J Ethol (2011) 29:197–201
DOI 10.1007/s10164-010-0239-8
SHORT COMMUNICATION
Lethal sibling rivalry for nest inheritance among virgin ant queens
Jürgen Heinze • Matthias Weber
Received: 27 April 2010 / Accepted: 17 September 2010 / Published online: 7 October 2010
Ó Japan Ethological Society and Springer 2010
Abstract Fights among conspecific animals are normally
restricted to ritualized interactions. They may escalate to
serious injury and death when the contested resource has a
very high value and the chances of finding alternative
resources later in life are low. This appears to be the case in
young queens of the ant Cardiocondyla ‘‘latifrons’’, a
species that builds its nests in rather stable rock crevices.
Young queens in small colonies without a mature queen
fought violently for inheritance of the nest site and its
workers. Queen aggression and subsequent attacks by
workers killed about 50% of the young queens in our
experimental nests. Queen killing differs qualitatively from
previously reported dominance interactions among prospective female reproductives in other ants, which are
mostly ritualized and allow losers to pursue alternative
ways of increasing their direct or indirect fitness. Our
observations add a novel case of siblicide to the previously
reported lethal aggression among nestling birds, parasitoid
larvae, and honey bee queens. They corroborate the
hypothesis that relatedness does not play a significant role
in local competition for highly limited resources.
Keywords Cardiocondyla Siblicide Fatal fighting Nest inheritance Local resource competition
Introduction
Aggression among conspecific animals is usually restricted
to ritualized interactions or sham attacks and rarely leads to
J. Heinze (&) M. Weber
Biologie I, Universität Regensburg,
93040 Regensburg, Germany
e-mail: juergen.heinze@biologie.uni-regensburg.de
serious injury or death. Fatal fighting may evolve when the
contestants differ greatly in fighting strength and the risks
of being injured are negligible for the individual that
escalates the fight, as in the case of infanticide or coalitionary killing (e.g., Hrdy 1979; Wrangham 1999). Furthermore, fatal fighting can be stable in evolution when
individuals competing for a resource cannot expect to find
an alternative resource later in life (Enquist and Leimar
1990). For example, wingless fig wasp males engage in
lethal combat for mating chances (Cook et al. 1997),
nestling birds conduct siblicide to obtain greater shares of
parental investment (Rodrı́guez-Gironés 1996), and the
larvae of parasitoid wasps kill one another to monopolize
consumption of the host they live in (Pexton and Mayhew
2002). Ants provide another classical example of fatal
fighting. Directly after mating, young, unrelated queens
may cooperate to jointly start a new colony (‘‘pleometrosis’’). This mutual aid usually comes to an end once first
workers have emerged, and the number of nestmate queens
is quickly reduced to one through deadly fighting among
the queens or aggression from the workers (e.g., Bernasconi and Strassmann 1999). In contrast, related queens in
mature colonies rarely engage in overt aggression (e.g.,
Keller 1995). Prospective reproductives, queens and, in
some species, totipotent workers, may establish rank orders
by means of ritualized antennal boxing and biting (e.g.,
Heinze and Smith 1990; Ito and Higashi 1991; Monnin and
Peeters 1999; Tsuji et al. 1999; Heinze 2004). Such contests do not normally result in death or severe injuries, but
subordinates instead emigrate to start their own colony
away from the maternal nest or stay in the nest to help or,
as hopeful reproductives, to later replace the dominant
(e.g., Heinze and Oberstadt 2003).
Here, we report on fatal fighting among related, virgin
queens for the inheritance of their natal nest and its work
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force. The small colonies of the southeast Asian ant Cardiocondyla ‘‘latifrons’’ (provisional name; species to be
described by B. Seifert) usually consist of a few dozen
workers (Yamauchi et al. 2007; S. Frohschammer, personal
communication) and one or several queens. The wingless
males of this species locally compete for access to young
virgin queens in their natal nests. The first male to emerge
from the brood usually kills all younger rivals and
monopolizes matings for several months (Yamauchi et al.
2006). Mother queens are therefore selected to produce
sons earlier than other queens in the nest. This has led to a
peculiar reversal of the usual sequence of reproduction in
insect societies, in that males are among the first individuals to emerge in freshly founded multi-queen societies
(Yamauchi et al. 2006). In addition, in medium-sized colonies, adult nestmate queens establish social and reproductive hierarchies by biting and antennal boxing
(Yamauchi et al. 2007).
Cardiocondyla ‘‘latifrons’’ inhabits nest sites, such as
rock crevices, which are rather stable but limited. An
established nest is therefore a highly valuable resource. We
hypothesized that virgin queens compete for the inheritance of the nest after the death of their mother(s) and that
this competition is particularly strong in small colonies
with a low ‘‘queen carrying capacity.’’ As preliminary
observations suggested some aggression among virgin
queens (Yamauchi et al. 2007), we conducted a more
thorough analysis of their behavior in queenless colonies.
Materials and methods
Cardiocondyla ‘‘latifrons’’ is one of several species of the
C. ‘‘argentea’’ species complex (names in quotation marks
refer to recognized morphospecies that are currently
described by B. Seifert. These names are taxonomically
invalid according to the rules of the ICZN). Ants ascribed
to C. ‘‘latifrons’’ occur in large areas of southeast Asia,
including Malaysia, Indonesia, and the Philippines. Colonies used for this study were collected in June 2007 by
A. Schulz and S. Frohschammer near Kuching, Sarawak,
Malaysia. They originally contained one to several queens,
but because of lethal fighting among males (Yamauchi
et al. 2006) all offspring in a multi-queen colony is normally fathered by the same male. Virgin queens produced
by multi-queen colonies are therefore usually related at
least by sharing the genes of their father.
In the laboratory, individual colonies were housed as
previously described (e.g., Heinze et al. 1998) in plastic
boxes with a plaster floor in incubators with 14 h 28°C/
10 h 21°C temperature rhythms. Droplets of honey and
pieces of cockroaches were provided three times per week.
We choose a small size for our experimental colonies (10
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workers) reflecting the lower end of the range of natural
colony sizes (n = 21, worker number, median, quartiles
20, 6, 40; queen number 3, 1, 10). The number of queens in
natural colonies is significantly correlated with worker
number (Spearman’s rank correlation, rS = 0.678, p \ 0.001;
S. Frohschammer, personal communication), and colonies
with 20 workers or fewer normally have only a single
queen. We therefore set up two different types of experimental colonies consisting each of ten larvae, ten workers,
a pupa of a wingless male and four pupae of virgin queens,
all from the same stock colony. In series A (n = 5), pupae
of virgin queens were of similar age and eclosed to
adulthood on the same day; in series B (n = 7), pupae were
chosen in a way that they eclosed on successive days (two
colonies contained only three pupae each). This allowed
the determining of whether the order of emergence influences fighting. Queens were individually marked by tarsal
clipping (Hagler and Jackson 2003; Holehouse et al. 2003).
Queens that died in colonies of series B were replaced by a
new virgin queen pupa. Workers which died or escaped
from the nest box were replaced by new worker pupae from
the stock colonies. Behavior of all queens was observed
under a binocular microscope three times per day for
10 min each. The location of queens (outside of nest, in
nest away from brood, on the edge of the brood pile, on the
brood pile) and aggressive and sociopositive behavior
involving queens were recorded. Observations were
conducted as long as colonies contained three or more
queens for up to 25 days.
As data were not normally distributed and variances
were unequal, we compared samples by permutation tests
(10000 permutations). Significance values for Wilcoxon
matched pairs tests were estimated using a Monte Carlo
method with 100000 random assignments of values to
columns. All analyses were conducted using the software
PAST 1.75b (Hammer et al. 2001).
Results
In all 12 experimental colonies, virgin queens engaged in
aggressive interactions. Aggression consisted mostly of
violent antennal boxing, e.g., one individual rapidly
drummed its antennae over the head of an opponent. Other
types of aggression observed were biting, threatening with
opened mandibles, and stepping onto an opponent. In total,
we observed 1189 acts of aggression. The level of
aggressiveness differed tremendously among experimental
colonies and individual queens, from 0 to 0.6 attacks/min.
Over all colonies, queens differed highly in activity, and
queens that were active in attacking also received more
attacks from other queens (Fig. 1; Spearman’s rank correlation, total attacks: rs = 0.710, p \ 0.001; attacks per
J Ethol (2011) 29:197–201
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Fig. 1 Correlation between the total number of aggressive acts
initiated and the total number of aggressive acts received by virgin
queens of Cardiocondyla ‘‘latifrons’’ during the total observation time
(for details, see text)
Fig. 2 Median (squares) and quartiles (whiskers) of the frequency of
different types of aggression initiated by virgin queens of Cardiocondyla ‘‘latifrons’’ in experimental colonies of series A (queens of
same age, black squares) and series B (queens differ in age, white
squares; for details, see text)
minute: rs = 0.431, p \ 0.002). The frequency of aggressive interactions per min observation did not differ between
queens of the same age (series A, n = 20) and queens of
different age (series B, n = 29, permutation tests: antennation, p = 0.327; biting, p = 0.839; mandible threat,
p = 0.240, stepping onto opponent, p = 0.595). There was
a marginally significant trend for aggression among queens
of series A to be more often ritualized (fraction of antennal
boxing in total aggression per queen, median, quartiles,
range 0.42, 0, 0.57, 0–0.65) than among queens of series B
(median, quartiles, range 0, 0, 0.35; 0–0.78; permutation
test, p = 0.10; Fig. 2).
In both series, fights frequently escalated to biting,
which resulted in injuries and death (fraction of biting in
total aggression per queen, median, quartiles, range; A: 0,
0, 0.13, 0–1; B: 0, 0, 0.14; 0–0.74; permutation test,
p = 0.63). In series A, 12 of 20 queens were killed, in
series B 10 of 29 (Yates corrected v2 = 1.51, p = 0.22).
One additional queen of series B died during the experiment, but we did not observe it being attacked. Killed
queens (n = 23) and surviving queens (n = 26) differed
neither in their aggressiveness (permutation tests, all four
categories of aggression, p [ 0.4) nor in the number of
queen attacks received per minute (all four categories of
aggression, p [ 0.2). Severe fighting among queens occasionally lead to the participation of workers in queen killing (series A: 4 of 12 killings; series B: 5 of 11 killings).
Queens that were killed received on average significantly
more aggression from workers than queens that survived
(killed queens, attacks per min., median, quartiles 0.063,
0.025, 0.156; surviving queens 0.058, 0.025, 0.108; permutation test, p \ 0.001). In series B, the order of emergence did not consistently affect the outcome of aggression
(3 of 7 oldest and 5 of 8 youngest queens were killed). The
oldest and youngest queens did not differ significantly in
respect of aggression, except that the oldest queens more
frequently stepped onto other queens (Wilcoxon matched
pairs test, p = 0.031), while the youngest queens were
more frequently stepped onto (p = 0.062). However, these
results are not significant after Bonferroni correction for
multiple tests.
Aggression did not cause attacked queens to flee from
the nest. In contrast, a detailed analysis of the whereabouts
of queens showed that five queens in series A and eight
queens in series B were killed without ever being observed
outside the nest. Queens stayed on or near the brood pile
and left the nest only for maximally 8.3% of the observation time (median, quartiles: 0, 0, 0.4%). Queen killing
therefore is not an artefact of our experimental design not
allowing attacked queens to disperse far from the nest.
Queens only infrequently engaged in sociopositive
interactions with other queens. In total, we observed only
106 cases of one queen grooming another. Queens that were
most aggressive also engaged most frequently in grooming
(Spearman’s rank correlation, rS = 0.647, p \ 0.001), and
queens that were most frequently attacked were also
groomed most often by other queens (rS = 0.393, p =
0.005), but not by workers (rS = 0.197, p = 0.174).
Despite the fighting, all queens were courted by males.
Active queens, i.e., those that were more frequently
involved in aggression, had significantly more contact with
males than queens with lower activity levels (rS = 0.695,
p \ 0.001). Mating and egg laying did not protect queens
from being killed: two of six queens, which were observed
copulating, and one of two queens, which were observed
laying eggs, were killed.
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Discussion
Our study documents that virgin queens in small colonies
of Cardiocondyla ‘‘latifrons’’ engage in aggressive competition for inheritance of the natal nest. Aggression frequently escalates to fatal fighting, and 23 of 49 of the
queens were killed during the experiment. Given that the
species nests in rather stable rock crevices, which, however, are often too small to harbor very large colonies with
multiple queens, our observations corroborate predictions
from ESS models that fatal fighting can evolve when a
resource has a very high value (Enquist and Leimar 1990).
An established nest and workforce appears to be such a
highly valuable resource.
On a first glance, fatal fighting in C. ‘‘latifrons’’
resembles the regulation of queen number in multi-queen
founding colonies of other ants, where unrelated queens
fight for the exclusive possession of the nest (e.g.,
Bernasconi and Strassmann 1999). Our finding differs from
these previously reported cases of queen aggression in that
competing queens in C. ‘‘latifrons’’ are usually close relatives. Queen killing in C. ‘‘latifrons’’ therefore constitutes
a special case of siblicide not yet described from ants. It
matches the situation in honeybee colonies after a mother
queen and part of her workers have left the nest to found a
new society during swarming. Virgin honeybee queens
may secure the possession of the hive and its workers by
killing other virgin queens (Gilley 2001; Tarpy and Gilley
2004).
Queen killing is qualitatively different from previously
reported cases of kin conflict in insect societies, in which
prospective reproductives compete for egg laying rights by
ritualized dominance interactions (reviewed in Heinze
2004). The losers of such fights usually survive. They may
pursue alternative ways of increasing their fitness, either
directly by emigrating from the natal nest and founding an
own society (e.g., Heinze and Smith 1990) or by staying as
hopeful reproductives and later replacing the dominant, or
indirectly by helping (e.g., Heinze and Oberstadt 2003).
Obviously, defeated queens of C. ‘‘latifrons’’ and honeybees and subordinate, surplus queens that are policed by
workers, as in Leptothorax muscorum (Lipski et al. 1992),
Linepithema humile (Keller et al. 1989) or Aphaenogaster
senilis (Chéron et al. 2009; Cronin and Monnin 2009), do
not have such options.
Interestingly, the order of eclosion of queens did not
strongly affect the outcome of interactions. This is very
different from interactions among C. ‘‘latifrons’’ males
(Yamauchi et al. 2006) or virgin queens of Aphaenogaster
senilis (Chéron et al. 2009; Cronin and Monnin 2009). This
might be explained by the small difference of age (1 day)
among queens in series B. A larger time lag between
queens might have given the first emerging queen a more
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significant head start by allowing it to fully sclerotize its
cuticula.
By eliminating other queens, virgin queens of C. ‘‘latifrons’’ not only gain the nest and its workers but in addition
alleviate the intensity of male–male competition for their
sons. Like in other species of Cardiocondyla, wingless
males fight to monopolize access to virgin queens within
their natal nests (Kinomura and Yamauchi 1987; Yamauchi
et al. 2006). The male eclosing first usually kills all rival
males, which later emerge from the brood. In agreement
with local mate competition theory (Hamilton 1967),
queens produce a highly female-biased sex ratio when they
are the only reproductive in the nest, but rear many more
males from unfertilized eggs in the presence of other
queens (Cremer and Heinze 2002). Eliminating rival
queens thus decreases male–male conflict and reduces the
investment in males, most of which are later killed anyway.
Note that the occurrence of fatal fighting among closely
related females is not in conflict with kin selection theory.
In contrast, it matches predictions that the intensity of
fighting at a local scale is independent of relatedness (e.g.,
West et al. 2001).
Acknowledgments Supported by DFG (He 1623/22). We thank
K. Yamauchi, R. Hashim, S. Frohschammer, and A. Schulz for
providing colonies of C. ‘‘latifrons,’’ B. Seifert for species determination and A. Schrempf for valuable comments on the manuscript.
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