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Behavioral and Chemical Correlates of Long-Term
Queen Adoption in the Facultative Polygynous Ant
Ectatomma tuberculatum
L. Zinck & D. Denis & R. R. Hora & C. Alaux &
A. Lenoir & A. Hefetz & P. Jaisson
Revised: 19 December 2008 /Accepted: 16 March 2009 /
Published online: 3 April 2009
#
Springer Science + Business Media, LLC 2009
Abstract In ants, queen adoption is a common way of achieving secondary
polygyny but the mechanisms involved are little known. Here we studied the process
of long-term adoptions of alien queens in the facultative polygynous ant Ectatomma
tuberculatum. In eight out of 10 successful adoption experiments, all the introduced
queens showed similar behavior and fecundity as the resident queens even after
J Insect Behav (2009) 22:362–374
DOI 10.1007/s10905-009-9178-z
L. Zinck (*)
:
D. Denis
:
P. Jaisson
Laboratoire d’Ethologie Expérimentale et Comparée (UMR CNRS 7153) Université Paris 13,
99 avenue J.-B. Clément, 93430 Villetaneuse, France
e-mail: zinck@leec.univ-paris13.fr
D. Denis
e-mail: denis@leec.univ-paris13.fr
P. Jaisson
e-mail: jaisson@leec.univ-paris13.fr
R. R. Hora
U.P.A. Laboratório de Mirmecologia, Convêncio UESC/CEPLAC, Centro de Pesquisas do Cacau,
C.P.7, 45600-000 Itabuna, Bahia, Brazil
e-mail: rivianer@hotmail.com
C. Alaux
Department of Entomology, University of Illinois, Urbana, IL 61801, USA
e-mail: calaux@life.uiuc.edu
A. Lenoir
Institut de Recherche sur la Biologie de l’Insecte (UMR CNRS 6035),
Université de Tours, Tours, France
e-mail: alain.lenoir@univ-tours.fr
A. Hefetz
Department of Zoology, Tel Aviv University, Ramat Aviv, 69978 Tel Aviv, Israel
e-mail: hefetz@post.tau.ac.il
Present address:
R. R. Hora
Departamento de Biologia Geral, Universidade Federal de Viçosa,
Viçosa 36570-000 Minas Gerais, Brazil
2 months, indicating complete integrati on into the colony. Chemical analysis
revealed that the cuticular hydrocarbon profiles of resident and introduced queens
were clearly distinct from those of workers and that they did not change after
adoption. We p ropo se that queen -specific cuticular hydrocarbon profile may
represent a reliable signal of queen’s fertility and discuss about the evolution of
high level of queen acceptance in E. tuberculatum.
Keywords Formicidae
.
secondary polygyny
.
nestmate recognition
.
cuticular hydrocarbons
.
fertility signal
Abbreviations
Qr resident queen
Qa adopted queen
SPME solid phase micro extraction
GC/MS gas chromatography mass spectroscopy
CHC cuticular hydrocarbon
PCA principal component analyses
DA discriminant analysis
MSMD mean squared Mahalanobis distance
Introduction
The evolution of sociality in insects has been enlightened by inclusive fitness theory
of Hamilton (1964) which emphasizes that relatedness between individuals can
promote cooperation in certain circumstances. Queen number per colony has thus
been the subject of numerous studies since polygyny is likely to decrease within-
colony relatedness demoting cooperation (Keller 1993; Bourke and Franks 1995).
However, in several cases polygyny was shown to be compatible with kin selection
theory (Nonacs 1988 ; Pamilo 1991; Keller 1995). First, nestmate queens can be
related and thus lead to a relatively high relatedness between nestmate workers
(Pamilo and Rosengren 1984; Douwes et al. 1987; Pamilo 1991; Lipski et al. 1992;
Trontti et al. 2005). Second, polygyny facilitates larger colony size (i.e. worker
force) thus increasing overall colony productivity (Rosengren and Pamilo 1983;
Rissing et al. 1989). Furthermore, pleometrosis (colony foundation by multiple
queens) enhances the success rate of colony foundation compared with haplomet-
rosis (colony foundation by a single queen) (Herbers 1993; Bourke and Heinze
1994). Polygyny can either be achieved by pleometrosis which leads to primary
polygyny, or by queen adoptions which result in secondary polygyny (Rissing and
Pollock 1988). Although secondary polygyny is common in ants (Hölldobler and
Wilson 1977, 1990) only a few studies investigated the dynamics of queen
acceptance and the mechanisms by which queen number per colony is regulated
(Bennett 1988; Fortelius et al. 1993; Stuart et al. 1993; Evans 1996; Sundström
1997; Mori and Le Moli 1998; Hora et al. 2005 ; Souza et al. 2005; Vásquez and
Silverman 2008). Moreover, most of the studies on secondary polygyny were short-
term and overlooked the possibility that queens might be rejected at a later stage of
the introduction. Most studies focused on workers’ ability to discriminate between
reproductive females depending on their nest of origin (nestmate or non-nestmate)
J Insect Behav (2009) 22:362–374 363
and on their mating status, with varying, species specific, results. For example, no
discrimination occurred between mated and virgin females neither in Formica
podzolica (Bennett 1988) nor in F. lugubris (Fortelius et al. 1993), but in
F. truncorum mated females were discriminated against at greater rates than virgin
females when co-introduced into the colony (Sundström 1997). Moreover,
monogynous and polygynous colonies of F. truncorum showed differences in the
propensity of adopting queens, which was propos ed to be associated with differences
in dispersal strategies found in each population (Sundström 1997). Queen adoption
was also studied in two facultative polygynous ant species, Myrmica tahoensis
(Evans 1996) and Ectatomma tuberculatum (Hora et al. 2005), colonies of which
coexist as monogynous or polygynous in the same population, the latter likely
resulting from queen adoptions (i.e. secondary polygyny). In both above-mentioned
studies, alien mated queens were introduced into monogynous colony and the
queens’ behavior was monitored for a short time post-introduction (15–19 and
8 days, respectively). Although adoptions were considered as succes sful, in both
species the resident queens behaved differently than the introduced queens in
showing greater brood attendance. Queen adoption was also reported in the slave-
making ant Formica sanguinea (Mori and Le Moli 1998) and in the monogynous
leaf-cutting ant Acromyrmex subterraneu s molestans (Souza et al. 2005). Recently,
Vásquez and Silverman (2008) showed that queen acceptance in the invasive
Argentine ant Linepithema humile depends on resident queen number and not
adopted queen fecundity.
Queen discrimination leading to adoption or rejection probably involves the use
of olfactory cues. While the usurpation and subsequent adoption of queens of
parasitic ants was demonstrated to rely on chemical cues and chemical dece ption
(Allies et al. 1986; Topoff et al. 1988; Lenoir et al. 1997), no chemical data exists, to
our knowledge, pertaining to the adoptions of conspecific queens in the context of
secondary polygyny. One factor that might intervene in queen adoption is colony
insularity, e.g. acceptance or rejection of queen based on similarity of recognition
cues (Vander Meer and Morel 1998; Lenoir et al. 1999). Alternatively, queens might
be recognized as such in having caste specific odors, in addition to colonial identity.
These separately, or in concert may affect the process of adoption. Finally, the
resident queens may acquire the colony odor through mechanisms that results in
Gestalt colony odor (Crozier and Dix 1979; Soroker et al. 1994; Lenoir et al. 2001).
This is supported by findings in M. tahoensis in which workers groomed adopted
queens at higher rates after adoption compared to that occurring in naturally
polygynous colonies (Evans 1996).
Here, we studied some of the behavioral and chemical correlates of queen
adoption in the facultative polygynous ant Ectatomma tuberculatum. In this species,
colony and population genetic study showed that limited female dispersal and
polydomy are associated with genetic viscosity (Zinck et al. 2007). This suggests
that females seeking adoption are likely to be related to resident queens and it may
explain secondary polygyny evolution in this species. Since cuticular hydrocarbons
were demonstrated as serving both as nestmate and queen recognition cues
(reviewed in Monnin 2006; Le Conte and Hefetz 2008) we focused our chemical
analyses on these compounds. We determined whether adopte d queens were
behaviorally integrated over long term (i.e. after 2 months), and we studied the
364 J Insect Behav (2009) 22:362–374
dynamic of cuticular hydrocarbon profiles of both the resident and adopted queens,
and that of host colony workers during adoption. We also discuss the ultimate causes
of queen adoption in connection with colony insularity and nestmate recognition in
E. tuberculatum.
Materials and Methods
Colony Collection and Ant Maintenance
Ten polygynous and ten monogynous colonies of E. tuberculatum were collected in
Buerarema and Itabuna, Bahia state in Brazil. Given that E. tuberculatum is
polydomous we ascertained that the adopted and resident queens were neither
nestmates nor related queens by selecting colony-pairs that were at least 50 m apart
(adoptions 1–6 from Itabuna; Table 1) (Zinck et al. 2007). The colonies used for
adoptions 7 to 10, which were also used for chemical analyses, corresponded to
cross-adoptions between two different populations (i.e. Buerarema and Itabuna)
located 17 Km apart (Table 1). Colonies were maintained in the laboratory in
artificial nests made of plaster-of-Paris connected to an outside arena at 28±2°C and
70±2 % RH. They were fed twice a week with frozen crickets and honey. The
experiments were started after an acclimatization period of 2–3 months to these
laboratory conditions.
Behavioral Assay
Monogynous host colonies containing the queen (resident queen, Qr), individually
marked workers, and brood were placed in new nests for 1 week for acclimation. In
order to standardize colony size among the experiments we reduced the number of
workers per colony to 64 (monogynous colonies of E. tuberculatum generally
contain around 200 workers (Hora et al. 2005)). Before introducing an alien queen
into these monogynous host colonies, the behavior of the resident queen was scored
during 5 days by performing ten scan-samplings per day for each nest (n=500).
Table 1 Summary of Experimental Queen Adoptions and the Origin of Queen Colonies Used for
Adoptions
Monogynous colony Polygynous colony
(resident queen) (adopted queen)
Adoption 1–6 Itabuna Itabuna
Adoption 7
a,b
Buerarema Itabuna
Adoption 8
a,b
Buerarema Itabuna
Adoption 9
a
Itabuna Buerarema
Adoption 10
a
Itabuna Buerarema
a
indicate adoption experiments used for chemical analysis
b
indicate adoption experiments that failed
J Insect Behav (2009) 22:362–374 365
Behavioral items consisted of queen’s oviposit ion, brood attendance by the queens,
and queen grooming by workers (Hora et al. 2005). Prior to the alien queen
introduction (adopted queen, Qa) we removed the brood of the resident queen, so
that all the brood at the end of the experiment (i.e. 2 months later) corresponded to
eggs laid after the adoption. Alien queens used for the adoption experiments were
mature mated queens (recognized by their matte cuticle (Hora et al. 2008 )) that came
from polygynous colonies. Queen adopti ons were performed as described in Hora et
al. (2005) by introducing the alien queen into the exterior arena of the host colony.
Behavioral observations were conducted during the first and eighth weeks post-
introduction by scan sampling as described above.
Chemical Analysis
Chemical characterization of queen and worker cuticular hydrocarbons was done
both using solvent extraction and solid phase micro extraction (SPME) using a
polydimethylsiloxane, 7 μm bonded fiber (Arthur and Pawliszyn 1990). Initial
chemical analyses of queen and worker profiles were performed by combined gas
chromatography mass spectroscopy (GC/MS) (Perkin Elmer, at the EI mode with
turbo mass electron energy of 70 eV). Compounds identification was deduced from
their respective fragmentation patterns. Further characterization of cuticular hydro-
carbons was done by GC (Varian 3900) equipped with a 30-m-long DB-5 fused
silica capillary column and flame ionization detection. The fiber was desorbed into
the column for 5 min (injector and column temperatures set at 280°C and 100°C,
respectively; Helium was used as carrier gas at a flow rate of 28.57 cm/s).
Thereafter, the column was temperature programmed from 100–250°C at 20°C/min
and then to 320°C at 3°C/min with a final hold of 5 min. Peak integration was done
with Varian system control (version 6.20). Sampling of resident and introduced
queens as well as five randomly selected workers of each colony was done by SPME
prior to introduction and 1 and 8 weeks post-introduction. Fiber loading was
achieved by rubbing it for 10 min against the last intersegmental membranes of the
gaster. Replicates of queen profiles were achieved by repeated sampling (n=5) at
approximately 45 min intervals between sampling. For workers, replicates consisted
of profiles that were obtained by sampling once each of five workers.
Statistical Analyses
Queens’ behaviors were compared by using nonparametric tests (StatXact 3.1).
Oviposition and brood atte ndance were compared by paired permutation tests using
the queen (adopted versus resident) and the week (week 1 versus week 8) as
variables. Statistical analysis of the number of grooming received by resident versus
adopted queens was also done by paired permutation tests. For all the permutation
based analyses, the unit s permuted between classes were single observatio ns.
For comparing between cuticular hydrocarbon (C HC) compositions of the v arious
queens and workers we first subjected the quantifiable CHC (marked with an
asterisk in the legend of Fig. 2) to a Principal Component Analyses (PCA), to reduce
the number of variables (CHC) in the subsequent Discriminant Analysis (DA)
(Heinze et al. 2002). The first five factors of the PCA that explained a high
366 J Insect Behav (2009) 22:362–374
proportion of the variance (92.32% and 93.38% for the experimental adoption 9 and
10, respectively) were used to perform standard DA. To investigate chemical
differences between adopted and resident queens’ profiles, we compared the mean
squared Mahalanobis distance (MSMD) between each replicate of the hydrocarbon
profile of adopted queens and the centroid of the corresponding resident queens for
each adoption experiment. Similarly, to study the chemical differences between
workers and adopted or resident queens, we compare the MSMD between workers
and queens in each colony, prior queen adoption. Kruskall-Wallis and permutation
tests (StatXact 3.1) were then conducted to make comparison between these
Mahalanobis distances.
Results
Behavioral Observation of Queen Adoption
Eight out of the ten introduced queens were adopted by the host colonies and two
queens were rejected. In the eight successful adoptions, neither the resident workers
nor the resident queen were aggressive toward the adopted queen. There were no
significant differences in queen’s brood attendance at any time of the experiment
between the adopted and resident queens (Paired permutation tests: p=0.297 and
p=0.109 for weeks 1 and 8 post-introduction, respectively) (Table 2). Although the
resident queens tended to lay more eggs than the adopted queens 8 weeks after
adoption (Table 2), no signi ficant difference was found in oviposition between them
neither 1 week nor 8 weeks post-introduction (Paired permutation tests: p=0.313 and
p=0.063, respectively). Figure 1 depicts worker behavior towards the resident or
introduced queens. The number of grooming events towards the adopted queens was
significantly higher than that towards the resident queens during the first week after
adoption (Permutation test: p=0.043) but both equally subsided in the 8th week
post-adoption and were not significantly different from each other (Perm utation test:
p=0.866) (Fig. 1).
The two adoptions that failed (Adoption 7 and 8, Table 1) ended in the death of
the newly introduced queens. In these two cases, the workers initially transported the
introduced queen from the foraging area into the nest like the queens in the
successful introductions, but afterwards they continuously assaulted the newly
Table 2 Mean Occurrence of Oviposition and Brood attendance by Resident (Qr) and Adopted (Qa)
Queens in Successful Adoptions (n=8) Before the Adoption, 1 week After and 8 weeks After the
Adoption
Behavior occurrence Before adoption 1 week after adoption 8 weeks after adoption
Queen Qr Qr Qa Qr Qa
Oviposition 2.6±2.6 1.6±0.7 2.9±2.2 3.9±2.1 2±0.8
Brood attendance 31.4±7.9 26±8.6 29.4±9.7 41.4±5.7 45.9±2.8
J Insect Behav (2009) 22:362–374 367
introduced queen, culminating in her death within the 24 h. The resident queens did
not participate in these aggressions, but behaved normally.
Chemical Investigation of Queen Adoption
Figure 2 presents the cuticular hydrocarbon profiles of queens and workers. Queens
profile was identical to that previously described (Hora et al. 2008), and the ratio of
heptacosane to nonacosane indicates that the queen presented was mated. The profile
of workers is drastically different from that of queens. The major mated-queen
compound, heptadecane, occurs only as traces in workers. Also the amount of
nonacosane, the second major queen component is greatly reduced in workers. On
the other hand, the major worker peak is a mixture of 11-; 13-; and 15-
methylnonacosane, and the second largest component is a similar mixture of
methylhentriacontane. Two other pronounced worker components are 12,14
dimethyloctacosane and hentriacontene (double bond position undetermined). To
test the hypothesis that queen adoption is accompanied by chemical changes in
cuticular hydroca rbon composition, we compared the profiles of adopted queens,
resident queens and host workers (Fig. 3). As expected from the qualitative chemical
differences between queens and workers, these were completely separated in the
discriminant analysis, irrespective of colonial origin. However, neither the profiles of
queens nor those of workers appeared to change significantly following an alien
queen introduction. This refutes the hypothesis that queen adoption is accompanied
by convergence of the adopted queen profile with that of the queen or workers from
the host colony.
Qr Qr Qa Qr Qa
Before
ado
p
tion
1 week after
ado
p
tion
8 weeks after
ado
p
tion
Median
25%-75%
Min-Max
0
20
40
60
80
100
120
Nb of groomings of queens by workers
*
ns
Fig. 1 Grooming by E. tuberculatum workers of resident (Qr) and adopted (Qa) queens before the
adoption, and 1 week and 8 weeks post-adoption. Levels of significance are indicated by * if p<0.05, ** if
p<0.01, *** if p<0.001 and ns if they were not significant.
368 J Insect Behav (2009) 22:362–374
We also wished to examine whether disparity of profiles between the
introduced and resident queens is at the basis of acceptance or rejection of the
introduced queens. To that effect we compared the mean squared Mahalanobis
distances ( MSMD) between pairs of adopted and resident queens in each
experiment. Significant differences were found among all adoption experiments
(MSMD±SE=15.8±7.5, Adoption 7; 175.4±25.0, Adoption 8; 124.5±21.6,
Adoption 9; and 12.3±5.8, Adoption 10) (Kruskall-Wallis test: H=32.12,
N=40, p<0.001), but no significant difference were found between mean squared
Mahalanobis distances in failed adoptions (MSMD±SE=95.6±81.9, Adoption 7
and 8) and in successful adoptions (MSMD±SE=68.4±58.3, Adoption 9 and 10)
(Permutation test: p=0.421). Cuticular hydrocarbon profiles of adopted queens
Fig. 2 Chromatograms of E. tuberculatum worker (a) and queen (b). Peak numbers correspond to the
following compounds. The compounds marked with an asterisk were utilized for the PCA. 1) Pentacosane; 2)
Hexacosane*; 3) Heptacosa ne*; 4) 11-+13 -Methyl heptacosan e; 5) 5-Meth ylheptaco sane*; 6)
3-Methylheptacosane*; 7) 5,9,-Dimethylheptacosane; 8) Octacosane*; 9) 11,13,15-Trimethylheptacosane;
10) 2-Methyloctacosane*; 11) Nonacosene; 12) Nonacosane*; 13) 11+13+15-Methylnonacosane*;
14) 7-Methylnonacosane*; 15) 5-Methylnonacosane*; 16) 11,15+13,15-Dimethylnonacosane; 17)
3-Methylnonacosane*; 18) 7,9 +7,11-Dimethylnonacosane; 19) 5,23-Dimethylnoacosane*; 20) 5,11-
Dimethylnoacosane; 21) 8 -Methyltr iacontane *; 22) 12,1 4 Dimeth yltriacontane* ; 23) 8,12-D imethyltr iacontan e;
24) 7,17,23-Trimethylnonacosane; 25) 5,15,23-Trimethylnonacosane; 26) Hentriacotene; 27) 15 +17-
Methylhentriacontene; 28) 11-+13-Methylhentriacontane*; 29) 11,15 +13,15-Dimethylhentriacontane;
30) 5,7-Dimethylhentriacontene; 31) 7,11,13-Trimethylhentriacontane; 32) 5,11,13-Trimethylhentriacontane;
33) 12 +14+16-Methyldotriacontane; 34) 11 +13 +15 +17-Methyltritriacontane; 35)?
J Insect Behav (2009) 22:362–374 369
were thus not found to be more similar to those of resident queens in successful
adoption experiments, compared to those of rejected and resident queens in failed
adoption experiments. Moreover, the mean squared Mahalanobis distance between
workers a nd adopted queens was found to be significantly less important than
between workers and resident queens among all adoption experiments (MSMD±
SE=34.3±21.8, Workers - Qa; 63.7±48.3 Workers - Qr) (Permutation test:
p=0.002). However this result was only due to chemical differences between
workers and queens in a single experimental adoption (Table 3, Adoption 8).
Cuticular hydrocarbon profiles of workers were thus not found to be more similar
to those of resident queens than adopted queens.
Discussion
Our results revealed that long-term queen adoptions can occur in Ectatomma
tuberculatum resulting in functional polygyny, which is consistent with the existence
of secondary polygyny in this species (Hora et al. 2005; Zinck et al. 2007). While
queen adoption was already demonstrated in E. tuberculatum (Hora et al. 2005), this
A1
W1
R1
A3
W3
R3
-5 -4 -3 -2 -1 0 1 2 3 4 5
Function 1 (69.7%)
-5
-4
-3
-2
-1
0
1
2
3
4
5
6
Function 2 (18.2%)
Fig. 3 Discriminant analysis of the cuticular hydrocarbon profiles of the workers (W), the resident (R)
and the adopted (A) queens, before adoption (W1, R1 and A1), and 8 weeks after adoption (W3, R3 and
A3) in the experimental adoption 9. Ellipses represent 95% confidence limits. The percentages of variance
explained by each of the two discriminant functions are provided in parenthesis on the axis labels.
370 J Insect Behav (2009) 22:362–374
was short-term experiments (8 days only), which cannot exclude the possibility of
rejection at a later stage. For example, in Formica sanguinea out of ten queens
introduced, five were rejected immediately, but two more were killed 2 weeks after
adoption, and only three lasted long enough to be considered as successful adoptions
(Mori and Le Moli 1998). In the study presented here, both resident and adopted
E. tuberculatum queens behaved similarly even 2 months after adoption. This study
thus shows that short -term experimental queen adoptions can be performed to
accurately study secondary polygyny phenomenon, at least in E. tuberculatum.
Moreover, similar egg-laying rates of resident and adopted queens indicate that they
equally participated in reproduction. Furthermore equal egg-laying rates likely leads
to equal worker production since oophagy (i.e. egg eating) by queens or workers
does not exist in polygynous colonies from this population (Hora et al. 2005) and
workers do not show nepotistic queen care behavior (Zinck et al. 2009).
However, worker behavior towards the adopted queen differed from that towards
the resident queen. There was significantly greater grooming of the adopted
compared to the resident queens during the first week of adoption. But this subsided
in the eighth week post-adoption. Similar worker propensity to groom newly
introduced queens was also found in the facultative polygynous ant Myrmica
tahoensis (Evans 1996). The possibility that workers may have attempted to
homogenize colony odor after the introduction of a new queen in the colony (Crozier
and Dix 1979) was refuted by the chemical analyses. We attribute the increased
interest in the adopted queen to the novelty of its odor, and the decline in interest to
odor familiarization. Alternatively workers may have been attracted to the queen
specific substances as was shown for honeybees (Slessor et al. 1988; Katzav-
Gozansky et al. 2001), and the fire ant Solenopsis invicta (Vander Meer and Alonso
2002).
Queen chemical specificity is also supported by the chemical analyses. Workers
lacked completely heptacosane and had only minor amounts of nonacosane, the
queen’s major components. The discriminant analyses also revealed that worker and
queen clustering was according to caste not colony origin. Furthermore similar
chemical distances between workers and adopted or resident queens (in 3 over 4
experimental adoptions) also suggest the existence of a caste signature. Caste-
specific cuticular hydrocarbon profiles are rather common among social insects, and
Table 3 Mean Squared Mahalanobis Distance (MSMD±SE) Between Workers and Adopted (Qa) or
Resident (Qr) Queens for Each Experimental Adoption, Before The Adoption
Experimental adoption MSMD±SE Permutation test
Workers - Qa Workers - Qr
Adoption 7
a
19.1±9.0 23.1±9.6 ns
Adoption 8
a
30.3±9.4 133.2±25.3 0.008
Adoption 9 65.6±15.1 75.0±15.6 ns
Adoption 10 22.3±11.8 23.4±11.2 ns
a
indicate adoption experiments that failed
ns means not significant
J Insect Behav (2009) 22:362–374 371
in many species they are correlated with ovarian activity supporting their postulated
role as fertility signals (reviewed in Monnin 2006; Hefetz 2007; Le Conte and
Hefetz 2008). In E. tuberculatum mated and virgin queens show significant
differences in proportions of heptacosane and nonacosane that could allow worker
assessment of queen mated stat us (Hora et al. 2008). Our results on the stability of
adopted queen cuticular hydrocarbon profiles over time, in spite of numerous worker
grooming, therefore suggest that queen-specific cuticular hydrocarbon profile may
correspond to a reliable signal of queen’s fertility in E. tuberculatum.
Dyadic aggression tests and field experiments had revealed that E. tuberculatum
workers are characterized by an open recognition system (Zinck et al. 2008). Such
low insularity may explain the high rate of success (80%) of long-term adoptions of
alien completely unrelated queens (i.e. non-nestmate and unrelated). However as a
result of polydomy and limited queen dispersal (Zinck et al. 2007) E. tuberculatum
queens seeking adoption are likely to be related to the workers making the decision
to accept them or not in the colony. Workers may thus commonly accept any alien
queen presenting a signal of fertility, in order to avoid costly rejection errors (Reeve
1989). Moreover, even if adoption is of an unrelated female, the decrease in within-
nest relatedness may be outweighed by the benefits of increased colony development
(Rosengren and Pamilo 1983; Rissing et al. 1989). Indeed the presence of multiple
queens per colony allows it to reach larger colony size (e.g. Hora et al. 2005 ), which
can increase in turn colony productivity (Herbers 1984; Walin et al. 2001) especially
as genetic diversity among matrilines can increase division of labor efficiency
(Carlin et al. 1993; Blatrix et al. 2000). In E. tuberculatum, Hora et al (2005) showed
that polygynous colonies contain more workers than monogynous colonies and that
queen number is correlated with the number of worker. However, in polygynous
colonies, the authors did not find any correlation between queen number and colony
size, which suggests that queen adoption may not increase per capita productivity in
polygynous colonies. As a consequence, productivity benefits of polygyny would
not explain the acceptance of unrelated alien q ueens in some colonies of
E. tuberculatum, but one should keep in mind that in nature, queens seeking
adoption are expected to be related to some extent to the workers and resident
queens (discussed above). Finally, as it was postulated in F. truncorum by
Sundström (1997) queen adoptions, independently of the level of relatedness, likely
enhances the ability of the colony to reproduce by budding and thus to monopolize
the entire habitat. It is therefore possible that queen adoptions in E. tuberculatum
may have been favored because of its effects on maintaining ecological dominance
(Zinck et al. 2007).
Our results show that high queen acceptance threshold in E. tuberculatum
colonies generally lead to multiple-queen colonies and increased colony size (Hora
et al. 2005). High genetic viscosity and particular constraints of the mosaic of
arboreal ants that characterize Neotropical habitats likely favored secondary
polygyny in E. tuberculatum, facilitating ecological dominance (Zinck et al. 2007).
Here we propose that caste-specific cuticular hydrocarbon profiles which could
correspond to reliable signal of queen fertility may favor queen adoptions, while
colony-specific cuticular hydrocarbon profiles could rather result in higher rejection
rate and lower queen acceptance. As a consequence natural selection may have
selected for caste and fertility signaling rather than colony signature due to their
372 J Insect Behav (2009) 22:362–374
respective effects on queen adoptions and the consequences on E. tuberculatum
ecological dominance.
Acknowledgements L. Zinck received financial support from the French Ministry of Research and
Technology and R.R. Hora from CNPq, Brazil (3098552003-9). Research was permitted by the Brazilian
Minister of Science and Technology (licence 0107/2004).
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