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The Handicap Principle a Missing Piece of DarwinS Puzzle

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The Handicap Principle� a Missing Piece of Darwin�S Puzzle Jumping to Bold Conclusions A Review of The Handicap Principle A Missing Piece of Darwins Puzzle by Amotz Zahavi and Avishag Zahavi Oxford University Press Pp $ Seth Bullo ck Center for Adaptive Behavior and Cognition Max Planck Institute for Human Development Lentzeallee D Berlin Dahlem Tel Fax Email bullockmpibberlinmpgde Occasionally a grazing gazelle notices the approach of a predatory lion Rather than immediately taking ight at top sp eed she often jumps high in the air several times b efore eeing Perhaps these stots are warnings to closeby p ossibly related gazelles If this is the case why is the warning so energetic Surely evolution would favor less exhausting signals since exhaustion is to b e avoided when one is ab out to b e pursued by a predator Amotz and Avishag Zahavi op en their recent b o ok with a dierent explanation for this b ehavior They maintain that the stotting gazelle is not warning consp ecics of danger but informing the lion of its own escap e ability Because the lion has no desire to waste time and energy fruitlessly chasing uncatchable prey this information is of use to it but only if the information is truthful It is here the Zahavis claim that an explanation is to b e found for the otherwise inexplicable brio of the gazelles display The authors construe the stotting display as a handicap a signaling b ehavior that incurs the depletion of the very quality it advertises They interpret the gazelles vigorous leaping to convey the honest message that she is t enough and fast enough to waste just so much of her time and energy on jumping The handicap principle which underwrites the account of stotting oered ab ove has b een the sub ject of energetic debate within the evolutionary biology literature since Israeli ornithologist Amotz Zahavi rst presented it over years ago Zahavi Despite initially attracting considerable skepticism and enjoying only intermittent empirical and theoretical supp ort over the next decade and a half it has achieved increasing notoriety More recently the central tenets of the theory have earned acceptance as a result of the publication of a numb er of successful game theoretic mo dels Grafen b eing foremost among these While the handicap principle has yet to gain the status of canonical edict Zahavi having thus far for instance failed to garner much supp ort for his contention that it eclipses most of Darwins theory of sexual selection b oth the vo cabulary and explanatory p ersp ective asso ciated with it have attained a central p osition within current evolutionary thinking In addition to critiquing the Zahavis new b o ok this review will give a avor of the p ersp ective aorded by the handicap principle and in doing so will highlight an area of biological thinking that might prot from the attention of the adaptive b ehavior community But rst some understanding of the theoretical and metho dological context into which the handicap principle was intro duced is required Group Therapy Following the mids decline of group selection as an acceptable explanatory strategy many widespread and welldo cumented natural phenomena which had previously b een accounted for through some app eal to the worth of b ehavior at the level of so cial groups were left drifting aimlessly without explanatory anchor Topics as familiar as fo o d sharing o cking and predator mobbing in birds for instance were temp orarily rendered rudderless loaded up with wellorganized empirical data but lacking a theoretical helmsman While several of these phenomena were quickly explained the concepts of inclusive tness and kin selection Hamilton for example providing a unifying account of altruism among relatives that could explain the existence of sterile castes allofeeding among relatives etc signaling b ehaviors remained for some time the single largest and most embarrassingly unpiloted vessel on the high seas of evolutionary thought Mating displays aggressive p osturing informative dances b egging cries warning coloration and danger signals if honest enable the ecient distribution of resources fo o d sex shelter etc This eciency derives from the ow of useful information b etween the memb ers of an honest signaling system Contrast a b eehive foraging as a unit on the basis of shared information with the less ecient b ehavior of the same b ees denied recourse to each others signals However although the increased eciency aorded by honest signaling is of b enet to those groups that employ such signals the individual pro ducers and consumers of signals b enet from their memb ership in an honest signaling system only on average While a group of individuals employing an honest signaling system might do b etter than a group of taciturn comp etitors it is not clear that any individual memb er of an honest signaling system might not outp erform its fellow group memb ers through freeloading blung cheating lying doublecrossing exaggerating misleading or crying wolf If such malpractice reaps dividends which in the case of highly related insects such as b ees it may not then it is plain that honesty within such a group is not the b est p olicy In such cases the reasoning runs surely natural signaling systems must collapse undermined by the p ernicious canker of falsity and deceit Nevertheless innumerable observations suggest that making and attending to signals is ubiquitous in nature In addition to intercourse b etween birds b ees and b easts the cells within these creatures have also b een demonstrated to trac in information and even the DNA inside these cells has b een characterized as a genetic co de Zahavis handicap principle was one of a numb er of attempts to reconcile the theoretically motivated suggestion that honest signaling should b e evolutionarily unstable with the empirical evidence that signaling systems were the frequent pro duct of evolution What distanced the handicap principle from its comp etitors was its emphasis on honesty and co op eration rather than selshness and comp etition and what made Zahavis suggestion particularly problematic was his assertion that waste rather than economy would provide an explanation for the existence and p ersistence of honest signaling in nature On one front Zahavis handicap accounts which were predicated up on a notion of extravagance confronted grouptheoretic accounts of signaling that had b een underwritten by the well established notion of evolution favoring eciency Simultaneously the handicap principle challenged more recent individualistic accounts of communication which regarded signaling systems as inherently unstable evolutionary arms races spiraling toward inevitable breakdown Krebs Dawkins with the notion that telling the truth could b e a reasonable evolutionary strategy With hindsight it seems inevitable that the theory would excite opp osition The Economy of Waste Zahavis reasoning closely parallels although was probably arrived at indep endently from that of Thorstein Veblen a turnofthecentury so ciologist who prop osed the notion of conspicuous consumption For Veblen the overindulgence exhibited by memb ers of what he termed the leisure class could b e understo o d as a demonstration of class memb ership that is the purchase of prohibitively exp ensive go o ds and services could b e understo o d as an indicator of the pro curers wealth This index of so cietal status was an eective one b ecause those of lower status could not aord to make the advertisements of which wealthier individuals were capable Indeed at the lower extreme of the scale the funds of the p o orest individuals were more than accounted for by the demands of simply staying alive leaving no extra money to waste up on unpro ductive consumption Zahavi suggested that the utility of waste as an honest indicator was resp onsible for the form of all natural signals As an initial line of supp ort for this hyp othesis Zahavi noted that many signaling systems involved what app eared to b e needlessly costly signals The p eaco cks tail an image that was to b ecome a p otent symb ol of the handicap principle and that graces the cover of the Zahavis recent b o ok was highlighted as one such overly exp ensive signal The long feathers that make up the males tail serve no useful function other than attracting mates Furthermore they require considerable resources to develop are hard to maintain limit the males ability to evade predators or resist parasites and imp ose signicant energetic costs in courtship during which they are held erect and shaken vigorously Darwin had noted the seemingly unjustied extravagance of such mating displays and had b een forced to explain it as resulting from the aesthetic sensibilities of the selecting sex In contrast Zahavi prop osed that far from satisfying the arbitrary co quettish whim of a cho osy p eahen the displaying p eaco ck was demonstrating his quality in a manner selected precisely for its capacity to reveal useful facts ab out his value as a prosp ective mate by b earing a handicap Zahavi employs the term handicap in much the same manner as it is used in certain sp orts to denote a millstone that reduces p erformance by squandering some valuable resource For racehorses handicaps are additional ballast for golfers additional strokes for archers additional distance from the target However whereas these sp orting handicaps are imp osed to level the eld Zahavi p ointed out that they also reveal the quality of the sp ortsmen Thus Zahavis claim was that although the sp ecic form of natural signals was still essentially arbitrary they might b e visual
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