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Abstract

Social insects excel in discriminating nestmates from intruders, typically relying on colony odours. Remarkably, some wasp species achieve such discrimination using visual information. However, while it is universally accepted that odours mediate a group level recognition, the ability to recognise colony members visually has been considered possible only via individual recognition by which wasps discriminate ‘friends’ and ‘foes’. Using geometric morphometric analysis, which is a technique based on a rigorous statistical theory of shape allowing quantitative multivariate analyses on structure shapes, we first quantified facial marking variation of Liostenogaster flavolineata wasps. We then compared this facial variation with that of chemical profiles (generated by cuticular hydrocarbons) within and between colonies. Principal component analysis and discriminant analysis applied to sets of variables containing pure shape information showed that despite appreciable intra-colony variation, the faces of females belonging to the same colony resemble one another more than those of outsiders. This colony-specific variation in facial patterns was on a par with that observed for odours. While the occurrence of face discrimination at the colony level remains to be tested by behavioural experiments, overall our results suggest that, in this species, wasp faces display adequate information that might be potentially perceived and used by wasps for colony level recognition.
SHORT COMMUNICATION
Facial patterns in a tropical social wasp correlate with colony
membership
David Baracchi
1,2
&Stefano Turillazzi
3
&Lars Chittka
2
Received: 30 June 2016 /Revised: 7 September 2016 /Accepted: 9 September 2016
#Springer-Verlag Berlin Heidelberg 2016
Abstract Social insects excel in discriminating nestmates
from intruders, typically relying on colony odours.
Remarkably, some wasp species achieve such discrimination
using visual information. However, while it is universally ac-
cepted that odours mediate a group level recognition, the abil-
ity to recognise colony members visually has been considered
possible only via individual recognition by which wasps dis-
criminate friendsand foes. Using geometric morphometric
analysis, which is a technique based on a rigorous statistical
theory of shape allowing quantitative multivariate analyses on
structure shapes, we first quantified facial marking variation
of Liostenogaster flavolineata wasps. We then compared this
facial variation with that of chemical profiles (generated by
cuticular hydrocarbons) within and between colonies.
Principal component analysis and discriminant analysis ap-
plied to sets of variables containing pure shape information
showed that despite appreciable intra-colony variation, the
faces of females belonging to the same colony resemble one
another more than those of outsiders. This colony-specific
variation in facial patterns was on a par with that observed
for odours. While the occurrence of face discrimination at
the colony level remains to be tested by behavioural experi-
ments, overall our results suggest that, in this species, wasp
faces display adequate information that might be potentially
perceived and used by wasps for colony level recognition.
Keywords Face recognition .Insect cognition .Individual
recognition .Nestmate recognition .Visual signals
Introduction
A number of vertebrate species such as members of the mam-
mals (Halpin 1980), birds (Bonadonna and Nevitt 2004)andfish
(Höjesjö et al. 1998), and invertebrates such as hermit crabs
(Gherardi and Tiedemann 2004), social bees, ants and wasps
(Barrows 1975;dEttorre and Heinze 2005; Tibbetts 2002)are
known to recognise individual conspecifics. This ability is ad-
vantageous in diverse situations such as parental care in species
with synchronous nesting [pinnipeds (Insley 2000; Charrier et al.
2003), bats (Balcombe 1990)], territoriality [penguins (Aubin
and Jouventin 1998), songbirds (Godard 1991)], dominance in-
teractions and aggressive competitions [insects (Tibbetts 2002;
dEttorre and Heinze 2005), aquatic invertebrates (Karavanich
and Atema 1998), fish (Höjesjö et al. 1998), monkeys (Silk
1999)]. In social animals, however, recognising members of a
society or colony is often as important as individual recognition.
In social insects, such colony level recognition is often mediated
by odour cues (van Zweden and dEttorre 2010), though visual
colony cues are likely to be used in some stingless bees that build
unique colony nest entrance structures (Chittka et al. 1997).
In at least two subfamilies of wasps, visual recognition of
individuals also plays a role in individual, rank and nestmate
recognition (Beani and Turillazzi 1999;Tibbetts2002;
Communicated by Sven Thatje
Electronic supplementary material The online version of this article
(doi:10.1007/s00114-016-1406-8) contains supplementary material,
which is available to authorized users.
*David Baracchi
david.baracchi@gmail.com
1
Université Paris 13, Sorbonne Paris Cité, Laboratoire dEthologie
Expérimentale et Comparée, 93430 Villetaneuse, France
2
Biological and Experimental Psychology, School of Biological and
Chemical Sciences, Queen Mary University of London, Mile End
Road, London E1 4NS, UK
3
Università degli Studi di Firenze, Dipartimento di Biologia, Via
Madonna del Piano 6, Sesto Fiorentino, Italy
Sci Nat (2016) 103:80
DOI 10.1007/s00114-016-1406-8
Tibbetts and Dale 2004; Baracchi et al. 2013). Several paper
and hover wasp species have variable facial and abdominal
cuticular markings that are used for social communication
(Cervo et al. 2015). For instance, Polistes gallicus,Polistes
exclamans,Polistes dominula and Liostenogaster vechti fe-
males use black clypeal spots as conventional signals to con-
vey information on their agonistic qualities such as dominance
status and aggressiveness (Tibbetts and Dale 2004; Tibbetts
and Sheehan 2011; Baracchi et al. 2013;Petrocellietal.
2015). By contrast, experiments in which facial markings of
Polistes fuscatus and Liostenogaster flavolineata females
were experimentally manipulated indicate that workers can
visually recognise individual nestmates (Tibbetts 2002;
Baracchi et al. 2013).
So far, nestmate recognition via visual information has
been considered possible only via individual recognition
where individuals must remember the facial features of all
colony members (Tibbetts 2002; Tibbetts and Dale 2007;
Baracchi et al. 2013). However, at least in principle, all mem-
bers of a colony might be identified as nestmates according to
shared common features of their facial pattern.
In the wasp L. flavolineata, a species whose colonies rarely
have more than six individuals, both vision and olfaction me-
diate nestmate recognition, and unfamiliar odours or faces
induces residents to assault colony intruders (Baracchi et al.
2013,2015). When the facial marking of conspecifics was
experimentally altered by adding yellow or brown paint to
the clypeus in order to slightly change its appearance, they
were treated more aggressively than those with unaltered faces
by resident nestmates (Baracchi et al. 2013). Vision seems to
be prioritized by resident females over odours early in an
encounter and olfactory cues are used later to enhance accu-
racy in the recognition process (Baracchi et al. 2015). This
species builds small nests typically in large aggregations
(Coster-Longman et al. 2002). As a consequence, landing at-
tempts by neighbouring alien wasps, some of which are occa-
sionally received peacefully, are quite frequent (Coster-
Longman et al. 2002). Dominance order is age based and
the older female monopolises reproduction until her death,
while young females may disperse or become helpers on their
natal nest queuing for inheriting dominance (Bridge and Field
2007). A previous study (Cervo et al. 2002)demonstratedthat
nestmates have more similar cuticular hydrocarbon profiles
(CHCs) than non-nestmates, suggesting that CHCs can be
effective cues to identify nest membership. By contrast, to
date it is unknown whether wasps from the same colony have
more similar facial patterns than do wasps from different col-
onies. As a consequence, it is unclear whether visual nestmate
recognition is based on a common face pattern shared by
nestmates by which all members of a colony can be identified
or whether there is an individual recognition via facial mark-
ings which is used to recognise colony members. In the pres-
ent work, we first determined whether facial patterns contain
sufficient information about colony membership by quantify-
ing within- and between-colony variation of faces. Then, we
compared statistically this level of information with the one
contained in the cuticular hydrocarbon profiles to determine
face and odour potential reliability in discriminating between
nestmate and alien wasps.
Materials and Methods
Twelve colonies of L. flavolineata with a total of 44 females
(mean: 3.5 females per colony, range 36) were collected in
Malaysia (03° 42.774 N101° 46.319 E). Morphometric
analysis of the facial marking was used to describe within-
and between-colony facial variation (Fig. 1a). The general
procedure was similar to that used to classify stenogastrine
species using wing morphology (Baracchi et al. 2011). We
took pictures of the faces of each wasp with a Fujifilm
AX550 digital camera under a stereo microscope. Fifty-six
points on the face were chosen as landmarks (5) or semi-
landmarks (51) for geometric morphometrics, so that for
each wasp we obtained a landmark configuration as the
one showed in Fig. 1a. Landmarks correspond to evolution-
arily homologous anatomical parts that are the same in all
the specimens (i.e. the tip of the clypeus, the upper joint of
the left and the right mandibles and the left and the right
ends of the front in its widest point, Fig. 1a). Semi-
landmarks are non-homologous points (i.e. points whose
position along a curve is arbitrary but which provide infor-
mation about the curvature of the silhouette of clypeal mark-
ing, Fig. 1a). By definition, a shape consists in all the geo-
metric features of an object except for its size, position and
orientation in the space (Dryden and Mardia 1998). Wasp
faces have different sizes and differed slightly also in their
orientation and location in the pictures. In order to compare
the shape of the clypeal markings, we removed all these
non-shape information using a standard statistical method
commonly used in geometric morphometrics (i.e. the gener-
alized procrustes analysis (GPA, (Gower 1975))), which al-
lows to superimpose a population of shape instances anno-
tated by landmark and semi-landmark points in a common
coordinate system (Rohlf and Slice 1990). Precisely, by
translating, rotating and scaling the pictures of the faces to
find the best fit between landmark shapes and to minimize
the differences between them, the generalized procrustes
analysis optimally aligned and superimposed the facial
markings and extracted sets of variables containing pure
shape information called partial warps (PWs). A principal
component analysis (PCA) was applied to the PWs in order
to convert these set of possibly correlated variables into a
lower number of uncorrelated variables called relative warps
(RWs). Shape variation in the facial markings can be visu-
alized by entering the RWs in the thin-plate-spline
80 Page 2 of 6 Sci Nat (2016) 103:80
deformation grids (i.e. a mathematically rigorous implemen-
tation of DArcy Thompsons Cartesian transformation grids
(Bookstein 1989), Fig. 1be). To give a visual representation
of the average facial marking of three colonies, we first
computed the mean RW1 and RW2 as the geometric cen-
troid of the RW1 and RW2 belonging to all the wasps of
each colony. We then entered these two RWs in the thin-
plate-spline deformation grids. All the analyses were carried
out using the TPS series of software (Rohlf 2015). Published
data on chemical profiles obtained for 12 additional colonies
from the same location (n= 41 wasps, 3.5 females on aver-
age per colony, range 25) of L. flavolineata (Cervo et al.
2002) were used for a direct statistical comparison with our
morphological data. Principal component analysis (PCA)
and discriminant analysis (DA) applied to the variables con-
taining chemical (PCs) and morphological information
(RWs) were used to assess the extent to which facial pattern
and chemical profile provide good cues for nestmate recog-
nition. In order to obtain a conservative output for the DA,
we performed a full cross-validation test (CV test) using the
leave-one-out technique (Baracchi et al. 2010). All analyses
were performed using Paws Statistics 19.00 (Chicago, IL,
USA).
Results
Twenty-seven chemical compounds were identified on the
cuticle of the wasps (Cervo et al. 2002). The PCA applied to
those compounds extracted five PCs (functions of variables
containing chemical information) that explained 78 % of the
total variance in our sample when combined. PCA applied to
the shape variables extracted 59 relative warps (RWs, func-
tions of variables containing shape information). To be more
conservative, since the PCA applied on chemical data provid-
ed only five PCs, we used the same number of RWs
(explaining a cumulative variance of 75 %) for successive
analyses.
PC
1
and PC
2
explained 28.0 and 21.6 % of variance of the
chemical profiles (Fig. ESM 1) while RW
1
and RW
2
ex-
plained 45.8 and 10.1 % of variance of the facial markings
(Fig. ESM 2), respectively. These percentages suggest that,
regardless of colony membership, the variation of both the
chemical profiles and the facial markings in the overall popu-
lation is similar although they represent two completely dif-
ferent types of cue. The variation in the facial marking in the
studied population is illustrated by deformation grids (Fig. 1).
The RW
1
indicated that almost half ofthe variation (45.8 %) in
the facial markings is due to the different top-to-bottom length
of the brownish marking along the vertical axis of the clypeus
(Fig. 1b, c). In particular, at the one end of the variation along
the RW
1
, there are wasps with the two external cusps far
longer than the one in the middle (Fig. 1b), while at the other
end there are wasps whose facial marking almost entirely
lacks the two external cusps and has the middle one more
prominent (Fig. 1c). A clear example of this latter facial pat-
tern is represented by some females belonging to colony 1
reported in Fig. 3.TheRW
2
, which is the second most impor-
tant function explaining about the 10 % of the facial variation
in our population, mainly reassumed the variation along the
Fig. 1 a Landmarks (in red)and
semi-landmarks (in blue)
positioned on the face of 44
L. flavolineata females. be
Variation in shape of the female
facial marking. The red lines
connect semi-landmarks (facial
marking) while the black lines
connect landmarks. b,crepresent
facial markings of hypothetical
wasps located at the left and the
right ends of the RW1 axis
(Fig. ESM2). d,erepresent facial
markings of hypothetical wasps
located at the top and the bottom
edge of the RW2 axis
Sci Nat (2016) 103:80 Page 3 of 6 80
horizontal axis of the clypeus at the level of both the three
cusps and the junction between the upper end of the clypeus
and the lower end of the front, where the facial marking ex-
tends to and above the antennal sockets. Precisely, at one end
of the variation along the RW
2
, there are wasps with a quite
narrow facial marking at the level of the frontal-clypeal junc-
tion but a wide trident composed of three long cusps of equal
length (Fig. 1e). At the other end of RW
2
variation, there are
wasps with an evident square facial marking and a much re-
duced length of the three cusps (Fig. 1d). The individuals
belonging to colony 3 shown in Fig. 3are clear examples of
this latter condition.
DA correctly assigned 58.5 % (26.8 % in the CV test) of
the females to their colony using CHC profiles (function 1:
Wilksλ= 0.022, P< 0.001, explained variance 43.8 %;
function 2: Wilksλ=0.084,P< 0.001, explained variance
25.8 %, Fig. 2) and 61.4 % (25 % in CV test) of females to
their colony using facial markings (function 1: Wilks
λ=0.034,P< 0.001, explained variance 52.1 %; function
2: Wilksλ=0.014,P= 0.004, explained variance 28.1 %,
Fig. 2) indicating that within- and between-colony variation of
the facial patterns and the chemical profiles are similar. Some
examples of the variation in the facial marking of wasps be-
longing to different colonies from the same population are
reported in Fig. 3. The modelled average faces (Fig. 3)give
clues as to the elements of faces that might actually be used by
wasps for colony recognition showing that the most differen-
tiation is seen at the lower end of the brownish markings as
well as in the overall top-to-bottom length of the brownish
markings as explained above.
Discussion
Our findings, for the first time, open the possibility that visual
nestmate recognition in social wasps may not depend exclu-
sively on individual recognition. We showed that, although
each L. flavolineata female has a unique facial marking even
within a colony, females belonging to the same colony resem-
ble one another more than wasps belonging to different ones.
Based on our analyses, within- and between-colony variation
in the visual patterns is on a par with that in chemical profiles,
suggesting that, similarly to CHCs, the wasp faces display
adequate information for colony level recognition. Even
though waspsperception of their conspecificsfacial mark-
ings remains to be tested by behavioural experiments, these
findings suggest that visual nestmate identification may rely
on common facial features rather than, or in addition to, indi-
vidual recognition. In the first case, each nest must have a
unique signature shared by nestmates, while in the latter case,
each individual must have a unique phenotype that has to be
memorized.
While extracting common features from a category of vi-
sual patterns may be more cognitively demanding, individual
recognition certainly requires more storage capacity. Indeed,
the existence of a common visual cue by which most of the
few nest members can be identified suggests that visual
nestmate recognition might require a memory of just one av-
erage defining feature (a colony label), as occurs when they
memorize the colony odour (Bos and dEttorre 2012). We do
not yet know what features the wasps might use in category
formation, but the average facial markings as well as other
Fig. 2 Plot of the scores of the two first discriminant functions obtained
by the discriminant analysis using facial markings (left) or chemical
profiles (right) belonging to 12 colonies. X-axis and Y-axis represent the
explained variance by the first and second function, respectively. Each
open circle represents a female wasp. In each plot, different colours
indicate different colonies. Black squares are the centroids (i.e. the
mean value for each colony). Each ellipsoid encloses all the wasps
belonging to the same colony. The size of the ellipsoids is indicative of
the within-colony variation in facial markings (left) and odours (right),
while their superimposition rate indicates the between-colony variation,
so that smaller and less overlapped ellipsoids correspond to colonies with
lower and higher within- and between-colony variation, respectively. The
colony-specific variation in facial patterns is on a par with that observed
for odours
80 Page 4 of 6 Sci Nat (2016) 103:80
elements like spatial frequency or amount of contrast might be
all suitable candidates. A similar mechanism based on visual
category formation might also occur in P. fuscatus (i.e. the
only other species of wasp that are known to use faces for
individual/nestmate recognition) even though, in this case,
the different parts of the faces vary in colouration and do not
display any dots or shapes (Tibbetts 2002).
Individual and class level recognition do not exclude each
other and the same facial cues may be used for multiple levels
of recognition. Our analysis left 25 % of the total variance of
the facial marking in our sample unexplained, indicating that
many aspects of the shape of the facial markings varied across
individuals. Thus, facial markings are clearly unique and they
may inform the viewer about both colony membership and
individual identity. Behavioural experiments that manipulated
the facial signals of L. flavolineata already provided conclu-
sive proof of the effectiveness on information transfer by in-
dividual facial markings (Baracchi et al. 2013,2015).
Previous field experiments showed that resident wasps
responded aggressively towards nestmates whose facial mark-
ings were experimentally altered, either by slightly enlarging
or reducing the brownish facial marking using brown or yel-
low paint, respectively (Baracchi et al. 2012). Our new data
open the possibility for the existence of group level visual
recognition. The percentage of correct assignment as
nestmates and non-nestmates obtained in our discriminant
analyses was only about 60 % either using odours or facial
markings. Even though this percentage can vary depending on
the relative number of variables entered in the analysis, it
agrees with the findings that nestmate recognition system of
L. flavolineata is far from perfect. Indeed, when visual cues or
chemical cues were experimentally presented in isolation in
field tests, this caused erroneous responses towards alien fe-
males in 31 and 45 % of cases, respectively (Baracchi et al.
2015).
The similarities in the facial markings of nestmates suggest
a genetic basis and the heritability of these clypeal traits. In
L. flavolineata, similarly to most primitively eusocial species,
the colony is started by a single female and other related or
unrelated females can occasionally join the new foundation
(Samuel 1987). Moreover, young females can leave the natal
nest soon after eclosion and it has been suggested that those
individuals could be not the daughters of the dominant fe-
males but rather of a previous one (Samuel 1987). Larval
development is relatively long in this species (about 110 days)
and sometimes dominant females die long before daughters
emergence (Samuel 1987). An early study settled on an intra-
colony female relatedness as rather moderate (i.e. 0.22; be-
cause of the haplodiploid sex-determination system, 0.75
would be the value if all the females were fully sisters) using
allozymes (Strassmann et al. 1994). However, more recent
and reliable analyses based on DNA microsatellite markers
provided much higher values of relatedness (i.e. 0.52 and
0.56 (Sumner et al. 2002), 0.45 (Sumner 1999) and 0.46
(Bridge 2005)). Hence, it is reasonable to conclude that many
colony members are actually relatives and that the face resem-
blance among nestmates is most likely linked to their kinship,
as it has been suggested for the visual quality signal in
P. dominula (Tibbetts 2010).
While our finding showed a correlation between facial pat-
terns we measured and colony membership, this does not
prove that wasps are able to perceive and rely on these colony
similarities. The occurrence of face discrimination at the col-
ony level remains to be tested in the field. For instance, wasp
colonies might be presented either with alien females with
increasingly dissimilar facial features from those of resident
wasps or with artificial face stimuli that are members of the
group cluster but are individually different to all other faces on
a nest, similar to the experiments performed by Baracchi and
co-workers (Baracchi et al. 2013). Intruders with faces more
similar to those of their hosts might have more chances of
being erroneously adopted by colonies than females with
more dissimilar faces. In L. flavolineata, young unrelated in-
dividuals occasionally join alien colonies (Coster-Longman
et al. 2002) and females looking for a new colony where to
settle on might find it by a trial-and-error approach. The exis-
tence of a visual nestmate recognition rather than, or in addi-
tion to, an individual recognition would provide us with the
opportunity to delineate pros and cons of different recognition
systems and their implications for group living organisms.
Fig. 3 Modelled average facial markings obtained from the real face images of females belonging to three different colonies
Sci Nat (2016) 103:80 Page 5 of 6 80
Acknowledgments The authors thank Prof. Rosly Hashim and Dr.
Iacopo Petrocelli for their support in Malaysia and Drs. Francesca
Romana Dani and Alessandro Massolo for providing chemical data.
DB was supported by a Marie Curie Intra European Fellowship. LC is
supported by an ERC Advanced Grant and a Royal Society Wolfson
Research Merit Award.
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... Members attach to an individual's appearance detailed information about social status, affective relationships, fighting ability, territory boundaries, and cooperation [35]. Insect societies were until recently not thought to exhibit individual recognition, but to make only simple ingroup/outgroup distinctions [36], where, for example, the guards at a nest entrance can tell rightful entrants from intruders [37][38][39][40][41][42]. ...
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Insects feature some of the most complex societies in the animal kingdom, but a historic perception persists that such complexity emerges from interactions between individuals whose behaviours are largely guided by innate routines. Challenging this perception, recent work shows that insects feature many aspects of social intelligence found in vertebrate societies, such as individual recognition, learning object manipulation by observation, and elements of cultural traditions. Insects also display emotion-like states, which may be linked to social behaviours such as rescuing others from danger. We review recent developments in insect social cognition and speculate that some forms of now-hardwired behaviour (e.g., nest construction) could have initially been the result of individual innovation and subsequent cultural spread, with evolution later cementing these behaviours into innate behaviour routines.
... Despite the potentially smaller informative content of visual cues compared to chemical ones (but see Baracchi et al., 2016) and their static nature (individual color patterning remains stable after emergence, while CHC blend is continuously updated), visual cues might be advantageous over chemical ones to enable NMR as they can be quickly processed and do not require contact or really close distance (contrary to CHCs), thus enabling a faster NMR decision. Indeed, when assessing a potential intruder, colony members are faced with a trade-off between speed and accuracy of recognition and, depending on the context, speed might be prioritized over accuracy ( Chittka et al., 2009;Baracchi et al., 2015). ...
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Nestmate recognition, i.e., the ability to discriminate nestmates from foreign individuals, is a crucial feature of insect societies, and it has been traditionally considered to be predominantly based on chemical cues. Recent empirical evidence, however, suggests a relevant plasticity in the use of different communication channels according to cue availability and reliability in different contexts. In particular, visual cues have been shown to influence various types of social recognition in several social insects, but their role in nestmate recognition is still under-investigated. We tested the hypothesis of plasticity in the use of visual and chemical recognition cues in the primitively eusocial wasp Polistes dominula, in which the availability and reliability of recognition cues vary across the colony cycle. Indeed, before the emergence of workers, P. dominula colonies are rather small (one to few individuals), and the variability in the facial pattern might allow resident wasps to use visual cues for nestmate recognition. After workers’ emergence, the increase in the number of colony members reduces the reliability of visual cues, thus leaving chemical cues as the most reliable nestmate recognition cues. We thus predict a differential use of chemical and visual cues along colony life. We experimentally separated visual and chemical cues of nestmates and non-nestmates and presented them alone or in combination (with coherent or mismatched cues) to resident wasps to test which communication channel was used in the two stages and, in case, how visual and chemical cues interacted. Our results show, for the first time in a social insect, the differential use of visual and chemical cues for nestmate recognition in two different phases of colony, which supports the hypothesis of a plastic, reliability-based use of recognition cues in this species according to the different colonial contexts.
... Within a colony, foundresses live as cooperative breeders with a single dominant female who lays all or most of the eggs [35]. While there is some evidence that eusocial wasps use facial pattern cues to identify individual nest mates [36], the majority of the literature has focussed on cuticular hydrocarbon profile as a potential cue for discerning kin [3]. It has been suggested that Polistes wasps can recognise hydrocarbon profiles of their nest mates but cannot necessarily distinguish relatives from non-relatives that share their natal nest origin or hibernaculum group [37][38][39]. ...
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Cooperation among kin is common in animal societies. Kin groups may form by individuals directly discriminating relatives based on kin recognition cues, or form passively through natal philopatry and limited dispersal. We describe the genetic landscape for a primitively eusocial wasp, Polistes dominula, and ask whether individuals choose cooperative partners that are nearby and/or that are genetic relatives. Firstly, we genotyped an entire sub-population of 1361 wasps and found genetic structuring on an extremely fine scale: the probability of finding genetic relatives decreases exponentially within just a few meters of an individual's nest. At the same time, however, we found a lack of genetic structuring between natural nest aggregations within the population. Secondly, in a separate dataset where ~2000 wasps were genotyped, we show that wasps forced experimentally to make a new nest choice tended to choose new nests near to their original nests, and that these nests tended to contain some full sisters. However, a significant fraction of wasps chose nests that did not contain sisters, despite sisters being present in nearby nests. Although we cannot rule out a role for direct kin recognition or natal nest-mate recognition, our data suggest that kin groups may form via a philopatric rule-of-thumb, whereby wasps simply select groups and nesting sites that are nearby. The result is that most subordinate helpers obtain indirect fitness benefits by breeding cooperatively.
... This faculty favors the evolution and maintenance of sociality because it allows rejecting alien competitors (nonnestmate con-and heterospecifics) while being tolerant toward group members, which are typically related (Hamilton 1987). Apart from the rare exception of few social wasp species, where vision also plays a role in nestmate discrimination (Tibbetts 2002;Baracchi et al. 2016), the recognition of colony members in social insects is predominantly mediated by chemical cues (Lenoir et al. 1999; van Zweden and d'Ettorre 2010). Insect cuticles are covered by complex mixtures of hydrocarbons forming a waterproof layer (Blomquist and Bagnères 2010) that prevents body dehydration and plays a prominent communication role in insects living in groups (Blomquist and Bagnères 2010). ...
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The ecological and evolutionary success of social insects relies on their ability to efficiently discriminate between group members and aliens. Nestmate recognition occurs by phenotype matching, the comparison of the referent (colony) phenotype to the one of an encountered individual. Based on the level of dissimilarity between the two, the discriminator accepts or rejects the target. The tolerated degree of mismatch is predicted by the acceptance threshold model, which assumes adaptive threshold shifts depending on the costs of discrimination errors. Inherent in the model is that rejection (type I) and acceptance (type II) errors are reciprocally related: if one type decreases, the other increases. We studied whether alarm pheromones modulate the acceptance threshold. We exposed Camponotus aethiops ants to formic acid and subsequently measured aggression toward nestmates and nonnestmates. Formic acid induced both more nonnestmate rejection and more nestmate acceptance than a control treatment, thus uncovering an unexpected effect of an alarm pheromone on responses to nestmates. Nestmate discrimination accuracy was improved via a decrease in both types of errors, a result that cannot be explained by a shift in the acceptance threshold. We propose that formic acid increases the amount of information available to the ants, thus decreasing the perceived phenotypic overlap between nestmate and nonnestmate recognition cues. This mechanism for improved discrimination reveals a novel function of alarm pheromones in recognition processes and may have far-reaching implications in our understanding of the modus operandi of recognition systems in general.
... The individual recognition model assumes that individuals become familiar from previous encounters. Paper wasps use individual recognition and visually discriminate between different colony members based on their individual facial patterns (Baracchi et al., 2015(Baracchi et al., , 2016. In ants, individual recognition based on visual cues is not known and individual recognition based on chemical cues is rare. ...
... The use of new taxonomic techniques is of paramount importance to elucidate identification problems that morphology and linear morphometry cannot alone solve (Rohlf & Marcus 1993). It is for this reason that geometric morphometry analyses have been widely used in many taxonomic studies of different groups of insects (Jaramillo et al. 2002;Pizzo et al. 2011;Baracchi et al. 2016). ...
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Almost 30% of female American sand flies are morphologically indistinguishable from one another. These females belong to species-complexes or groups with closely related species, making species-level identification difficult or even impossible. This fact has implications for public health since several of these groups include species which are vectors of human pathogens. Thus, new tools are needed to minimize species-level identification problems. In this context, our research sought to use geometric morphometry in the study of the head of females of closely related species of the genus Psychodopygus, Chagasi series, which includes the following species: P. chagasi, P. complexus, P. squamiventris maripaensis, P. squamiventris squamiventris, and P. wellcomei. We have used ten landmarks distributed on the head of these species. All species were clearly distinguished using the centroid size and shape together. These results highlight the head analysis as an effective tool for future geometric morphometry studies in sand flies.
... This evidence from P. fuscatus wasps shows that individual recognition via subtle visual discrimination is also possible in insects with potential convergence of visual strategies based on configural processing with mammals (Avarguès-Weber, 2012; Chittka and Dyer, 2012). Further works on wasps suggest that face recognition may have evolved several times in insects depending upon ecological constraints (Baracchi et al., 2015(Baracchi et al., , 2016. ...
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The expertise of humans for recognizing faces is largely based on holistic processing mechanism, a sophisticated cognitive process that develops with visual experience. The various visual features of a face are thus glued together and treated by the brain as a unique stimulus, facilitating robust recognition. Holistic processing is known to facilitate fine discrimination of highly similar visual stimuli, and involves specialized brain areas in humans and other primates. Although holistic processing is most typically employed with face stimuli, subjects can also learn to apply similar image analysis mechanisms when gaining expertise in discriminating novel visual objects, like becoming experts in recognizing birds or cars. Here, we ask if holistic processing with expertise might be a mechanism employed by the comparatively miniature brains of insects. We thus test whether honeybees (Apis mellifera) and/or wasps (Vespula vulgaris) can use holistic-like processing with experience to recognize images of human faces, or Navon-like parameterized-stimuli. These insect species are excellent visual learners and have previously shown ability to discriminate human face stimuli using configural type processing. Freely flying bees and wasps were consequently confronted with classical tests for holistic processing, the part-whole effect and the composite-face effect. Both species could learn similar faces from a standard face recognition test used for humans, and their performance in transfer tests was consistent with holistic processing as defined for studies on humans. Tests with parameterized stimuli also revealed a capacity of honeybees, but not wasps, to process complex visual information in a holistic way, suggesting that such sophisticated visual processing may be far more spread within the animal kingdom than previously thought, although may depend on ecological constraints.
Article
Decision-making processes face the dilemma of being accurate or faster, a phenomenon that has been described as speed-accuracy trade-off in numerous studies on animal behaviour. In social insects, discriminating between colony members and aliens is subjected to this trade-off as rapid and accurate rejection of enemies is of primary importance for the maintenance and ecological success of insect societies. Recognition cues distinguishing aliens from nestmates are embedded in the cuticular hydrocarbon (CHC) layer and vary among colonies. In walking carpenter ants, exposure to formic acid (FA), an alarm pheromone, improves accuracy of nestmate recognition by decreasing both alien acceptance and nestmate rejection. Here we studied the effect of FA exposure on the spontaneous aggressive mandible opening response of harnessed Camponotus aethiops ants presented with either nestmate or alien CHCs. FA modulated both MOR accuracy and the latency to respond to odours of conspecifics. In particular, FA decreased MOR towards nestmates but increased it towards aliens. Furthermore, FA decreased MOR latency towards aliens but not towards nestmates. As response latency can be used as a proxy of response speed, we conclude that contrary to the prediction of the speed-accuracy trade-off theory, ants did not trade off speed against accuracy in the process of nestmate recognition.
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Predatory social wasps (Vespidae) are opportunistic, invasive and generalist foragers which employ distinct foraging strategies to meet the nutritional needs of adults and larvae. They are agile, visual predators that can hunt on the fly, scavenge on carcasses and collect tree sap, honeydew, nectar and sugars from rotting fruits. Their diverse foraging strategies make them an excellent model system to study cognition and context specific use of sensory information. Few studies have addressed visual associative learning and olfactory preferences of predatory social wasps in the context of flower-feeding, although nectar is one of their main carbohydrate sources. A deeper understanding of their sensory ecology and learning abilities in the flower foraging context is important, as they are invasive and major predators of honeybee colonies in many parts of the world. We investigated visual associative learning and olfactory preference in the Greater banded hornet Vespa tropica. We found that V. tropica foragers readily associate colour with sugar reward and exhibit colour generalisation. They also learn to associate shapes with sugar rewards. Our results suggest that colour learning and shape discrimination might play a role in the context of flower search in V. tropica. Finally, we show that V. tropica preferred honeybee hive-related odours over a generic floral odour, indicating that the preference for hive odours could potentially help hornets home in on bee colonies.
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Most animals communicate using complex signals that convey information in multiple sensory modalities. Testing receiver responses to each signal in isolation as well as the composite signal provides crucial information about how receivers use and integrate information from complex signals. Polistes fuscatus wasps have facial patterns that are visual signals of individual identity and cuticular hydrocarbons (CHCs) that are used for nestmate recognition. Because wasps learn the unique facial pattern of each nestmate, they could potentially use both visual and chemical signals to assess group membership. We test whether P. fuscatus integrate information from visual and chemical signals when assessing conspecifics that approach their nest. We challenged wasps with conspecifics that had color patterns and CHCs of nestmates, color patterns of nestmates and CHCs of non‐nestmates, color patterns of non‐nestmates and CHCs of nestmates, and color patterns and CHCs of non‐nestmates. Wasps with non‐nestmate CHCs were treated aggressively, and wasps with nestmate CHCs were treated non‐aggressively, regardless of whether the wasps had nestmate or non‐nestmate color patterns. Therefore, wasps use chemical signals alone to identify nestmates versus non‐nestmates. Receivers do not integrate information from visual and chemical signals during assessment of potential intruders. Instead, visual and chemical signals convey different information and are used in different contexts.
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The development and the present state of the “tps” series of software for use in geometric morphometrics on Windows-based computers are described. These programs have been used in hundreds of studies in mammals and other organisms.
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Social insects have evolved sophisticated recognition systems enabling them to accept nest-mates but reject alien conspecifics. In the social wasp, Liostenogaster flavolineata (Stenogastrinae), individuals differ in their cuticular hydrocarbon profiles according to colony membership; each female also possesses a unique (visual) facial pattern. This species represents a unique model to understand how vision and olfaction are integrated and the extent to which wasps prioritize one channel over the other to discriminate aliens and nest-mates. Liostenogaster flavolineata females are able to discriminate between alien and nest-mate females using facial patterns or chemical cues in isolation. However, the two sensory modalities are not equally efficient in the discrimination of 'friend' from 'foe'. Visual cues induce an increased number of erroneous attacks on nest-mates (false alarms), but such attacks are quickly aborted and never result in serious injury. Odour cues, presented in isolation, result in an increased number of misses: erroneous acceptances of outsiders. Interestingly, wasps take the relative efficiencies of the two sensory modalities into account when making rapid decisions about colony membership of an individual: chemical profiles are entirely ignored when the visual and chemical stimuli are presented together. Thus, wasps adopt a strategy to 'err on the safe side' by memorizing individual faces to recognize colony members, and disregarding odour cues to minimize the risk of intrusion from colony outsiders. © 2015 The Author(s) Published by the Royal Society. All rights reserved.
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Conventional signals are maintained via social costs and commonly used in the animal kingdom to assess conspecifics' agonistic ability during disputes over resources. In the last decade, some experimental studies reported the existence of visual conventional signals in several social wasp species, being good rank predictors in different social contexts. Females of the social wasp Polistes gallicus do not cooperate to start nests but they often try to usurp conspecific nests. Here, we showed that the reproductive females of this species have variable facial colour patterns that function as conventional signals. Wasps with larger black spots on their clypeus are more likely to successfully overwinter, are larger, and are better at fighting and at holding a nest. Furthermore, in field experiments, resident foundresses rely on facial pattern to assess usurpers' fighting abilities, modulating their defence reaction accordingly, so that rivals with larger black spot receive more aggression than rivals with smaller or no black spots on the clypeus. Our study reveals that visual recognition abilities are widespread among paper wasps that, regardless of their social biology, face similar selective pressures within competitive contexts.
Thesis
Females of facultatively eusocial insects are all capable of laying eggs and therefore all have the potential to practice different reproductive strategies. Direct reproduction can be achieved by being dominant in a group or by nesting alone. Indirect reproduction is achieved by helping to raise the offspring of relatives. The choice of strategy depends on how reproductive conflicts are resolved and this may be determined by genetic and ecological factors. In this thesis I examine the factors affecting reproductive conflicts in hover wasps (Stenogastrinae, Hymenoptera). Using highly polymorphic microsatellite markers, developed by screening partial genomic libraries, I estimate relatedness among colony members in three species of Stenogastrinae (Parischnogaster alternata, Liostenogaster flavolineata and L. vechtii). Relatedness in P. alternata was significantly lower than in L. flavolineata.. I attribute the low relatedness in P. alternata to the movement of females between nests, their tendency to found nests in groups and that they often nest with females from other groups. Liostenogaster flavolineata was previously perceived as only being incipiently eusocial because of low relatedness among female nestmates (r = 0.22 0.1 - Strassmann et al 1994). I re-examine colony fine genetic structure in this species. By genotyping brood and adults, I show that there is normally only one reproductive laying female eggs, but that subordinates occasionally lay male eggs. I conclude that reproductive strategies in L. flavolineata are typical of a eusocial insect. I discuss the parameters from reproductive skew models that may explain the high skew. The little variation in skew amongst colonies of L. flavolineata meant that the models could be evaluated only at the interspecific level. A comparative analysis across 21 hymenopterans revealed a positive relationship between relatedness and skew. This result is consistent with a prediction of the Incentives model for reproductive skew (Reeve and Ratnieks 1993).
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The decomposition of deformations by principal warps is demonstrated. The method is extended to deal with curving edges between landmarks. This formulation is related to other applications of splines current in computer vision. How they might aid in the extraction of features for analysis, comparison, and diagnosis of biological and medical images is indicated.
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Social recognition, i.e. The ability to recognize and assign individual membership to a particular and relevant class, such as caste, dominance status, gender or colony, shapes the amazing organization of insect societies. Traditionally, it has been assumed that social recognition in social insects is mainly governed by chemicals. However, social insects also share information via many other sensory channels, and it has been recently demonstrated that visual signals can mediate several types of social recognition in some species of social wasps. Primitively social wasps, such as paper wasps of Polistes genus, are suitable models to investigate visual communication because their combs lack of envelops allowing light to produce visual cues, their colonies are small, they have a good vision, they show a remarkable individual within-colony colour variation and, finally, they show an intense social life based on social recognition. In this chapter we reviewed the role of visual cues in social recognition inside and outside social wasp colonies focusing both on the intraspecific and interspecific recognition contexts.