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 . Accessed: 20/10/2012 18:02 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to The Quarterly Review of Biology. http://www.jstor.org THE EVOLUTION OF RECIPROCAL ALTRUISM BY ROBERT L. TRIVERS BiologicalLaboratories, Harvard University, Cambridge,Mass. 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)in 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,friendship, dislike, moralisticaggression, gratitude, sympathy, trust, suspicion, trustworthiness,aspects of guilt, and some forms of dishonestyand hypocrisycan 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. INTRODUCTION own perpetuation,regardless of which individ- ual the genes appear in. The term "kin selec- LTRUISTIC behavior can be de- A tion" will be used in this paper to cover in- finedas behavior that benefitsan- stancesof this type-that is, of organismsbeing otherorganism, not closelyrelated, selected to help theirrelatively close 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, benefitand detrimentbeing de- venientlydenoted as "altruistic" (or "recipro- fined in termsof contributionto inclusive fit- cally altruistic")can be selected for even when ness. One human being leaping into water, at the recipient is so distantlyrelated to the or- some danger to himself, to save another dis- ganism performingthe altruisticact that kin tantly related human from drowning may be selection can be ruled out. The model will said to display altruisticbehavior. If he were apply, for example, to altruisticbehavior be- to leap in to save his own child, the behavior tween membersof differentspecies. It will be would not necessarilybe an instance of "al- argued that under certain conditions natural -truism";he may merelybe contributingto the selection favors these altruistic behaviors be- survivalof his own genes investedin the child. cause in the long run theybenefit the organism Models that attemptto explain altruisticbe- performingthem. havior in termsof natural selectionare models designed to take the altruismout of altruism. THE MODEL For example, Hamilton (1964) has demon- strated that degree of relationship is an im- One human being saving another,who is not portant parameterin predictinghow 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 drowningman dying is one-half if no relationships of the organisms involved, be one leaps in to save him, but that the chance explicable in termsof natural selection: those that his potentialrescuer will drown if he leaps genes being selectedfor that contributeto 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 drowningman always This argumentcan be made precise. Assume drowns when his rescuer does and that he is there are both altruistsand non-altruistsin a always saved when the rescuersurvives the res- population of size N and that the altruistsare cue attempt. Also assume that the energycosts characterizedby the fact that each performs involvedin rescuingare trivialcompared to the altruisticacts when the cost to the altruist is survival probabilities. Were this an isolated well below the benefitto the recipient,where event, it is clear that the rescuer should not cost is defined as the degree to which the be- bother to save the drowningman. But if the havior retardsthe reproductionof the genes of drowningman reciprocatesat some futuretime, the altruistand benefitis the degree to which and if the survival chances are then exactly the behavior increasesthe rate of reproduction reversed,it will have been to the benefitof each of the genes of the recipient. Assume that the participantto have riskedhis life for the other. altruisticbehavior of an altruist is controlled Each participant will have traded a one-half by an allele (dominant or recessive),a2, at a chance of dying for about a one-tenthchance. given locus and that (for simplicity)there is If we assume that the entire population is only one alternativeallele, a1, at that locus and sooner or later exposed to the same risk of that it does not lead to altruistic behavior. drowning,the 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 drowningon their own. Note the population; (2) they dispense it nonran- that the benefitsof reciprocitydepend on the domly by regarding their degree of genetic unequal cost/benefitratio of the altruisticact, relationshipwith possible recipients;or (3) they that is, the benefitof the altruisticact to the dispense it nonrandomlyby regarding the al- recipient is greaterthan the cost of the act to truistictendencies of possible recipients. the performer,cost and benefitbeing defined here as the increase or decrease in chances of (1) Random dispensationof altruism the relevant alleles propagating themselvesin There are three possible genotypes: a1a1, the population. Note also that,as defined,the a2al, and a2a2' Each allele of the heterozygote benefitsand costs depend on the age of the will be affectedequally by whatevercosts and altruist and recipient (see Age-dependent benefitsare associatedwith the altruismof such changes below). (The odds assigned above may individuals (if a2 is dominant) and by whatever not be unrealistic if the drowning man is benefitsaccrue to such individuals from the drowningbecause of a cramp or if the rescue altruismof others,so they can be disregarded. can be executed by extending a branch from If altruisticacts are being dispensed randomly shore.) throughouta large population, then the typi- Why should the rescued individual bother to cal a1ai individual benefitsby (1/N)lb1, where reciprocate? Selection would seem to favor be- bi is the benefit of the ith altruisticact per- ing saved fromdrowning without endangering formedby the altruist. The typical a2a2 indi- oneself by reciprocating. Why not cheat? vidual has a net benefitof (l/N)Jbi - (I/N)Icj, this paper ("Cheating" is used throughout wherec; is the cost to the a2a2 altruistof his jth solely for convenience to denote failure to altruistic act. Since -(1 /N)Icj is always less reciprocate;no conscious intent or moral con- than zero, allele a1 will everywherereplace notationis implied.) Selectionwill discriminate allele a2. against the cheaterif cheatinghas later adverse affectson his life which outweighthe benefitof (2) Nonrandom dispensationby reference not reciprocating.This may happen if the al- to kin truistresponds to the cheatingby curtailingall future possible altruisticgestures to this indi- This case has been treated in detail by vidual. Assumingthat the benefitsof 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,all that is needed for Hamilton's form question sometimesor oftendirectly benefits its of selection to operate is that an individual duplicate in anotherorganism. with an "altruisticallele" be able to distinguish If an "altruisticsituation" is definedas any between individuals with and without this al- in which one individual can dispense a benefit lele and discriminateaccordingly. No formal to a second greaterthan the cost of the act to analysishas been attemptedof the possibilities himself,then the chances of selecting for al- for selection favoringindividuals who increase truisticbehavior, that is, of keeping jcj+?bm their chances