The Evolution of Reciprocal Altruism - Greater Good

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The Evolution of Reciprocal Altruism
Author(s): Robert L. Trivers
Reviewed work(s):
Source: The Quarterly Review of Biology, Vol. 46, No. 1 (Mar., 1971), pp. 35-57
Published by: The University of Chicago Press
Stable URL: http://www.jstor.org/stable/2822435 .
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THE EVOLUTION OF RECIPROCAL ALTRUISM
BY ROBERT L. TRIVERS
BiologicalL aboratoriesH, arvardU niversity,
Cambridge,M ass. 02138
ABSTRACT
A model is presented to account for the natural selection of what is termed recipro-
cally altruistic behavior. The model shows how selection can operate -against the
cheater (non-reciprocator)i n the system. Three instances of altruistic behavior are
discussed, the evolution of which the model can explain: (1) behavior involved in
cleaning symbioses; (2) warning cries in birds: and (3) human reciprocal altruism.
Regarding human reciprocal altruism, it is shown that the details of the psycho-
logical system that regulates this altruism can be explained by the model. Spe-
cifically,f riendship,d islike, moralistica ggression,g ratitude,s ympathy,t rust,s uspicion,
trustworthinessa,s pects of guilt, and some forms of dishonestya nd hypocrisyc an be
explained as important adaptations to regulate the altruistic system. Each individual
human is seen as possessing altruistic and cheating tendencies, the expression of
which is sensitive to developmental variables that were selected to set the tendencies
at a balance appropriate to the local social and ecological environment.
A INTRODUCTION own perpetuation,r egardlesso f which individ-
ual the genes appear in. The term "kin selec-
LTRUISTIC behavior can be de-
tion" will be used in this paper to cover in-
fineda s behavior that benefitsa n-
stanceso f this type-that is, of organismsb eing
othero rganism,n ot closelyr elated,
selected to help theirr elativelyc lose kin.
while being apparently detrimen-
The model presented here is designed to
tal to the organism performing
show how certain classes of behavior con-
the behavior, benefita nd detrimentb eing de-
venientlyd enoted as "altruistic" (or "recipro-
fined in termso f contributiont o inclusive fit-
cally altruistic")c an be selected for even when
ness. One human being leaping into water, at
the recipient is so distantlyr elated to the or-
some danger to himself, to save another dis-
ganism performingt he altruistica ct that kin
tantly related human from drowning may be
selection can be ruled out. The model will
said to display altruisticb ehavior. If he were
apply, for example, to altruisticb ehavior be-
to leap in to save his own child, the behavior
tween memberso f differenstp ecies. It will be
would not necessarilyb e an instance of "al-
argued that under certain conditions natural
-truism"h; e may merelyb e contributingt o the
selection favors these altruistic behaviors be-
survivalo f his own genes investedi n the child.
cause in the long run theyb enefitt he organism
Models that attemptt o explain altruisticb e-
performingth em.
havior in termso f natural selectiona re models
designed to take the altruismo ut of altruism.
THE MODEL
For example, Hamilton (1964) has demon-
strated that degree of relationship is an im- One human being saving another,w ho is not
portant parameteri n predictingh ow selection closely related and is about to drown, is an
will operate, and behavior which appears instance of altruism. Assume that the chance
altruistic may, on knowledge of the genetic of the drowningm an dying is one-half if no
relationships of the organisms involved, be one leaps in to save him, but that the chance
explicable in termso f natural selection: those that his potentialr escuerw ill drown if he leaps
genes being selectedf or that contributet o their in to save him is much smaller, say, one in
35
36 TH E QUARTERLY REVIEW OF BIOLOGY [VOLUME 46
twenty. Assume that the drowningm an always This argumentc an be made precise. Assume
drowns when his rescuer does and that he is there are both altruistsa nd non-altruistsin a
always saved when the rescuers urvivest he res- population of size N and that the altruistsa re
cue attempt. Also assume that the energyc osts characterizedb y the fact that each performs
involvedi n rescuinga re trivialc ompared to the altruistica cts when the cost to the altruist is
survival probabilities. Were this an isolated well below the benefitt o the recipient,w here
event, it is clear that the rescuer should not cost is defined as the degree to which the be-
bother to save the drowningm an. But if the havior retardst he reproductiono f the genes of
drowningm an reciprocatesa t some futuret ime, the altruista nd benefiti s the degree to which
and if the survival chances are then exactly the behavior increasest he rate of reproduction
reversed,it will have been to the benefito f each of the genes of the recipient. Assume that the
participantt o have riskedh is life for the other. altruisticb ehavior of an altruist is controlled
Each participant will have traded a one-half by an allele (dominant or recessive),a 2, at a
chance of dying for about a one-tenthc hance. given locus and that (for simplicity)t here is
If we assume that the entire population is only one alternativea llele, a1, at that locus and
sooner or later exposed to the same risk of that it does not lead to altruistic behavior.
drowning,t he two individuals who risk their Consider three possibilities: (1) the altruists
lives to save each other will be selected over dispense their altruism randomly throughout
those who face drowningo n their own. Note the population; (2) they dispense it nonran-
that the benefitso f reciprocityd epend on the domly by regarding their degree of genetic
unequal cost/benefirt atio of the altruistica ct, relationshipw ith possible recipients;o r (3) they
that is, the benefito f the altruistica ct to the dispense it nonrandomlyb y regarding the al-
recipient is greatert han the cost of the act to truistict endencieso f possible recipients.
the performerc, ost and benefitb eing defined
(1) Random dispensationo f altruism
here as the increase or decrease in chances of
the relevant alleles propagating themselvesi n There are three possible genotypes: a1a1,
the population. Note also that,a s defined,t he a2al, and a2a2' Each allele of the heterozygote
benefitsa nd costs depend on the age of the will be affectede qually by whateverc osts and
altruist and recipient (see Age-dependent benefitsa re associatedw ith the altruismo f such
changes below). (The odds assigned above may individuals (if a2 is dominant) and by whatever
not be unrealistic if the drowning man is benefitsa ccrue to such individuals from the
drowningb ecause of a cramp or if the rescue altruismo f others,s o they can be disregarded.
can be executed by extending a branch from If altruistica cts are being dispensed randomly
shore.) throughouta large population, then the typi-
Why should the rescued individual bother to cal a1ai individual benefitsb y (1/N)lb1, where
reciprocate? Selection would seem to favor be- bi is the benefit of the ith altruistica ct per-
ing saved fromd rowningw ithout endangering formedb y the altruist. The typical a2a2 indi-
oneself by reciprocating. Why not cheat? vidual has a net benefito f (l/N)Jbi - (I/N)Icj,
("Cheating" is used throughout this paper
wherec ; is the cost to the a2a2 altruisto f his jth
solely for convenience to denote failure to
altruistic act. Since -(1 /N)Icj is always less
reciprocate;n o conscious intent or moral con-
than zero, allele a1 will everywherer eplace
notationi s implied.) Selectionw ill discriminate
allele a2.
against the cheateri f cheatingh as later adverse
affectos n his life which outweight he benefito f (2) Nonrandom dispensationb y reference
not reciprocating.T his may happen if the al- to kin
truistr espondst o the cheatingb y curtailinga ll
future possible altruisticg esturest o this indi- This case has been treated in detail by
vidual. Assumingt hat the benefitso f these lost Hamilton (1964), who concluded that if the
altruistic acts outweigh the costs involved in tendency to dispense altruism to close kin is
reciprocating, the cheater will be selected great enough, as a function of the disparity
against relative to individuals who, because between the average cost and benefit of an
neither cheats, exchange many altruistic acts. altruistic act, then a2 will replace a1. Tech-
MARCH 1971] RECIPROCAL ALTRUISM 37
nically,a ll that is needed for Hamilton's form question sometimeso r oftend irectlyb enefitsi ts
of selection to operate is that an individual duplicate in anothero rganism.
with an "altruistica llele" be able to distinguish If an "altruistics ituation" is defineda s any
between individuals with and without this al- in which one individual can dispense a benefit
lele and discriminatea ccordingly. No formal to a second greatert han the cost of the act to
analysish as been attemptedo f the possibilities himself,t hen the chances of selecting for al-
for selection favoringi ndividuals who increase truisticb ehavior, that is, of keeping jcj+?bm
their chances of receivinga ltruistica cts by ap- small,a re greatest( 1) when therea re manys uch
pearing as if they were close kin of altruists, altruistics ituations in the lifetime of the al-
although selection has clearly sometimes fa- truists,( 2) when a given altruist repeatedly
vored such parasitism (e.g., Drury and Smith, interactsw ith the same small set of individuals,
1968). and (3) when pairs of altruistsa re exposed "sym-
metrically"t o altruistics ituations, that is, in
(3) Nonrandom dispensation by referencet o
such a way that the two are able to render
the altruistic tendencies of the recipient
roughly equivalent benefits to each other at
What is required is that the net benefita c- roughly equivalent costs. These three condi-
cruing to a typicala 2a2 altruiste xceed that ac- tions can be elaborated into a set of relevant
cruing to an alai non-altruisto, r that biological parameters affectingt he possibility
that reciprocally altruistic behavior will be
(I /p2) (lb k - Cj) > (I /q2)lbm, selected for.
whereb k is the benefitt o the a2a2 altruist (1) Length of lifetime.L ong lifetimeo f indi-
of the kth altruistic act performed toward viduals of a species maximizest he chance that
him, where ci is the cost of the jth altruistic any two individuals will encounter many al-
act by the a2a2 altruist,w here bm is the benefit truistics ituations,a nd all other things being
of the mth altruistic act to the alai nonal- equal one should searchf ori nstanceso f recipro-
truist,a nd where p is the frequency in the cal altruismi n long-liveds pecies.
population of the a2 allele and q that of the a, (2) Dispersal rate. Low dispersalr ate during
allele. This will tend to occur if Ibm is kept all or a significantp ortion of the lifetimeo f
small (which will simultaneouslyr educe Ici). individuals of a species increases the chance
And this in turn will tend to occur if an al- that an individual will interactr epeatedlyw ith
truistr esponds to a "nonaltruistica ct" (that is, the same set of neighbors,a nd other thingsb e-
a failure to act altruisticallyt owardt he altruist ing equal one should search for instances of
in a situationi n which so doing would cost the reciprocala ltruismi n such species. Mayr (1963)
actor less than it would benefitt he recipient) has discusseds ome of the factorst hatm ay affect
by curt ailing future altruistica cts to the non- dispersalr ates.
altruist. (3) Degree of mutual dependence. Interde-
Note that the above form of altruism does pendence of members of a species (to avoid
not depend on all altruistic acts being con- predators,f or example) will tend to keep indi-
trolled by the same allele at the same locus. viduals near each other and thus increase the
Each altruistc ould be motivatedb y a different chance theyw ill encounter altruistics ituations
allele at a differentlo cus. All altruistica lleles together. If the benefit of the mutual de-
would tend to be favored as long as, for each pendence is greatestw hen only a small number
allele, the net average benefitt o the homozy- of individuals are together,t his will greatly
gous altruiste xceeded the average benefitt o the increase the chance that an individual will re-
homozygousn onaltruist;t his would tend to be peatedly interact with the same small set of
true if altruistsr estrictt heir altruismt o fellow individuals. Individuals in primate troops,f or
altruistsr, egardlesso f what allele motivatest he example, are mutually dependent for protec-
other individual's altruism. The argumentw ill tion fromp redation,y et the optimal troop size
thereforea pply, unlike Hamilton's (1964), to for foragingi s often small (Crook, 1969). Be-
altruistica cts exchanged between members of cause they also meet the other conditions out-
differenstp ecies. It is the exchange that favors lined here, primatesa re almost ideal species in
such altriusm,n ot the fact that the allele in which to search for reciprocala ltruism. Clean-
38 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME4 6
ing symbiosesp rovide an instance of mutual to that of the modern chimpanzeet han to that
dependence between memberso f differentsp e- of the modern baboon (see, for example, Rey-
cies, and this mutual dependence appears to nolds, 1966).
have set the stage for the evolution of several (6) Aid in combat. No matter how domi-
altruisticb ehaviors discussed below. nance-orienteda species is, a dominant indi-
(4) Parental care. A special instance of mu- vidual can usually be aided in aggressivee n-
tual dependence is that found between parents countersw ith other individuals by help froma
and offsprinign species thats how parental care. less dominant individual. Hall and DeVore
The relationshipi s usually so asymmetricatlh at (1965) have described the tendencyf or baboon
few or no situationsa rise in which an offspring alliances to formw hich fighta s a unit in ag-
is capable of performingan altruistica ct fort he gressive encounters (and in encounters with
parents or even for another offspringb,u t this predators). Similarly,v ervet monkeys in ag-
is not entirelyt rue for some species (such as gressive encounters solicit the aid of other,
primates)i n which the period of parental care often less dominant, individuals (Struhsaker,
is unusuallyl ong. Parental care, of course,i s to 1967). Aid in combat is then a special case in
be explained by Hamilton's (1964) model, but which relativelys ymmetricarl elations are pos-
there is no reason why selection for reciprocal sible between individuals who differi n domi-
altruismc annot operate between close kin, and nance.
evidence is presentedb elow that such selection The above discussioni s meant only to suggest
has operatedi n humans. the broad conditions that favor the evolu-
(5) Dominance hierarchy.L inear dominance tion of reciprocal altruism. The most impor-
hierarchiesc onsist by definitiono f asymmetri- tant parameterst o specifyf or individuals of a
cal relationships; a given individual is domi- species are how many altruistics ituationso ccur
nant over another but not vice versa. Strong and how symmetricatlh eya re, and thesea re the
dominance hierarchies reduce the extent to most difficultt o specify in advance. Of the
which altruistics ituations occur in which the three instanceso f reciprocal altruismd iscussed
less dominant individual is capable of perform- in this paper only one, human altruism,w ould
ing a benefitf or the more dominantw hich the have been predicted from the above broad
more dominant individual could not simply conditions.
take at will. Baboons (Papio cynocephalus)p ro- The relationship between two individuals
vide an illustrationo f this. Hall and DeVore repeatedly exposed to symmetricalr eciprocal
(1965) have described the tendency for meat situations is exactly analogous to what game
caught by an individual in the troop to end up theoristsc all the Prisoner'sD ilemma (Luce and
by preemptioni n the hands of the most domi- Raiffa, 1957; Rapoport and Chammah, 1965),
nant males. This ability to preempt removes a game that can be characterizedb y the payoff
any selectivea dvantage that food-sharingm ight matrix
otherwiseh ave as a reciprocal gesture for the
most dominantm ales, and therei s no evidence A2 C2
in this species of any food-sharingt endencies. Al R, R S, T
By contrast, Van Lawick-Goodall (1968) has C1 T, S P, P
shown that in the less dominance-oriented
chimpanzeesm ore dominant individuals often where S < P < R < T and where A1 and A2
do not preempt food caught by the less domi- representt he altruisticc hoices possible for the
nant. Instead, they besiege the less dominant two individuals, and C1 and C2, the cheating
individual with "begging gestures,"w hich re- choices (the firstl etter in each box gives the
sult in the handing over of small portions of payofff or the firsti ndividual, the second letter
the catch. No stronge vidence is available that the payoff for the second individual). The
this is part of a reciprocallya ltruistics ystem, other symbolsc an be given the followingm ean-
but the absence of a strongl inear dominance ings: R stands for the reward each individual
hierarchyh as clearly facilitated such a possi- gets from an altruistic exchange if neither
bility. It is very likely that early hominid cheats; T stands for the temptationt o cheat;
groups had a dominance systemm ore similar S stands for the sucker'sp ayofft hat an altruist
MARCH 1971] RECIPROCAL ALTRUISAM 39
gets when cheated; and P is the punishment for it means that only under highlys pecialized
that both individuals get when neither is al- circumstancesc an the altruist be reasonably
truistic (adapted from Rapoport and Cham- guaranteed that the causal chain he initiates
mah, 1965). Iterated games played between the with his altruistica ct will eventuallyr eturnt o
same two individuals mimic real life in that him and confer,d irectlyo r indirectlyi,t s bene-
they permit each player to respond to the be- fit. Only under these conditions will the
havior of the other. Rapoport and Chammah cheater be selected against and this type of
(1965) and othersh ave conducted such experi- altruisticb ehavior evolve.
ments using human players,a nd some of their Althought he preconditionsf or the evolution
results are reviewedb elow in the discussiono f of reciprocal altruism are specialized, many
human altruism. species probably meet them and display this
W. D. Hamilton (pers. commun.) has shown type of altruism. This paper will limit itself,
that the above treatmento f reciprocala ltruism however, to three instances. The first,b e-
can be reformulatedc onciselyi n termso f game havior involvedi n cleaning symbiosesi,s chosen
theorya s follows. Assuming two altruistsa re because it permits a clear discriminationb e-
symmetricalleyx posed to a series of reciprocal tween this model and that based on kin selec-
situations with identical costs and identical tion (Hamilton, 1964). The second, warning
benefits, then after 2n reciprocal situations, calls in birds, has already been elaborately
each has been "paid" nR. Were one of the two analyzed in terms of kin selection; it is dis-
a nonaltruista nd the second changed to a non- cussed here to show how the model presented
altruisticp olicy after firstb eing cheated, then above leads to a very differentin terpretation
the initial altruistw ould be paid S + (n - I)P of these familiar behaviors. Finally, human
(assuming he had the firsto pportunityt o be reciprocal altruism is discussed in detail be-
altruistic) and the non-altruistw ould receive cause it representst he best documentedc ase of
T + (n - I)P. The important point here is reciprocal altruism known, because there has
that unless T >> R, then even with small n, apparently been strong selection for a very
nR should exceed T + (n - I)P. If this holds, complex systemr egulating altruisticb ehavior,
the nonaltruistict ype,w hen rare, cannot start and because the above model permitst he func-
to spread. But there is also a barrier to the tional interpretationo f details of the system
spread of altruismw hen altruistsa re rare, for that otherwiser emain obscure.
P > S implies nP > S + (n-1)P. As n in-
creases,t hese two total payoffst end to equality,
ALTRUISTIC BEHAVIOR IN CLEANING SYMBIOSES
so the barriert o the spread of altruismi s weak
if n is large. The barrierw ill be overcome if The preconditionsf or the evolution of re-
the advantages gained by exchanges between ciprocal altruism are similar to those for the
altruists outweigh the initial losses to non- operation of kin selection: long lifetime,l ow
altruistict ypes. dispersal rate, and mutual dependence, for ex-
Reciprocal altruismc an also be viewed as a ample, tend to increase the chance that one is
symbiosise, ach partnerh elping the other while interactingw ith one's close kin. This makes it
he helps himself. The symbiosish as a time lag, difficultto discriminatet he two alternativeh y-
however;o ne partnerh elps the other and must potheses. The case of cleaning symbiosis is
then wait a period of time before he is helped importantt o analyze in detail because altruistic
in turn. The returnb enefitm ay come directly, behavior is displayed that cannot be explained
as in human food-sharingt,h e partner directly by kin selection,s ince it is performedb y mem-
returningt he benefita fter a time lag. Or the bers of one species for the benefito f members
returnm ay come indirectlya,s in warningc alls of another. It will be shown instead that the
in birds (discussed below), where the initial behavior can be explained by the model pre-
help to other birds (the warning call) sets up sented above. No elaborate explanation is
a causal chain through the ecological system needed to understand the evolution of the
(the predatorf ails to learn useful information) mutually advantageous cleaning symbiosis it-
which redounds aftera time lag to the benefit self; it is several additional behaviorsd isplayed
of the caller. The time lag is the crucial factor, by the host fish to its cleaner that require a
40 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 46
special explanation because they meet the Soonw e watchedo ur seconds urpriset:h eg rouper
criteriaf ora ltruisticb ehavioro utlined above- made a movementw hich in the precedings ix
thati s, theyb enefitt he cleanerw hilea pparently yearsw e had nevers eenh imm ake:h e spreadt he
rightg ill-coverinsgo wide that the individual
beingd etrimentatl o theh ost.
gill-platesw ere separatedf rome ach other at
Feder (1966) and Maynard (1968) have re-
greatd istancesw, ide enough to let the cleaner
centlyr eviewedt he literatureo n cleaning sym-
through( translatedf romH ediger,1 968 p. 93).
bioses in the ocean. Brieflyo, ne organism( e.g.,
the wrasse, Labroides dimidiatus) cleans an- When Hediger added two additional L. di-
other organism( e.g., the grouper,E pinephelus midiatus to the tank, all three cleaned the
striatus) of ectoparasites (e.g., caligoid cope- grouper with the result that within several
pods), sometimese ntering into the gill cham- days the groupera ppeared restlessa nd nervous,
bers and moutho f the "host" in order to do so. searchedo ut places in the tank he had formerly
Over forty-fivspe ecies of fisha re known to be avoided, and shook himselfo ften (as a signal
cleaners,a s well as six species of shrimp. In- that he did not wish to be cleaned any longer).
numerables pecies of fishs erve as hosts. Stom- Apparently three cleaners working over him
ach analyses of cleaner fish demonstratet hat constantlyw as too much for him, yet he still
they vary greatlyi n the extent to which they failed to eat any of them. When Hediger re-
depend on theirc leaning habits for food,s ome moved two of the cleaners, the grouper re-
apparentlys ubsistingn early entirelyo n a diet turned to normal. There is no indication the
of ectoparasites.L ikewise, stomacha nalyses of groupere ver possesseda ny edible ectoparasites,
host fishr eveal that cleaners differi n the rate and almost two yearsl ater (in December, 1968)
at which theye nd up in the stomachso f their the same cleaner continued to "clean" the
hosts, some being apparently almost entirely grouper (pers. observ.) although the cleaner
immunet o such a fate. It is a strikingf actt hat was, in fact, fed separatelyb y its zoo-keepers.
theres eems to be a strongc orrelationb etween Eibl-Eibesfeldt(1 959) has described the mor-
degree of dependence on the cleaning way of phology and behavior of two species (e.g., As-
life and immunityt o predation by hosts. pidontutst aeniatus) that mimic cleaners (e.g.,
Cleaning habits have apparentlye volved in- L. dimidiatus) and that rely on the passive
dependentlym any times( at least threet imesi n behavior of fishw hich suppose they are about
shrimps alone), yet some remarkable conver- to be cleaned to dart in and bite offa chunk
gence has taken place. Cleaners, whether of their fins. I cite the evolution of these
shrimp or fish, are distinctivelyc olored and mimics, which resemble their models in ap-
behave in distinctivew ays (for example, the pearance and initial swimming behavior, as
wrasse,L . dimidiatus,s wimsu p to its host with evidence of strongs electionf or hosts with no
a curious dipping and rising motion that re- intentiono f harmingt heir cleaners.
minds one of the way a finchf lies). These dis- Of especial interesti s evidence that thereh as
tinctivef eaturess eem to serve the functiono f been strongs election not to eat one's cleaner
attractingf isht o be cleaned and of inhibiting even aftert he cleaning is over. Eibl-Eibesfeldt
any tendencyi n themt o feed on theirc leaners. (1955) has made some strikingo bservationso n
There has apparentlyb een strongs election to the goby,E lacitinus oceanops:
avoid eating one's cleaner. This can be il-
lustrated by several observations. Hediger I nevers awva groupers nap up a fisha fteri t had
cleaned it. On the contraryi,t annoounceidt s
(1968) raised a grouper (Epinephelus) from
impendindge parturbe y twod efinitsei gnalm ove-
infancya lone in a small tank for six years,b y
ments. Firsti t closed its mouthv igorouslya,l -
which time the fish was almost four feet in
thoughn ot completelya,n d immediateloyp ened
length and accustomed to snapping up any-
it wide again. Upon this intentionm ovement,
thing dropped into its tank. Hediger then all the gobiesl eft the mouthc avity.T hen the
dropped a small live cleaner (L. dimidiatus) groupers hooki ts bodyl aterallya fewt ines,a nd
into the grouper'st ank. The groupern ot onily all the cleanierrs eturnedt o theirc oral. If onie
failed to snap up the cleaner but opened its frightenead grouperi t never neglectedt hese
moutha nd permittedt he cleaner freee ntrya nd forewarninmg ovements(t ranslatedf rom Eibl-
exit. Eibesfeldt1, 955,p . 208).
MARCH 1971] RECIPROCAL ALTRUISM 41
Randall has made similar observationso n a parasites may be sufficientt o inhibit hunger.
moray eel (Gymnothoraxj aponicus) that sig- Both possibilitiesa re contradictedb y Hediger's
nalled with a "sharp lateral jerk of the eel's observation,c ited above, and seem unlikelyo n
head," after which "the wrasse fairlyf lew out functionalg roundsa s well.
of the mouth, and the awesome jaws snapped A fisht o be cleaned seems to performs everal
shut" (Randall, 1958, 1962). Likewise, Hedi- "altruistic" acts. It desists from eating the
ger's Kasper Hauser grouper shook its body cleaner even when it easily could do so and
when it had enough of being cleaned. when it must go to special pains (sometimes
Why does a large fishn ot signal the end to a at danger to itself)t o avoid doing so. Further-
cleaning episode by swallowing the cleaner? more, it may performt wo additional behaviors
Natural selection would seem to favor the which seem of no direct benefitt o itself (and
double benefito f a good cleaning followed by which consume energya nd take time), namely,
a meal of the cleaner. Selection also operates, it signals its cleaner that it is about to depart
of course,o n the cleaner and presumablyf avors even when the fishi s not in its mouth, and it
mechanismst o avoid being eaten. The distinc- may chase offp ossible dangers to the cleaner:
tive behavior and appearance of cleaners has
While diving with me in the Virgin Islands,
been cited as evidence of such selection. One Robert Schroederw atched a Spanish hogfish
can also cite the distinctiveb ehavior of the fish groominga bar jack in its bronze color state.
being cleaned. Feder (1966) has pointed out When a second jack arrivedi n the pale color
that hostsa pproachinga cleaner react by "stop- phase, the firstja ck immediatelydr ovei t away.
ping or slowing down, allowing themselvest o But later when anotherj ack intrudedo n the
assume awkwardp ositions,s eeminglyi n a hyp- scenea nd changedi ts pale color to dark bronze
it was not chased. The bronzec olorw ould seem
notic state." Fishes sometimesa lter their color
to mean "no harm intended;I need service"
dramaticallyb efore and while being cleaned,
(Randall,1 962p . 44).
and Feder (1966) has summarizedi nstances of
this. These forms of behavior suggest that The behavior of the host fishi s interpreted
natural selection has operated on cleaners to here to have resulted from natural selection
avoid attemptingt o clean fish without these and to be, in fact,b eneficialt o the host because
behaviors,p resumablyt o avoid wasting energy the cleaner is worthm ore to it alive than dead.
and to minimize the dangers of being eaten. This is because the fisht hat is cleaned "plans"
(Alternatively,t he behaviors, including color to returna t later dates form ore cleanings,a nd
change, may aid the cleaners in findinge cto- it will be benefitedb y being able to deal with
parasites. This is certainly possible but not, the same individual. If it eats the cleaner, it
I believe, adequate to explain the phenomenon may have difficultyfi nding a second when it
completely. See, for example, Randall, 1962.) needs to be cleaned again. It may lose valuable
Once the fisht o be cleaned takes the proper energy and be exposed to unnecessaryp reda-
stance, however,t he cleaner goes to work with tion in the search for a new cleaner. And it
no apparent concernf ori ts safety: it makes no may in the end be "turned down" by a new
effortt o avoid the dangerous mouth and may cleaner or serviced very poorly. In short, the
even swim inside,w hich as we have seen, seems host is abundantly repaid for the cost of its
particularlyf oolhardy,s ince fishb eing cleaned altruism.
may suddenly need to depart. The apparent To support the hypothesist hat the host is
unconcern of the cleaner suggestst hat natural repaid its initial altruism,s everal pieces of evi-
selection acting on the fishb eing cleaned does dence mustb e presented: that hostss ufferf rom
not, in fact, favor eating one's cleaner. No ectoparasites;t hat findinga new cleaner may
speculation has been advanced as to why this be difficulot r dangerous; that if one does not
may be so, although some speculation has ap- eat one's cleaner,t he same cleaner can be found
peared about the mechanismsi nvolved. Feder and used a second time (e.g., that cleaners are
advances two possibilities, that of Eibl- site-specific)t;h at cleaners live long enough to
Eibesfeldt (1955) that fishc ome to be cleaned be used repeatedly by the same host; and if
only aftert heira ppetite has been satisfieda, nd possible, that individual hosts do, in fact,r euse
one of his own, that the irritation of ecto- the same cleaner.
42 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 46
(1) The cost of ectoparasites. It seems al- Cleaning fishesa nd cleaning shrimpsh ave regular
most axiomatic that the evolution of cleaners stations to which fishes wanting to be cleaned
entirely dependent on ectoparasites for food can come (p. 367).
implies the selective disadvantage for the
Limbaugh, Pederson, and Chase (1961) have
cleaned of being ectoparasite-riddenW. hat is
reviewed available data on the six species of
perhaps surprisingi s the effectt hat removing
cleaner shrimps, and say:
all cleaners froma coral reef has on the local
"hosts" (Limbaugh, 1961). A, '<eder (1966) said The known cleaner shrimpsm ay convenientlyb e
in his review: divided into two groups on the basis of behavior,
habitat and color. The five species comprising
Within a few days the numbero f fishesw as one group are usually solitary or paired....
drasticallyr educed. Within two weeks almost All five species are territorial and remain for
all exceptt erritoriafli shesh ad disappeareda, nd weeks and, in some cases, months or possibly
manyo f theseh ad developedw hitef uzzyb lotches, years within a meter or less of the same spot.
swellingsu,l cerateds ores,a nd frayedf ins( p. 366). They are omnivorous to a slight extent but seem
to be highly dependent upon their hosts for
Clearly, once a fish'sp rimaryw ay of dealing
food. This group is tropical, and the individuals
with ectoparasites is by being cleaned, it is
are brightlym arked. They display themselvest o
quickly vulnerable to the absence of cleaners. their hosts in a conspicuous manner. They prob-
(2) The difficultyan d danger of finding a ably rarely serve as prey for fishes. A single
cleaner. There are naturallyv ery few data on species, Hippolysmata californica, comprises the
the difficultoyr dangero f findinga new cleaner. second group. . . . This species is a gregarious,
This is partiallyb ecause, as shown below, fish wandering, omnivorous animal . . . and is not
tend repeatedlyt o return to familiar cleaners. highly dependent upon its host for survival. So
far as is known, it does not display itself to
The only observationo f fishb eing disappointed
attractf ishes( p. 238).
in their search for cleaners comes from Eibl-
Eibesfeldt (1955): "If the cleaners fail to ap- It is H. californica that is occasionally found in
pear over one coral in about half a minute,t he the stomachs of at least one of its hosts. The
large fishes swim to another coral and wait striking correlation of territoriality and soli-
there a while" (translatedf romp . 210). It may tariness with cleaning habits is what theory
be that fish have several alternative cleaning would predict. The same correlation can be
stationst o go to, since any particular cleaning found in cleaner fish. Labroides, with four
station may be occupied or unattended at a species, is the genus most completely dependent
given moment. So manyf isht end to be cleaned on cleaning habits. No Labroides has ever been
at coral reefs (Limbaugh, 1961, observed a found in the stomach of a host fish. All species
cleaner service3 00 fishi n a 6-hourp eriod), that are highly site-specific and tend to be solitary.
Randall (1958) reports that an individual
predatorsp robablyf requentc oral reefsi n search
L. dimidiatus may sometimes swim as much as
of fishb eing cleaned. Limbaugh (1961) suggested
60 feet from its cleaning station, servicing fish
that good human fishings ites are found near
on the way. But he notes,
cleaning stations. One finalr eason whyc oming
to be cleaned mayb e dangerousi s thats ome fish This was especially true in an area where the
must leave their element to do so (Randall, highly territoriald amsel fish Pomacentris nigri-
1962): cans (Lepede) was common. As one damsel fish
was being tended, another nearby would assume
Most impressive were the visits of moray eels,
a stationaryp ose with finse rect and the Labroides
which do not ordinarily leave their holes in the
would move oni to the latter with little hesita-
reef during daylight hours, and of the big jacks
tion (p. 333).
which swam up from deeper water to the reef's
edge to be "serviced" before going on their way Clearly, what matters for the evolution of re-
(p. 43). ciprocal altruism is that the same two indi-
(3) Site specificityo f cleaners. Feder (1966) viduals interact repeatedly. This will be facili-
has reviewed the strikinge vidence for the site tated by the site specificityo f either individual.
specificityof cleaners and concludes: Of temperate water cleaners, the species most
MARCH 1971] RECIPROCAL ALTRUISM 43
specialized to cleaning is also apparently the of cleaning organismsp erforms everal kinds of
most solitary( Hobson, 1969). altruisticb ehavior, including not eating their
(4) Lifespan of cleaners. No good data exist cleaner after a cleaning, which can be ex-
on how long cleaners live, but several observa- plained on the basis of the above model. A
tions on both fisha nd shrimps uggestt hat they review of the relevant evidence suggestst hat
easily live long enough for effectives election the cleaner organismsa nd theirh osts meet the
against cheaters. Randall (1958) repeatedly preconditionsf or the evolution of reciprocally
checked several ledges and found that different altruisticb ehavior. The host's altruismi s to be
feedings tationsw ere occupied for" long periods explained as benefitingh im because of the
of time," apparently by the same individuals. advantage of being able quickly and repeatedly
One such feeding station supported two indi- to return to the same cleaner.
viduals for over three years. Of one species of
cleaner shrimp,S tenopus hispidus, Limbaugh, WARNING CALLS IN BIRDS
Marler (1955, 1957) has presented evidence
Pederson, and Chase (1961) said that pairs of
that warningc alls in birds tend to have charac-
individuals probably remain months, possibly
teristicst hat limit the informationa predator
years,w ithin an area of a square meter.
gets fromt he call. In particular,t he call char-
(5) Hosts using the same cleaner repeatedly.
acteristicsd o not allow the predator easily to
There is surprisinglyg ood evidence that hosts
determinet he location of the call-giver.T hus,
reuse the same cleaner repeatedly. Feder (1966)
it seems that giving a warningc all must result,
summarizest he evidence:
at least occasionally,i n the otherwiseu nneces-
Many fishess pend as mucht imeg ettingc leaned sary death of the call-giver,e ithera t the hands
as theyd o foragingf orf ood. Some fishesr eturn
of the predator that inspired the call or at the
again and again to the same stationa, nd showa
hands of a second predatorf ormerlyu naware of
definitet ime pattern in their daily arrival.
the caller'sp resenceo r exact location.
Othersp ass froms tationt o stationa nd return
Given the presumed selection against call-
manyt imesd uringt he day; this is particularly
trueo f an injuredo r infectedf ish( p. 368). giving, Williams (1966) has reviewed various
models to explain selection for warning cries:
Limbaugh, Pederson, and Chase (1961) have (1) Warning calls are functional during the
presentede vidence that in at least one species breeding season in birds in that they protect
of cleaner shrimp (Stenopus scutellus), the one's mate and offspringT. hey have no func-
shrimp may reservice the same individuals: tion outside the breeding season, but they are
One pair was observedin the same football-sized not deleted then because "in practice it is not
coral boulder fromM ay throughA ugust 1956. worth burdening the germ plasm with the in-
Duringt hatp eriod,w e changedt he positiona nd formationn ecessaryt o realize such an adjust-
orientationof the boulders everalt imesw ithina ment" (Williams, 1966, p. 206).
radius of approximatelyse ven metersw ithout (2) Warning calls are selected for by the
disturbingt he shrimp.V isitingf ishesw ere mo- mechanismo f group selection( Wynne-Edwards,
mentarilyd isturbedb y the changes,b ut they
1962).
soon relocatedt he shrimps(p . 254).
(3) Warning calls are functionalo utside the
Randall (1958) has repeatedly observed fish breeding season because therei s usually a good
swimmingf rom out of sight directlyt o clean- chance that a reasonably close kin is near
ing stations,b ehavior suggestingt o him that enough to be helped sufficiently(H amilton,
they had prior acquaintance with the stations. 1964; Maynard Smith, 1964). Maynard Smith
During two months of observationsa t several (1965) has analyzed in great detail how closely
feeding stations,E ibl-Eibesfeldt( 1955) became related the benefitedk in mustb e, at what bene-
personally familiar with several individual fit to him the call must be, and at what cost
groupers (Epinephelus striatus)a nd repeatedly to the caller, in order for selection to favor
observed them seeking out and being cleaned call-giving.
at the same feedings tations,p resumablyb y the The firsti s an explanation of last resort.
same cleaners. While it must sometimesa pply in evolutionary
In summaryi,t seemsf air to say that the hosts arguments,it should probablyo nly be invoked