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Cheating and punishment in cooperative
animal societies
rstb.royalsocietypublishing.org
Review
Cite this article: Riehl C, Frederickson ME.
2016 Cheating and punishment in cooperative
animal societies. Phil. Trans. R. Soc. B 371:
20150090.
http://dx.doi.org/10.1098/rstb.2015.0090
Accepted: 19 November 2015
One contribution of 18 to a theme issue
‘The evolution of cooperation based on direct
fitness benefits’.
Subject Areas:
behaviour, cognition, ecology, genetics,
evolution, theoretical biology
Keywords:
cooperation, cheating, punishment,
eusociality, policing, reciprocity
Author for correspondence:
Christina Riehl
e-mail: [email protected]
Christina Riehl1 and Megan E. Frederickson2
1
Department of Ecology and Evolutionary Biology, Princeton University, 106A Guyot Hall, Princeton,
NJ 08544, USA
2
Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto,
Ontario, Canada M5S 3B2
Cheaters—genotypes that gain a selective advantage by taking the benefits
of the social contributions of others while avoiding the costs of cooperating—are thought to pose a major threat to the evolutionary stability of
cooperative societies. In order for cheaters to undermine cooperation, cheating must be an adaptive strategy: cheaters must have higher fitness than
cooperators, and their behaviour must reduce the fitness of their cooperative
partners. It is frequently suggested that cheating is not adaptive because
cooperators have evolved mechanisms to punish these behaviours, thereby
reducing the fitness of selfish individuals. However, a simpler hypothesis
is that such societies arise precisely because cooperative strategies have
been favoured over selfish ones—hence, behaviours that have been interpreted as ‘cheating’ may not actually result in increased fitness, even
when they go unpunished. Here, we review the empirical evidence for cheating behaviours in animal societies, including cooperatively breeding
vertebrates and social insects, and we ask whether such behaviours are primarily limited by punishment. Our review suggests that both cheating and
punishment are probably rarer than often supposed. Uncooperative individuals typically have lower, not higher, fitness than cooperators; and when
evidence suggests that cheating may be adaptive, it is often limited by frequency-dependent selection rather than by punishment. When apparently
punitive behaviours do occur, it remains an open question whether they
evolved in order to limit cheating, or whether they arose before the evolution
of cooperation.
1. Introduction
Why should an animal cooperate when it could cheat? By definition,
cooperation benefits others, often at some cost to the cooperator. Thus, selection
should favour ‘cheaters’ that benefit from the social contributions of others
while offering little or nothing in return. But nature tells a different story: cooperative behaviour is taxonomically widespread, and it has persisted and even
flourished over long periods of evolutionary time [1–4]. This apparent contradiction has led the evolution of cooperation to be regarded as one of
evolutionary biology’s greatest puzzles [5–8].
The evolution of cooperation among non-relatives is especially perplexing
because it cannot be explained by kin selection. Hamilton [9] famously
showed that when cooperation is directed at relatives, it can increase the cooperator’s inclusive fitness, even if it decreases the cooperator’s direct fitness.
However, although cooperation among relatives is common, not all
cooperation is directed at kin [4,8,10]. Thus, partners need not be related for
cooperation to evolve.
Game theory has advanced our understanding of the evolution of
cooperation among non-relatives. The ground-breaking works of Trivers [11]
and Axelrod & Hamilton [12] discussed the parallels between the Prisoner’s
Dilemma game and cooperative animal behaviours ranging from alloparental
care in birds to fig pollination by wasps. Axelrod & Hamilton [12] introduced
their paper by noting that, prior to the 1960s, ‘cooperation was always considered adaptive’ because of misguided group-selectionist thinking. They
& 2016 The Author(s) Published by the Royal Society. All rights reserved.
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empirical examples
proposed examples of
cheating
proposed examples
of punishment
proposed alternative
mechanism
shared genes —
cooperation increases the
cooperative brood care
by related helpers in
reproduction by
subordinates (primarily
worker policing
queen control
none documented
frequency-dependent
selection
eviction from social
group; physical
none proposed
inclusive fitness of
cooperative individuals
birds, fish, mammals,
and social insects
in social insects)
through kin selection
mutual benefits —
cooperation generates
immediate fitness benefits
to cooperative individuals
pay-to-stay — individuals
receive future benefits
cooperative hunting,
territory defence, and
‘freeloaders’ —
individuals that profit
mobbing of predators
from collective actions
but do not participate
cooperative brood care
by unrelated helpers
‘lazy helpers’ —
individuals that
when cooperative and bear
withhold alloparental
immediate costs when
non-cooperative
care or deceive
dominant group
reciprocity — individuals
allogrooming; blood
members
‘defectors’ — individuals
alternately give and receive
sharing in vampire
that benefit from a
goods or services
bats; food sharing in
primates
partner’s contribution
but do not reciprocate
then went on to show that individuals playing a one-shot
Prisoner’s Dilemma game always get a higher pay-off from
‘defecting’ than from cooperating, even though mutual
cooperation generates a higher pay-off than mutual defection.
Probably as a result of the lasting influence of the Prisoner’s
Dilemma on thinking about the evolution of cooperation, the
antithetical view now dominates: cheating is almost always
considered adaptive, begging the question of how cooperation
between non-relatives can be evolutionarily stable (e.g. [13]).
Here, we review the empirical literature on cooperation in
animal societies and ask whether animals that cooperate less
than other members of their social group are really ‘cheating’.
We define cheating as an ‘adaptive uncooperative strategy’
[14] that increases the cheater’s fitness at the expense of its
partner or social group [15]. This is very similar to the
recent definition of Ghoul et al. [13], who said that cheating
is ‘a trait that is beneficial to a cheat and costly to a cooperator
in terms of inclusive fitness’.
This definition has two key components: first, cheaters
must prosper from cheating, and second, they must reduce
the fitness of the individual being cheated. A failure to
cooperate, therefore, does not always represent cheating; for
example, individuals with few resources may invest little in
cooperation but also generally have low fitness. The empirical
literature is rife with examples of individuals that cooperate
little or not at all in social interactions; here, we critically
examine whether these behaviours satisfy the evolutionary
definition of cheating given above. We organize these
examples into four categories, not because these represent
the only scenarios in which cheating might be favoured, but
harassment
physical harassment
partner choice
because these are the behaviours most commonly cited as evidence that cheating and punishment have co-evolved in
cooperative animal societies. These categories are (table 1):
(i) ‘lazy’ group members that fail to provide alloparental
care to a shared or communal brood; (ii) subordinates that
reproduce themselves instead of caring for relatives;
(iii) defectors on reciprocal partnerships; and (iv) free-riders
on collective action. Although there is abundant evidence
of animals that fall into each of these categories, our review
reveals that the fitness consequences of not cooperating
are often assumed, but rarely measured. Furthermore,
uncooperative individuals almost never prosper. More
frequently, uncooperative individuals appear to have low fitness, an observation with important implications for the
evolutionary dynamics of cooperation.
There are several reasons why uncooperative individuals
might have low fitness: (i) poor overall condition may result
in lower levels of cooperation, (ii) cheating may be subject
to negative frequency-dependent selection, (iii) cheaters
may be punished by other members of their social group,
or (iv) cooperation may confer direct or indirect fitness
benefits that accrue either immediately or incrementally
over the lifetime of the cooperator, making failing to
cooperate maladaptive even in the absence of punishment.
In the Prisoner’s Dilemma game, cooperation and defection are discrete strategies, but in nature, cooperation is
usually a continuous trait. Furthermore, the expression of
cooperation is likely to be condition-dependent, with higher
condition individuals often being better able to make
larger investments into cooperation than lower condition
Phil. Trans. R. Soc. B 371: 20150090
evolutionary model of
cooperation
2
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Table 1. Empirical examples of cheating and punishment in cooperative animal societies. Classification of types of cheating that have been empirically
documented in animal societies, within a general framework of the evolution of cooperation adapted from Sachs and Rubenstein [15]. Rather than providing an
exhaustive list of models for the evolution of cooperation, we focus here on types of cooperative societies that have been proposed to be vulnerable to
exploitation by cheaters.
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3
individuals. For example, in some cooperatively breeding birds
and mammals, a helper’s condition affects how much alloparental care it provides, and experimentally improving a
helper’s condition increases cooperation [16,17]. (Alternatively,
the converse relationship may also be possible—i.e. helpers in
good condition might provide less alloparental care because
they are less reliant on the benefits that helping generates—
but we are not aware of empirical examples from animal
societies.) Recently, Friesen [18] cleverly called lowfitness partners that cooperate little in interspecific mutualisms
‘defective, not defectors’, and this label probably also applies
to many animals in poor condition that fail to cooperate in
their social groups. Importantly, unlike defectors, ‘defective’
genotypes do not threaten the evolutionary stability of
cooperation because they are not favoured by selection and
thus do not spread within populations of cooperators.
A second reason that uncooperative individuals can have
low fitness is negative frequency-dependent selection. The
idea that frequency-dependent selection might limit cheating
has received comparatively little attention from behavioural
ecologists, partly because Hamilton’s [9] original formulation
of inclusive fitness showed that the fitness benefits of cooperating with kin remain constant regardless of the proportion of
cooperators in the population. However, frequency-dependent
game theoretical models have explored the evolutionary stability of mixes of cheating and cooperative strategies in groups
of non-relatives (e.g. [19,20]). These models assume that freeriders do well when they are rare because they exploit the
efforts of a large number of cooperators. But as cheating
becomes more common, the benefits of cooperating (and
hence, the benefits of associating with the group) diminish,
and more cooperative groups outcompete groups with more
free-riders (e.g. [21]). Thus, the solution to the game is a
stable equilibrium frequency of each tactic, potentially explaining how variation in cooperative behaviour is maintained in
natural populations. Note, however, that at equilibrium, all
strategies have equal average fitness in this scenario.
A final possibility is that cheating has led to the evolution
of punishment in animal societies, and thus that uncooperative individuals have low fitness because other members of
their social group punish them. The term ‘punishment’ is
usually reserved for behaviours that go beyond simply withholding the rewards of cooperation [22,23]. Preferentially
rewarding more cooperative partners is termed ‘positive
reciprocity’ or ‘partner choice’ instead [6,15,22], whereas punishment is generally defined as paying a cost to harm a
cheating partner, for example by harassing or attacking uncooperative individuals in a social group [22–24]. Punishment
will be selectively favoured only if it generates an inclusive
fitness benefit, so the short-term cost of punishment must
be recouped through either a long-term direct fitness benefit
to the punisher or an indirect fitness benefit to related members of the social group (termed ‘selfish’ and ‘altruistic’
punishment, respectively, by West et al. [25]). We also restrict
our definition of punishment to those behaviours that have
evolved in order to reduce the fitness of uncooperative individuals and enforce cooperation, excluding many acts of
aggression among individuals in social groups. As CluttonBrock & Parker [22] pointed out, aggressive behaviours
occur in a variety of social contexts, including in dominance
and competitive interactions, but these behaviours will often
be favoured even in the absence of cheating and thus need
not have evolved in response to cheating.
Here, we ask whether apparently punitive animal behaviours likely evolved in response to cheating. To select for
punishment, cheating must reduce the fitness of the individuals
being cheated. However, our review of the literature reveals surprisingly scarce or weak evidence that behaviours often called
‘cheating’ actually decrease the fitness of other social group
members, suggesting that cheating does not drive the evolution
of punishment. Furthermore, the evolution of punishment
presents a number of conceptual difficulties (box 1).
Because our review reveals few systems in which punishment is parsimoniously interpreted as an adaptation to
Phil. Trans. R. Soc. B 371: 20150090
Evolutionary origins. Any scenario in which cooperation is maintained by punishment is subject to a ‘chicken-and-egg’ problem [26]: did punishment give rise to cooperation, or did cooperation give rise to punishment? If punishment is necessary
for cooperation to be favoured over cheating, then it had to be present before cooperation first evolved. But if punishment is
an adaptation to cheating within social groups, then it is evolutionarily derived [7,26]. Yet some mechanism that conditions
an individual’s fitness on its level of cooperation had to exist for cooperation to evolve, in which case cooperation was adaptive in the absence of punishment. And if cooperation is adaptive without punishment, then there should be little selection
for cheaters and subsequently for punishment. So, which came first?
Co-evolutionary dynamics. The coevolution of cheating and either punishment or partner choice is paradoxical [27–29]: if
cheating selects for punishment, and punishment selects for cooperation, then punishment removes the selective incentive for
its own maintenance. Whether punishment selects for more cooperation or more cheating is open to debate, as it is often
suggested that animals evolve ways to cheat that go unpunished (e.g. [15,17,30,31]). Nonetheless, if punishment is ineffective
against these new cheaters, they do not help to maintain punishment in the population.
Timescale of enforcement. The timescale over which punishment potentially ‘enforces cooperation’ differs between animals
capable of learning or otherwise modifying their behaviour in response to harassment or aggression, and animals in which
selfishness may be a fixed property of a genotype [30]. If animals can learn, punishment may cause individuals to cooperate
as a learned behaviour and thus may generate immediate benefits to the punisher if they repeatedly interact [23]. But if punishment selects for cooperation only in future generations of animals, then costly punishment may fail to produce immediate
benefits within the lifetime of the punisher and should be selected against (but see [32]).
Second-order cheaters. If punishment involves individual costs but group benefits, selection may favour ‘lazy’ punishers
that are in effect a kind of ‘second-order’ cheater [22,23,33]. This simply punts the question from ‘what prevents individuals
from cheating instead of cooperating?’ to ‘what prevents individuals from cheating instead of punishing’?
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Box 1. Conceptual difficulties with the evolution of punishment.
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(a) Withholding alloparental care
Complex cooperative societies often include ‘helpers’, nonbreeding subordinates that help to raise the offspring of
dominant breeders. Helpers are often closely related to the
brood that they help to raise, so indirect fitness benefits
may prevent selection for cheating. In some societies, however, genetic relatedness is low, and cheating behaviours
could be adaptive if group members are able to gain direct
fitness benefits from group membership without paying the
costs of helping [4,35,36]. The direct fitness benefits for an
unrelated helper that joins a social group are reasonably
well documented, including future mating opportunities,
territory inheritance or increased survival [37,38]. But if
unrelated individuals can access the benefits of group membership without helping to rear the group’s young, what
prevents them from withholding alloparental care? Do helpers ever fail to help, and if so, can dominant individuals
punish or coerce them into cooperating?
Many studies have found that helpers vary in the amount
of help they provide, often substantially [39,40]. However,
‘lazy’ helpers are not necessarily increasing their fitness by
avoiding the costs of alloparental care. Instead, individuals
that do little alloparental care may be in low condition and
unable to invest much in helping, often resulting in low fitness. Most available evidence suggests that lazy helpers do
not enjoy enhanced fitness compared with cooperative
members of a group. In fact, one reason that helping is evolutionarily stable may be that the levels of care that helpers
provide are typically dependent on body condition, lowering
the long-term costs of helping [41]. In meerkats, for example,
levels of alloparental care by subordinate females are positively correlated with body mass and rate of weight gain,
so lazy helpers are apparently in poorer condition than
hard-working ones [42]. Food supplementation experiments
suggest that the same is true in cooperatively breeding
moorhens (Gallinula chloropus) [43] and carrion crows
(Corvus corone) [44].
Even when withholding alloparental care might be adaptive for the helper, it may not reduce the brood’s fitness: the
benefits of helping are subject to diminishing returns as the
level of care (or the number of helpers) increases, so once a
sufficiently high level of provisioning is reached, additional
helping no longer augments offspring fitness (reviewed in
[45]). Therefore, helpers may adaptively lower their levels
of effort without selecting for retaliatory behaviours by
dominant breeders.
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Phil. Trans. R. Soc. B 371: 20150090
2. Empirical evidence for cheating and
punishment in cooperative animal societies
Another complication is that helpers that appear to be
lazy in one context may participate in other activities or at
other times [46]. Context-dependent division of labour
should not be confounded with ‘laziness’, since division of
labour can increase efficiency and benefit all parties [47].
Baglione et al. [40] found that 27% of subordinate carrion
crows were lazy helpers, failing entirely to provision nestlings. When dominant individuals were experimentally
removed, however, lazy helpers voluntarily began visiting
the nest and provided enough food to fully compensate for
the loss of a breeder, indicating that they may in fact represent a sort of ‘insurance’ workforce. Removal experiments
suggest that the same may be true for lazy workers in eusocial insect colonies, who—unlike vertebrates—generally
cannot increase their own future reproductive fitness by withholding care since many are functionally or completely sterile
[48 –50]. ‘Lazy’ workers in eusocial insect colonies therefore
pose an interesting comparison to cooperatively breeding
vertebrates, since inactive individuals appear to be widespread, generally cannot increase their own fitness by
withholding help, and are well tolerated by dominants [51].
In vertebrates, a different interpretation for this ‘tolerance
of laziness’ is that helpers deceive dominant group members
into believing that they are providing higher levels of care
than is actually the case. ‘False-feeding’, in which helpers
bring food to the brood but then consume the food themselves rather than delivering it, has been reported in
several species and is often interpreted as a deceptive strategy. In the most frequently cited example, Boland et al. [16]
found that young white-winged chough helpers (Corcorax
melanorhamphos) frequently brought food to the nest and
even placed it into the bill of a nestling, but then removed
the item and consumed the food themselves. Helpers were
most likely to false-feed when they were alone at the nest
(i.e. when other group members could not witness the
deception), and dominant breeders sometimes aggressively
chased helpers that arrived without food. In every other
study of this behaviour, however, results have indicated
that false-feeding is unlikely to have evolved to deceive
dominants. Instead, it appears to reflect a simple trade-off
between the hunger of the helper and the needs of the nestlings: helpers that perform false-feeding are more likely to be
young, inexperienced or in poor condition; and they are
generally insensitive to the presence or absence of other
group members [17,52 –54]. In most of these societies,
though not in choughs, helpers are related to the brood
that they feed, so it is unlikely that false-feeding behaviours
would be selectively favoured if they actually reduced
nestling growth or survival.
But why is cheating so rare in cooperative societies where
helpers are unrelated to the group’s offspring [55 –57]? One
hypothesis proposes that cheaters are rare because the threat
of punishment is ubiquitous—essentially, that cheating and
punishment have co-evolved to the point that neither is
observed in natural populations, though both lurk under
the surface [30,58]. Empirical support for the ubiquity of
punishment comes from manipulative studies in which subordinates are experimentally prevented from helping. In cichlids
and fairy-wrens, dominant individuals were observed to
harass apparent defectors when they were experimentally
prevented from helping [59,60]; and in naked mole-rats and
paper wasps, subordinates became ‘lazier’ when dominant
females were experimentally prevented from punishing
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cheating, we suggest several alternative explanations for the
evolution of the apparently punitive behaviours many animals exhibit in their social groups. In many cases, these
behaviours have probably evolved in the absence of cheaters
and are selectively favoured in contexts unrelated to cheating.
Furthermore, in many animals, harassment or aggression
towards uncooperative individuals likely predates the evolution of cooperation and represents the ancestral state. In
other words, in many systems, ‘punishment’ is probably
not derived from cheating, but is the background against
which cooperation first evolved [27,34].
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5
them, increasing their levels of effort only when the dominants
were restored [58,61]. Although these studies do not demonstrate that cheating itself should be selectively favoured
(or, indeed, that cheating occurs) under natural conditions,
they provide strong behavioural evidence that dominants
can, and do, monitor the actions of subordinate group
members; and that aggression by dominants can induce
cooperation by subordinates [30,62–64].
It remains an open question, though, whether punishment by dominants evolved as a response to cheating by
subordinates, or whether such responses existed before cheaters did [26,27]. Particularly in cooperative breeding systems,
where helping is typically facultative, it is possible that dominant breeders tolerated extra-group individuals that showed
submissive behaviours or provided help, and attacked or
evicted those that did not (e.g. [65]). Helping behaviour
might therefore function as a type of ‘pre-emptive appeasement’ [34] that propitiates aggressive dominants. In either
case, credible threats and punishment may help to maintain
cooperation by subordinate helpers, particularly unrelated
ones; the key question is whether punishment may have
played a primary role in the origins of helping behaviour,
rather than having subsequently evolved to lower the benefits
of cheating [26,66].
(b) Reproduction by subordinates
Another behaviour that may or may not represent cheating is
to reproduce instead of helping to rear the offspring of the
dominant breeder(s). A well-studied potential example is
worker reproduction in social insect colonies, although subordinate reproduction is also known from cooperatively
breeding vertebrates [30,67]. In eusocial Hymenoptera,
workers usually rear the offspring of their mother, the
queen, instead of their own young, presumably because
doing so increases their inclusive fitness [9]. It is nonetheless
relatively common for workers to lay eggs that may develop
into males (worker-produced males or WPMs) or occasionally into females [68]. Are reproductive workers ‘cheating’
and how has ‘punishment’ evolved in social insects (box 2)?
Although we usually expect cheaters to invade populations of cooperators, it is possible that worker reproduction
has simply been retained since before the evolution of eusociality (to quote Bourke [68, p. 304], ‘workers may have been
selected to produce sons and rear sisters’). In fact, current evidence suggests that worker sterility is highly derived within
eusocial Hymenoptera and that workers continued to reproduce in many lineages long after the evolution of eusociality
[1]. Recent phylogenies could be further leveraged to explore
how often hymenopteran lineages with reproductive workers
are nested in clades in which complete worker sterility is the
ancestral condition, and thus whether cheating invades
cooperation at macroevolutionary timescales.
Much as helpers vary substantially in the amount of help
they provide, workers vary substantially in how much they
reproduce [68,73–77]. A leading explanation to account for
some of this variation is worker ‘policing’, which is possibly
the most widely cited example of punishment in any animal
society. In some social Hymenoptera, workers eat eggs laid
by other workers or act aggressively towards workers with
activated ovaries, thereby reducing the number of adult
males that are worker-produced. Worker policing was first
studied empirically in the honeybee, Apis mellifera [78], and
has subsequently been described in some ants, wasps and
other bees [79].
There are two main hypotheses about the evolution of
worker policing in social insects: the relatedness and colony
productivity hypotheses (box 2). The former predicts that policing is selectively favoured because workers increase their
relatedness to the colony’s males by policing (box 2 and
[31]). However, under this hypothesis, worker policing does
not really ‘enforce cooperation’ so much as bias relatedness
Phil. Trans. R. Soc. B 371: 20150090
Theory has focused on two, not necessarily mutually exclusive hypotheses [69] explaining the evolution of worker ‘policing’
in social Hymenoptera.
Relatedness. In a seminal article, Ratnieks [31] showed that a ‘police allele’ will spread when workers are more closely
related to queen-laid than worker-laid male eggs. Workers are always related to their own sons by a coefficient of relatedness
(r) of 0.5, but their relatedness to the sons of queens and the sons of other workers depends on the colony kin structure.
Because Hymenoptera are haplodiploid, when a colony has one queen that has mated once, workers are more related to
the sons of other workers (r ¼ 0.375) than to the sons of the queen (r ¼ 0.25), precluding the evolution of worker policing
through relatedness considerations alone. When queens mate with enough males, however, workers are more related to
the queen’s sons (still r ¼ 0.25) than to the sons of other workers (r decreases to 0.125 as the number of males that mate
with a queen increases), meaning that workers can increase their inclusive fitness by policing egg-laying by other workers.
Colony productivity. Ratnieks [31] also showed that a police allele can be selectively favoured if ‘colony-level efficiency
increases as a result of worker policing’. This hypothesis hinges on worker reproduction reducing colony productivity, for
example because reproductive workers invest time or resources in their own brood at the expense of the queen’s brood. If
policing reduces worker investment in reproduction, in principle, it can increase colony productivity.
Frank [70,71] proposed a more general model for the evolution of any trait that represses competition within groups and
thus increases group productivity, and El-Mouden et al. [72] extended Frank’s model to incorporate more realistic costs and
benefits of policing. Although Frank [70,71] originally found that policing evolves relatively easily (specifically, whenever
r , 1 2 c, in which r is relatedness and c is the cost of policing; thus, policing in this model evolves even at very low relatedness), El-Mouden et al. [72] showed that the conditions favouring the evolution of policing are likely to be much more
restrictive. For example, in the El-Mouden et al. [72] model, policing cannot evolve at low relatedness and cannot fully suppress within-group conflicts, leading the authors to conclude that, ‘policing may be harder to evolve than originally thought’.
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Box 2. Policing in theory.
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(c) Failure to reciprocate, or ‘defecting’ in a reciprocal
interaction
Perhaps the most frequently proposed explanation of
cooperation between unrelated individuals is that it is maintained by reciprocal exchanges of goods or services, in which
one individual suffers a temporary fitness cost in order to
help a partner who later reciprocates the cooperative act
[11]. Axelrod & Hamilton [12] showed that the Prisoner’s
Dilemma can lead to cooperation only if the game is repeated
many times with the same participants: in a one-shot game, it
always pays to defect. Models of the repeated Prisoner’s
Dilemma have shown that the strategies most likely to lead
to stable cooperation are those in which individuals copy
the previous behaviour of their partners, cooperating when
they do and ceasing to cooperate if their partners defect
(‘tit-for-tat’), especially if cooperative players occasionally
forgive defectors (‘generous’ tit-for-tat [7]).
Recent models have extended the original two-partner
dyad to encompass larger cooperative networks, considering
situations in which many individuals can repeatedly interact
to trade commodities under conditions that are less restrictive
and more socially complex than those envisioned by original
solutions of the Prisoner’s Dilemma game [104]. Several
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Phil. Trans. R. Soc. B 371: 20150090
There are several other potential explanations for the evolution of worker policing behaviours that also have little to do
with punishment of cheating. For example, workers may
kill all eggs not laid by the queen as a defence against
brood parasitism [69,98]. Or colony members may eat
worker-laid eggs more often than queen-laid eggs because
worker-laid eggs are less viable ([99], but see [69,100]).
Much as punishment of lazy helpers is often documented
by experimentally preventing subordinates from helping (see
previous section), worker policing is often documented by
experimentally manipulating workers to lay eggs. Experiments demonstrating worker policing usually generate
large numbers of worker-laid eggs by ‘orphaning’ groups
of workers (i.e. separating workers from the queen;
e.g. [78,86,87]) because workers rarely lay eggs when the
queen is present [68]. The fact that workers lay few eggs in
the presence of the queen suggests that it is often the queen
that represses worker reproduction, not other workers.
Recently, Van Oystaeyen et al. [101] identified highly conserved
queen pheromones that prevent worker reproduction in ants,
bees and wasps, perhaps giving new life to the old hypothesis
(e.g. [93]) that most worker reproduction is prevented by queen
traits (e.g. pheromones, aggressive behaviour, etc.). The relative
contribution of worker policing to ‘reproductive harmony’ in
social insect colonies may be fairly small; one estimate is that
worker policing reduces the proportion of WPMs produced
by A. mellifera from approximately 7–0.12% [102], although
Kärcher & Ratnieks [103] recently found only 14 worker-laid
eggs in over 3000 empty drone cells in six A. mellifera colonies.
In general, more studies are needed in which researchers
measure how many eggs are actually laid by workers in
un-manipulated queenright colonies, and how many are
subsequently killed by workers before reaching adulthood
(especially under natural conditions). One possibility is that
worker reproduction is so rare that it imposes little selection
for worker policing, and thus that the worker behaviours that
have been called ‘policing’ have evolved for reasons other
than punishment of cheating.
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in workers’ favour. In other words, the relatedness hypothesis
predicts that not all worker reproduction is policed (i.e. it is not
cheating per se that is punished), just the production of male
eggs related to workers at r , 0.25. A significant phylogenetic
correlation between worker reproduction and colony kin
structure provides some support for this hypothesis, although
there is substantial unexplained variation; colonies produce
few WPMs when workers are more related to the queen’s
sons than other workers’ sons and many WPMs when this
relatedness difference is reversed [75]. Models have also
explored how worker policing and worker adjustment of
colony sex ratio may evolve in tandem [73,77].
There is less evidence for the colony productivity hypothesis, in which worker policing recoups reductions in
colony productivity caused by selfish worker reproduction
(i.e. cheating; box 2). Although several studies have attempted
to measure the costs of worker reproduction to the colony
as a whole, the resulting evidence of costs is very mixed
[21,80 –86]. To our knowledge, no studies have documented
a negative correlation between the number of WPMs and
the number of queen-produced reproductive offspring
made by a colony. The time or energy that workers invest
in rearing their own offspring may trade off with investments
in other tasks, but how this affects colony productivity is largely unknown ([31,80,84,87–89]; but see [21]). Most
experiments comparing colonies that vary in their number
of reproductive workers have found few, if any, differences
in colony productivity [82,83,85,86], although Dobata &
Tsuji [21] recently showed that brood production decreased
when there were more ‘cheaters’ (i.e. reproductive workers)
in laboratory colonies of the parthenogenetic ant Pristomyrmex
punctatus. However, while unrestrained worker reproduction
appears to be costly to P. punctatus colonies, there is no evidence of policing in this ant species [21]; instead, the
authors suggest that cheating and cooperative lineages of
P. punctatus could be maintained by frequency-dependent
selection. Worker policing occurs in other clonal ants
(e.g. [90]), but there are no cheaters in these taxa because
nest-mates are genetically identical (in contrast, the ‘cheaters’
in P. punctatus colonies are a distinct genetic lineage [21]).
Thus, collectively, the results of these studies provide little
evidence that cheating workers select for policing to increase
colony productivity.
‘Policing’ could also be a manifestation of reproductive
competition among subordinates in both social insects
[68,91,92] and vertebrates [30]. In the bumblebee Bombus
terrestris, both queens and workers eat large numbers of
worker-laid eggs, and when workers consume eggs they
often have activated ovaries, though not always [92]. In both
cooperative and non-cooperative breeders, selection should
generally favour females that gain access to a greater share of
local resources for their own offspring by acting aggressively
towards other reproductive females or the other females’
young. Furthermore, brood cannibalism and aggression
among reproductive females is likely ancestral to eusociality
in Hymenoptera; both solitary and primitively eusocial taxa
often engage in these behaviours (e.g. [68,92– 97]). This
suggests that worker policing is not a de novo adaptation in
highly social lineages like Apis, but instead evolved in the
context of a pre-existing behavioural repertoire that included
egg eating and aggression among females. In addition, the
expression of a ‘police allele’ [31] in workers could result
from it being selectively favoured in queens.
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(d) Free-riding on collective action
Collective actions occur when many individuals simultaneously contribute to a common good, such as cooperative
hunting, predator mobbing or defence of a shared territory
[8,117]. Although collective actions do occur in the context of
cooperative breeding societies, we draw a distinction here
between the alloparental care behaviours discussed earlier
and examples of collective action, largely because collective
actions often involve unrelated individuals and in most cases
the immediate fitness pay-offs of cooperating are more
evenly shared among participants. Consider, for example, a
group of white-faced monkeys (Cebus capuchinus) that collectively defends the boundaries of its foraging territory against
neighbouring groups. When two groups are equally motivated to fight, the size of the group is the most important
determinant of success. Each additional group member
increases the odds of winning the interaction by 10% [118].
Individuals that hold back—‘laggards’ that do not participate
in the fight—contribute nothing to their group’s strength,
thereby increasing the probability that their group will suffer
a loss [119].
In this case, cooperation generates immediate, synergistic
rewards that are shared by all group members. Laggards
decrease their own fitness as well as that of their groupmates, so ‘free-riding’ is in fact quite costly. Cheating is limited
because the relative pay-offs of cooperating and defecting
create a stable equilibrium: if other group members do their
part, it is best for the laggard to do his as well [120]. Maynard
Smith & Szàthmary [121] likened this pay-off structure to that
of two people in a rowboat, each with one oar on opposite
sides of the boat. The boat can only move forward if both
row (both players benefit). If only one rows, the boat moves
in circles (neither benefits, but one pays a cost); and if neither
7
Phil. Trans. R. Soc. B 371: 20150090
The sole report of systematic punishment of non-cooperators in a system characterized by reciprocal exchange is from
Hauser & Marler [115], who studied food-associated calls in
rhesus macaques. Rhesus macaques often give characteristic
calls upon finding food, a response that may have evolved
in order to alert group members to share food. Hauser &
Marler [115] experimentally provided free-ranging macaques
with food and observed the responses of discoverers and
fellow group members. They found that macaques that
failed to call when they found food were more likely to be
attacked than were those that did call, a result widely interpreted as punishment for defecting [116]. However, these
results are also consistent with manipulation or coercion:
attacks were usually directed at lower ranking females, and
males that discovered food were rarely attacked even
though they typically did not call [115]. Nor is it clear that
aggressive punishment was costly to enforce—in fact, ‘punishers’ often chased the discoverers away and consumed
the food themselves, suggesting that the primary benefit to
punishing was immediate access to food rather than ensuring
that the discoverer would cooperate in the future. (It is not
even obvious that ‘defectors’ stayed silent in order to conceal
the food from other group members and increase their own
consumption, since individuals were more likely to call
when they were hungry than when they were satiated.)
Given the lack of empirical evidence for costly punishment,
it seems unlikely to play an important role in enforcing
reciprocity in non-human societies.
rstb.royalsocietypublishing.org
models support the hypothesis that generalized reciprocity
can create evolutionarily stable levels of cooperation in a
Prisoner’s Dilemma situation by the simple decision rule of
‘help anyone if helped by someone’, and that following
these rules need not be cognitively demanding [105,106].
Although empirical evidence for reciprocal cooperation in
natural, non-captive settings still lags behind theory, recent
studies on alloparental care have convincingly interpreted
helping behaviour by non-relatives as a type of commodity
trading—essentially, that helpers ‘pay to stay’ in the social
group by providing cooperative services [57,59].
One of the best examples of direct reciprocity in a natural
setting is food sharing by common vampire bats (Desmodus
rotundus), in which reciprocal exchanges of blood meals closely resemble the repeated dyadic encounters originally
envisioned by Trivers [11]. Vampire bats feed exclusively
on blood, and bats that return to the communal roost without
having fed are in danger of starvation unless another bat
regurgitates blood to them. Although the interpretation of
this behaviour as reciprocal altruism [107] has been criticized
on the grounds that bats also feed kin [8], a recent study
found that reciprocity was a stronger predictor of blood
donations than genetic relatedness: individuals preferentially
donated blood to those that had previously donated to them,
and the proportion of partnerships that formed between
unrelated individuals did not differ significantly from that
predicted by random assortment [10]. In order for vampire
bats to preferentially repay those that have helped them,
they must be able to recognize individuals as well as to
remember who has given what, when—perhaps a valid
assumption in vampire bats, since individuals sniff one
another before donating blood and can recognize relatives,
suggesting that odour plays a role in individual recognition.
Moreover, interaction networks are relatively small, with each
bat sharing blood with an average of fewer than four partners. Reciprocal interactions may be further stabilized by
the asymmetry between the costs and benefits of blood
donations: a well-fed individual pays a relatively low fitness
cost when it donates blood, whereas the relative benefit to the
recipient is much larger [107]. The prediction, therefore, is
that cheating is not favoured because defectors should pay
a large direct fitness cost in future losses, although this has
not been tested directly.
Vampire bats appear to meet the crucial requirement of
theoretical solutions of the Prisoner’s Dilemma: cooperators
help those that have previously helped them; therefore, they
presumably fail to help defectors. Recent theory, too, shows
that reciprocity remains stable only when partners are able to
end the relationship when faced with a defector (for example,
by leaving or threatening to leave the social group [108,109]).
But despite a substantial theoretical literature on costly punishment (that largely fails to support its evolutionary stability
[110–112]), there is almost no empirical evidence for punishment that goes beyond withdrawing from a partnership in
interactions involving sequential reciprocal exchanges. In the
most robust examples of reciprocity, such as food exchange in
vampire bats and allogrooming in ungulates, aggression and
physical harassment have not been observed even though individuals sometimes fail to reciprocate [10,113]. Punishment
might evolve more readily in primates, in which social bonds
and individual recognition are well established and interindividual aggression is frequent; but here too evidence is
lacking (thoroughly reviewed by Silk [114]).
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3. Conclusion and future directions
We find little evidence to suggest that cheating and punishment behaviours have co-evolved in cooperative animal
societies. When cheating does occur—for example, when
free-riding monkeys fail to participate in inter-group
fights—punishment behaviours are rare or non-existent,
and the effect of cheating seems to be to limit optimal
group size rather than to select for retaliatory aggression
[118,119]. By contrast, the best-documented examples of punishment come from manipulative experiments in which
cheaters are artificially created, as when dominant cichlids
or fairy-wrens attack subordinates that they perceive to be
unhelpful [59,60] or when worker honeybees police eggs
transferred from queenless colonies [78]. Therefore, there is
evidence that cheating occurs at low frequencies in some
societies and that policing or physical aggression may help
to maintain cooperation in others, but not that the latter has
evolved in response to the former.
In many cases, cooperation appears to be evolutionarily
stable not because cooperators were able to evolve responses
to punish uncooperative cheats, but because such responses
probably existed from the outset, selecting for cooperative
partners. This conclusion has important implications for the
evolutionary dynamics of cooperation, including its origins.
8
Phil. Trans. R. Soc. B 371: 20150090
collective action. Heinsohn & Packer [131] noted that although
leading female lions appeared to recognize laggards—and
remembered their past failures to cooperate—they failed to
punish them directly (through aggression) or indirectly (by
withdrawing further cooperation). Although this finding was
initially considered to be surprising, it now appears to be the
rule rather than the exception. A growing number of studies
have explicitly sought behavioural evidence for punishment
and have failed to find it, even when laggards are obvious
(for example, in lemurs [127]; chimpanzees [139]; dogs [126];
and sociable weavers [140]).
A promising alternative hypothesis is that free-riding on
collective action is adaptive only in certain contexts—as
above, when group size is sufficiently large that cheating is
cost-free—and at low frequencies. Although the role of frequency-dependent selection in stabilizing cooperation has
recently received increased attention, most empirical support
comes from social microbes rather than cooperative vertebrates. For example, several studies have found that
cooperative microbial strains—those that produce a public
good, such as antibiotic compounds, biofilm polymers or
iron-scavenging molecules—can coexist in stable equilibria
with cheating strains, which avail themselves of these goods
without producing any in return. Cheaters have higher fitness
than cooperators when they are rare, since producing these
goods is costly; but their fitness diminishes rapidly as their
prevalence in the population increases [141,142]. It remains
to be seen whether similar dynamics may help explain the
coexistence of leaders and laggards in cooperative vertebrate
groups, since selection for cooperative traits may be weaker
than in social microbes, and animal groups are less highly
structured [143]. Nevertheless, recent intriguing evidence
that negative frequency dependence limits cheating in socially
polymorphic spiders (Anelosimus studiosus) [144] and bark beetles (Dendroctonus frontalis) [145] suggests that this hypothesis
warrants further research in cooperative animal groups.
rstb.royalsocietypublishing.org
rows, the boat does not move at all (neither benefits and
neither pays a cost). N-person rowing games (also known as
stag hunts in game theory) may explain the evolutionary
stability of many instances of collective action [120,122].
As relative group size increases, the magnitude of these
shared benefits declines since a smaller proportion of group
members is needed to provide the same collective good
[123,124]. When non-cooperating group members are able
to profit from the actions of cooperative group-mates, cheating is no longer costly and cheaters should increase their
direct fitness relative to that of cooperators. Empirical studies
on cheating in inter-group encounters support the prediction
that cheating may become profitable in larger groups, finding
that some individuals consistently fail to participate in
aggressive inter-group conflicts (e.g. black howler monkeys,
Alouatta pigra [125]; free-ranging dogs, Canis lupus familiaris
[126]; ring-tailed lemurs, Lemur catta [127]; and wolves,
Canis lupus [128]).
As with lazy helpers in alloparental care systems, though,
it is not always clear whether individual variation in the level
of cooperation represents free-riding. There is little evidence
that laggards profit from their actions, although the fitness
consequences of such behaviours are notoriously hard to
measure. More importantly, lagging is generally correlated
with asymmetries in the benefits accrued from an intergroup conflict and the costs incurred (reviewed in [129]). In
other words, some individuals may invest less in collective
actions simply because they have less to gain or more to
lose, so their failure to participate may reflect individual
differences in age or condition among group members
rather than an attempt to cheat. A comprehensive review of
inter-group interactions in non-human primates found that
most occurrences of free-riding are correlated with variation
in dominance rank, kinship ties and mating success rather
than with immediate gains in direct fitness [130].
In a few cases, however, certain individuals fail to participate in inter-group conflicts regardless of any of these
variables. An influential study by Heinsohn & Packer [131]
found that group-territorial female lions (Panthera leo) could
consistently be assigned to four categories: unconditional
cooperators, who always led the way in territory defence;
conditional cooperators, who participated only when most
needed; conditional laggards, who participated less when
most needed; and unconditional laggards, who always
stayed behind regardless of the group’s need. Along with
the finding that the occurrence of laggards tends to increase
with group size [119,126,132], these results suggest that individuals that hold back from collective actions do sometimes
increase their own fitness at the expense of cooperative
group-mates, though not as frequently as often supposed.
What role, if any, does punishment play in these situations? Despite a large theoretical literature, the evidence
that punishment can suppress free-riders in public goods
games is equivocal at best. Depending on the assumptions
of the model, theory predicts that punishment can promote
cooperation [133,134], have no effect on cooperation [135],
or even undermine cooperation by favouring retaliation
[136,137]. Empirical studies of humans playing N-player
public goods games under laboratory settings suggest that
punishment can be evolutionarily stable, but only under a
very restricted set of conditions (reviewed in [23,138]).
In non-human animal societies, by contrast, there is virtually no empirical evidence that punishment enforces
Downloaded from http://rstb.royalsocietypublishing.org/ on January 4, 2016
phenotypes may be maintained only in mutation-selection
balance [149]. If cheaters are therefore rare, they are unlikely
to impose much selection for punishment. These results are
consistent with recent theory, which has increasingly shown
that punishment—even in humans—can be evolutionarily
stable only under limited circumstances [72,135,138,150],
and that cooperation is unlikely to evolve when cheating is
truly advantageous.
Authors’ contributions. C.R. conceived the review. Both authors contribu-
Competing interests. We have no competing interests.
Funding. C.R. was supported by the Harvard Society of Fellows and by
Princeton University. M.E.F. was supported by an NSERC Discovery
grant and the University of Toronto.
Acknowledgements. We thank Deborah M. Gordon, Egbert G. Leigh Jr.,
Dustin R. Rubenstein, Michael Taborsky and two anonymous
reviewers for their thoughtful and constructive criticisms on earlier
versions of this manuscript; and we thank Meghan J. Strong for editorial assistance in manuscript preparation.
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