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Absence of Nepotism in Worker–Queen Care in Polygynous
Colonies of the Ant Ectatomma tuberculatum
L. Zinck &N. Châline &P. Jaisson
Revised: 1 July 2008 / Accepted: 9 October 2008 /
Published online: 18 October 2008
#Springer Science + Business Media, LLC 2008
Abstract The question of the occurrence of nepotism in insect societies is central to
inclusive fitness theory. Here we investigated the existence of nepotism in the
facultative polygynous ant Ectatomma tuberculatum because various characteristics
of this species may have favored the evolution of nepotistic behavior toward queens.
We thus studied worker–queen care toward their mother queen vs. an unrelated
unfamiliar queen, to determine if workers cared preferentially for their mother.
Although we tried to facilitate the expression of nepotistic behaviors, we did not
detect significant nepotism confirming the general trend of an absence of nepotism
in social insects. We discuss about the specific causes that can explain the absence of
nepotism in E. tuberculatum regarding the particular social organization of this
species and its ecological dominance in the mosaic of arboreal ants.
Keywords Ants .nepotism .polygyny .queen care .grooming
Introduction
Kin selection is a major driving force that can explain the evolution of sociality and
cooperation among individuals. Inclusive fitness theory proposed for the first time a
framework to explain how the level of relatedness between individuals can
compensate the costs associated with altruism and influence the occurrence of social
behavior (Hamilton 1964). Social insects are particularly interesting models to study
altruism because the haplodiploidy which characterizes Hymenoptera can lead to high
levels of relatedness between individuals, as among full sisters for example. However,
insect colonies show a great variability in their social organization which results in
highly variable levels of relatedness among colony members. Polygyny (i.e. several
J Insect Behav (2009) 22:196–204
DOI 10.1007/s10905-008-9165-9
L. Zinck (*):N. Châline :P. Jaisson
Laboratoire d’Ethologie Expérimentale et Comparée UMR CNRS 7153, Université Paris 13,
99 avenue J.-B. Clément, 93430 Villetaneuse, France
e-mail: Lea.Zinck@leec.univ-paris13.fr
reproductive queens per colony) and polyandry (i.e. several mates per queen) typically
give rise to genetically distinct matrilines and patrilines respectively. According to kin
selection theory workers from these different maternal and paternal lines could
increase their inclusive fitness by attending preferentially more related queen or brood
(Châline et al. 2003; Osborne and Oldroyd 1999; Tarpy and Fletcher 1998;reviewed
in Tarpy et al. 2004).
However, the expression of such nepotism requires an ability to discriminate
between various levels of relatedness inside the colony. While kin recognition
appears to be common in the animal kingdom (Hepper 1991) it has not been clearly
shown to exist within colonies of social insects (Blatrix and Jaisson 2002; Breed et
al. 1994; Carlin et al. 1993; DeHeer and Ross 1997; Heinze et al. 1997; Kirchner and
Arnold 2001; Strassmann et al. 2000). However, ant recognition and discrimination
abilities are well developed since they can discriminate between neighbours and
strangers (Gordon 1989), between nestmates and non-nestmates (Vander Meer
and Morel 1998) and between nestmate queens on the basis of fertility (Ortius and
Heinze 1999) or even on the basis of individual traits (D’Ettorre and Heinze 2005).
Even in the absence of kin discrimination, preferential interactions among
individuals can also result from past familiarization or imprinting processes
(Isingrini et al. 1985; Jaisson 1973,1980). Nevertheless, kin discrimination appears
to be rare, apart from the particular case of inbreeding avoidance existing in the
Argentine ant Linepithema humile (Keller and Passera 1993). In fact, nepotism
appears to be generally absent in ants (Keller 1997). Even the only conclusive
evidence of nepotism found in polygynous colonies of Formica fusca (Hannonen
and Sundström 2003) has been recently questioned (Holzer et al. 2006). The broad
failure in detecting nepotism within social insect colonies was often due to
experimental problems. Indeed, biased interactions among individuals may have
resulted from the use of artificial colonies, non-neutral markers or inappropriate
statistical analysis (reviewed in Breed et al. 1994). Other natural phenomenon such
as genetically determined task specialization may have lead to mistaken conclusion
of nepotism (Châline et al. 2005; Oldroyd et al. 1991). Patriline and matriline
specializations are known to occur in relation to division of labour in honey bees (e.g.
Breed et al. 1990) and in ants (e.g. Blatrix et al. 2000). As a consequence preferential
interactions can take place among lineages in response to their task specializations
rather than to nepotism.
Here by analysing nepotism in individual worker behavior rather than in matriline
(i.e. one behavior per worker) (Châline et al. 2005; Gilley 2003), we prevented
confusion between matriline specialization and nepotism. Moreover, we investigated
the existence of nepotism in polygynous colonies of Ectatomma tuberculatum since
various characteristics of this species may have favored the evolution of nepotistic
behavior toward queens. First, facultative polygyny of E. tuberculatum, which
presents colonies that contain either one or several queens (Hora et al. 2005), is
associated with highly variable relatedness between nestmate workers, ranging from
r=0 to r=0.74 (Zinck et al. 2007). This high relatedness variance and the occurrence
of unrelated queen adoptions (Hora et al. 2005; Zinck et al. submitted) may have
therefore favored the evolution of kin recognition and discrimination. Second the
occurrence of polydomy with several spatially separated nests per colony (Zinck et
al. 2007,2008) also results in spatial separation of queens which could be associated
J Insect Behav (2009) 22:196–204 197
with nepotism. Since brood transport has never been observed (personal observa-
tion), larvae and callows probably cluster around their mother, and this could allow
early familiarization or imprinting processes independently of kin recognition ability
(Isingrini et al. 1985; Jaisson 1973,1980). Finally the absence of reproductive
hierarchy among queens in polygynous colonies of E. tuberculatum (Hora et al.
2005) prevents any influence of queen social status on worker behavior (Ortius and
Heinze 1999) and possible confusions between dominance rank and relatedness
effects in this study. We thus tested the existence of nepotism in E. tuberculatum by
setting-up artificial colonies where two queens and their corresponding matrilines
were unrelated and unfamiliar. To favor the expression of nepotistic behavior, queens
were also isolated in different nest chamber and only workers could move freely and
care preferentially for their mother. However, even in these optimal conditions for
reproductive competition we did not detect nepotism.
Materials and Methods
Colony Collection and Ant Maintenance
Twelve polygynous colonies of E. tuberculatum distant of at least 50 m were
collected in Bahia state, Brazil. In the laboratory, one queen per colony was isolated
in a plaster nest connected to an outside arena with 40–50 marked workers. They
were maintained at 28±2°C and 70±2% RH, and fed twice a week with frozen
crickets and honey. We waited for 6 months to allow the production of new workers
which were all daughters of the resident queen. Since E. tuberculatum queens mate
generally with a single male (Zinck et al. 2007) this isolation procedure resulted in
the production of a matriline of full sister workers for each queen. The 12 queens
and 20 young workers (i.e. from the same cohort) from each colony were
individually marked. Each queen and her daughters were anesthetized with carbon
dioxide (CO
2
), and paired with an alien queen and workers that had received the
same treatment. Paired queens were most likely unrelated because their original
colonies were distant of at least 50 m (Zinck et al. 2007), reflecting natural situations
of unrelated queen adoptions due to secondary polygyny (Hora et al. 2005). Both
matrilines and queens were set up in an experimental nest (n= 6) in which the two
queens were isolated in separated chambers while only workers were able to move in
the whole nest freely (Fig. 1).
Behavioral Study
Scan sampling observations of queen and worker behavior started 1-day after the
experimental set-up (Lehner 1996). During 3 weeks, a total of 198 scans per queen
were performed (n=2,376), with at least 45 min between two scans to ensure the
independence of the data. Queen oviposition behavior, workers present with the
queens and worker grooming behavior toward the queens were observed. Non-
parametric statistical analyses of the data were performed using StatXact-3.1. Paired
permutation tests (Good 2000) between pairs of queens (Queen 1 vs. Queen 2, or
Mother vs. Alien) were used to analyze both behavioral differences of workers
198 J Insect Behav (2009) 22:196–204
toward each queen over all colonies, and individual worker behavior toward each
queen among each matriline. Analyses of differences between queens in each colony
were conducted using Pearson chi-square exact tests and spearman’s correlation tests
were performed between the number of worker present around queens or the number
of grooming they received, and the number of eggs they laid.
Results
First, we did not observe any aggressive behavior either between matrilines or
between workers and alien queens. All the queens laid eggs (mean ± SE =8.7 ± 3.3)
and for all six colonies the queen laying the most eggs (mean±SE = 10.5 ± 2.5) did
not lay significantly more eggs than the queen egg-laying the least (mean ± SE = 6.8 ±
2.9) (Paired permutation test, P=0.063). However, analyses per colony still showed
significant differences in queen egg-laying rate (dyad 1: χ
2
=22.3, P=0.000; dyad 2:
Isolated
Queen 1
Isolated
Queen 2
Free workers
1 and 2
Free workers
1 and 2
Isolated
Queen 1
Isolated
Queen 2
Free workers
1 and 2
Free workers
1 and 2
Fig. 1 Top view of the experi-
mental nest allowing queen
isolation and workers moving
in the whole nest.
J Insect Behav (2009) 22:196–204 199
χ
2
=11.0, P=0.001, dyad 3: χ
2
=16.0, P=0.0001, dyad 4: χ
2
=3.7, P=0.070, dyad 5:
χ
2
=0.3, P=0.688, dyad 6: χ
2
=0, P=1). In all colonies queen eggs were
systematically carried by workers to a common chamber (Fig. 1) and settled in a
single egg pile. No egg eating (i.e. oophagy) by workers was observed.
Second, the analysis of queen care by workers along with queen fertility revealed
that the number of workers present around queens was significantly correlated with
the number of eggs laid by the queens (Rs= 0.75, N= 12, P=0.005) while the number
of worker grooming was not (Rs=−0.45, N= 12, P= 0.144). Workers tended to be
more present around one of the queens (Paired permutation tests P=0.063, Fig. 2a),
likely to be the most fertile. Workers also appear to groom significantly more one of
the queen compared to the other (Paired permutation tests P= 0.031, Fig. 2b).
Workers from both matrilines in some dyads actually attended significantly more one
of the queens which was more attractive than the other for workers (dyad 1, 4 and 5,
Table 1). While in all dyads workers of all matrilines were found to groom equally
both queens independently of kinship (Table 1).
Discussion
As queen care by workers is likely to enhance queen reproduction and thus the
indirect fitness of related workers, we could expect that nepotism occurs toward
workers’mother queens in polygynous colonies of E. tuberculatum. Indeed this
reproductive competition context might have favored the expression of nepotistic
behavior, as found in male rearing or worker manipulation of colony sex-ratios
(Ratnieks et al. 2006). However, we did not find any evidence of nepotism in queen
care by E. tuberculatum workers. Queens were either equally attended and groomed
by workers, or when one of them received more care it was not necessarily from her
0
200
400
600
800
1000
1200
1400
1600
1800
2000 NS
Queen p+ Queen p-
A
*
Queen g+ Queen g-
0
10
20
30
40
50
60
B
Fig. 2 a Mean number of workers around the most and the least surrounded queens (Queen p+ and p−
respectively) and bmean number of worker groomings toward the most and the least groomed queens
(Queen g+ and g−respectively). Bars show standard errors and levels of significance are indicated by
asterisk if P<0.05 and NS if Pis not significant.
200 J Insect Behav (2009) 22:196–204
daughters. Although we tried to facilitate the expression of nepotistic behaviors by
(1) rearing matrilines with their respective mother to allow a possible early
familiarization with the queen and queen odour learning by workers, (2) confronting
workers with a completely unrelated and unfamiliar queen against their familiar
mother and (3) setting-up experimental nests constraining queens to isolation which
may favor nepotistic behavior expression by workers, we did not detect any
significant nepotism in E. tuberculatum. Our results therefore confirm the general
trend of an absence of nepotism in social insects (Keller 1997; Ratnieks et al. 2006;
Wenseleers 2007) and leave unsolved the question of the existence of kin
recognition based on genetic cues (Carlin 1989; Grafen 1990).
A proximate explanation for the lack of nepotism in E. tuberculatum may be the
impossibility to discriminate between individuals on the basis of kin. This may result
either from the absence of genetic recognition cues, or from the absence of kin
discrimination by workers. As cuticular hydrocarbons were demonstrated to serve as
nestmate recognition cues (Bonavita-Cougourdan et al. 1987; Lahav et al. 1999;
Thomas et al. 1999; Wagner et al. 2000) we could expect them to provide genetic
recognition cues supporting kin recognition. However, cuticular hydrocarbon
differences among E. tuberculatum queens from different colonies are low (Zinck
et al. submitted). Within-nest cuticular hydrocarbon differences that could allow kin
discrimination in natural E. tuberculatum polygynous colonies may thus not exist. In
contrast, cuticular hydrocarbons were proposed to serve as reliable cues of ovarian
activity in E. tuberculatum (Zinck et al. submitted) as in numerous ant species
(Ayasse et al. 1995; Bonavita-Cougourdan et al. 1991; Cuvillier-Hot et al. 2001;
D’Ettorre et al. 2004; Liebig et al. 2000; Monnin et al. 1998). This role of cuticular
hydrocarbons is besides in agreement with our results of preferential worker–queen
attendance based on queen fertility, independently of kinship.
In fact, other social insects species also show low informative recognition cues
(Boomsma et al. 2003; Dani et al. 2004) suggesting that the evolution of kin
recognition cues may have been generally counter-selected. Such informational
constraint may be explained by the costs associated with nepotism evolution due to
Table 1 Mean Individual Worker Attendance and Grooming Toward Each Queen, Depending on
Matriline as Matriline 1 and 2 Are the Daughters of the Queen 1 and 2 Respectively
Mean worker presence PMean worker grooming P
Queen 1 Queen 2 Queen 1 Queen 2
Dyad 1 Matriline 1 24.1± 21.1 12.1 ± 8.7 0.010 1.3 ± 1.6 2.4± 1.7 ns
Matriline 2 25.8± 35.2 9.9 ±10.8 0.010 3.3 ± 2.8 1.4± 2.0 ns
Dyad 2 Matriline 1 18.3± 9.4 19.7 ±10.3 ns 2.1± 1.9 1.0 ±0.8 ns
Matriline 2 7.8± 10.1 6.0± 7.1 ns 2.3±3.8 0.8 ± 0.7 ns
Dyad 3 Matriline 1 11.7± 13.6 10.6 ±13.3 ns 1.9± 1.3 1.8 ±2.3 ns
Matriline 2 4.1± 4.5 12.6± 19.5 0.020 0.7± 0.7 1.0 ±0.5 ns
Dyad 4 Matriline 1 9.2± 11.0 64.7 ±55.4 0.000 1.4 ± 1.0 1.1± 1.1 ns
Matriline 2 4.0± 3.9 21.8± 27.9 0.002 1 ± 0.9 0.6±0.7 ns
Dyad 5 Matriline 1 21.2± 39.7 82.6 ±70.3 0.025 1.1 ± 2.3 2.2± 2.0 ns
Matriline 2 12.0 ± 14.0 41.0 ±47.2 0.018 0.8 ± 1.0 1.4± 1.3 ns
Dyad 6 Matriline 1 10.0± 11.5 1.3 ±1.2 ns 1.3± 0.8 1.0± 1.0 ns
Matriline 2 25.7 ± 48.5 24.9 ±47.2 ns 1.8± 2.2 1.3±2.1 ns
J Insect Behav (2009) 22:196–204 201
the existence of such cues. Indeed at the colony level nepotism can decrease overall
colony efficiency (Ratnieks and Reeve 1992) and errors of kin discrimination can
result in decreased inclusive fitness for all colony members (Keller 1997; Reeve
1989). Costs and constraints associated with nepotism can therefore dominate
relatedness effects and prevent the evolution of nepotism (Wenseleers 2007). In E.
tuberculatum the absence of kin discrimination likely plays an important role in its
social organization. Indeed it allows both the existence of polydomy and the
occurrence queen adoptions which are responsible of E. tuberculatum ecological
dominance in the mosaic of arboreal ants (Zinck et al. 2007,2008). Moreover the
strong population genetic structure of this species may have also favored mutualism
rather than nepotism evolution, because of (1) the lack of benefits of kin
discrimination among related individuals, and (2) low costs and high benefits of
caring related individuals (Zinck et al. 2007).
In conclusion, this study reveals that E. tuberculatum workers do not care
preferentially their mother compared to an alien queen, at least in our experimental
set-up. Our results thus support the general view that nepotism could have been
counter-selected in social insects due to possible costs and constraints at the colony
level (Keller 1997; Queller and Strassmann 2002; Tarpy et al. 2004). This does not
necessarily mean that inclusive fitness theory is mistaken. Indeed in certain contexts,
the evolution of nepotism may be restrained by costs and constraints outweighing
effects of relatedness (Wenseleers 2007). This appears to be particularly true in E.
tuberculatum in which the absence of discrimination is a key feature of its social
organization and its ecological dominance in the mosaic of arboreal ants (Zinck et al.
2007,2008).
Acknowledgments We thank R. R. Hora and the Laboratório de Mirmecologia, CEPEC/CEPLAC, de
Itabuna, Bahia, Brazil, for their great help in colony collection. Research was permitted by the Brazilian
Minister of Science and Technology (licence 0107/2004).
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