-mouth transfer of CHCs; Figure 4G). This presumably
results in a shared colony signature incorporating heritable and
environment-derived compounds. In bees and wasps, CHC ho-
mogenization seems to be achieved via contact to nest paper
or comb wax (van Zweden and d’Ettorre 2010). This colony
odor is likely learned as ants show reduced aggression to
non-nestmate cues encountered before. This indicates that
they familiarize with, and subsequently tolerate, profiles of
other colonies (Leonhardt et al., 2007) or even other species
(Errard et al., 2006; Menzel et al., 2008). However, the exact
neural processes involved in what is typically described as
learning of nestmate cues are not well understood and
currently under debate. The hypotheses put forward range
from receptor adaptation to colony-odor templates stored in
the long-term memory (e.g., Ozaki et al., 2005; van Zweden
and d’Ettorre, 2010; Ozaki and Hefetz, 2014; Esponda and
Gordon, 2015). Although odor homogenization explains how
nestmate recognition can function based on a shared cue,
1282 Cell 164, March 10, 2016 ª2016 Elsevier Inc.
Figure 5. Evolution of Complex Signal
(Queen Signal) in Eusocial Insect Species
from Signal/Cue that Changes with Physio-
logical State (Ovarian Activity) in Solitary
Ancestor
The CHC profiles of females of several solitary
species change with the onset of ovarian activity
and thus following mating (above left and center)
(e.g., in the Dawson’s burrowing bee Amegilla
dawsoni). This chemical change can be used to
inform a male about a female’s mating status and
thus spares males unsuccessful mating attempts
(above right). In communal or facultative eusocial
species where several females compete for
reproductive dominance, the relationship between
CHC profile and ovarian activity informs both
competitors and potential helpers about the
reproductive potential of each female and can be
used to establish dominance and induce helping
behavior (center) (e.g., in some wasps, bees). In
eusocial species, the signal can then be used to
inform workers on the presence and reproductive
potential of the queen, thereby facilitating division
of labor and cooperative brood care (e.g., in ants,
honeybees).
members of the same colony still
differ chemically: queens and workers
possess different odors, and many spe-
cies possess chemically different worker
castes such as foragers and nurses
(Box 2). To our knowledge, it is still un-
known how these differences are maintained despite contin-
uous exchange of CHCs.
Recruitment to Food Sources
Recruitment is the process of directing foraging workers to a
resource, in most cases food. Insects have invented a wide va-
riety of recruitment strategies and use tactile or chemical sig-
nals, or both. The most famous example of recruitment is the
waggle dance in honeybees (von Frisch, 1967). The dance,
pheromones, and flower odors motivate nestmates to forage,
and the complex behavioral sequence of tactile and vibrational
signals communicates the location of a food resource (Thom
et al., 2007).
Recruitment Strategies
In general, a recruiting insect has two tasks: (1) raise attention
and motivate others to forage and (2) direct them to the food
source, which can be achieved through either the same or sepa-
rate signals. For example, bumblebees only inform nestmates
about a food resource and its scent through ‘‘excited runs’’
and the release of a recruitment pheromone but do not provide
information on its location (Dornhaus and Chittka 1999, 2001;
Dornhaus et al., 2003). Stingless bees similarly excite their nest-
mates but additionally guide them by chemically marking the
food patch and/or leaving scent trails (Jarau, 2009), which
consist of pheromone markings left in a ‘‘line’’ between the
nest and a flower (Figure 4C). Although such scent trails are un-
known in other bees or wasps, honeybees and bumblebees
leave scent marks directly at the food resource. Depending on
their foraging success at marked flowers, the other workers learn
 Box 2. CHCs—Encoding Multiple Messages

CHCs cover the body surface of virtually all insects and protect them against desiccation and pathogens (Blomquist and Bagnères, 2010). The
CHC layer can consist of more than 100 different compounds, and their quantitative and qualitative composition is highly variable across and
within species. Typical compounds include n-alkanes, alkenes, and methyl-branched alkanes (Blomquist and Bagnères, 2010). Their compo-
sition is mainly genetically driven, but also influenced by the insects’ food, nest material (d’Ettorre and Lenoir, 2010), or climatic conditions
(Wagner et al., 2001). CHCs are structurally simple molecules, and many compounds (n-alkanes, monomethyl alkanes) are shared by many
different species. Thus, signal complexity arises not through complex molecules but rather through complex mixtures of structurally simple
compounds.
In solitary insects, CHC profiles contain information about an individual’s species membership and its sex (Thomas and Simmons, 2008). In eusocial
insects, however, CHC profiles encode a multitude of other messages, including fertility or reproductive status (see Queen Signaling) and colony
membership (see Nestmate Recognition). Besides, they can carry information on the bearer’s behavioral caste (scouts, foragers, nurses) (Pam-
minger et al., 2014; Wagner et al., 2001). This facilitates self-organization of division of labor (Greene and Gordon, 2003).
Interestingly, multiple signals encoded in the CHC can override each other. For example, non-nestmate queens are usually accepted in Camponotus
ant nests, likely because the ‘‘queen’’ signal overrides the nestmate recognition signal. As a consequence, the queen is accepted and tended even if
she is a non-nestmate (Helanterä and Ratnieks, 2009; Moore and Liebig, 2010).
How such different information is encoded in the CHC profile has been intensely investigated. Although some information (e.g., queen signals)
might be represented by single substances (Van Oystaeyen et al., 2014), most messages seem to be encoded by quantitative composition of
several compounds, rather than the presence or absence of certain substances (van Zweden and d’Ettorre, 2010). Eusocial insects and especially
ants can effectively discriminate structurally similar hydrocarbons (Sharma et al., 2015). This capacity is reflected on a neuronal and a genetic level:
The numbers of glomeruli and olfactory and gustatory receptor genes increase drastically from non-social (i.e., Nasonia) to eusocial insects
(i.e., bees and ancestors of modern ants) (Tsutsui, 2013; Zhou et al., 2012). At the same time, there is a vast diversification of CHC-producing
gene families (desaturases; Helmkampf et al., 2015), which may be related to the evolution of complex communication systems.

to either avoid or approach them (Saleh and Chittka 2006; Stout
and Goulson 2001).
In ants and termite recruiters, recruitment strategies seem to
depend on colony size (Hölldobler and Wilson, 2009). Species
with small colonies often have solitary foragers or perform tan-
dem running, where the recruiters touch recruits to get their
attention and guide them to the food source. Tandem running
can also involve additional chemical signals (Hölldobler and Wil-
son, 2009). Group recruitment occurs in larger colonies (several
100 workers) and involves trail pheromones to guide a group of
foragers to the source. Trail pheromones both motivate and
direct foragers.
Evolutionary Trajectories
Dornhaus and Chittka (1999, 2001) suggest that the exciting
movements of stingless bees and bumblebees derive from
ancestral excitatory motor displays of successful foragers that
became ritualized. The honeybee dance, however, is much
more precise and probably evolved independently from ritual-
ized intention movements (aborted flights toward the target)
(von Frisch, 1967).
In ants, trail pheromones originate from several different
glands. The gland of origin is usually specific to the ant subfamily
(Hölldobler and Wilson, 1990; Morgan, 2009), suggesting that
the trail-laying behavior evolved several times independently.
Termites, in contrast, invariably use trail pheromones from the
sternal gland, suggesting a single evolutionary origin (Jaffe
et al., 2012).
In the ant Paratrechina, compounds from the Dufour’s gland
excite nestmates, whereas compounds from the hind gut trigger
trail-following. Dufour’s gland products are typically volatile and
function as alarm pheromones in many ant species, which may
explain their exciting effect. The less volatile, longer-lived hind-
gut excretions used to demarcate the trail (Witte et al., 2007)
may have originated from ritualized feces deposition (Hölldobler
and Wilson, 1990). In the ant Tapinoma, excretions from the
pygidial gland provoke trail-following at low concentrations but
alarm at high concentrations (Morgan, 2009). Thus, a complex
interplay of different glands enables finely tuned recruitment,
which likely evolved from the combination of originally separate
messages.
Alarm Signaling
Giant hornets prey on honeybees directly at their hives.
When hornet scouts find a suitable prey hive, they call in their
nestmates for a mass raid. Some honeybee species (e.g., Apis
cerana japonica, Apis mellifera cypria) evolved a specific and
effective defense behavior. They can prevent raids by quickly
killing the much bigger hornet scouts through concerted action
with thousands of workers forming a ball around the attacking
wasp and producing enough heat to roast it to death (Abrol,
2013; Ono et al., 1995). To quickly recruit so many defenders,
honeybees evolved a multitude of alarm signals of chemical,
acoustic, and potentially visual nature (Abrol, 2013; Ono et al.,
1995).
Signals Used
Most insect alarm signals are chemical. The honeybee alarm
pheromone is composed of several substances (Verheggen
et al., 2010). Its main component is isopentyl acetate (IPA), which
is released from the sting apparatus and dispersed by wing
fanning. IPA is emitted during the stinging process but also
when the sting apparatus remains stuck in a victim, thereby trig-
gering more honeybees to sting (Bortolotti and Costa, 2014). The
response to the alarm pheromone differs with individual, age,
and context. For example, honeybees only react to IPA when
they are in groups, and they are most sensitive when they are
close to the colony entrance (Bortolotti and Costa, 2014).
Alarm pheromones vary among species but are common in all
eusocial insect lineages and occur in every ant species studied
(Hölldobler and Wilson, 1990). They are emitted from a number of
different glands and comprise a surprising diversity of substance

Cell 164, March 10, 2016 ª2016 Elsevier Inc. 1283

classes, from hydrocarbons to spiroacetals, but are typically of
low molecular weight so that they are volatile and can transmit
information over a distance (Bruschini et al., 2008; Hölldobler
and Wilson, 1990; Verheggen et al., 2010).
There are two typical responses to alarm pheromones. Spe-
cies with small colonies and ephemeral nests seem to quickly
retrieve brood and disperse upon alarm (‘‘panic alarms,’’ Wil-
son and Regnier, 1971), whereas species with large compact
colonies tend to attack the cause of the alarm and defend
the nest.
When it comes to communication over a distance, acoustic
signals travel much faster and further than chemicals and should
thus be superior when messages, such as threats, are urgent
(Hölldobler, 1999; Nehring et al., 2013). Consequently, acoustic
alarm signals also evolved in some social insects, such as
termite species that produce substrate-borne vibrations
(Inta et al., 2009; Virant-Doberlet and Cockl, 2004) or ants of
the genus Camponotus, which drum their abdomen on the sub-
strate. This drumming increases awareness of nestmates but
does not directly elicit an aggressive response. However, when
ants are alarmed by drumming, they respond faster and more
aggressively to subsequently emitted alarm pheromones than
without prior drumming (Hölldobler, 1999).
Evolutionary Trajectories
Chemical alarm cues are supposedly old and evolutionarily
widespread. In their simplest form, they are chemical sub-
stances leaking from injured bodies and can be used by other
individuals as cues to flee, shoal, seek shelter, or ramp up de-
fenses. Receivers subsequently improve perception to reduce
the predation risk. Emitters, on the other hand, may often not
benefit directly from warning others, unless the receivers’
behavior (e.g., agitated movements) disturbs and confuses
predators. As soon as emitters benefit, dynamic co-evolution
between senders and receivers can occur, resulting in powerful
alarm signals.
A second evolutionary trajectory of alarm pheromones are
defensive chemicals excreted by insects when attacked. Similar
to leaking substances, these secretions can be used by
bystanders to sense danger and have evolved into more sophis-
ticated alarm signals suitable for communication over long
distances. The subsequent use of defensive substances as alarm
pheromones is still verifiable in several eusocial species. For
example, honeybee stinging releases alarm pheromones (Borto-
lotti and Costa, 2014), and ants spraying toxic formic acid like-
wise induce alarm behavior (Hölldobler and Wilson, 1990).
The ancestral chemical alarm signals in eusocial Hymenoptera
appear to be components of the sting venom, as is still found in
vespine and polistine wasps (Bruschini et al., 2008; Moritz and
Bürgin, 1987; Sledge et al., 1999). In honeybees, pheromone
production is spatially removed from the venom glands to Ko-
schevnikov and sting sheath glands (Bortolotti and Costa,
2014) and to the mandibular glands, which are also used across
all clades of ants (Hölldobler and Wilson, 1990). Various ant
clades additionally use compounds from Dufour’s and pygidial
glands. Formicine ants further revert to a defensive secretion,
formic acid, to alarm nestmates (Hölldobler and Wilson, 2009).
Termites, however, evolved a different system of chemical de-
fense. Species with soldiers often secrete defensive chemicals
1284 Cell 164, March 10, 2016 ª2016 Elsevier Inc.
from head glands, which contain alarm-eliciting volatile chemi-
cals (Pasteels and Bordereau, 1998).
Chemical Complexity and Diversification
The phylogenetically most widespread alarm pheromones in
ants and wasps are ketones, which may indicate that their
biophysical properties are particularly suited for this function.
Common additions are alcohols, esters, aldehydes, and terpe-
noids. Wasp venom alarm volatiles can contain similar sub-
stances but typically contain spiroacetals and pyrazines
(Bruschini et al., 2008; Moritz and Bürgin, 1987; Sledge et al.,
1999). Termites mostly rely on terpenes, e.g., farnesene, which
is also used for alarm signaling in aphids (Verheggen et al.,
2010). Other than that, there is very little taxonomic coherence
concerning the substances used by different species, which
suggests that alarm pheromone blends underlie strong ecolog-
ical selection (Wilson and Regnier, 1971) or evolved indepen-
dently multiple times. Across species, the same substances
can be used as alarm and trail pheromones, so that alarm pher-
omones may have been co-opted as recruitment pheromones,
and potentially vice versa, which would further explain variability
in alarm pheromones (Hölldobler and Wilson, 1990; Witte et al.,
2007).
Perspective
Although our current knowledge on the evolution of communica-
tion in eusocial insects has drastically advanced in the last de-
cades, many questions still await further research. Most studies
on communication in eusocial insects have largely focused on a
few model organisms such as the honeybee (Apis mellifera) and
some ant species (e.g., Camponotus, Lasius). Most of these
model systems are highly derived eusocial species compared
to often simpler structured societies in other species. Thus, it
is unclear to what extent generalizations can be made. For a bet-
ter understanding of general evolutionary trajectories of specific
messages in eusocial insects, we need more information from a
variety of phylogenetically independent eusocial species.
Studies of solitary and subsocial insects will help to identify po-
tential precursors of signals and the origin of messages used in
eusocial insects. Future research should focus on comparing
chemical signals and message types between multiple, phyloge-
netically independent lineages of both solitary and eusocial
species. Although there is little debate that increasing social
complexity requires a higher diversity of signals being sent and
received, we have not even begun to understand how the diver-
sity of messages are communicated without interfering with
each other. This is all the more surprising as the chemical
complexity of the involved cues and signals (e.g., CHC) does
not seem to increase with social complexity. Thus, it remains
unclear how the same cue or signal can encode multiple
messages that do not seem to interfere. Several contexts of
communication, such as queen signaling and nestmate recogni-
tion, have been subject to intense research but still lack an inte-
gration of concepts and data. In both cases, several partly
opposing hypotheses have been put forward, none of which
can explain all the data. This includes the question of to what
extent communication between queens and workers is honest
signaling versus coercion. Thus, future research should aim
at formulating testable hypotheses that help to distinguish
between alternative explanations and their rigorous testing
among multiple eusocial species in a robust phylogenetic
framework. First steps in this direction are being taken, but
there is still a long way to go until we gain enough evidence
for solid conclusions on the evolution of communication in the
context of social complexity.
ACKNOWLEDGMENTS
We apologize to all the colleagues whose work we were not able to include due
to space limitations. We are very grateful for the helpful comments provided by
our working groups and three anonymous reviewers. We further thank Stefan
Jarau, Judith Korb, Alexander Wild, and Heiko Bellmann for allowing us to use
their photographs.
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