doi:10.1111/j.1420-9101.2004.00832.x
Crossing the taxonomic divide: conflict and its resolution in
societies of reproductively totipotent individuals
A. G. HART & F. L. W. RATNIEKS
Laboratory of Apiculture and Social Insects, Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK
Keywords:
Abstract
Dinoponera quadriceps;
Heterocephalus glaber;
honest signalling;
Ponerinae;
queen replacement;
reproductive skew.
Reproduction in groups may be unequal, with one or a few individuals
monopolizing direct reproduction assisted by nonbreeding helpers. In social
insects this has frequently led to a pronounced queen-worker dichotomy and a
loss of reproductive totipotency among workers. However, in some invertebrate and all vertebrate societies, all or most individuals remain reproductively
totipotent. In these groups, conflicts of interest over reproduction are
potentially greatest. Here, we synthesize previous analyses of reproductive
conflict, aggression and breeder replacement in haplodiploid societies of
totipotent individuals and extend them to cover diploid (vertebrate) examples.
We test predictions arising from this approach using the best-studied
invertebrate (Dinoponera queenless ants) and vertebrate (naked mole-rat,
Heterocephalus glaber) examples, although in principle our analysis applies to all
similar groups. We find that premature replacement of a parent breeder by
nonbreeders (overthrow) is rare. Dominant coercive control of nonbreeders by
the breeder is often unnecessary and honest signalling of breeder vitality can
maintain group stability and resolve conflicts over reproduction. We hope that
by providing an explicit transfer of social theory between ants and naked
mole-rats we will stimulate further cross-taxonomic studies that will greatly
broaden our understanding of sociality.
Introduction
In social groups, there is often inequality or skew in
direct reproduction (e.g. Reeve & Ratnieks, 1993; Keller
& Reeve, 1994; Clutton-Brock, 1998). In some groups all
individuals may reproduce, but in others inequality may
be so extreme that only one breeder of each gender
monopolizes reproduction (Keller & Reeve, 1994).
Species with highly skewed groups and nonbreeders that
care for the breeders’ offspring may be said to be eusocial
(first defined by Batra, 1966). Eusociality has evolved
numerous times in Hymenoptera (all ants, some bees and
some wasps are eusocial) (Wilson, 1971) and occurs in all
termites (e.g. Thorne, 1997), some thrips (Crespi, 1992),
a species of platypodid beetle (Kent & Simpson, 1992),
Correspondence: Adam G. Hart, Laboratory of Apiculture and Social Insects,
Department of Animal and Plant Sciences, University of Sheffield,
Sheffield S10 2TN, UK.
Tel.: 0044 (0)114 2220144; fax: 0044 (0)114 2220002;
e-mail: [email protected]
some aphids (Stern & Foster, 1996), two species of
African mole-rats (Jarvis & Bennett, 1993; Faulkes &
Bennett, 2001) and snapping shrimps, Synalpheus (Duffy,
1996).
Kin selection theory explains how nonbreeders in
eusocial societies obtain indirect fitness benefits by
helping to rear relatives (Hamilton, 1964). Helpers may
forego all direct reproduction, becoming morphologically, physiologically and/or behaviourally sterile (or
virtually sterile) with adaptations that enhance their
helping ability. These ‘workers’ assist reproductive breeders who may themselves be adapted for their reproductive role. Social Hymenoptera workers may retain ovaries
and although being unable to mate, they can lay
unfertilized eggs, which develop into males because of
haplodiploid sex determination. In some social Hymenoptera, unmated workers may produce a large proportion
of the males, e.g. in Melipona favosa, 95% of males are
workers’ sons (Sommeijer et al., 1999) but female offspring are only ever produced by the queen and
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
383
384
A . G . H A R T A N D F. L . W . R A T N I E K S
reproductive males. [In exceptionally rare cases, workers
can produce female offspring through parthenogenesis,
but this has only been recorded in four species of ants
(Cagniant, 1979; Itow et al., 1984; Heinze & Hölldobler,
1995; Tsuji & Yamauchi, 1995), occasionally in queenless
honey bee colonies (Onions, 1912; Mackensen, 1943)
and in the cape honey bee Apis mellifera capensis
(Anderson, 1963; Moritz & Harberl, 1994).] The inability
of workers to produce female offspring, either through
total sterility [e.g. in the Termitidae (Thorne, 1997, and
references therein), several genera of ants (Bourke &
Franks, 1995), some stingless bees (e.g. Boleli et al., 2000;
Tóth et al., 2002 and references therein)] or through an
inability to mate (most ants, most Apidae, all Vespidae),
is typical in eusocial Hymenoptera (Bourke, 1988).
In most social insects, workers cannot take over the
reproductive role of the queen because they cannot
reproduce (usually being unable to mate) or can have
only male offspring. In eusocial species with a pronounced queen/worker dimorphism and loss of worker
reproductive potency (e.g. most ants, honey bees, bumble bees, stingless bees, higher termites, and Vespinae
wasps) there is no potential for direct conflict between
queen and workers over the breeder role. However, in
some social insects, and in all vertebrate societies (Stacey
& Koenig, 1990; Solomon & French, 1997), individuals
within a group have the same morphology and nonbreeding individuals have not permanently ceded reproductive ability to breeders. Of those species normally
considered eusocial, reproductive totipotency (i.e. where
all or many individuals have the ability to produce
offspring of both sexes) occurs in lower termites (Thorne,
1997), polistine wasps (Reeve, 1991; Strassman et al.,
2002), halictid bees (Breed & Gamboa, 1977), allodapine
bees (Michener, 1974), queenless ponerine ants (Monnin
& Ratnieks, 2001) and naked and Damaraland mole-rats
(Faulkes & Bennett, 2001). However, regardless of
individual reproductive potential, reproduction in these
societies is still typically monopolized by a single
individual of both sexes (although polygyny and polyandry does occur). Because nonbreeders could replace
breeders there is great potential for conflict in skewed
groups where individuals retain reproductive totipotency.
Inter-individual conflict and breeder replacement in
groups of reproductively totipotent individuals have
been particularly well-studied in Dinoponera, a genus of
queenless ponerine ant (Monnin & Peeters, 1998, 1999;
Monnin et al., 2002, 2003) and analyses of relatedness,
colony structure and breeder condition have led to a
reasonably good understanding of reproductive conflict
and behaviour (Monnin & Ratnieks, 2001). Other
highly skewed groups of reproductively totipotent
individuals have relatedness structures similar to Dinoponera, with a single breeder of each sex heading a
group of reproductively totipotent individuals, who are
generally the breeders’ offspring (e.g. naked mole-rats,
Heterocephalus glaber). Can analyses of reproductive
conflict in ants enhance our understanding of conflict
in groups with similar group structure but from very
different taxa?
This paper has two aims. First, we will synthesize and
extend previous analyses of reproductive conflict using
haplodiploid social insect (particularly queenless ant)
models. This will, for the first time, bring together the
relevant social insect theory and extend it to cover
diploid, vertebrate examples. Our synthesis leads to
specific predictions regarding conflict in groups of
reproductively totipotent individuals. For example, we
show that, in a high-relatedness society, breeders who
are the parents of the nonbreeders need only demonstrate that they are alive and well to restrain attempts
at overthrow (see also, Alexander et al., 1991;
Alexander, 1991; Monnin & Ratnieks, 2001). This
may result in signals that demonstrate their physical
ability and vitality without the need for escalated
aggression. Our second aim is to test these predictions
by reviewing empirical data from two model examples
crossing taxonomic divides, Dinoponera queenless ants
(invertebrate, haploid) and naked mole-rats, H. glaber
(vertebrate, diploid). We have confined our analysis to
these species because they are well-characterized and
have a literature rich with qualitative and quantitative
descriptions of inter-individual aggression and conflict.
Other candidate species have not generally benefited
from studies of individual behaviour but, in principle,
our analysis could be extended to any other highly
skewed group of reproductively totipotent individuals.
Although often alluded to, useful comparisons between
vertebrate and invertebrate societies have not been
forthcoming despite longstanding calls for more inclusive analyses (Seger, 1993; Keller & Reeve, 1994). It is
our hope that this explicit transfer of theory developed
for social insects to a social vertebrate will serve to
stimulate further cross-taxon comparisons in empirical
and theoretical studies of sociality.
Reproductive options
In a colony of reproductively totipotent individuals with
high reproductive skew, nonbreeders have several
options for direct reproduction within the group. One is
to overthrow the current same-sex breeder, and another
is breeder supersedure. (We define overthrow as the
replacement of a nonfailing breeder by a previously
nonbreeding individual from within the colony. This is
distinct from a colony member replacing a failing
breeder, which we term supersedure.) A third option,
becoming an additional co-breeder, may occur in some
social groups. Co-breeders could be overt, breeding
openly in the group, or covert ‘sneaky’ breeders. Additionally, in haplodiploid societies, workers may gain
direct reproduction by producing sons. Reproductive
options in mole-rat and queenless ant societies are
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Reproductive conflict in totipotent societies
Table 1 Reproductive options of nonbreeding individuals in colonies of queenless ponerine ants, Dinoponera, and eusocial African
mole-rats, Heterocephalus glaber.
Queenless
ponerine ant
Dinoponera
Naked mole-rat
Heterocephalus
glaber
Reproductive option
Female Male Female
Produce male offspring
Become an
additional breeder
Overthrow current breeder
Supersede current breeder
Inbreed with
related breeder
Disperse from natal colony
Yes
No
No
No
Yes
Yes
No
No
No
No
No
Yes
Independently
found a colony
No
No
Male
No
No
Occasionally Yes
(but usually >3)
Yes
Yes
Yes
Yes
Yes*
Yes*
Yes
(very rarely)
Yes Yes (rarely)
Yes *Outbreeding is preferred is the opportunity arises (Braude, 2000;
Ciszek, 2000).
As an unrelated pair (Braude, 2000; Ciszek, 2000).
The existence of a potential opportunity to reproduce does not imply
that such opportunities available to more than a small proportion of
nonbreeders. See text for further discussion, references and definition of terms.
compared in Table 1, and Table 2 further compares and
contrasts these societies.
Breeder overthrow in haplodiploids
Consider a colony of haplodiploid (males are haploid and
arise from unfertilized eggs) totipotent eusocial organisms, headed by a single, singly mated female breeder
who is the mother of the other colony members. [The
breeding individual in a queenless ant colony is termed
the gamergate (Peeters, 1993).] The male parent exists
only as stored sperm in the female’s spermatheca and
male offspring play no part in the social life of the colony.
There is out-breeding (with dispersive males), no individual other than the breeder has any direct reproduction
and individuals cannot found colonies. These conditions
are typical of queenless ants.
Under these conditions, nonbreeders are usually the
daughters of the breeder, and they help to rear their
siblings. Consequently, nonbreeders are not in conflict
with the breeder over her reproductive position because
on average they are as related to her offspring (sisters
r ¼ 0.75; brothers r ¼ 0.25; average r ¼ 0.5) as they are
to their own offspring (r ¼ 0.5). [Nonbreeders can be in
conflict over male production if they are able to lay
unfertilized eggs, because they would favour their own
sons over queen’s sons (sons r ¼ 0.5; brothers, r ¼ 0.25)]
Therefore, overthrow of the breeder is not beneficial to
the potential new breeder and, indeed, would be opposed
both by the breeder [trading offspring (r ¼ 0.5) for
385
grand-offspring (r ¼ 0.25)] and the other nonbreeders
[trading siblings (average r ¼ 0.5) for nieces and nephews (r ¼ 0.375)].
A focal daughter can seem to benefit from overthrow
of her mother if there is competition between nonbreeders, because the focal individual will be more related to
her own offspring (r ¼ 0.5) than to a sister’s offspring
(r ¼ 0.375) (Monnin & Peeters, 1999). Therefore, it can
be better to overthrow your mother before one of your
sisters do (Monnin et al., 2002). However, were a focal
individual to overthrow a relatively young mother
breeder then, over time, she could actually reduce her
relatedness to offspring reared by the colony. Consider a
scenario when a breeder is overthrown by a focal
daughter. The focal daughter trades siblings for offspring,
and this incurs no relatedness cost or benefit. When the
focal daughter is replaced it will probably be by one of
her own daughters, at which point she trades offspring
for grandchildren (r ¼ 0.25). However, had the mother
breeder not been overthrown then she would be replaced
by a daughter at, or near, the end of her life. Without
overthrow, the colony rears siblings of the focal daughter
for the lifetime of the mother breeder, followed by nieces
and nephews of the focal daughter (r ¼ 0.375) following
breeder replacement. An extreme case would be a newly
emerged daughter overthrowing her young mother.
Assuming no further overthrows, the colony rears
offspring of the daughter breeder (r ¼ 0.5) for her
lifetime, grand-offspring (r ¼ 0.25) for one of her daughter’s lifetimes and so on. If the newly emerged daughter
had not overthrown her mother, then the colony would
help rear her siblings (r ¼ 0.5) for her mother’s lifetime,
which will only be slightly shorter than her own, and
then nieces and nephews (r ¼ 0.375). The average
relatedness to offspring over two breeder lifetimes will
be only [1/2 · (0.5 + 0.25)] r ¼ 0.375 with overthrow,
compared with [c. 1/2 · (0.5 + 0.375)] c. r ¼ 0.4375
without overthrow (the exact value being dependent
on how much of the mother breeder’s life was left when
the daughter emerged).
If overthrow is to be attempted then timing is critical.
An analysis of queenless ants (Monnin & Ratnieks,
2001) suggests that the way that subordinates are
organized is important in determining when overthrow
should be attempted. In Dinoponera, subordinates form
a near-linear dominance hierarchy of around 3–5 highranking individuals, with the breeder or gamergate
having the alpha rank (described below). These highrankers are hopeful reproductives that do little work
and if the breeder is replaced it is always by a highranker (usually beta). Since only high-rankers can
overthrow the breeder and high rank is held only for
a short-time, overthrowing the breeder is selectively
favoured for high-ranking individuals in some scenarios
(T. Monnin, F.L.W. Ratnieks, unpublished data; cited
in Monnin & Ratnieks, 2001). However, every
other colony member, and the breeder herself, favour
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
386
A . G . H A R T A N D F. L . W . R A T N I E K S
Attribute
Invertebrate or vertebrate
Ploidy
Eusocial
Both sexes involved in colony life
Totipotent working individuals
Extreme reproductive skew
Colony size
Nesting ecology
Colony foundation through fission
Polygyny
Polyandry
Inbreeding
Outbreeding
Hierarchy among nonbreeders
Breeder aggression to
high-ranking nonbreeders
Aggression between nonbreeders
Breeder overthrow
Elevated aggression after
breeder replacement
Queenless ponerine
ant Dinoponera
Naked mole-rat
Heterocephalus glaber
Invertebrate
Haplodiploid
Yes
No (female societies)
Yes
Yes
80 (range 26–238)
in D. quadriceps
Subterranean
Yes (obligate)
No
No
No
Yes
Yes (roughly linear,
>5 individuals)
Yes
Vertebrate
Diploid
Yes
Yes
Yes
Yes
80 (range 75–295)
Yes
Rarely
Yes
Yes
Very Rarely
Yes
Table 2 Colony attributes, social structure
and aggressive behaviour in the queenless
ponerine ant Dinoponera and the naked
mole-rat, Heterocephalus glaber.
Subterranean
Yes (but unrelated pairs may found)*
Occasionally
Yes (but effective paternity not known)
Yes (but outbreeding preferred)
Yes (through dispersers)
Yes (high rankers larger in both sexes)
Yes
Further explanation and references can be found within the appropriate sections of text.
*Braude (2000) and Ciszek (2000).
overthrow only under more restrictive conditions
leading to conflict over breeder replacement. Evidence
of this conflict is that low-rankers of Dinoponera
quadriceps often immobilize high rankers, a form of
worker policing (see below; Monnin et al., 2002).
In conclusion, overthrow of the breeder is either not
favoured at all or is favoured by a focal individual but is
generally opposed by other colony members. There is a
point when all individuals, including the breeder, favour
replacement (Reeve & Sherman, 1991) but this comes at
the end of the breeder’s life when replacement is more
usefully termed supersedure. For a focal worker, it can be
worthwhile attempting to overthrow the mother breeder
(e.g. if high rank is held for a short-time) but in many
scenarios every other colony member and the breeder
will likely oppose the overthrow and generally it is only
worthwhile replacing your mother breeder at the end of
her life when she is failing. Overall, a breeder should not
face a constant threat of overthrow for the majority of
her life, and if she does, pretenders will normally also be
opposed by her other daughters.
Breeder overthrow in diploids
In diploid societies it is usual for males to play an active
role in colony life and overthrow of either sex can occur.
In contrast, males do not play a role in colony life in
haplodiploid Hymenoptera [although they do play a role
in colony life in the haplodiploid eusocial thrips (Crespi,
1992)] and the male breeder (existing only as stored
sperm) is replaced whenever the female breeder is
replaced. In diploids, as in haplodiploids, the overthrow
of a parent breeder results in trading siblings for
offspring, with no relatedness advantage. Additionally,
diploids (whether male or female) are related to their
nephews and nieces by 0.25, rather than 0.375 (as is the
case in haplodiploids). Consequently diploid colony
members lose more inclusive fitness than their haplodiploid counterparts do if a sibling overthrows their
mother.
Nonrelatedness costs of overthrow
Relatedness to colony offspring is not the only costbenefit factor to consider in breeder overthrow.
A pretender must physically challenge the breeder and
this challenge may be individually costly to the pretender
even if successful. The resident breeder has the most to
lose by being overthrown and will likely fight to retain its
status (unless its fecundity has decreased to such an
extent that even they favour their replacement). Additionally, overthrow (or attempted overthrow) of a functioning breeder will probably reduce colony productivity,
since a resident breeder may be injured defending their
position and, if overthrow is successful, there will almost
always be a delay between overthrowing the old breeder
and the new breeder producing offspring. This delay
arises from difficulties in finding a suitable mate and the
time required to develop physiologically as a breeder.
Furthermore, the post-overthrow period will probably be
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Reproductive conflict in totipotent societies
associated with a period of colony instability as other
colony members (trading siblings for nieces and nephews) attempt to overthrow their sibling or increase their
own dominance status (as occurs in D. quadriceps;
Monnin & Peeters, 1998). Thus, an initial overthrow
may stimulate further overthrows, further reducing
colony productivity.
The effects of polygyny, polyandry and
inbreeding
In both haplodiploid and diploid organisms, polygyny
and polyandry will reduce the relatedness between
colony members thereby reducing the value of nondescendent kin and the inclusive fitness benefit attained
by helping to rear them. Thus, in both types of
societies, polyandry makes overthrow more likely
(Reeve & Sherman, 1991). Another situation proposed
to encourage parent-offspring conflict over reproduction is if a focal daughter can overthrow her mother
and is able to inbreed with her father (Reeve &
Sherman, 1991). This incestuous mating would result
in offspring that are more related to the focal daughter
than full-siblings. In addition, if incestuous mating is
possible then there is no cost in finding a mate (see
above), which reduces the colony productivity costs
associated with breeder overthrow. Both limited polyandry and inbreeding occur in naked mole-rats and
these are discussed below.
Predictions
(1) Conflict will be increased by polyandry, polygyny
and inbreeding.
(2) The level of conflict will vary through time. Most of
the time, conflict should be relatively low, but it will
increase as breeders near the end of their lives, even
if breeders are not failing. Conflict should be greatest
during and immediately after breeder replacement,
when individuals suffer the greatest loss in inclusive
fitness and have the most to gain from competing
with the new breeder who is now a sibling rather
than a parent.
(3) Attempted overthrow is likely to be rare in societies
with close kin structure and breeder replacement is
expected to occur by supersedure, at the end of
breeder’s lifetime.
(4) Colony members would gain from being able to
assess reliably the breeder’s age, condition and/or
fecundity (Alexander et al., 1991; Monnin & Ratnieks, 2001) and there may be ritualized behaviours
to enable assessment of the breeder.
(5) In highly related groups, diploid nonbreeders stand
to lose more than haplodiploid nonbreeders by
breeder overthrow. Therefore, post-overthrow (or
breeder replacement) instability is expected to be
greater in diploids than in haplodiploids.
387
Problems in interpreting aggressive
behaviour
A fundamental issue in considering reproductively
skewed groups concerns whether skew is forced on
nonbreeders by the breeder (the coercive Dominant
Control Model, Snowdon, 1996) or whether nonbreeding individuals show restraint in not breeding in order to
gain inclusive fitness benefits (the altruistic self-restraint
model, Snowdon, 1996) (also Creel & Macdonald, 1995;
Cant, 1998). Our predictions are concerned with conflict
in groups manifested as aggressive interactions between
group members and a similar confusion over cause and
motivation occurs in interpreting behaviours performed
by breeders and directed at subordinate nonbreeders.
Aggressive behaviours performed by dominants towards
subordinates may be interpreted in at least three ways.
These different interpretations have further implications
for interpreting any subordinate reproduction that may
occur. It is useful to consider these alternative interpretations and their implications for reproductive skew
before discussing specific examples.
First, aggressive acts by dominants directed at subordinates may be physically dominating, escalated, behaviours that serve to directly suppress reproduction in
recipients by, for example, by elevating physiological
stress or by preventing mating. Although physical suppression does occur in some species, in others, like naked
mole-rats, subordinates can occasionally reproduce [e.g.
some naked mole-rat females may develop perforate
vaginas and enlarged nipples and can sometimes breed
as secondary females (Jarvis, 1991; Faulkes & Abbott,
1996)], indicating that dominants are unable to control
completely subordinate reproduction through physical
suppression. Thus, it is possible to interpret subordinate
reproduction in the face of aggression from dominants as
something that occurs when dominants are unable to
exert complete control (Clutton-Brock, 1998; CluttonBrock et al., 2001). Alternatively, subordinate reproduction could be interpreted as an example of a reproductive
‘concession’ (Clutton-Brock, 1998; Clutton-Brock et al.,
2001), whereby subordinates are allowed to reproduce in
exchange for staying in the group (a ‘staying incentive’)
or for not challenging the dominant (a ‘peace incentive’)
(Reeve & Ratnieks, 1993; Keller & Reeve, 1994; CluttonBrock, 1998). Second, aggressive acts performed by the
breeder may be responses to subordinates testing the
physical abilities of dominants (Reeve & Ratnieks, 1993).
Under this interpretation, dominant aggression is merely
a response to the ongoing power struggle between
dominants and subordinates (Cant & Johnstone, 2000).
Any subordinate reproduction could be viewed as an
example of incomplete dominance by the breeder,
reproductive concession or perhaps the beginning of an
attempt by the subordinate to replace the breeder. Third,
aggressive acts may be signals conveying the message ‘do
not challenge me, I am big and strong’, indirectly
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
388
A . G . H A R T A N D F. L . W . R A T N I E K S
suppressing reproduction by convincing recipients that
challenges to the breeder are either unnecessary or will
likely fail. Such behaviours may be more ritualized and
less escalated than behaviours aimed at direct physical
suppression.
Conflict in eusocial societies of totipotent
individuals
Queenless ants
Around 100 species of ponerine ant have no queen caste
and colonies of these queenless species are headed by one
(or more) mated workers, gamergates, who play the
queen role and are assisted in rearing their offspring by
morphologically identical nonreproductive workers. We
focus on the exclusively queenless genus Dinoponera (see
Peeters, 1997, p. 376, for an overview of the occurrence
of the queenless condition), in which all workers are
potentially capable of mating and producing both male
and female offspring.
Dinoponera is an exclusively South American genus
comprising six described species (Kempf, 1971; Monnin
& Peeters, 1998). Mean colony size ranges from 13
[D. australis: SD ¼ 6, n ¼ 37, range 3–31, Paiva &
Brandão, 1995 (Table 1, ibid); range stated as 3–37 in
Monnin & Ratnieks, 2001] to 80 (D. quadriceps: range
26–238, cited in Monnin & Ratnieks, 2001 based on
Monnin & Peeters, 1999 and unpublished data). All
species studied to date are monogynous (D. quadriceps:
Monnin & Peeters, 1998; D. gigantea: Haskins & Zahl,
1971; Monnin et al., 2003; D. australis: Paiva & Brandão,
1995) and probably monandrous. Female ponerines are
usually monandrous and in the laboratory D. quadriceps
only mates once with a nonnestmate male (Monnin &
Peeters, 1998). Independent colony founding is not
known to occur, and colony reproduction is by fission.
Reproduction in Dinoponera is regulated by a short
near-linear dominance hierarchy with the mated worker
holding the alpha rank (D. quadriceps: Monnin & Peeters,
1999; D. australis and D. gigantea: Monnin et al., 2003).
Although high-ranking workers are involved in many
agonistic interactions (described below), and consequently do less work than low ranking workers do, the
dominance hierarchy includes only a minority of nonbreeding individuals (c. >5%). Hierarchy length varies
across species as colony size increases but rarely exceeds
five individuals even in the largest colonies (Monnin
et al., 2003).
Eusocial African mole-rats
Naked mole-rats are the closest vertebrate analogue to
the eusocial insects. Mole-rats (Bathyergidae) exhibit an
extremely broad variation in sociality ranging from
solitary breeding through co-operative breeding to eusociality (Table 2 in Burda et al., 2000). It is generally
accepted that the naked mole-rat (H. glaber) and the
Damaraland mole-rat (Cryptomys damarensis), fit the
classic definition of eusociality (Jarvis, 1981; Jarvis &
Bennett, 1993; Jarvis et al., 1994; Burda et al., 2000;
Faulkes & Bennett, 2001). However, naked mole rats are
more comparable with Dinoponera than Damaraland
mole-rats are, having practically identical colony size
(c. 80 individuals, compared with c. 16, Jarvis et al.,
1994), and extreme reproductive skew (Jarvis et al.,
1994). Consequently, we will focus on naked mole-rats,
but our conclusions will likely apply to similar social
organisms.
Naked mole-rats occur in arid areas of Kenya, Ethiopia
and Somalia (Brett, 1991a). They live completely underground in tunnel systems up to several kilometres which
consist of shallow foraging tunnels overlaying deeper
nesting, toilet, storage and refuge tunnels and chambers
(Jarvis, 1981, 1985; Brett, 1991a,b). They are herbivores
and use the shallower tunnels to forage on the subterranean parts of plants, primarily tubers and other storage
organs. They are highly adapted to their fossorial lifestyle,
possessing short limbs, cylindrical bodies and reduced
eyes and ear pinnae (leading to poor visual and auditory
acuity). They also have large, procumbent incisors
protruding well outside the mouth, which are used
aggressively and for digging. Naked mole-rats are furless
although scattered hairs occur and are poor thermoregulators. Colony size, based on wild-caught colonies,
ranges between 75 and 295 (reported in Faulkes &
Bennett, 2001), with a typical colony containing around
80 individuals (Brett, 1991a).
It is clear, from both laboratory and field data, that
H. glaber is predominantly monogynous (Jarvis, 1981;
Lacey & Sherman, 1997; reviewed in Burda et al.,
2000). In general, colonies are headed by a single
breeding female who consorts with one to three males
(possibly one to two; Brett, 1991a, p. 120) although
two breeding females have been reported in some
breeding groups [up to 11% of colonies may be
polygynous (Sherman et al., 1992)]. The remaining
members of the colony do not breed but work to
extend and defend the tunnel system, collect food and
assist both directly and indirectly in caring for pups
(Sherman et al., 1992), although allolactation does not
generally occur (but see Ciszek, 2000 for a report of
allolactation in a colony with two breeding sisters).
Female breeders and nonbreeders are physically dimorphic (O’Riain et al., 2000). When a female becomes a
breeder perhaps because of the death or overthrow of
her mother, she undergoes a secondary, physical
lengthening of the lumbar vertebrae, which extends
the abdomen. This extension increases the capacity for
gestating young, and gaterointestinal hypertrophy may
enable elongated breeding females to meet the increased nutrient requirements demanded by breeding
(O’Riain et al., 2000). Despite the existence of a
specialized reproductive morphology naked mole-rats
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Reproductive conflict in totipotent societies
are reproductively totipotent, because the specializations occur by divergent growth in reproductively
totipotent individuals.
Inter-individual aggression, conflict and
breeder overthrow
Dinoponera queenless ants
Aggression and conflict
The Dinoponera hierarchy is characterized by agonistic
behaviours such as blocking, gaster rubbing, gaster
curling (the gaster is the swollen part of the abdomen
behind the ‘waist’), antennal boxing, immobilization and
leg biting (described in Monnin & Peeters, 1999)
(Table 3). Blocking, a ritualized behaviour whereby the
actor stretches her antennae on either side of the head of
389
a recipient (Monnin & Peeters, 1999), is in most cases
performed by the alpha towards beta. Gaster rubbing (an
active individual bites an antenna of a recipient and rubs
it against her gaster), gaster curling and the leg biting
(Table 3) are also mostly directed by the alpha towards
the other high-ranking individuals (most often beta). In
contrast, antennal boxing (an active individual harmlessly hitting the head of a recipient with her antennae),
by far the commonest agonistic behaviour (44.5% of
total interactions), is not primarily performed by alpha
but by individuals with rank beta and lower, and is
directed to subordinates. The final behaviour, immobilization, involves one to six generally low ranking
individuals grasping a generally high-ranking target
individual by the legs, antennae or mandibles and
immobilizing her for several hours or even days.
Interestingly, the gamergate can mark high-ranking
Table 3 Intra-colony aggression in Dinoponera and the naked mole-rat, Heterocephalus glaber.
Species
Behaviour
Description
Actor
Recipient
Dinoponera*
Blocking
Actor stretches her antennae
around the recipient’s head
Actor’s gaster bend forward
towards recipient
As gaster curling, but an antenna
of the recipient is bitten and
rubbed against actor’s gaster
Actor bites recipient’s leg
Recipient’s head is hit repeatedly
by actor’s antennae
Recipient is spread-eagled by
1–6 actors
Gamergate (94.1%)
High-rankers (beta ¼ 68.6%)
0
Gamergate (45.2%)
High-rankers
0
Gamergate (55.8%)
High-rankers
1
Gamergate (23.9%), beta (21.9%)
Beta (18.8%), gamma (19.5%)
and delta (15.3%
Lower rankers (ranks 3–8 ¼ 53.2%)
Ranks 2–6 (63.2%)
Ranks 3–7
2
1
Ranks 2–6 (70.6%) 3
Breeders (mostly female)
High-rankers
1
Nonbreeders
Resource competition
2
Colony defenders
Colony intruders–
1
Nonbreeders
Nonbreeders§
3
Nonbreeders
Nonbreeders
Colony intruders or nonbreeders§
Nonbreeders
Gaster curling
Gaster rubbing
Leg biting
Antennal boxing
Immobilization
Naked
mole-ratà
Shoving
Tooth fencing
Gaping
Batting
Biting
Tugging
Actor shoves recipient worker
backwards for up to 1 m
Two individuals stand face-to-face
and lock incisors and pushing
and rocking the head
Two individuals stand face-to-face,
open their mouths with incisors
separated and expel air through
the mouth with a hissing sound
Two individuals swat each other’s
muzzles with their forepaws
Actor closes its jaws on recipient
Actor grasps target’s skin with
incisors and pulls backwards
AI
3
2 (3**)
Aggressive behaviours have been categorized on a numerical aggression index (AI): 0, noncontact and nonharmful; 1, contact but nonharmful;
2, potentially harmful; 3, harmful and/or potentially fatal.
Behaviours typically performed by the breeder to nonbreeders are in plain type. Behaviours associated with nonbreeders fighting for rank or
resources are underlined. Behaviours performed by low-rankers towards high rankers are in italics. Gaping in naked mole-rats is involved with
colony defence (Pepper et al., 1991).
*Data and descriptions for Dinoponera quadriceps taken from Monnin & Peeters (1999).
Gamgergate can be immobilized if she is failing (Monnin & Peeters, 1999).
àDescriptions from Lacey et al. (1991).
–Pepper et al. (1991).
§Batting, tugging and biting are interactions associated with competition among females for a breeding vacancy.
**Tugging is associated both with resource competition and competition for breeding vacancies. It can result in injury and death if it is between
females for a breeding vacancy.
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
390
A . G . H A R T A N D F. L . W . R A T N I E K S
individuals with a chemical (sting-smearing) that causes
low-ranking individuals to immobilize the marked individual (Monnin et al., 2002). In this way, the gamergate
and lower-rankers actively co-operate when their interests coincide. Neither party would benefit if their mother
gamergate was overthrown.
Most individuals within Dinoponera colonies, despite
being reproductively totipotent, are not high-rankers and
are therefore not in line to become the new gamergate if
the current gamergate dies or is killed. Consequently,
most individuals are neither potentially nor actually in
conflict with their mother breeder. High-rankers are a
threat to the gamergate but she is generally able to
maintain her status with nonaggressive behaviours like
blocking and gaster curling. Genuinely coercive behaviours like immobilization are actually performed by lower
rankers, not the gamergate, although the gamergate can
target pretenders for immobilization. The ‘agonistic’
behaviours directed by the gamergate to her subordinates
(blocking, gaster curling, gaster rubbing) are ritualized
and seem not to serve a coercive function. That is they
are not physically forceful escalated acts that directly
prevent the recipient from breeding. Rather, they appear
to be honest signals of status and condition, which
prevent overthrow of a healthy functional gamergate by
informing recipients that the gamergate is present and
healthy. Blocking could be a physical measure or test of
coordination, with recipients judging the gamergate’s
condition just as female Drosophila can judge a male’s
quality from its ability to track her during a courtship
dance (Maynard Smith, 1956). Additionally, gamergates
are chemically distinct (Monnin et al., 1998; Peeters et al.,
1999) and gaster rubbing could provide a direct assessment of cuticular hydrocarbons. Consequently, in the
presence of a gamergate of sufficient quality and relatedness, individuals do not attempt to become a breeder.
However, aggression does escalate after gamergate
replacement, as sisters compete with each other for
reproductive status or dominance rank. This postreplacement instability can last a few weeks (Monnin &
Peeters, 1999) but does not result in the death of colony
members.
Overthrow
Dinoponera nonbreeders may have the potential to usurp
the gamergate and successfully reproduce, but data from
laboratory colonies show that gamergates were ‘not often
replaced and that [they were] usually reproductively
failing when replaced’ (Monnin & Ratnieks, 2001; data
from Monnin & Peeters, 1999). Thus we may conclude
that gamergate overthrow is rare.
Naked mole-rats
Aggression and conflict
Individuals within colonies are extremely similar genetically (Reeve et al., 1990; Honeycutt et al., 1991; Faulkes
et al., 1997) and yet agonistic behaviours are frequently
observed between females (Alexander, 1991; Reeve &
Sherman, 1991) although fighting between males is
generally very rare (Jarvis, 1991; Lacey & Sherman,
1991; Clarke & Faulkes, 1998). Male–male aggression
may increase during early colony development (Ciszek,
2000) (and possibly after breeder overthrow and destabilization) but data suggest that soon after colonies are
formed males establish a stable and linear breeding
hierarchy, which reduces male–male aggression to a very
low-level (Ciszek, 2000).
Shoving, prolonged head-to-head pushes between two
individuals (Lacey et al., 1991), is the most common
agonistic behaviour (Lacey et al., 1991; Clarke & Faulkes,
2001) although other ‘mild’ (Reeve & Sherman, 1991)
agonistic behaviours like tugging, biting, tooth fencing
and batting (Lacey et al., 1991) are also observed
(Table 3). Occasionally, serious aggression such as biting
is observed and this can be fatal to the recipient (Jarvis,
1991; Lacey & Sherman, 1991). As with blocking in
Dinoponera, shoving is primarily performed by breeders
(Reeve & Sherman, 1991; Clarke & Faulkes, 2001).
Breeding females initiate most shoves and most of the
remaining shoves are carried out by breeding males
(Reeve & Sherman, 1991). The recipients of shoves are
mostly large, high-ranking individuals (Clarke & Faulkes,
2001).
Several hypotheses have been proposed to explain
shoving in naked mole-rats. The ‘work conflict hypothesis’ (Reeve, 1992) proposes that shoving serves to
activate ‘lazy’ workers, since there may be conflict over
the level of aid nonbreeders provide to breeders. However, subsequent studies (Jacobs & Jarvis, 1996; Clarke &
Faulkes, 2001) have found no support for this hypothesis. Clarke & Faulkes (2001) conclude that it is possible
that shoving ‘is used to establish reproductive dominance, and, once achieved, other cues may maintain
suppression in subordinates’. Shoving is, therefore,
interpreted as an initial mechanism of dominant control
(Snowdon, 1996). However, removal of the breeders of
either sex results in the deaths of some nonbreeding
individuals through escalated violent interactions with
each other (Lacey & Sherman, 1991; Clarke & Faulkes,
2001), which suggests that the establishment of initial
dominance might rely on more escalated behaviour than
mere shoving. Like blocking and gaster rubbing in
Dinoponera, shoving could act as an honest signal of
vitality (Alexander, 1991) conveying two types of
information; the simple message ‘I am here…’ and the
quantitative message ‘…and I am strong/young’. If the
nonbreeders are satisfied with the breeder then they can
elect to remain with the status quo rather than attempt
overthrow. This is similar to the ‘threat reduction
hypothesis’ (TRH) proposed by Reeve & Sherman
(1991), except that the TRH explains shoving within a
framework of ‘dominant control’. Under this interpretation, shoving is seen as a dominant act of a breeder to
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Reproductive conflict in totipotent societies
reduce the threat posed by a nonbreeder by ‘informing a
recipient [of shoving] of the breeding female’s willingness or ability to fight, of her high probability of breeding
successfully…and/or by actually reducing the recipients
fighting ability’ (Reeve & Sherman, 1991). However, our
earlier analysis encourages a framework of interpretation
under which shoving can be viewed as an honest signal
of breeder condition. In Dinoponera, most ritualized
agonistic behaviours were performed by the gamergate
and directed towards high-ranking individuals. Similarly,
in naked mole-rats, shoving is principally initiated by
breeders and the vast majority of shoves were carried out
by the female breeder (Clarke & Faulkes, 2001).
Although shoving is less ritualized than Dinoponera
blocking, it is a relatively mild aggressive act when
compared with biting, tugging or batting (Table 3) and
would certainly be a good indicator of breeder strength
and agility. The finding that shoving by queens and
reproductive males is positively correlated with size, rank
(Reeve & Sherman, 1991; Clarke & Faulkes, 2001) and
plasma luteinizing hormone concentrations of recipients
(and therefore their ability to reproduce) (van der
Westhuizen et al., 2002) is also evidence for shoving
being an honest signal of breeder condition. A breeding
individual might be expected to display status to subordinate individuals in a position to breed imminently. It is
also notable that breeders are more likely to shove
individuals less related to them (Reeve & Sherman,
1991). These individuals gain more by overthrowing the
breeder than closer relatives of the breeder do and they
may receive more shoving because they are a greater
threat to the breeder.
Overthrow
Overthrow of a breeding female is extremely rare and, to
date, has been only been documented once in a captive
colony (Faulkes, 1990). However, the death or experimental removal of the breeding female in captive
colonies provokes an extremely aggressive and destabilizing reaction. For example, following the removal of the
breeding female and one breeding male from a colony,
violent fighting broke out among the remaining siblings
that continued sporadically for 16 months. All fighting,
with one exception, involved the current behaviourally
dominant individual and in total three females sequentially rose to behavioural dominance with associated
physical development into breeding condition (e.g. teat
enlargement). Over the 16 months of colony instability,
nine individuals out of a population of 24 died as a result
of fighting (Lacey & Sherman, 1991). In a long-lived
animal it not surprising that post-overthrow conflict can
be prolonged. Following replacement of the mother
breeder, it will take some time for the colony to revert
to a mother/daughter kin structure from the sister–sister
kin structure that follows replacement. As long as the
latter kin structure prevails then there is a large relatedness benefit to ousting the current breeder. Overall, we
391
can conclude that overthrow is rare or nonexistent in
eusocial mole-rats and, if it does occur, can cause
extreme colony destabilization and the death of colony
members as they fight for breeder status.
Testing predictions of conflict
We made a number of predictions of conflict and conflict
resolution in societies of totipotent individuals. We then
surveyed conflict and breeder overthrow in two wellstudied examples. How well do our predictions fit the
empirical evidence?
Prediction: Conflict will be increased by polyandry, polygyny
and the opportunity for inbreeding.
Dinoponera colonies are exclusively monogynous and
monoandrous, which increases relatedness among offspring and decreases conflict between breeder and
nonbreeders. In naked mole-rats, data on paternity are
lacking, but it is clear that polyandry does occur to a
greater or lesser extent (with one to three males usually
consorting with the female breeder) (Faulkes et al., 1997)
and that polygyny, although rare, is not unknown.
Consequently, situations can occur when colonies produce half-siblings (or nonsiblings if multiple breeders of
both sex occur). This alone may explain why Dinoponera
gamergates, heading monogynous and monandrous colonies, can use infrequent and ritualized behaviours like
blocking to indicate condition, while naked mole-rat
breeders, sometimes heading less-related colonies, may
have to use more direct and escalated signals and even
real aggression. The plasticity of mating structure seen in
naked mole-rats (ranging from monogyny and monandry to polygyny and polyandry) and the capacity for both
peaceful and aggressive colony states lead to the prediction that colony members may be able to assess colony
mating structure and act accordingly to increase their
inclusive fitness (as occurs in a social wasp, Foster &
Ratnieks, 2000; and in Formica ants, Sundstrom et al.,
1996). The high genetic similarity between individual
mole-rats (Faulkes et al., 1997) and a common rearing
environment make fine-scale kin recognition problematic, but we predict that studies of conflict and aggression
in naked mole-rat colonies may reveal that breeder
aggression and nonbreeder challenges are greater in
polygynous and polyandrous colonies than in monogynous and monandrous colonies.
Reeve & Sherman (1991) predicted that parent-offspring conflict over reproduction is encouraged if a focal
daughter can overthrow her mother and is able to
inbreed with her father. This incestuous mating results in
offspring that are more related to the focal daughter than
full-siblings. Certainly, naked mole-rats do inbreed but
recent studies of both laboratory and field colonies
indicate that inbreeding is not the default system of
mating and that outbreeding is preferred (Clarke &
Faulkes, 1997; Braude, 2000; Ciszek, 2000). In support of
this a dispersive, and predominantly male, morph exists,
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
392
A . G . H A R T A N D F. L . W . R A T N I E K S
which although rare, is morphologically, physiologically
and behaviourally distinct from other colony members
(O’Riain et al., 1996). Overall, father–daughter unions
can be predicted both to occur and to increase intracolonial conflict but these predictions cannot yet be
supported with empirical data.
Prediction: Conflict will vary through time, increasing as the
breeder nears the end of her life and should be greatest
immediately after breeder replacement.
Conflict varies across time in both Dinoponera and
naked mole-rats. Extreme aggression is associated with
breeder replacement although data relating aggression to
breeder age/condition are not available. Inclusive fitness
analysis suggests that the initial aggression associated
with the period after breeder replacement is caused by
sibling–sibling competition for breeding rights. However,
once a breeder is established and the colony reverts to
parent-offspring kin structure, behaviours like blocking
(Dinoponera) and shoving [in naked mole-rats, perhaps in
conjunction with vocal and nonvocal behaviour (Clarke
& Faulkes, 2001)] are probably honest signals of breeder
condition and are sufficient to prevent offspring from
attempting overthrow. The relative frequency of peaceful
and nonpeaceful periods will be affected by colony kin
structure and their duration is likely to be affected by lifespan. In long-lived animals like naked mole-rats it may
take longer to revert to a parent-offspring colony
structure than it will for a shorter-lived animal like
Dinoponera.
The only extremely aggressive act found in Dinoponera
is immobilization. This behaviour is particularly interesting since it is actually performed by low-rankers and
normally serves to reduce the rank of (or even kill) highrankers who challenge the gamergate. Immobilization is
an effective combination of the gamergate’s ability to
identify challengers and the collective ability of workers
to punish them. Immobilization is only expected when
the interests of the gamergate and low-rankers coincide,
with both parties wishing to prevent a daughter (from
the gamergate’s perspective), or a sister (from the lowrankers’ perspective), from overthrowing the gamergate.
Similar breeder/nonbreeder coalitions are possible in
naked mole-rats. However, naked mole-rats live in
narrow tunnels and confrontations are often confined
to dyads, with individuals meeting and fighting face-toface. In such a confined arena, pitched battles are
unlikely although it is possible that in natural colonies
with nonuniform tunnel systems and, perhaps, more
room to manoeuvre, ‘unison teams’ of lower-ranked
individuals may gang-up on high-rankers as occurs in
Dinoponera. In a situation almost directly analogous to
immobilization in Dinoponera, Kaufmann (1986) reports
four instances in which nonbreeding males were
attacked by groups of colony members after the breeders
of both sexes gave an ‘up-sweep’ call (reported in Pepper
et al., 1991). In this situation, the vocalization seems
analogous to the chemical smear of the gamergate,
marking an individual out for aggression from nonbreeding colony members.
Prediction: Overthrow is likely to be rare and breeder
replacement is expected to occur at the end of a breeder’s
lifetime.
Overthrow of the gamergate in Dinoponera is rare and
does appear to occur when the gamergate is reproductively failing (Monnin & Ratnieks, 2001). Overthrow has
been recorded once in naked mole-rats (Faulkes, 1990),
although field data are understandably lacking, and
laboratory studies are limited by ethical considerations.
Prediction: Colony members should be able to assess reliably
the breeder’s condition.
Our analysis shows that in monogynous and monandrous colonies, breeders’ offspring should be content to
rear siblings provided the breeder is in good condition.
Therefore, honest signalling of breeder condition is likely
to be central to reducing reproductive conflict in societies
of totipotent individuals. In Dinoponera, all of the
gamergate’s agonistic behaviours (with the exception of
leg biting) are more plausibly interpreted as ritualized
signals of condition than as dominant, coercive behaviours aimed at subduing potentially rebellious nonbreeders. Naked mole-rats are ‘not perfectly harmonious
societies’ (Reeve & Sherman, 1991) and aggression in
naked mole-rats has been interpreted as dominance
behaviour associated with directly suppressing subordinate reproduction. Indeed, naked mole-rats have been
generally regarded as a ‘classic example of a dominant
control model’ (Faulkes & Bennett, 2001). However, the
exact causal mechanism of reproductive suppression in
naked mole-rats remains elusive and our analysis, and
the evidence from Dinoponera and naked-mole-rats,
suggests that dominant control and coercive behaviours
are less important than honest signalling and inclusive
fitness in societies of related totipotent individuals. We
doubt that it is possible for a single individual to
physically suppress reproduction in such populous and
spatially distributed colonies as are typical in naked
mole-rats. However, whatever the fine details of reproductive suppression, it is clear that shoving could act as an
honest signal of breeder condition and that the initiators
and recipients of shoving (breeders shove large, highranking and less-related individuals) are consistent with
honest signalling.
Prediction: Post-overthrow (or breeder replacement) instability is expected to be greater in diploid groups than in
haplodiploid groups.
Experimental removal of the breeder in naked molerats (simulating an overthrow event) caused considerable
colony instability over a total 16 months and the death of
large number of colony members. Natural replacement of
the gamergate through usurpation in Dinoponera, invoked instability but this was qualitatively less than in
naked mole-rats, lasting for only few weeks (Monnin &
Peeters, 1999) and did not result in the death of colony
members. However, this evidence must be interpreted
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Reproductive conflict in totipotent societies
cautiously. First, we are only comparing two species with
different ploidy, which clearly weakens the support for
our prediction. Second, as discussed above life-span is
likely to affect the duration of post-overthrow instability
since long-lived animals like naked mole-rats may take
longer to revert to a parent-offspring colony structure
than shorter-lived Dinoponera will and this may play a
greater role than ploidy in prolonging post-overthrow
instability. However, even in Dinoponera it can take
months for a new gamergate’s offspring to emerge and
perhaps a year or more to replace all the previous
gamergate’s offspring. Furthermore, naked mole-rats can
relatively easily maim and kill each other in head-tohead confrontations, whereas Dinoponera can only kill
when several individuals act in concert to immobilize a
focal individual for several days. Therefore, regardless of
ploidy, aggression may be less escalated and less frequent
in Dinoponera than in naked mole-rats.
Given that breeder replacement changes the colony
structure from parent-offspring to siblings, a new breeder
might be predicted to commit siblicide, thereby hastening
the reversion to a parent-offspring colony and reducing
colony conflict. Wholesale slaughter of siblings will likely
lead to greatly reduced colony productivity, but we might
predict that high ranking, strong individuals could be
selectively eradicated. Gamergate-directed immobilization of high rankers can result in death in Dinoponera and
this, were it to happen after overthrow, would be an
example of breeder siblicide (albeit by proxy). Similar
behaviours are not known in naked mole-rats but might
be predicted to occur.
Conclusions
Our examples and inclusive fitness analyses show that
conflicts over breeder replacement in high relatedness
societies may be limited because nonbreeders actually
benefit more by allowing the existing breeder to retain
their role than they do by overthrowing them. Many of
the behaviours performed by breeders can be better
interpreted as honest signals of vitality than as aggressive
acts of reproductive coercion.
Why aggression occurs in naked mole-rat colonies has
been considered an ‘unanswered question’ in naked
mole-rat society (Alexander, 1991). However, conflict
and aggression between breeders and nonbreeders and
between siblings are well characterized and understood
in Dinoponera, a queenless ant with a similar social
structure. Taking the similarity of queenless ants and
eusocial mole-rats as a starting point, we developed an
analysis which made predictions of aggressive behaviour,
kin structure and honest signalling in societies of totipotent individuals. By surveying aggression and overthrow
in Dinoponera and naked mole-rats we were able to show
that different levels of aggression between societies,
aggression variation over time within societies and
specific aggressive situations (such as post-overthrow
393
instability and breeder-triggered group attacks) are all
explicable within this theoretical framework.
A number of mammal and bird species form groups of
reproductively totipotent individuals with extreme
reproductive skew (e.g. meerkats, dwarf mongooses,
wolves, African wild dogs, white-winged choughs, acorn
woodpeckers). Furthermore, there are insects other than
queenless ants that have societies of reproductively
totipotent individuals. We did not intend to make a
broad review of conflict and conflict resolution across all
these societies, and indeed the necessary data are not
available in most cases. Rather, we focused on two types
of well-characterized societies that are both extremely
different yet strikingly similar. However, we predict that
conflict and conflict resolution is fundamentally similar
in other societies of reproductively totipotent individuals. Explicit comparisons of vertebrate (diploid) and
invertebrate (particularly haplodiploid) societies are
rare, but such comparisons can greatly enhance our
understanding of the underlying principles of societal
organization, and help to explain the behaviours
observed.
References
Alexander, R.D. 1991. Some unanswered questions about naked
mole-rats. In: The Biology of the Naked Mole-Rat (P. W.
Sherman, J. U. M. Jarvis & R. D. Alexander, eds), pp. 446–
465. Princeton University Press, Princeton, NJ.
Alexander, R.D., Noonan, K.M. & Crespi, B.J. 1991. The
evolution of eusociality. In: The Biology of the Naked Mole-Rat
(P. W. Sherman, J. U. M. Jarvis & R. D. Alexander, eds), pp.
3–42. Princeton University Press, Princeton, NJ.
Anderson, R.H. 1963. The laying worker in the cape honeybee,
Apis mellifera capensis. J. Apic. Res. 2: 85–92.
Batra, S.W.T. 1966. Nests and social behaviour of halictine bees
of India. Indian J. Entomol. 28: 375–393.
Boleli, I.C., Paulino-Simõnes, Z.L. & Bitondi, M.M.G. 2000.
Regression of the lateral oviducts during larval-adult transformation of the reproductive system of Melipona quadrifasciata
and Frieseomelitta varia. J. Morphol. 243: 141–151.
Bourke, A.F.G. 1988. Worker reproduction in the higher
eusocial Hymenoptera. Q. Rev. Biol. 63: 291–311.
Bourke, A.F.G. & Franks, N.R. 1995. Social Evolution in Ants.
Princeton University Press, Princeton, NJ.
Braude, S. 2000. Dispersal and new colony formation in wild
naked mole-rats: evidence against inbreeding as the system of
mating. Behav. Ecol. 11: 7–12.
Breed, M.D. & Gamboa, G.J. 1977. Behavioral control of
workers by queens in primitively eusocial bees. Science 195:
694–696.
Brett, R.A. 1991a. The population structure of naked mole-rat
colonies. In: The Biology of the Naked Mole-Rat (P. W. Sherman,
J. U. M. Jarvis & R. D. Alexander, eds), pp. 97–136. Princeton
University Press, Princeton, NJ.
Brett, R.A. 1991b. The ecology of naked mole-rat colonies:
borrowing, food, and limiting factors. In: The Biology of the
Naked Mole-Rat (P. W. Sherman, J. U. M. Jarvis & R. D.
Alexander, eds), pp. 137–184. Princeton University Press,
Princeton, NJ.
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
394
A . G . H A R T A N D F. L . W . R A T N I E K S
Burda, H., Honeycutt, R.L., Begall, S., Locker-Grütjen, O. &
Scharff, A. 2000. Are naked and common mole-rats eusocial
and if so, why? Behav. Ecol. Sociobiol. 47: 293–303.
Cagniant, H. 1979. La parthenogenese thelytoque et arrhenotoque chez la fourmi Cataglyphis cursor Fonsc. (Hym. Form.)
cycle biologique en elevage des colonies avec reine et des
colonies sans reine. Insectes Soc. 26: 51–60.
Cant, M.A. 1998. A model for the evolution of reproductive
skew without reproductive suppression. Anim. Behav. 55: 163–
169.
Cant, M.A. & Johnstone, R.A. 2000. Power struggles, dominance
testing, and reproductive skew. Am. Nat. 155: 406–417.
Ciszek, D. 2000. New colony formation in the ‘highly inbred’
eusocial naked mole-rat: outbreeding is preferred. Behav. Ecol.
11: 1–6.
Clarke, F.M. & Faulkes, C.G. 1997. Kin discrimination and
female mate choice in the naked mole-rat, Heterocephalus
glaber. Proc. R. Soc. Lond. B Biol. Sci. 266: 1995–2002.
Clarke, F.M. & Faulkes, C.G. 1998. Hormonal and behavioural
correlates of male dominance and reproductive status in
captive colonies of the naked mole-rat Heterocephalus glaber.
Proc. R. Soc. Lond. B Biol. Sci. 265: 1391–1399.
Clarke, F.M. & Faulkes, C.C. 2001. Intracolony aggression in the
eusocial naked mole-rat, Heterocephalus glaber. Anim. Behav. 61:
311–324.
Clutton-Brock, T.H. 1998. Reproductive skew, concessions and
limited control. Trends Ecol. Evol. 13: 288–292.
Clutton-Brock, T.H., Brotherton, P.N.M., Russell, A.F., O’Riain,
M.J., Gaynor, D., Kansky, R., Griffin, A., Manser, M., Sharpe,
L., McIlrath, G.M., Small, T., Moss, A. & Monfort, S. 2001.
Cooperation, control and concession in meerkat groups.
Science 291: 478–481.
Creel, S.R. & Macdonald, D.W. 1995. Sociality, group size and
reproductive suppression among carnivores. Adv. Study Behav.
24: 203–257.
Crespi, B.J. 1992. Eusociality in Australian gall thrips. Nature
359: 724–726.
Duffy, J.E. 1996. Eusociality in a coral-reef shrimp. Nature 381:
512–514.
Faulkes, C.G. 1990. Social suppression of reproduction in the
naked mole-rat, Heterocephalus glaber. Unpublished PhD
thesis, University of London, London, pp. 162–164
Faulkes, C.G. & Abbott, D.H. 1996. Proximate regulation of a
reproductive dictatorship: a single dominant female controals
male and female reproduction in colonies of naked mole-rats.
In: Cooperative Breeding in Mammals (N. G. Solomon & J. A.
French, eds), pp. 302–334. Cambridge University Press, New
York.
Faulkes, C.G. & Bennett, N.C. 2001. Family values: group
dynamics and social control of reproduction in African molerats. Trends Ecol. Evol. 16: 184–190.
Faulkes, C.G., Abbott, D.H., O’Brien, H.P., Lau, L., Roy, M.R.,
Wayne, R.K. & Bruford, M.W. 1997. Micro- and macrogeographical genetic structure of colonies of naked mole-rats
Heterocephalus glaber. Mol. Ecol. 6: 615–628.
Foster, K.R. & Ratnieks, F.L.W. 2000. Social insects – facultative
worker policing in a wasp. Nature 407: 692–693.
Hamilton, W.D. 1964. The genetical evolution of social behaviour, I & II. J. Theor. Biol. 7: 1–52.
Haskins, C.P. & Zahl, P.A. 1971. The reproductive pattern of
Dinoponera grandis Roger (Hymenoptera, Ponerinae) with
notes on the ethology of the species. Psyche 78: 1–11.
Heinze, J. & Hölldobler, B. 1995. Thelytokous parthenogenesis
and dominance hierarchies in the ponerine ant, Platythyrea
punctata. Naturwissenschaften 82: 40–41.
Honeycutt, R.L., Nelson, K., Schlitter, D.A. & Sherman, P.W.
1991. Genetic variation within and among populations of the
naked mole-rat: evidence from nuclear and mitochondrial
genomes. In: The Biology of the Naked Mole-Rat (P. W. Sherman,
J. U. M. Jarvis & R. D. Alexander, eds), pp. 195–208. Princeton
University Press, Princeton, NJ.
Itow, T., Kobayashim, K., Kubota, M., Ogata, K., Imai, H.T. &
Crozier, R.H. 1984. The reproductive cycle of the queenless
ant Pristomyrmex pungens. Insectes Soc. 31: 87–102.
Jacobs, D.S. & Jarvis, J.U.M. 1996. No evidence for the workconflict hypothesis in the eusocial naked mole-rat (Heterocephalus glaber). Behav. Ecol. Sociobiol. 39: 401–409.
Jarvis, J.U.M. 1981. Eusociality in a mammal: cooperative
breeding in naked mole-rat colonies. Science 212: 571–573.
Jarvis, J.U.M. 1985. Ecological studies on Heterocephalus glaber, the
naked mole-rat, in Kenya. Nat. Geog. Soc. Res. Rep. 20: 429–437.
Jarvis, J.U.M. 1991. Reproduction of naked mole-rats. In: The
Biology of the Naked Mole-Rat (P. W. Sherman, J. U. M. Jarvis &
R. D. Alexander, eds), pp. 384–425. Princeton University
Press, Princeton, NJ.
Jarvis, J.U.M. & Bennett, N.C. 1993. Eusociality has evolved
independently in 2 genera of bathyergid mole-rats – but
occurs in no other subterranean mammal. Behav. Ecol. Sociobiol. 33: 253–260.
Jarvis, J.U.M., O’Riain, M.J., Bennett, N.C. & Sherman, P.W.
1994. Mammalian eusociality: a family affair. Trends Ecol. Evol.
9: 47–51.
Kaufmann, E. 1986. Vocalisations in the naked mole-rat
(Heterocephalus glaber). Undergraduate Honors Thesis, Cornell
University, Ithaca, NY.
Keller, L. & Reeve, H.K. 1994. Partitioning of reproduction in
animal societies. Trends Ecol. Evol. 9: 98–103.
Kempf, W.W. 1971. A preliminary review of the ponerine ant
genus Dinoponera Roger (Hymenoptera: Formicidae). Studia
Entomol. 14: 369–394.
Kent, D.S. & Simpson, J.A. 1992. Eusociality in the beetle
Austroplatypus incompertus (Coleoptera, Curculionidae). Naturwissenschaften 79: 86–87.
Lacey, E.A. & Sherman, P.W. 1991. Social organization of naked
mole-rat colonies: evidence for divisions of labor. In: The
Biology of the Naked Mole-Rat (P. W. Sherman, J. U. M. Jarvis &
R. D. Alexander, eds), pp. 275–336. Princeton University
Press, Princeton, NJ.
Lacey, E.A. & Sherman, P.W. 1997. Cooperative breeding in
naked mole-rats: implications for vertebrate and invertebrate
sociality. In: Cooperative Breeding in Mammals (N. G. Solomon &
J. A. French, eds), pp. 267–301. Cambridge University Press,
New York.
Lacey, E.A., Alexander, R.D., Braude, S.H., Sherman, P.W. &
Jarvis, J.U.M. 1991. An ethogram for the naked mole-rat:
non-vocal behaviours. In: The Biology of the Naked Mole-Rat (P.
W. Sherman, J. U. M. Jarvis & R. D. Alexander, eds), pp. 209–
242. Princeton University Press, Princeton, NJ.
Mackensen, O. 1943. The occurrence of parthenogenetic females
in some strains of honeybees. J. Econ. Entomol. 36: 465–467.
Maynard Smith, J. 1956. Fertility, mating behaviour and sexual
selection in Drosophila subobscura. J. Genet. 54: 261–279.
Michener, C.D. 1974. The Social Behavior of the Bees. The Belknap
Press, Cambridge, MA.
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Reproductive conflict in totipotent societies
Monnin, T. & Peeters, C. 1998. Monogyny and regulation of
worker mating in the queenless ant Dinoponera quadriceps.
Anim. Behav. 55: 299–306.
Monnin, T. & Peeters, C. 1999. Dominance hierarchy and
reproductive conflicts among subordinates in a monogynous
queenless ant. Behav. Ecol. 10: 323–332.
Monnin, T. & Ratnieks, F.L.W. 2001. Policing in queenless
ponerine ants. Behav. Ecol. Sociobiol. 50: 97–108.
Monnin, T., Malosse, C. & Peeters, C. 1998. Solid-phase
microextraction and cuticular hydrocarbon differences related
to reproductive activity in queenless ant Dinoponera quadriceps.
J. Chem. Ecol. 24: 493–490.
Monnin, T., Ratnieks, F.L.W., Jones, G.R. & Beard, R. 2002.
Pretender punishment induced by chemical signalling in a
queenless ant. Nature 419: 61–65.
Monnin, T., Ratnieks, F.L.W. & Brandão, C.R.F. 2003. Reproductive conflict in animal societies: hierarchy increases with
colony size in queenless ponerine ants. Behav. Ecol. Sociobiol.
54: 71–79.
Moritz, R.F.A. & Harberl, M. 1994. Lack of meiotic recombination in thelytokous parthenogenesis of laying workers of Apis
mellifera capensis (the Cape honeybee). Heredity 73: 98–102.
O’Riain, M.J., Jarvis, J.U.M. & Faulkes, C.G. 1996. A dispersive
morph in the naked mole-rat. Nature 380: 619–621.
O’Riain, M.J., Jarvis, J.U.M., Alexander, R., Buffenstein, R. &
Peeters, C. 2000. Morphological castes in a vertebrate. Proc.
Natl Acad. Sci. USA 97: 13194–13197.
Onions, G.W. 1912. South African ‘fertile-worker bees’. S. Afr.
Agric. J. 1: 720–728.
Paiva, R.V.S. & Brandão, C.R.F. 1995. Nests, worker population,
and reproductive status of workers, in the true giant queenless
ponerine ant Dinoponera Roger (Hymenoptera: Formicidae).
Ethol. Ecol. Evol. 7: 297–312.
Peeters, C. 1993. Monogyny and polygyny in ponerine ants with
or without queens. In: Queen Number and Sociality in Insects (L.
Keller, ed.), pp. 235–261. Oxford University Press, Oxford.
Peeters, C. 1997. Morphologically ‘primitive’ ants: comparative
review of social characters, and the importance of queenworker dimorphism. In: The Evolution of Social Behavior in
Insects and Arachnids (J. Choe & B. Crespi, eds), pp. 372–391.
Cambridge University Press, Cambridge.
Peeters, C., Monnin, T. & Malosse, C. 1999. Cuticular hydrocarbons correlated with reproductive status in a queenless ant.
Proc. R. Soc. Lond. B Biol. Sci. 266: 1323–1327.
Pepper, J.W., Braude, S.H., Lacey, E.A. & Sherman, P.W. 1991.
Vocalisations of the naked mole-rat. In: The Biology of the Naked
Mole-Rat (P. W. Sherman, J. U. M. Jarvis & R. D. Alexander,
eds), pp. 243–274. Princeton University Press, Princeton, NJ.
Reeve, H.K. 1991. Polistes. In: The Social Biology of Wasps (K. G.
Ross & R. W. Matthews, eds), pp. 99–148. Cornell University
Press, Itahca, NY.
Reeve, H.K. 1992. Queen activation of lazy workers in colonies
of the eusocial naked mole-rat. Nature 358: 147–149.
Reeve, H.K. & Ratnieks, F.L.W. 1993. Queen-queen conflict in
polygynous societies: mutual tolerance and reproductive
395
skew. In: Queen Number and Sociality in Insects (L. Keller, ed.),
pp. 45–85. Oxford University Press, Oxford.
Reeve, H.K. & Sherman, PW. 1991. Intracolonial aggression and
nepotism by the breeding female naked mole-rat. In: The
Biology of the Naked Mole-Rat (P. W. Sherman, J. U. M. Jarvis &
R. D. Alexander, eds), pp. 337–357. Princeton University
Press, Princeton, NJ.
Reeve, H.K., Westneat, D.F., Noon, W.A., Sherman, P.W. &
Aquadro, C.F. 1990. DNA fingerprinting reveals high levels of
inbreeding in colonies of the eusocial naked mole-rat. Proc.
Natl Acad. Sci. USA 87: 2496–2500.
Seger, J. 1993. Opportunities and pitfalls in co-operative
reproduction. In: Queen Number and Sociality in Insects (L.
Keller, ed.), pp. 1–15. Cambridge University Press, Cambridge.
Sherman, P.W., Jarvis, J.U.M. & Braude, S.H. 1992. Naked
mole-rats. Sci. Am. 267: 72–78.
Snowdon, C.T. 1996. Infant care in cooperatively breeding
species. Adv. Study Behav. 25: 643–689.
Solomon, N.G. & French, J.A. 1997. Cooperative Breeding in
Mammals. Cambridge University Press, Cambridge.
Sommeijer, M.J., Chinh, T.X. & Meeuwsen, F.J.A.J. 1999.
Behavioural data on the production of males by workers in
the stingless bee Melipona favosa (Apidae, Meliponinae).
Insectes Soc. 46: 92–93.
Stacey, P.B. & Koenig, W.D. 1990. Cooperative Breeding in Birds.
Long Term Studies of Ecology and Behaviour. Cambridge
University Press, Cambridge.
Stern, D.L. & Foster, W.A. 1996. The evolution of soldiers in
aphids. Biol. Rev. 71: 27–79.
Strassman, J.E., Sullender, B.W. & Queller, D.C. 2002. Caste
totipotency and conflict in a large-colony social insect. Proc. R.
Soc. Lond. B Biol. Sci. 269: 263–270.
Sundstrom, L., Chapuisat, M. & Keller, L. 1996. Conditional
manipulation of sex ratios by ant workers: a test of kin
selection theory. Science 274: 993–995.
Thorne, B.L. 1997. The origin of eusociality in termites. Annu.
Rev. Ecol. Syst. 28: 27–54.
Tóth, E., Strassman, J.E., Nogueira-Nato, P., Imperatriz-Fonseca,
V. & Queller, D.C. 2002. Male production in stingless bees:
variable outcomes of queen-worker conflict. Mol. Ecol. 11:
2661–2667.
Tsuji, K. & Yamauchi, K. 1995. Production of females by
parthenogenesis in the ant, Cerapachys biroi. Insectes Soc. 42:
333–336.
van der Westhuizen, L.A., Bennett, N.C. & Jarvis, J.U.M. 2002.
Behavioural interactions, basal plasma luteinizing hormone
concentrations and the differential pituitary responsiveness to
exogenous gonadotrophin-releasing hormone in entire colonies of the naked mole-rat (Heterocephalus glaber). J. Zool.
(Lond.) 256: 25–33.
Wilson, E.O. 1971. The Insect Societies. The Belknap Press,
Cambridge, MA.
Received 24 June 2004; revised 19 July 2004; accepted 9 August 2004
J. EVOL. BIOL. 18 (2005) 383–395 ª 2004 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY