REVIEW

observe cooperation between unrelated indi-

viduals or even between members of different

Five Rules for the Evolution

species. Such considerations led Trivers (10) to
propose another mechanism for the evolution of
cooperation, direct reciprocity. Assume that
of Cooperation there are repeated encounters between the same
two individuals. In every round, each player has
Martin A. Nowak a choice between cooperation and defection. If I
cooperate now, you may cooperate later. Hence,
Cooperation is needed for evolution to construct new levels of organization. Genomes, cells, it might pay off to cooperate. This game theoretic
multicellular organisms, social insects, and human society are all based on cooperation. Cooperation framework is known as the repeated Prisoner’s
means that selfish replicators forgo some of their reproductive potential to help one another. But Dilemma.
natural selection implies competition and therefore opposes cooperation unless a specific mechanism But what is a good strategy for playing this
is at work. Here I discuss five mechanisms for the evolution of cooperation: kin selection, direct game? In two computer tournaments, Axelrod
reciprocity, indirect reciprocity, network reciprocity, and group selection. For each mechanism, a simple (11) discovered that the “winning strategy”
rule is derived that specifies whether natural selection can lead to cooperation. was the simplest of all, tit-for-tat. This strat-
egy always starts with a cooperation, then it
volution is based on a fierce competition well-mixed populations needs help for establish- does whatever the other player has done in the

E between individuals and should therefore

reward only selfish behavior. Every gene,
ing cooperation. previous round: a cooperation for a coopera-
tion, a defection for a defection. This simple

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every cell, and every organism should be de- Kin Selection concept captured the fascination of all enthu-
signed to promote its own evolutionary success When J. B. S. Haldane remarked, “I will jump siasts of the repeated Prisoner’s Dilemma.
at the expense of its competitors. Yet we ob- into the river to save two brothers or eight Many empirical and theoretical studies were
serve cooperation on many levels of biolog- cousins,” he anticipated what became later known inspired by Axelrod’s groundbreaking work
ical organization. Genes cooperate in genomes. as Hamilton’s rule (1). This ingenious idea is that (12–14).
Chromosomes cooperate in eukaryotic cells. natural selection can favor cooperation if the But soon an Achilles heel of the world
Cells cooperate in multicellular organisms. There donor and the recipient of an altruistic act are champion was revealed: If there are erroneous
are many examples of cooperation among ani- genetic relatives. More precisely, Hamilton’s rule moves caused by “trembling hands” or “fuzzy
mals. Humans are the champions of cooperation: states that the coefficient of relatedness, r, must minds,” then the performance of tit-for-tat de-
From hunter-gatherer societies to nation-states, exceed the cost-to-benefit ratio of the altruistic act: clines (15, 16). Tit-for-tat cannot correct mis-
cooperation is the decisive organizing principle takes, because an accidental defection leads to a
of human society. No other life form on Earth is r > c/b (1) long sequence of retaliation. At first, tit-for-tat
engaged in the same complex games of cooper- was replaced by generous-tit-for-tat (17), a strat-
ation and defection. The question of how natural Relatedness is defined as the probability of egy that cooperates whenever you cooperate,
selection can lead to cooperative behavior has sharing a gene. The probability that two brothers but sometimes cooperates although you have
fascinated evolutionary biologists for several share the same gene by descent is 1/2; the same defected [with probability 1 − (c/b)]. Natural
decades. probability for cousins is 1/8. Hamilton’s theory selection can promote forgiveness.
A cooperator is someone who pays a cost, became widely known as “kin selection” or Subsequently, tit-for-tat was replaced by
c, for another individual to receive a benefit, “inclusive fitness” (2–7). When evaluating the win-stay, lose-shift, which is the even simpler
b. A defector has no cost and does not deal fitness of the behavior induced by a certain gene, idea of repeating your previous move when-
out benefits. Cost and benefit are measured in it is important to include the behavior’s effect on ever you are doing well, but changing other-
terms of fitness. Reproduction can be genetic kin who might carry the same gene. Therefore, wise (18). By various measures of success,
or cultural. In any mixed population, defectors the “extended phenotype” of cooperative behav- win-stay, lose-shift is more robust than either
have a higher average fitness than cooperators ior is the consequence of “selfish genes” (8, 9). tit-for-tat or generous-tit-for-tat (15, 18). Tit-
(Fig. 1). Therefore, selection acts to increase for-tat is an efficient catalyst of cooperation in a
the relative abundance of defectors. After some Direct Reciprocity society where nearly everybody is a defector,
time, cooperators vanish from the population. It is unsatisfactory to have a theory that can ex- but once cooperation is established, win-stay,
Remarkably, however, a population of only plain cooperation only among relatives. We also lose-shift is better able to maintain it.
cooperators has the highest average fitness,
whereas a population of only defectors has
the lowest. Thus, natural selection constantly
C C C C C D
reduces the average fitness of the popula-
C C
Mutation
C
Selection
D C Selection
D D D
tion. Fisher’s fundamental theorem, which
C C C
states that average fitness increases under
C C D D D D D
constant selection, does not apply here be-
cause selection is frequency-dependent: The
fitness of individuals depends on the fre- Declining average fitness
quency (= relative abundance) of cooperators in Fig. 1. Without any mechanism for the evolution of cooperation, natural selection favors defectors. In a
the population. We see that natural selection in mixed population, defectors, D, have a higher payoff (= fitness) than cooperators, C. Therefore, natural
selection continuously reduces the abundance, i, of cooperators until they are extinct. The average
fitness of the population also declines under natural selection. The total population size is given by N. If
Program for Evolutionary Dynamics, Department of Or-
ganismic and Evolutionary Biology, and Department of there are i cooperators and N − i defectors, then the fitness of cooperators and defectors, respectively,
Mathematics, Harvard University, Cambridge, MA 02138, is given by fC = [b(i − 1)/(N − 1)] − c and fD = bi/(N − 1). The average fitness of the population is given
USA. E-mail: martin_nowak@harvard.edu by ‾f = (b − c)i/N.

1560 8 DECEMBER 2006 VOL 314 SCIENCE www.sciencemag.org

 REVIEW
The number of possible strategies for the reciprocity also leads to the evolution of morality a certain size, it can split into two. In this case,
repeated Prisoner’s Dilemma is unlimited, but (30) and social norms (21, 22). another group becomes extinct in order to con-
a simple general rule can be shown without The calculations of indirect reciprocity are strain the total population size. Note that only
any difficulty. Direct reciprocity can lead to the complicated and only a tiny fraction of this uni- individuals reproduce, but selection emerges
evolution of cooperation only if the probability, verse has been uncovered, but again a simple on two levels. There is competition between
w, of another encounter between the same two rule has emerged (19). Indirect reciprocity can groups because some groups grow faster and
individuals exceeds the cost-to-benefit ratio of only promote cooperation if the probability, q, split more often. In particular, pure cooperator
the altruistic act: of knowing someone’s reputation exceeds the groups grow faster than pure defector groups,
cost-to-benefit ratio of the altruistic act: whereas in any mixed group, defectors re-
w > c/b (2) produce faster than cooperators. Therefore, se-
q > c/b (3) lection on the lower level (within groups) favors
Indirect Reciprocity defectors, whereas selection on the higher level
Direct reciprocity is a powerful mechanism Network Reciprocity (between groups) favors cooperators. This model
for the evolution of cooperation, but it leaves The argument for natural selection of defection is based on “group fecundity selection,” which
out certain aspects that are particularly impor- (Fig. 1) is based on a well-mixed population, means that groups of cooperators have a higher
tant for humans. Direct reciprocity relies on where everybody interacts equally likely with rate of splitting in two. We can also imagine a
repeated encounters between the same two everybody else. This approximation is used by model based on “group viability selection,”
individuals, and both individuals must be able all standard approaches to evolutionary game
to provide help, which is less costly for the dynamics (31–34). But real populations are not
donor than it is beneficial for the recipient. well mixed. Spatial structures or social net-
But often the interactions among humans are works imply that some individuals interact

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asymmetric and fleeting. One person is in a more often than others. One approach of cap-
position to help another, but there is no possi- turing this effect is evolutionary graph theory
bility for a direct reciprocation. We help strangers (35), which allows us to study how spatial struc-
who are in need. We donate to charities that do ture affects evolutionary and ecological dy-
not donate to us. Direct reciprocity is like a barter namics (36–39).
economy based on the immediate exchange of The individuals of a population occupy the
goods, whereas indirect reciprocity resembles the vertices of a graph. The edges determine who
invention of money. The money that fuels the interacts with whom. Let us consider plain
engines of indirect reciprocity is reputation. cooperators and defectors without any strategic
Helping someone establishes a good reputa- complexity. A cooperator pays a cost, c, for
tion, which will be rewarded by others. When each neighbor to receive a benefit, b. Defec-
deciding how to act, we take into account the tors have no costs, and their neighbors receive
possible consequences for our reputation. We no benefits. In this setting, cooperators can
feel strongly about events that affect us directly, prevail by forming network clusters, where
but we also take a keen interest in the affairs of they help each other. The resulting “network
others, as demonstrated by the contents of reciprocity” is a generalization of “spatial rec-
gossip. iprocity” (40).
In the standard framework of indirect rec- Games on graphs are easy to study by com-
iprocity, there are randomly chosen pairwise puter simulation, but they are difficult to analyze
encounters where the same two individuals mathematically because of the enormous num-
need not meet again. One individual acts as ber of possible configurations that can arise.
donor, the other as recipient. The donor can Nonetheless, a surprisingly simple rule deter-
decide whether or not to cooperate. The inter- mines whether network reciprocity can favor
action is observed by a subset of the popu- cooperation (41). The benefit-to-cost ratio must
lation who might inform others. Reputation exceed the average number of neighbors, k, per
allows evolution of cooperation by indirect individual:
reciprocity (19). Natural selection favors strat- Fig. 2. Evolutionary dynamics of cooperators
egies that base the decision to help on the b/c > k (4) and defectors. The red and blue arrows indicate
reputation of the recipient. Theoretical and em- selection favoring defectors and cooperators,
pirical studies of indirect reciprocity show that Group Selection respectively. (A) Without any mechanism for the
people who are more helpful are more likely to Selection acts not only on individuals but also evolution of cooperation, defectors dominate. A
receive help (20–28). on groups. A group of cooperators might be mechanism for the evolution of cooperation can
Although simple forms of indirect reciprocity more successful than a group of defectors. There allow cooperators to be the evolutionarily stable
strategy (ESS), risk-dominant (RD), or advanta-
can be found in animals (29), only humans seem have been many theoretical and empirical studies
geous (AD) in comparison with defectors. (B)
to engage in the full complexity of the game. of group selection, with some controversy, and
Cooperators are ESS if they can resist invasion by
Indirect reciprocity has substantial cognitive recently there has been a renaissance of such defectors. (C) Cooperators are RD if the basin of
demands. Not only must we remember our own ideas under the heading of “multilevel selection” attraction of defectors is less than 1/2. (D)
interactions, we must also monitor the ever- (42–50). Cooperators are AD if the basin of attraction of
changing social network of the group. Language A simple model of group selection works as defectors is less than 1/3. In this case, the fixa-
is needed to gain the information and spread the follows (51). A population is subdivided into tion probability of a single cooperator in a finite
gossip associated with indirect reciprocity. Pre- groups. Cooperators help others in their own population of defectors is greater than the in-
sumably, selection for indirect reciprocity and group. Defectors do not help. Individuals re- verse of the population size (for weak selection).
human language has played a decisive role in produce proportional to their payoff. Offspring (E) Some mechanisms allow cooperators to domi-
the evolution of human intelligence (28). Indirect are added to the same group. If a group reaches nate defectors.

www.sciencemag.org SCIENCE VOL 314 8 DECEMBER 2006 1561

 REVIEW
where groups of cooperators are less likely to go measures of evolutionary success. Suppose a A mechanism for the evolution of cooper-
extinct. game between two strategies, cooperators C and ation can ensure that cooperators become
In the mathematically convenient limit of defectors D, is given by the payoff matrix ESS, RD, or AD (Fig. 2). Some mechanisms
weak selection and rare group splitting, we ob- even allow cooperators to dominate defectors,
tain a simple result (51): If n is the maximum C D which means a > g and b > d.
group size and m is the number of groups, then C a b
group selection allows evolution of cooperation, D g d Comparative Analysis
provided that We have encountered five mechanisms for the
The entries denote the payoff for the row evolution of cooperation (Fig. 3). Although the
b/c > 1 + (n/m) (5) player. Without any mechanism for the evolution mathematical formalisms underlying the five
of cooperation, defectors dominate cooperators, mechanisms are very different, at the center of
Evolutionary Success which means a < g and b < d. A mechanism for each theory is a simple rule. I now present a
Before proceeding to a comparative analysis of the evolution of cooperation can change these coherent mathematical framework that allows
the five mechanisms, let me introduce some inequalities. the derivation of all five rules. The crucial idea
1) If a > g, then cooperation is an evo- is that each mechanism can be presented as a
lutionarily stable strategy (ESS). An infinitely game between two strategies given by a 2 × 2
Kin selection large population of cooperators cannot be in- payoff matrix (Table 1). From this matrix, we
vaded by defectors under deterministic selec- can derive the relevant condition for evolution
tion dynamics (32). of cooperation.
1 r 2) If a + b > g + d, then cooperators are For kin selection, I use the approach of
risk-dominant (RD). If both strategies are inclusive fitness proposed by Maynard Smith

Downloaded from http://science.sciencemag.org/ on October 28, 2017

Direct reciprocity ESS, then the risk-dominant strategy has the (31). The relatedness between two players is r.
bigger basin of attraction. Therefore, your payoff multiplied by r is added
3) If a + 2b > g + 2d, then cooperators are to mine. A second method, shown in (53), leads
advantageous (AD). This concept is important to a different matrix but the same result. For
for stochastic game dynamics in finite pop- direct reciprocity, the cooperators use tit-for-tat
ulations. Here, the crucial quantity is the fix- while the defectors use “always-defect.” The
Indirect reciprocity ation probability of a strategy, defined as the expected number of rounds is 1/(1 − w). Two
probability that the lineage arising from a tit-for-tat players cooperate all the time. Tit-for-
single mutant of that strategy will take over tat versus always-defect cooperates only in the
the entire population consisting of the other first move and then defects. For indirect rec-
strategy. An AD strategy has a fixation proba- iprocity, the probability of knowing someone’s
bility greater than the inverse of the popu- reputation is given by q. A cooperator helps
lation size, 1/N. The condition can also be unless the reputation of the other person in-
expressed as a 1/3 rule: If the fitness of the in- dicates a defector. A defector never helps. For
Network reciprocity vading strategy at a frequency of 1/3 is greater network reciprocity, it can be shown that the
than the fitness of the resident, then the fix- expected frequency of cooperators is described
ation probability of the invader is greater than by a standard replicator equation with a trans-
1/N. This condition holds in the limit of weak formed payoff matrix (54). For group selection,
selection (52). the payoff matrices of the two games—within

Table 1. Each mechanism can be described by a simple 2 × 2 payoff matrix, which specifies the
interaction between cooperators and defectors. From these matrices we can directly derive the nec-
essary conditions for evolution of cooperation. The parameters c and b denote, respectively, the cost
for the donor and the benefit for the recipient. For network reciprocity, we use the parameter H =
Group selection [(b − c)k − 2c]/[(k + 1)(k − 2)]. All conditions can be expressed as the benefit-to-cost ratio
exceeding a critical value. See (53) for further explanations of the underlying calculations.

Cooperation is…
Payoff matrix
C D ESS RD AD
Kin C (b c)(1 r ) br c b 1 b 1 b 1
r…genetic relatedness
selection D b rc 0 c r c r c r
Cooperators Defectors

Fig. 3. Five mechanisms for the evolution of Direct C (b c) /(1 w) c b 1 b 2 w b 3 2w w…probability of next round
reciprocity D b 0 c w c w c w
cooperation. Kin selection operates when the
donor and the recipient of an altruistic act are
Indirect C b c c(1 q) b 1 b 2 q b 3 2q q…social acquaintanceship
genetic relatives. Direct reciprocity requires re- reciprocity D b(1 q ) 0 c q c q c q
peated encounters between the same two individ-
uals. Indirect reciprocity is based on reputation; a Network C b c H c b b b
helpful individual is more likely to receive help. reciprocity k k k k…number of neighbors
D b H 0 c c c
Network reciprocity means that clusters of coop-
erators outcompete defectors. Group selection is b n b n b n n…group size
Group C (b c)(m n) (b c)m cn 1 1 1
the idea that competition is not only between selection c m c m c m m…number of groups
D bn 0
individuals but also between groups.

1562 8 DECEMBER 2006 VOL 314 SCIENCE www.sciencemag.org

 REVIEW
and between groups—can be added up. The correlation. Therefore, kin selection theory also 32. J. Hofbauer, K. Sigmund, Evolutionary Games and
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Martin A. Nowak

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