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2016 - Cheating and Punishment in Cooperative Animal Societies
2016 - Cheating and Punishment in Cooperative Animal Societies
animal societies
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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,
Review Ontario, Canada M5S 3B2
Cite this article: Riehl C, Frederickson ME. Cheaters—genotypes that gain a selective advantage by taking the benefits
2016 Cheating and punishment in cooperative of the social contributions of others while avoiding the costs of cooperat-
animal societies. Phil. Trans. R. Soc. B 371: ing—are thought to pose a major threat to the evolutionary stability of
20150090. cooperative societies. In order for cheaters to undermine cooperation, cheat-
ing must be an adaptive strategy: cheaters must have higher fitness than
http://dx.doi.org/10.1098/rstb.2015.0090
cooperators, and their behaviour must reduce the fitness of their cooperative
partners. It is frequently suggested that cheating is not adaptive because
Accepted: 19 November 2015 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
One contribution of 18 to a theme issue
been favoured over selfish ones—hence, behaviours that have been inter-
‘The evolution of cooperation based on direct preted as ‘cheating’ may not actually result in increased fitness, even
fitness benefits’. when they go unpunished. Here, we review the empirical evidence for cheat-
ing behaviours in animal societies, including cooperatively breeding
Subject Areas: vertebrates and social insects, and we ask whether such behaviours are pri-
marily limited by punishment. Our review suggests that both cheating and
behaviour, cognition, ecology, genetics,
punishment are probably rarer than often supposed. Uncooperative individ-
evolution, theoretical biology uals typically have lower, not higher, fitness than cooperators; and when
evidence suggests that cheating may be adaptive, it is often limited by fre-
Keywords: quency-dependent selection rather than by punishment. When apparently
cooperation, cheating, punishment, punitive behaviours do occur, it remains an open question whether they
evolved in order to limit cheating, or whether they arose before the evolution
eusociality, policing, reciprocity
of cooperation.
& 2016 The Author(s) Published by the Royal Society. All rights reserved.
Table 1. Empirical examples of cheating and punishment in cooperative animal societies. Classification of types of cheating that have been empirically 2
documented in animal societies, within a general framework of the evolution of cooperation adapted from Sachs and Rubenstein [15]. Rather than providing an
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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.
shared genes — cooperative brood care reproduction by worker policing queen control
cooperation increases the by related helpers in subordinates (primarily
inclusive fitness of birds, fish, mammals, in social insects)
then went on to show that individuals playing a one-shot because these are the behaviours most commonly cited as evi-
Prisoner’s Dilemma game always get a higher pay-off from dence that cheating and punishment have co-evolved in
‘defecting’ than from cooperating, even though mutual cooperative animal societies. These categories are (table 1):
cooperation generates a higher pay-off than mutual defection. (i) ‘lazy’ group members that fail to provide alloparental
Probably as a result of the lasting influence of the Prisoner’s care to a shared or communal brood; (ii) subordinates that
Dilemma on thinking about the evolution of cooperation, the reproduce themselves instead of caring for relatives;
antithetical view now dominates: cheating is almost always (iii) defectors on reciprocal partnerships; and (iv) free-riders
considered adaptive, begging the question of how cooperation on collective action. Although there is abundant evidence
between non-relatives can be evolutionarily stable (e.g. [13]). of animals that fall into each of these categories, our review
Here, we review the empirical literature on cooperation in reveals that the fitness consequences of not cooperating
animal societies and ask whether animals that cooperate less are often assumed, but rarely measured. Furthermore,
than other members of their social group are really ‘cheating’. uncooperative individuals almost never prosper. More
We define cheating as an ‘adaptive uncooperative strategy’ frequently, uncooperative individuals appear to have low fit-
[14] that increases the cheater’s fitness at the expense of its ness, an observation with important implications for the
partner or social group [15]. This is very similar to the evolutionary dynamics of cooperation.
recent definition of Ghoul et al. [13], who said that cheating There are several reasons why uncooperative individuals
is ‘a trait that is beneficial to a cheat and costly to a cooperator might have low fitness: (i) poor overall condition may result
in terms of inclusive fitness’. in lower levels of cooperation, (ii) cheating may be subject
This definition has two key components: first, cheaters to negative frequency-dependent selection, (iii) cheaters
must prosper from cheating, and second, they must reduce may be punished by other members of their social group,
the fitness of the individual being cheated. A failure to or (iv) cooperation may confer direct or indirect fitness
cooperate, therefore, does not always represent cheating; for benefits that accrue either immediately or incrementally
example, individuals with few resources may invest little in over the lifetime of the cooperator, making failing to
cooperation but also generally have low fitness. The empirical cooperate maladaptive even in the absence of punishment.
literature is rife with examples of individuals that cooperate In the Prisoner’s Dilemma game, cooperation and defec-
little or not at all in social interactions; here, we critically tion are discrete strategies, but in nature, cooperation is
examine whether these behaviours satisfy the evolutionary usually a continuous trait. Furthermore, the expression of
definition of cheating given above. We organize these cooperation is likely to be condition-dependent, with higher
examples into four categories, not because these represent condition individuals often being better able to make
the only scenarios in which cheating might be favoured, but larger investments into cooperation than lower condition
3
Box 1. Conceptual difficulties with the evolution of punishment.
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Evolutionary origins. Any scenario in which cooperation is maintained by punishment is subject to a ‘chicken-and-egg’ pro-
blem [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 adap-
tive 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
individuals. For example, in some cooperatively breeding birds A final possibility is that cheating has led to the evolution
and mammals, a helper’s condition affects how much allopar- of punishment in animal societies, and thus that uncoopera-
ental care it provides, and experimentally improving a tive individuals have low fitness because other members of
helper’s condition increases cooperation [16,17]. (Alternatively, their social group punish them. The term ‘punishment’ is
the converse relationship may also be possible—i.e. helpers in usually reserved for behaviours that go beyond simply with-
good condition might provide less alloparental care because holding the rewards of cooperation [22,23]. Preferentially
they are less reliant on the benefits that helping generates— rewarding more cooperative partners is termed ‘positive
but we are not aware of empirical examples from animal reciprocity’ or ‘partner choice’ instead [6,15,22], whereas pun-
societies.) Recently, Friesen [18] cleverly called low- ishment is generally defined as paying a cost to harm a
fitness partners that cooperate little in interspecific mutualisms cheating partner, for example by harassing or attacking unco-
‘defective, not defectors’, and this label probably also applies operative individuals in a social group [22–24]. Punishment
to many animals in poor condition that fail to cooperate in will be selectively favoured only if it generates an inclusive
their social groups. Importantly, unlike defectors, ‘defective’ fitness benefit, so the short-term cost of punishment must
genotypes do not threaten the evolutionary stability of be recouped through either a long-term direct fitness benefit
cooperation because they are not favoured by selection and to the punisher or an indirect fitness benefit to related mem-
thus do not spread within populations of cooperators. bers of the social group (termed ‘selfish’ and ‘altruistic’
A second reason that uncooperative individuals can have punishment, respectively, by West et al. [25]). We also restrict
low fitness is negative frequency-dependent selection. The our definition of punishment to those behaviours that have
idea that frequency-dependent selection might limit cheating evolved in order to reduce the fitness of uncooperative indi-
has received comparatively little attention from behavioural viduals and enforce cooperation, excluding many acts of
ecologists, partly because Hamilton’s [9] original formulation aggression among individuals in social groups. As Clutton-
of inclusive fitness showed that the fitness benefits of cooperat- Brock & Parker [22] pointed out, aggressive behaviours
ing with kin remain constant regardless of the proportion of occur in a variety of social contexts, including in dominance
cooperators in the population. However, frequency-dependent and competitive interactions, but these behaviours will often
game theoretical models have explored the evolutionary stab- be favoured even in the absence of cheating and thus need
ility of mixes of cheating and cooperative strategies in groups not have evolved in response to cheating.
of non-relatives (e.g. [19,20]). These models assume that free- Here, we ask whether apparently punitive animal beha-
riders do well when they are rare because they exploit the viours likely evolved in response to cheating. To select for
efforts of a large number of cooperators. But as cheating punishment, cheating must reduce the fitness of the individuals
becomes more common, the benefits of cooperating (and being cheated. However, our review of the literature reveals sur-
hence, the benefits of associating with the group) diminish, prisingly scarce or weak evidence that behaviours often called
and more cooperative groups outcompete groups with more ‘cheating’ actually decrease the fitness of other social group
free-riders (e.g. [21]). Thus, the solution to the game is a members, suggesting that cheating does not drive the evolution
stable equilibrium frequency of each tactic, potentially explain- of punishment. Furthermore, the evolution of punishment
ing how variation in cooperative behaviour is maintained in presents a number of conceptual difficulties (box 1).
natural populations. Note, however, that at equilibrium, all Because our review reveals few systems in which punish-
strategies have equal average fitness in this scenario. ment is parsimoniously interpreted as an adaptation to
cheating, we suggest several alternative explanations for the Another complication is that helpers that appear to be 4
evolution of the apparently punitive behaviours many ani- lazy in one context may participate in other activities or at
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mals exhibit in their social groups. In many cases, these other times [46]. Context-dependent division of labour
behaviours have probably evolved in the absence of cheaters should not be confounded with ‘laziness’, since division of
and are selectively favoured in contexts unrelated to cheating. labour can increase efficiency and benefit all parties [47].
Furthermore, in many animals, harassment or aggression Baglione et al. [40] found that 27% of subordinate carrion
towards uncooperative individuals likely predates the evol- crows were lazy helpers, failing entirely to provision nest-
ution of cooperation and represents the ancestral state. In lings. When dominant individuals were experimentally
other words, in many systems, ‘punishment’ is probably removed, however, lazy helpers voluntarily began visiting
not derived from cheating, but is the background against the nest and provided enough food to fully compensate for
which cooperation first evolved [27,34]. the loss of a breeder, indicating that they may in fact rep-
resent a sort of ‘insurance’ workforce. Removal experiments
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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
them, increasing their levels of effort only when the dominants relatively common for workers to lay eggs that may develop
were restored [58,61]. Although these studies do not demon- into males (worker-produced males or WPMs) or occasion-
strate that cheating itself should be selectively favoured ally into females [68]. Are reproductive workers ‘cheating’
(or, indeed, that cheating occurs) under natural conditions, and how has ‘punishment’ evolved in social insects (box 2)?
they provide strong behavioural evidence that dominants Although we usually expect cheaters to invade popu-
can, and do, monitor the actions of subordinate group lations of cooperators, it is possible that worker reproduction
members; and that aggression by dominants can induce has simply been retained since before the evolution of eusoci-
cooperation by subordinates [30,62–64]. ality (to quote Bourke [68, p. 304], ‘workers may have been
It remains an open question, though, whether punish- selected to produce sons and rear sisters’). In fact, current evi-
ment by dominants evolved as a response to cheating by dence suggests that worker sterility is highly derived within
subordinates, or whether such responses existed before chea- eusocial Hymenoptera and that workers continued to repro-
ters did [26,27]. Particularly in cooperative breeding systems, duce in many lineages long after the evolution of eusociality
where helping is typically facultative, it is possible that domi- [1]. Recent phylogenies could be further leveraged to explore
nant breeders tolerated extra-group individuals that showed how often hymenopteran lineages with reproductive workers
submissive behaviours or provided help, and attacked or are nested in clades in which complete worker sterility is the
evicted those that did not (e.g. [65]). Helping behaviour ancestral condition, and thus whether cheating invades
might therefore function as a type of ‘pre-emptive appease- cooperation at macroevolutionary timescales.
ment’ [34] that propitiates aggressive dominants. In either Much as helpers vary substantially in the amount of help
case, credible threats and punishment may help to maintain they provide, workers vary substantially in how much they
cooperation by subordinate helpers, particularly unrelated reproduce [68,73–77]. A leading explanation to account for
ones; the key question is whether punishment may have some of this variation is worker ‘policing’, which is possibly
played a primary role in the origins of helping behaviour, the most widely cited example of punishment in any animal
rather than having subsequently evolved to lower the benefits society. In some social Hymenoptera, workers eat eggs laid
of cheating [26,66]. 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
(b) Reproduction by subordinates studied empirically in the honeybee, Apis mellifera [78], and
Another behaviour that may or may not represent cheating is has subsequently been described in some ants, wasps and
to reproduce instead of helping to rear the offspring of the other bees [79].
dominant breeder(s). A well-studied potential example is There are two main hypotheses about the evolution of
worker reproduction in social insect colonies, although sub- worker policing in social insects: the relatedness and colony
ordinate reproduction is also known from cooperatively productivity hypotheses (box 2). The former predicts that poli-
breeding vertebrates [30,67]. In eusocial Hymenoptera, cing is selectively favoured because workers increase their
workers usually rear the offspring of their mother, the relatedness to the colony’s males by policing (box 2 and
queen, instead of their own young, presumably because [31]). However, under this hypothesis, worker policing does
doing so increases their inclusive fitness [9]. It is nonetheless not really ‘enforce cooperation’ so much as bias relatedness
in workers’ favour. In other words, the relatedness hypothesis There are several other potential explanations for the evol- 6
predicts that not all worker reproduction is policed (i.e. it is not ution of worker policing behaviours that also have little to do
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cheating per se that is punished), just the production of male with punishment of cheating. For example, workers may
eggs related to workers at r , 0.25. A significant phylogenetic kill all eggs not laid by the queen as a defence against
correlation between worker reproduction and colony kin brood parasitism [69,98]. Or colony members may eat
structure provides some support for this hypothesis, although worker-laid eggs more often than queen-laid eggs because
there is substantial unexplained variation; colonies produce worker-laid eggs are less viable ([99], but see [69,100]).
few WPMs when workers are more related to the queen’s Much as punishment of lazy helpers is often documented
sons than other workers’ sons and many WPMs when this by experimentally preventing subordinates from helping (see
relatedness difference is reversed [75]. Models have also previous section), worker policing is often documented by
explored how worker policing and worker adjustment of experimentally manipulating workers to lay eggs. Exper-
colony sex ratio may evolve in tandem [73,77]. iments demonstrating worker policing usually generate
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Prisoner’s Dilemma situation by the simple decision rule of Hauser & Marler [115], who studied food-associated calls in
‘help anyone if helped by someone’, and that following rhesus macaques. Rhesus macaques often give characteristic
these rules need not be cognitively demanding [105,106]. calls upon finding food, a response that may have evolved
Although empirical evidence for reciprocal cooperation in in order to alert group members to share food. Hauser &
natural, non-captive settings still lags behind theory, recent Marler [115] experimentally provided free-ranging macaques
studies on alloparental care have convincingly interpreted with food and observed the responses of discoverers and
helping behaviour by non-relatives as a type of commodity fellow group members. They found that macaques that
trading—essentially, that helpers ‘pay to stay’ in the social failed to call when they found food were more likely to be
group by providing cooperative services [57,59]. attacked than were those that did call, a result widely inter-
One of the best examples of direct reciprocity in a natural preted as punishment for defecting [116]. However, these
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stag hunts in game theory) may explain the evolutionary remembered their past failures to cooperate—they failed to
stability of many instances of collective action [120,122]. punish them directly (through aggression) or indirectly (by
As relative group size increases, the magnitude of these withdrawing further cooperation). Although this finding was
shared benefits declines since a smaller proportion of group initially considered to be surprising, it now appears to be the
members is needed to provide the same collective good rule rather than the exception. A growing number of studies
[123,124]. When non-cooperating group members are able have explicitly sought behavioural evidence for punishment
to profit from the actions of cooperative group-mates, cheat- and have failed to find it, even when laggards are obvious
ing is no longer costly and cheaters should increase their (for example, in lemurs [127]; chimpanzees [139]; dogs [126];
direct fitness relative to that of cooperators. Empirical studies and sociable weavers [140]).
on cheating in inter-group encounters support the prediction A promising alternative hypothesis is that free-riding on
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erative breeding when it has occurred, but have ‘failed to impose much selection for punishment. These results are
miserably’ at predicting in which lineages it should consistent with recent theory, which has increasingly shown
evolve—or why it is absent in other lineages. Thinking that punishment—even in humans—can be evolutionarily
about punishment as a precondition for stable cooperation stable only under limited circumstances [72,135,138,150],
rather than as an evolved response to cheating may help us and that cooperation is unlikely to evolve when cheating is
to predict when cooperation can evolve. In the same way truly advantageous.
that understanding kin selection has generated testable pre-
dictions about which ancestral mating systems should be
most likely to give rise to cooperation (e.g. [1,3,147]), under- Authors’ contributions. C.R. conceived the review. Both authors contribu-
standing the life-history or behavioural traits that likely ted to conceptual development, wrote the review and approved the
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