Facial patterns in a tropical social wasp correlate with colony membership

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.

Full text

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 ‘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 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;d’Ettorre 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;
d’Ettorre 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 d’Ettorre 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 d’Ethologie
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 3–6) were collected in
Malaysia (03° 42.774 N–101° 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 D’Arcy Thompson’s Cartesian transformation grids
(Bookstein 1989), Fig. 1b–e). 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 2–5) 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. b–e
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:
Wilks’λ= 0.022, P< 0.001, explained variance 43.8 %;
function 2: Wilks’λ=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: Wilks’λ=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 wasps’perception of their conspecifics’facial 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 d’Ettorre 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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