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Absence of Nepotism in Worker–Queen Care in Polygynous Colonies of the Ant Ectatomma tuberculatum

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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.
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Absence of Nepotism in WorkerQueen 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 workerqueen 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) 22:196204
DOI 10.1007/s10905-008-9165-9
L. Zinck (*):N. Châline :P. Jaisson
Laboratoire dEthologie 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 (DEttorre 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) 22:196204 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 4050 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) 22:196204
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 spearmans 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) 22:196204 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
workersmother 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 grespectively). 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) 22:196204
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;
DEttorre 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 workerqueen
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) 22:196204 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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... Nepotism could not be shown in many social insect species, for instance Nasutitermes corniger (Atkinson et al. 2008), various ant species (Tsuji & Ito 1986;Keller 1997;Zinck et al. 2009;Kellner & Heinze 2011), and Apis mellifera (Rangel et al. 2009). The reason might be that group-level costs of nepotism (Ratnieks & Reeve 1992) and the risks of errors of KD can result in decreased inclusive fitness for all colony members (Keller 1997;Reeve 1989). ...
... Although nepotism is lacking in many social insect species (Keller 1997;Atkinson et al. 2008;Rangel et al. 2009;Zinck et al. 2009;Kellner & Heinze 2011) we found KD in C. ...
... full-sisters) or less-highly related kin (e.g. half-sisters) [56][57][58][59][60]. First, this was puzzling, because one might think that selection would favour operators (e.g. ...
Article
Many animals are able to perform recognition feats that astound us—such as a rodent recognizing kin it has never met. Yet in other contexts, animals appear clueless as when reed warblers rear cuckoo chicks that bear no resemblance to their own species. Failures of recognition when it would seem adaptive have been especially puzzling. Here, we present a simple tug-of-war game theory model examining how individuals should optimally invest in affecting the accuracy of discrimination between desirable and undesirable recipients. In the game, discriminating individuals (operators) and desirable and undesirable recipients (targets and mimics, respectively) can all invest effort into their own preferred outcome. We demonstrate that stable inaccurate recognition will arise when undesirable recipients have large fitness gains from inaccurate recognition relative to the pay-offs that the other two parties receive from accurate recognition. The probability of accurate recognition is often determined by just the relative pay-offs to the desirable and undesirable recipients, rather than to the discriminator. Our results provide a new lens on long-standing puzzles including a lack of nepotism in social insect colonies, tolerance of brood parasites and male birds caring for extra-pair young in their nests, which our model suggests should often lack accurate discrimination. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests'.
... Queen number has also been shown to negatively affect aggression levels toward non-nestmates (Starks, Watson, Dipaola, & Dipaola, 2010), which perhaps suggests a lower threshold of recognition cues in such high-polygynous nests. Indeed, to date the hypothesis of positive nepotism in eusocial insects, specifically in ants, has mostly been refuted (DeHeer & Ross, 1997;Friend & Bourke, 2012;Holzer, Kummerli, Keller, & Chapuisat, 2006;Zinck, Châline, & Jaisson, 2009), except for Formica fusca (Hannonen & Sundström, 2003), but see the criticism by Holzer, Kummerli, et al. (2006); e.g., selective brood mortality rather than preferential brood rearing), and Leptothorax acervorum ants (Gill & Hammond, 2011). Boomsma and d'Ettorre (2013) suggested that within-colony kin discrimination might be maintained in a secondary polygyny where there are a high queen turnover and fluctuating relatedness in the colony. ...
Article
Insect societies headed by multiple queens (polygyny) raise evolutionary questions, such as how does genetic heterogeneity among colony members affect in‐nest interactions; or, are all queens equally reproductive or equally treated by workers? Answering such questions requires intensive and continuous observations of in‐nest behavior. Here, we addressed these questions in the polygyne supercolonial ant, Cataglyphis niger, using a barcoding system that enables the tracking of individual interactions, together with polymorphic DNA microsatellite markers that indicate the matriline and patriline of all individuals. Our findings that both queens and workers have low interrelatedness corroborate earlier reports regarding the supercolony structure of C. niger. Ovary inspection and worker genotyping revealed that all the queens contribute similarly to nest demography. Tracking positions of individual workers through time revealed that only a small proportion of them are constantly engaged in tending the queens and can be considered as retinue workers. However, genotyping these workers and the attended queens revealed no relationship to genetic relatedness, again typical of a true polygyne and supercolonial species. Unlike invasive supercolonial species, C. niger is native to Israel, enabling us to address questions regarding the driving forces, other than kin selection, that stabilize this society.
... 64 Additionally, in most cases relatedness in these polygyne nests is low thus 65 questioning the benefits of inclusive fitness theory at all in these cases. In fact, so far 66 nepotism in eusocial insects, specifically in ants has been mostly rejected ((DeHeer 67 and Ross, 1997;Zinck, Châline and Jaisson, 2009;Friend and Bourke, 2012), except 68 . CC-BY-NC-ND 4.0 International license It is made available under a (which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. ...
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The basic ant colony structure is presumed to have evolved trough kin selection. However, ants show a remarkable diversity in social organizations from a monogynous and monoandrous queen to the more derived states of polygyny with polyandrous queens. It is not clear whether kin selection can still explain these derived societies. The existence of polygyny is still an evolutionary enigma since kin selection theory predicts that queens should thrive for reproductive monopoly on the one hand, and workers are predicted to favor their own matriline in rearing gynes, on the other hand. Using a Quick Response (QR) - barcoding system that allows tracking individual queens and workers interactions, along with polymorphic DNA microsatellite markers indicating the matriline and patriline of each worker in the nest, we demonstrate the complex social interactions in polygyne nests of Cataglyphis niger . C. niger is not only polygyne but constitute a supercolony in the study site. Our findings that both the residing queens and the workers in the nest are not necessarily related to each other, are first for this species, support the supercolony structure of the population. Also in line with such a social structure, we demonstrate that they contribute equally to the nest production and rearing of the queens. Unlike invasive supercolonial species, C. niger is native in Israel, raising questions about the driving forces that stabilize this society, apart from kin selection.
... The question of nepotism in eusocial insect colonies has been addressed in other species, as well. Several studies of ants have noted an absence of nepotistic behavior within colonies (Zinck et al. 2009;Kellner and Heinze 2011;Friend and Bourke 2012). In eusocial wasps the chemical information necessary for discrimations that would support nepotism is available, at least in some species (Dani et al. 2004) and data suggests that this information can be used in Polistes dominulus (Leadbeater et al. 2014). ...
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This review summarizes and evaluates the available information on honeybee nestmate recognition. Nestmate recognition is the ability of members of a colony to discriminate members of their own colony from others, particularly conspecifics, trying to enter the nest. Honeybee nestmate recognition is mediated by chemical cues that bees gain after emergence as adults. The comb wax in the nest is an important intermediary for transfer of cues among bees in the colony, resulting in a relatively uniform recognition profile which is carried by workers in the colony. Alkenes and free fatty acids are the primary chemical cues in the recognition profile. The ability of honeybees to discriminate nestmates from non-nestmates has raised the question of whether recognition mechanisms might exist to support nepotism within colonies. A variety of experimental approaches have failed to generate support for preferential behavior among highly related subgroups of bees in honeybee colonies. Other questions addressed in this review include queen recognition, response thresholds for expression of recognition, and sensory and information gathering aspects of the recognition system of honeybees. Nestmate recognition in honeybees is a valuable model system for the study of social recognition in animals.
... The improvement of molecular techniques since the early 1990s has allowed studies of within-colony kin discrimination that avoid many of the difficulties associated with earlier experiments. However, the majority of recent studies have found within-colony kin discrimination to be absent in the social insects, despite investigating a number of different social contexts, including adult-adult interactions, such as worker interactions with nestmate queens in polygynous colonies (DeHeer & Ross 1997;Strassmann et al. 1997;Blatrix et al. 2000;Kirchner & Arnold 2001;Gilley 2003;Châline et al. 2005;Atkinson et al. 2008;Zinck et al. 2009), adult-brood interactions (Strassmann et al. 2000;Blatrix & Jaisson 2002;Holzer et al. 2006), colony fission (Heinze et al. 1997a;Kryger & Moritz 1997;Rangel et al. 2009) and inbreeding avoidance (Keller & Fournier 2002). A few recent studies have detected within-colony kin discrimination in social insects, in the context of, for example, adult-adult interactions (Tarpy & Fletcher 1998;Adams & Balas 1999), adult-brood interactions (Osborne & Oldroyd 1999;Hannonen & Sundström 2003) and colony fission (Seppä et al. 2008). ...
... As Ratnieks and Visscher (1989) pointed out, worker policing can destroy much of the evidence for kin-biased behaviour. Negative results in tests for fine-tuned, within-colony nepotism apply to other social insects as well, such as the ant Platythyrea punctata (Kellner & Heinze, 2011), the ant Ectatomma tuberculatum (Zinck, Chaline, & Jaisson, 2009), and the termite Nasutitermes corniger (Atkinson, Teschendorf, & Adams, 2008). In a minority of published studies evidence for relatedness effects have been found, such as foreign queens having lower reproductive value in ants (Holzer, Chapuisat, & Keller, 2008). ...
Article
Kin selection stands among W. D. Hamilton's most influential ideas. The purpose of this review is to assess the impact of Hamilton's ideas about kin selection on studies of social recognition. Kin selection theory predicts that animals should direct aid-giving behaviour to closely related animals, provided that a positive net benefit in inclusive fitness is achieved from the altruistic act. Kin recognition is the key proximate mechanism by which animals can sort more related from less related interactants in a population. Kin recognition also has the potential to allow fine distinctions among animals based on identity by descent. Following the publications of Hamilton's 1964 papers on kin selection, studies of kin recognition focused on four disparate behavioural contexts: identification of group membership, inbreeding avoidance, alarm calls and other forms of aid-giving, and parent–offspring interactions. Investigations of eusocial insects have focused on identification of group membership by phenotypes that are shared among all members of a colony. In birds and mammals, social structure is often based on individual recognition. Some species, particularly rodents, have the ability to make discriminations based on relatedness among animals that they have not previously met. Future studies of kin recognition should be less reliant on assumptions that all forms of societal closure are due to factors related to kin selection. These studies should acknowledge that the role of individual recognition in vertebrate societies is key to understanding the full texture of social interactions, and that individual recognition may be equally important in many other types of animals. Of particular interest will be the discovery of how information about kinship is integrated with information about individual identity.
... This is because clear kin recognition cues should lead to costly conflict between different patrilines where workers may try to ensure the propagation of their genes at the expense of other patrilines. Nepotistic behavior is assumed to be costly at the colony level , and accordingly no definitive evidence for nepotism has been forthcoming (Châline et al. 2005a;Zinck et al. 2009). Both this hypothesis and the available evidence suggest that genetically determined kin discrimination is unlikely to be found in social insects, while many consider that colony nestmate recognition in social insects is wholly mediated by environmentally acquired chemical cues that would overwhelm any genetic signals that might be exploited for nepotistic ends (Sorvari et al. 2008). ...
Article
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Chemical recognition cues are used to discriminate among species, con-specifics, and potentially between patrilines in social insect colonies. There is an ongoing debate about the possible persistence of patriline cues despite evidence for the mixing of colony odors via a "gestalt" mechanism in social insects, because patriline recognition could lead to nepotism. We analyzed the variation in recognition cues (cuticular hydrocarbons) with different mating frequencies or queen numbers in 688 Formica exsecta ants from 76 colonies. We found no increase in the profile variance as genetic diversity increased, indicating that patriline effects were absent or possibly obscured by a gestalt mechanism. We then demonstrated that an isolated individual's profile changed considerably relative to their colony profile, before stabilizing after 5 days. We used these isolated individuals to eliminate the masking effects of the gestalt mechanism, and we detected a weak but statistically significant patriline effect in isolated adult workers and also in newly emerged callow workers. Thus, our evidence suggests that genetic variation in the cuticular hydrocarbon profile of F. exsecta ants (n-alkanes and alkenes) resulted in differences among patrilines, but they were obscured in the colony environment, thereby avoiding costly nepotistic behaviors.
... Several social insects have been shown to indirectly recognize the overall genetic structure of the society they live in and adaptively respond to it, e.g., in sex allocation (Boomsma et al. 2003; Hannonen & Sundströ m 2003) and facultative policing in a wasp species (Foster & Ratnieks 2000) and a leaf-cutting ant (Dijikstra et al. 2010 ). In contrast , unambiguous direct evidence for nepotism has so far only been found in drywood termites (Korb 2006), whereas evidence for the absence of nepotism has been found in numerous species (DeHeer & Ross 1997; Keller 1997; Holzer et al. 2006; Ratnieks et al. 2006; Goodisman et al. 2007; Atkinson et al. 2008; Zinck et al. 2009). If nepotistic behavior was present in the parthenogenetic ponerine ant P. punctata, we would expect a) workers of P. punctata in fused colonies compete more intensively for replacement of a removed reproductive and b) that worker policing against surplus reproductives is predominantly directed against unrelated nestmates. ...
Article
Insect societies are normally closed entities from which alien individuals are excluded. The occasional fusion of unrelated colonies of the thelytokous ant Platythyrea punctata is therefore puzzling, because it strongly intensifies competition among nestmates for the replacement of an old reproductive. Most colonies of P. punctata have only one or few reproductives, which produce female offspring from unfertilized eggs, and therefore have a clonal structure. Fusion leads to multi-clone colonies. We compared the occurrence of dominance and policing behavior between single- and double-clone colonies. We find that the frequency of aggression is higher in double-clone colonies, but that individuals do not preferentially direct attacks toward non-clonemates. This matches observations in other species that social insects perceive genetic homogeneity but are not capable of reliable discrimination among nestmates of different degree of relatedness.
Article
Inclusive fitness theory predicts that, other things equal, individuals within social groups should direct altruistic behaviour towards their most highly related group‐mates to maximise indirect fitness benefits. In the social insects, most previous studies have shown that within‐colony kin discrimination (nepotism) is absent or weak. However, the number of studies that have investigated within‐colony kin discrimination at the level of individual behaviour remains relatively small. We tested for within‐colony kin discrimination in the facultatively multiple‐queen (polygynous) ant, Leptothorax acervorum. Specifically, we tested whether workers within polygynous colonies treated queens differently as a function of their relatedness to them. Colonies containing two egg‐laying queens were filmed to measure the rate at which individually marked workers antennated and groomed or fed each queen. Relatedness between individual queens and workers was calculated from their genotypes at four microsatellite loci. The results showed there were no differences in the rates at which workers antennated or groomed/fed their more related queen and their less related queen. Workers interacted preferentially with their potential mother queen with respect to grooming/feeding but not with respect to antennation. However, because of high queen turnover, the frequency of adult workers with their potential mother queen still present within the colony was relatively low. Overall, therefore, we found no evidence for within‐colony kin discrimination in the context of the average worker's treatment of queens in polygynous L. acervorum colonies.
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Considers kin recognition systems as vehicles of social communication, and reviews 1) the contexts of kin recognition (parental care, especially in salamanders, schooling behaviour of tadpoles, territoriality and mating); 2) mechanisms of kin recognition, with emphasis on ontogeny and examination of sensory mechanisms; and 3) functional approaches to kin recognition (growth and development, responses to predators, and inbreeding and optimal outbreeding). -P.J.Jarvis
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Both behavioral and chemical analyses demonstrated that in the ant Camponotus vagus the colony recognition signal is strongly correlated with the composition of cuticular hydrocarbons. Variation of relative proportions of dimethylalkanes characterize the chemical signatures in different colonies.
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Primitive ant societies, with their relatively simple social structure, provide an opportunity to explore the evolution of chemical communication, in particular of mechanisms underlying within-colony discrimination. In the same colony, slight differences in individual odours can be the basis for discrimination between different castes, classes of age and social status. There is some evidence from correlative studies that such inter-individual variation is associated with differences in reproductive status, but direct proof that certain chemical compounds are detected and recognized by ants is still lacking. In the ponerine ant Pachycondyla inversa , fertile queens and, in orphaned colonies, dominant egg-laying workers are characterized by the predominance of a branched hydrocarbon, 3,11-dimethylheptacosane (3,11-diMeC27) on the cuticle. Using electroanntennography and gas chromatography with electroantennographic detection, we show that the antennae of P. inversa workers react to this key compound. 3,11-diMeC27 is correlated with ovarian activity and, because it is detected, is likely to assume the role of a fertility signal reflecting the quality of the sender.
Article
Kinship theory implies that individual social Hymenoptera should be able to identify kin. We tested kin discrimination in the polygynous ponerine ant Gnamptogenys striatula. Mate choice experiments showed that individuals did not pair according to kinship. Experiments on matriline discrimination revealed that workers did not preferentially groom, transport (after nest disturbance) or cannibalize (after starvation) larvae on the basis of kin, when both related and unrelated larvae were present. These results show the absence of kin discrimination for the criteria and experimental conditions used. The lack of kin discrimination during mate choice in G.striatula can be explained by male dispersion and female philopatry, which reduces the likelihood of mating between siblings and of kin-based mate choice reflected in incest avoidance. The lack of matriline discrimination by workers may reflect permanent intracolony mutualism or the high cost of discrimination. Finally, it appears that the absence of kin discrimination in such contexts in G.striatula is not incompatible with kinship theory and may have been secondarily selected during social evolution. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.
Article
Differential treatment of conspecifics (eg kin recognition) has 3 components. 1) The production component refers to the nature of the cues used by an individual (actor) to discriminate among classes of conspecifics (recipients) differing in their effects on the actor's fitness. 2) The perception component refers both to the internal template against which the actor matches these cues and to the matching algorithm that allows classification of a recipient. The action component refers to the determinants of an action taken by an actor that has calculated a particular degree of similarity between its internal template and a recipient's phenotype. The author attempts to provide a theory of the action component of conspecific discrimination, in particular, examining the factors that determine the optimal or evolutionarily stable acceptance threshold, ie the level of dissimilarity between the actor's template and the recipient's phenotype below which recipients are accepted and above which recipients are rejected. Analyses of 6 different classes of recognition contexts show how the optimal or evolutionarily stable acceptance threshold is a function of the relative frequencies of interaction with the different classes of recipients, of the fitness consequences of accepting or rejecting different classes of recipients, and of the ways in which the latter fitness consequences combine. -from Author
Article
Although kinship discrimination and nepotism have been extensively investigated in honeybees, Apis mellifera L., the significance of kin discrimination among worker bees is still unclear. One of the behavioural contexts in which nepotistic behaviour of worker bees has been described is the dance communication system: bees were reported to have a strong tendency to dance with their supersisters in colonies consisting of only two subfamilies. Using molecular markers, we reinvestigated this apparent case of nepotism. We found no evidence for subfamily discrimination among dancers and their followers in a colony consisting of only two subfamilies or in a colony consisting of 17 subfamilies.