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Phylogenetic Constraint in Evolutionary Theory: Has It Any Explanatory Power?

Author(s): Mary C. McKitrickSource: Annual Review of Ecology and Systematics, Vol. 24 (1993), pp. 307-330Published by: Annual ReviewsStable URL: http://www.jstor.org/stable/2097181 .

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Annu.Rev. Ecol. Syst. 993. 24:307-330Copyright? 1993byAnnualReviews nc. All rights eserved

PHYLOGENETIC CONSTRAINTIN EVOLUTIONARY THEORY:Has ItAnyExplanatoryower?MaryC. McKitrickMuseum fZoology,UniversityfMichigan, nnArbor,Michigan 8109KEY WORDS: constraint,hylogeny,volutionaryheory

AbstractThe notion fconstraintss a central ne nevolutionaryiology. hat imitsmayexist nthepatternsesultingrom iverse volutionaryrocesses, ndthepossibilityhat hese imits anbediscoveredndexplainedmechanistic-ally, suggests hat much of evolutionmay be interpretablehroughnintegratedheory fconstraint.hylogeneticonstraintasbeen nvokedna variety fcontexts ut s yet here s noconsensus n itsdefinition.t isdefined ere as anyresult r componentf thephylogeneticistoryf alineage thatprevents n anticipated ourse of evolutionn that ineage.Hypothesesf constraintan be testedwithin phylogeneticramework;understandinghenature f the onstraintshemselves illrequire mecha-nistic pproach hatdentifieshegenetic nddevelopmentalomponentsf"limits odesign."INTRODUCTIONThe concept fconstraintas been invokedn a varietyfcontextsn theevolutionaryiterature,o explain volutionaryatternsnd as a counteroadaptationistroptimalityrguments32, 39, 45), althoughne author astermedt "an argumentf lastresort"3:461). The literatureeflectsmuchconfusionboutthemeaning f constraint5); my goal here s to definephylogeneticonstraintnd to examine ts use in evolutionaryiology.Wimsatt& Schank 100:234-35) asserted hat "notions f evolutionaryprogressrchange reproductivelyiscussedn terms f the losely elated

3070066-4162/93/1120-0307$05.00

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308 MCKITRICKnotion f anevolutionaryonstraint...."lthoughdo not laim o resolve hequestion osed n thetitle f thispaper, do wish o explore t, toinvitemorerigorous xaminationf the meaningnd use of theconcept nd todetermine hetherhis oncept an be harnessedo helpus revealgreaterdetail n theevolutionaryatterns e attempto study.Other uthors aveadvocateduse of the phylogenetic ethod or exploringhe relationshipbetween daptationndhistoricalffects10, 14, 19, 24, 25, 27, 52, 58, 59,97, 98). I wish also to urge phylogeneticpproach o testing ypothesesformulatedpecificallyo mplicater dentifyhylogeneticonstraintnanevolutionaryystem.In the astdecade, a "nullmovement"as arisen n evolutionaryiologythat as offered restraintn a possible xcessof deterministicxplanationsfor ll evolutionaryatterns.his movementdvocates heprominencefstochasticactorsn evolution,venwhen bserved atternseem o ndicatea coherent, onrandomause. A pivotalpaper n the developmentf themovements that f Gould & Lewontin39), inwhich heauthors autionagainst ssumptionsf adaptation hen he historyf a lineagemayofferobvious cues to the statusquo. This paper fueleddiscussion n manydirections.lowinski Guyer 90) suggested rigorous uantitativeethodfor etermininghetheratternsfspeciation ithin lades,compared iththeir ister lades,deviate rom hose xpected ychance.The authors aidthat ejectinghenullmodel y hismethodestablishesnly hat eterministicdiversityvolutionccurs,notwhetherndividualhylogeniesequire eter-ministicxplanations; e will probably ever nowwhetherhe adiation fanoline izards epresentsonrandomvolution"p. 916).Despite thestartlingealism f such views,the futuref evolutionarybiologyneednotbe seen as a bleak one. Of course hetruthbouthistorycannot ver be known, utwe neednot becomenihilists s a result.Thepossibilityf excess exists nany ntellectual ave,andalthoughn excessof nullness"snotyet pparent,he angerf t an beanticipatedaswarnedin76). Theconcept f phylogeneticonstraintnsomeof tsusagesdescendsfromhenullmovementnd s notyetwelldeveloped.t should ot e nvokedas anultimatexplanation.uch nvocations ould eanalogouso Slowinski& Guyer's 90) example f a seriesof cointosses:We do notrequire nexplanationor hepattern e see because t s due to chance, ven thoughtheresult feach cointoss has an ultimate ause thatwe do notbother ostudy. n otherwords, t is notenough o discover hat heoccurrencerabsence fa certainraitsrelatedo tsretentionn a commonncestor,ndto christenhis etentionconstraint;his iscoverymerelyllowsus to shiftour attentionothe ppropriateierarchicalevel.There smore o be learnedbout he volutionaryatterns e studyvenafter ehaveofferedxplanationsasedonconstraint,nd suggest ow to

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PHYLOGENETIC CONSTRAINT 309proceed oward hisgoal. I begin by reviewing ome of the iteraturenconstraint;his ncludes apers hati) directlyeferophylogeneticonstraint;(ii) imply concept f phylogeneticonstraint;iii) discussphylogeneticr"taxonomic"ffects;iv) discuss omparative ethods;v) refer o imits odiversity;r vi) refer o a notion f key nnovationstheflip ide of imitstodiversity). also brieflyxplore he elationshipf phylogeneticonstrainttoother oncepts f onstraintuch s that sedbydevelopmentalvolutionarybiologists. aken ogether,his iteratures vast ndcannot e dealtwith erewithoutosing hefocus f this aper. offer hereforepreemptivepologyfor ot iting ll relevantnd mportantorks. n some ense, ll evolutionarystudiesmplicate hylogeneticonstraint,ndreviewinghe opic s ike ryingtocatch greased ig.DEFINITIONS OF PHYLOGENETIC CONSTRAINTDerrickson Ricklefs23) point ut thatmany iologists onfuse hyloge-netic onstraint ith hylogeneticffect;he atters the endencyf closelyrelated rganisms o be similar ue to their haredhistory. hey definephylogeneticonstraints "changesndiversificationfa clade,"or "differ-ences ntheevolutionarynteractionetween henotypend environment."Derrickson Ricklefs ropose a method f identifyingonstraintsingmultivariatenalysis o locatechanges n slope of quantitativeraitswithinandamong axa. Such a definitionf constrainteemstorefer o theresultofconstraintatherhan othe ctualphenomenonr tscause.Constraintngenerals a check n an expected ction r ackof action, ndthust mpliesthe absence of an anticipated utcome.Phylogeneticonstraintikewiseimpliesthe absence of an anticipated ourse of evolution, uch as, forexample, hefailure f birdsto evolveviviparity4, 9). I woulddefinephylogeneticonstraint,herefore,s anyresult r componentfthe hylo-genetic istoryfa lineage hat reventsn anticipatedourse fevolutionin that ineage. This definitions related o the "local" developmentalconstraintsfMaynard mith t al (55), i.e. themechanismsf constraintsareexamined t thedevelopmentalevel, and ocal, as opposed o universalorglobal, onstraintsre consideredo be those pplyingo a "limitedangeoftaxa." t is also similar oLigon's 51) use ofphylogeneticonstraintomean that ertain volutionaryathwaysre not ikely o be followed yaspeciesorgroup f relatedpecies, s a result fprior volutionaryistory.In short, esterday'sdaptation aybe today's onstraint."Thisviewmeans, fcourse, hat researcherad toask the uestion, hyhave birdsnever volvedviviparity? lthoughmost f the answers o thisquestion avefocused nphysiology,t s a fact hat he ncestorsf birdswere, ikebirds, viparous. hustheproximatenswer othe uestionmay

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310 MCKITRICKbe simply hat irdshave notdiverged rom heirncestorsthey reforever"constrained"hylogenetically).he morenearly ltimatenswerwouldbethatfora specific eason namely, he actual constraint,)heyhave notdivergedromheir ncestors et they retemporarilyonstrained;.e. theymust vercome hylogeneticnertia).n otherwords he bsence f viviparitywithin ves is a matterfvariationnrates f evolutionsee, e.g., 29, 90).Mammals, heonlyother lade of warm-bloodedrganisms,reprimarilyviviparous, ndfor omereason hey chieved his headof thebirds.Whytheymanaged hisbefore irds ould be forphysiologicaleasons avianphysiologys delaying he achievementfviviparity)rfor ny numberfother easons.Derrickson Ricklefs 23) were correct n surmisinghatconstraint ill manifesttself n variationn ratesof character volution;however, econstructingncestral tates t thenodesof a phylogeneticreewill be a more ccurate ndicator f such a manifestationhan nymethodrelying n a taxonomic ierarchy. y analogy, he ength ftime ne mustwaitbefore ne can spell theword quagmire" n a gameof Scrabblewillcertainlyepend nthe ettersnereceives t he utset f he ame. imilarly,dependingnthe tarting aterials,wo ineagesmaydiffern the engthftime ttakes hem o reach certain esult uchas a flipperto choose anexample f a type f structurehat as evolved nmore han ne lineage-obviouslywe cannot se an example fa structurenone lineage hatwilleventuallye evolved ndependentlynanother). s a reflectionfevolution-ary istory,he crabble nalogysquite mperfect,owever,ecausewhereaswemightet heproductionf"quagmire"s a goalatthe utset fthegame,the ineagehas no specific oals 45). In ourstudy fconstraint,owever,the nalogy s a goodone,because t sthe esearcher homustnventossibleendpointsor lineage n order ostudy volutionnthisway.Thisbrings sback to the questionof the usefulness f the conceptof constraintnevolutionaryiology.Canwelearn nythingystudyinghose henomena-namelyonstraints-thatreventr delay nanticipatedesult? believe hatwe can, althoughhere re imits o whatwe can learn.In the following eview of the literature, treat tudiesthatequatephylogeneticffectndphylogeneticonstraint,swellas studieshat ppearto be using phylogeneticonstraint"nthemanner envisionabove)to bemoremeaningful.he distinctionetween onstraintnd effects discussedfurtherna later ectionbelow).THE AUTOCORRELATIONFAMILY OF COMPARATIVEMETHODS FOR REVEALING CONSTRAINTCheverud t al (16) attemptedo define hylogeneticonstraintn a quantita-tivemanner,sing maximum-likelihoodethodnalogousothe ovarianceanalysisfor pportioningariance mongrelatives nto nvironmentalnd

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PHYLOGENETIC CONSTRAINT 311genetic omponents.n thismethod, roups fspecies re the ounterpartofamiliale.g. sibling) roups. he more losely trait racks hylogeny,hehigherwill be thephylogeneticutocorrelationoefficientp) for hat rait.As yet, heres no empirical asis for esting his elationship.ittlemanKot 36) attemptedo improve hemethod fCheverud t al (16) andapplyit to bodyweightn carnivoresnd clutch ize in birds.Grafen40) used akind of autocorrelation ethod, hephylogeneticegression,o deal withphylogeneticffect. or hemost art, pplicationsf utocorrelationethodshave leftconsiderable oom forerror n theiruse of poorlyresolvedphylogenies,lthough he methodsmay have potentialf used in a moreexplicitly istoricalontext30).VARIATIONSON INDEPENDENT CONTRASTSFelsenstein27) presented method or ealing tatisticallyith henon-in-dependence f closelyrelated rganismsn analyses fcausal relationshipsamong phenotypic nd/or nvironmentalariables.Previous uthors adpointeduttheproblemfnon-independence17, 33, 85) buthadattemptedtodeal with tby hiftingheir ttentionotaxonomicevelshigherhanpeciessuch as genera r families. he independentontrasts ethod27) has beendiscussed xtensivelynd furthereveloped ysubsequentuthors13, 29,31, 37, 43); numerous orkers aveusedvariationsn thismethodoexploreconstraintbelow).Lessios (49) used a variant f independentontrastso compare izemeasuresnpairs f sistergeminate) pecies ccurringndifferentnviron-ments.Lessios proposed hat nvironmentalactorsnfluence gg size inechinoderms,nd comparedgeminateswith an Atlantic nd a Pacificrepresentative.ix of seven omparisonshowed hat hePacific epresenta-tiveshadsmaller ggs. This method uggests hat ifferencesnthe rait finterest ayhave arisen ubsequento divergencef terminalpeciespairsfromhe ommon ncestor. hus,phylogeneticonstraintor effect)houldaffectachspecies f he erminalair qually, nddifferencesithinerminalpairs in the traitof interest an reasonably e attributedo ecologicaldifferences.his methods most ikely o be applicable omeasures f size(orotheruantifiableeatures)na homologoustructurenterminalranchesof a lineage. Lessios (49) pointed ut thatno lineage-independentgg sizecharacteristicsxisted or he wooceans, ndicatinghat gg morphologysnot nfinitely alleable ythe nvironment;n otherwords, gg morphologyis constrained.Whether his constraintan be identifieds phylogenetic,developmental,rothersopen oquestion. hat s, imits oeggmorphologymayhave esstodo with istoryhanwith tructural,hysiological,r otherrequirementsf beingan egg in general ratherhanbeingtheegg of anechinoderm).

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312 MCKITRICKA similar pproachwas suggested y M0ller& Birkhead64), who didpairwise omparisonsf conspecific opulations. lthoughhemaintenanceof traitsmay be studied y making hesepairwise omparisons,uestionsabout he rigin r oss of featurest nternalatherhanustterminal odes,andparticularlyeatureshat re omplex e.g. suites f ifehistoryraitsuch

as heteroecyn aphids; ee below) are not pproachabley suchmethods.Inthe uantitativetudies escribed bove,the uthorsitheri) comparedclosely elated pecies o determinehe elative oleofhistoryndecologynspecies' raits; r ii) examinedargerineages o assess hehistoricalburden"of a traitwhose currentdaptive ignificanceheywished o examine.Thequestions sked n many volutionarytudies re ftenmore eneralhan hoseaddressed y such quantitativepproaches. or example,we maywish tounderstandhyprimatesxhibit exual ize dimorphism,nd a phylogeneticmethodwould be more appropriatehan some of thestatisticalmethodsdiscussed.We might pproach ur question y firstxamining detailedphylogeneticypothesisor heprimatesnddetermininghepatternforigin(and loss) of size dimorphism.f we found hat, or xample,dimorphismarose wice,we would hen ave wodatapointstwo ineageswhose ommonancestorwas notdimorphic)o compare. We do needat leasttwo norderto test ertain ypothesesbout he ignificancefthe raitf nterestecauseonly ndependentrigins analogies) an be used to test uchhypotheses.)Thisanalysiswould ellus at a coarse evel the ffectsfphylogeny: ithineach ofthose wo ineages, heproximateandmost onservative)nswer othequestion, Whydo theseprimatesxhibitize dimorphism?"ouldbe,"becausetheir ncestors id."However,we are now na positionopursuetheultimatenswers y comparingherolesof selection nd chance ntheseparate rigins f the raitnthese wo ineages 10, 47, 59), andto dentifycandidates orphylogeneticonstraint.f thetrait roseonlyonce in theprimates, owever, ur cological omparisons ouldhave obeamongmoredistantlyelated roups; hiswould ntroducehepossibilityf errornourattemptsodrawgeneral onclusionsbout he volutionfthis rait, ecausewewouldhave to makemore ssumptionsbout heprecisionfthe nalogy(similarityf the rait)nthedifferentroupsnwhicht arose. Most of thestudiesreviewedhere seek to testoptimization ypothesesnd explaindeviations rom redictionss phylogeneticonstraint,r they xplore heroleofcertain eaturesn imitingrpromotingiversityithin lades.CONSTRAINTS ON ECOLOGICAL PATTERNS AND LIFEHISTORY PARAMETERSRyan& Brenowitz86) examined study yMorton69-70) in which heacoustical haracteristicsfhabitats ereproposeds an mportantnfluenceon the volution f bird ongfrequencies. yan& Brenowitz86) suggested

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PHYLOGENETIC CONSTRAINT 313that ody ize, whichmaybe related o phylogeny,onstrainsongfrequencyand hat hismay bscure he ole fhabitatn song volution. ossibly ertainhabitatsre dominated y birds f a single ineage and thereforef a certainsize), andthis ouldresultn a spurious elationshipetween abitatnd ongfrequency.n otherwords,phylogenymay constrain ize, which n turnconstrainsherelationshipf songfrequencyo habitat haracteristics.yan& Brenowitz86) found significantelationshipetween ody ize and ongfrequencymongbird pecies iving n the ame habitat. hey lso foundsignificantelationshipetween hese wovariableswithin womonophyleticgroups suboscines nd oscines) nd one paraphyleticroup nonpasserines)ofbirds; heregressions ere significantlyifferentor hese hree roups.The authorsoncluded rom hese esults hat hylogenynfluencesody izeand that ody ize influencesong frequency. owever, nce they actoredoutbody ize, they ound hat relationshipetween ird ongfrequencyndhabitat ype remained. n other words, phylogeny as not completelyconstrainedhe djustmentf songfrequencyohabitatn this ase. Similarconclusions ere eached yMiles& Dunham62),who xaminedifehistorypatternsn guanidizards nd attemptedoseparate hylogeneticffectsndecological esponse. hylogeneticffects ere dentifiedsing he utocorre-lationmethodnd hen emoved,nd he emainingariation ashypothesizedtoreflect daptation.Gittleman34) studied llometricndphylogeneticffectsn lifehistoryvariables n themammalianrder arnivorand found hat ifehistoryraitswerepositivelyorrelated ith odyweightnd brainweight. he slopesofthese elationships erenot ignificantlyifferentmong amilies, hich edGittleman34) to conclude hat hefamilys the ppropriateaxonomicevelfor xaminingcological orrelates ith ifehistoryraits. owever, ssoci-ations mong raits ithin amilies id not how onsistentor nterpretable)patterns. or example,within heCanidae, gestationengths longer nomnivoreshanncarnivores,utno suchdietary atterns evidentn otherfamilies fCarnivora. orest-dwellingelids ave heavier ittershanwood-landspeciesof felids.Significantifferencesnmost ifehistoryariableswerefound etween amilies,venafter izeeffects ere emoved. o cleartrends ere videntnthis historicalnalysis, owever,nd Gittleman34)was not able to suggestwhat olephylogeneticistorymayhaveplayed nthe volution f ifehistoryraitsnthisgroup f mammals.Stearns92) attemptedo control or hylogenyn hisstudy f ifehistoryvariationnreptiles, singmultivariatenalyses ndcomparisonsf lizardsindifferentrders nd families. his studywas criticized yVitt& Seigel(94) andby Hedges 44) for hefollowingeasons:Hedges 44) pointed utthat hephylogeneticomparisonshouldhave been madebetweenaxa thatweremore imilarcologicallyhan hose sedbyStearns92). Heemphasizedthegreat ifficultyf solatinghe ffects fphylogenyn lifehistoryraits

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314 MCKITRICKandsuggestedhat omparisonsetweenonvergentroupsmight avebeenmoremeaningful.his s true, lthoughgain, his nvolvesudgmentsboutthedegree ndprecision fthe imilarityfthe nalogous raits;.e. aretraitsthatare convergentlyimilar eallysimilar noughto makeworthwhilecomparisons?espite hehazards fmisjudginghe omparabilityfconver-gent raits, uchrisks re worthaking,s Mitter t al (63) havedone seebelow).Effortsuch as those alreadydescribed o examine imultaneouslyhecoincidence f ecologicalfactors ndphylogeneticistoryre a tremendousadvance n both he cological nd thephylogeneticiterature. uchofthisliterature,owever, xamines hylogeneticffect r taxonomicimilarity,and teither oes notdirectlyddress he ssueofphylogeneticonstraintrdoes notdistinguishhat henomenonrom ffect. errickson Ricklefs23)andBurt 13) suggestedhatmethodsuch as those fCheverudt al (16)assess "taxonomic"phylogenetic)imilarityather hanphylogeneticon-straintn the evolution f relationshipsmong variables.Phylogeneticconstraints definednthispaper s thefailure f an anticipatedesult uetohistory,hats, duetotheretentionffeatureshat or omereason imitor divert volutionary athways. axonomic imilaritys the sharing fapomorphiesrretentionfplesiomorphieshat e facto esultn thetaxabeing imilar, ut his imilarityoes notnecessarilymplicatenyparticulartraitnconstraintalthoughtcould). Attemptso "factor ut"this imilarityareusuallymade nthe ontextfstudyingdaptationnd the orrelationfcharacters.n suchcases theresearcher ishes o reduce hedatapoints oanappropriateumber, amely,henumberf imeshe raitf a(eres( rose.The confusion f phylogeneticonstraintnd effectmay also stemfromdifferingiews boutwhetherconstraint"s an active r a passive onditioninthehistoryf a lineage see furtheriscussion f the attern the ectionondevelopmentalonstraint,elow).Moritz t al (68) performedphylogeneticnalysis fCnemidophorusostudy istoricalatternsfthe rigin fparthenogenesis.hey uggestedhatbecausetrueparthenogenesismongvertebratess limited o "reptiles,"phylogeneticonstraintmust be operative. n otherwords, nonreptilessomehowface an obstacle constraint)o the origin f parthenogenesis,whereas eptilesrereleased rom hat bstacle.Moritz t al werenot bleto discoverwhy this shouldbe the case, although heydid findthat nCnemidophorust least, a certain evel of geneticdivergence etweenhybridizingpecies was necessarynorder orparthenogeneticffspringoresult. heuseof he oncept f onstraintn his ase smeant ocall attentionto the phylogeneticestrictionf a particularvolutionaryhenomenon(parthenogenesis)oone ineage nwhich t evolved everal imes. n effect,theuse ofthe oncept oints ut hat ecauseparthenogenesisslimited,here

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PHYLOGENETIC CONSTRAINT 315must e a constraint.his s simply escriptivendthushasnoexplanatorypower.In some cases, an actualcandidate or the constrainttselfhas beenproposed. arker 77) observed decrease nfrequencyfdisease-resistantlineages fthe egumeAmphicarpa racteata espite hepersistencef itspathogen ynchytriumecipiens.He suggested hat heplants'system fself-pollinationonstrainshe ncrease rmaintenancefdiseaseresistance,because election n traitsinkedwith enesfor iseaseresistance ay esultin nonadaptivehange n the atter.This may be a genetic atherhanphylogeneticonstraint,owever,fthe elf-pollinationystems notpresentin the closestrelatives f Amphicarpa racteata;discussion f geneticconstraints beyond he copeof this aper;for review ee 6.) Futuyma'sanalysis28) ofspeciation ndhostplant hiftsnthe eafbeetlesOphraellaindicated hat ivergence fhostplant pecies ongprecededpeciationndhost hiftsy thebeetles. uchearly ivergences in contrasto predictionsofclassicalparasitologyhat peciationnhosts ndtheir arasites hould econgruent26 in28). Futuyma28) didnot nterprethis ackofcorrespon-dencebetween ost hiftsybeetles ndhost lant peciations evidence orconstrainthost shiftswere, after ll, eventuallychieved); nstead,hesuggested hatnovel hostplantchemistriesepresentbstacles hatmayeventuallyeovercomey he nsects.nother ords, constraints"re imitstorates fchange nOphraella atherhan ochangetselfsee,for xample,11, 29).Numerous uthors 19, 47, 88, 89, 97) have advocatedthe use ofphylogenieso testhypothesesfconstraintrtransformationersus ypoth-eses ofoptimization,daptation,r quilibriumseeLauder47) for iscussionoftransformationersus quilibriumnalyses]. n whatwas among hefirstattempts y an ecologistto use a phylogeneticrameworko evaluatehypothesesfecological ptimizationersus hylogeneticonstraint,oran(65-66) examined he volutionfhost-plantlternationheteroecy)naphids(Aphidoidea). he examined ossiblepatternsf origin fheteroecyn aphylogenyfthegroup, ptimizinghecharacterssingdeterminationsfhomologybased on analysisof associated ife history haracters. heconcluded hat eteroecyvolved everal imesndependentlynaphids, nthe basis that he nature f thecycle between exual andparthenogeneticphases differs mong heteroecious pecies; the cycles (and thereforeheteroecy)reprobably othomologous.naddition,hefossil ndphyloge-netic vidence uggests hat eteroecys derivednaphids.Becauseheteroecyisfairlyommonmong phids ut aremong erbivorousnsectsngeneral,Moran uggestedhat omefeaturef aphidsmust redisposehem o theevolution fheteroecy.heexamined arious daptationalypothesesboutthe volution fthis rait,utnone eems o take ll the vidence nto ccount

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316 MCKITRICKsatisfactorily.s an alternative,he proposed hypothesisased on con-straint, hich tates hat he arly pring eneration as somehow ess abletoswitch osts ven houghwitchingoa herbaceous ostmight ring reaternutritionalewards han emainingn the ncestral oodywinter ost.Why hould heearly pring orms e constrained? orannoted hat hefirst pringgeneration n the winter ost is usually the "fundatrix,"parthenogeneticemalewhichnheteroeciouspecies sapparentlypecializedfor xtraordinaryecundity, ith oorly eveloped imbs nd senseorgans.In autoeciousphids, n the ther and, hefundatrixs very imilaro otherparthenogeneticemales. When nutritionallyuperiorherbaceousplantsappeared thishappened ater n evolutionaryime han heappearance fwoody lants), omegenerationsf aphidswere ble to switch osts, ut hespecialized fundatrixould not. The species as a whole was thereforecommittedotheancestral lant orpart fits ife ycle i.e. constrained),andthenew hostwas used for herest fthe ife ycle.Inorder otest he onstraintypothesisffectively,e wouldneed ohavea detailed hylogenyf theAphidoidea,howing hepatternf origin/lossfbothheteroecynd autoecy nAphidoidea, nd where n that hylogenyheexistence f specialized undatricesrose nthegroup. t is notenough oshow that the occurrence f specialized fundatricesnd heteroecyrecorrelated; e must howthat hey recausally orrelated25, 52, 58, 59).Thiswouldrequire hat pecialized undatricesvolved rior o the rigin fheteroecy.n one lineageof aphids, heAphidinae, econdaryutoecy asevolved ndthe pecialized undatrixorph as been ost 67). By nference,inthe phids hat etain he ssociation ith heprimitivewoody)host lant,the raits f he pecialized undatrixorphmayndeed onstituteconstraint.Constructingetailedphylogenetic ypothesesnd examining atternsftransformationn theecologicalor other arametersf interest ithin hatphylogeneticrameworkre key ounderstandingheroleofphylogenys aconstrainingnfluencencharactervolution.RELATIONSHIP BETWEEN PHYLOGENETIC ANDDEVELOPMENTAL CONSTRAINTAlthough ould 38) correctlyointedut hat ntogenys themilieu hroughwhichhistorical onstraints expressed, hylogeneticnd developmentalconstraintre overlappingut not dentical oncepts.Developmentalon-straint as beendefined s "a bias on theproductionfvariant henotypesora limitationn phenotypicariabilityausedbythe tructure,haracter,composition,rdynamicsfthe evelopmentalystem"55; see also73, 95).In otherwords,developments a seriesof branchingvents hatmaybestronglyonstrained;he esultingpecies- r ineage-specificatternsrethe

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PHYLOGENETIC CONSTRAINT 317result fthe veragingfnumerousuch vents. heconcept asnotyet eenwell-integratedith concept fphylogeneticonstraintbut ee47). Thesetwotypes fconstraintre ntimatelyelated, s canbe illustratedsing hesimple xample mployed y Alberch1) to clarifyhe oncept f develop-mentalconstraint.everal largedomestic aninebreedsshow a strongtendencyo develop sixth oe,whereas maller reeds uchas miniaturepoodlesnever o. Alberch 1) explained his nterms f thegreater umberofcells n the argerimb udofthe arger reeds. acking henecessaryellmass, smaller reeds re simply nabletoproduce his xtra oe. In otherwords,size presents simpledevelopmentalonstraint;orrespondingly,phylogeny aypresenthe nitial onstraintfsize (it should e noted hatlarge ize is independentlyerived umerousimes n this xample).Oster t al (75) pointed ut theremarkableniformityf vertebrateimbmorphologyhroughoutvast xpanse f ime. hey uggestedhathistoricalinertia" as an inadequatexplanation,eferringothephenomenonnsteadas resultingromhistoricallyonservedmechanismsfmorphogenesis"p.874). These lternativesuggest n mportantistinctionetween assive ndactivehistoricalnfluencessee below). Althoughhe uthors robably idnot ntend scenario fbalancingelection, hegeneralizedimbplancouldbe viewedas an optimal ne, andthe retentionf this imbplan mposeslimitsa bias orconstraint)nthevariantshat an be generatedromt see96 for urtheriscussion f these imits).Observations f natural nd experimentallynducedvariationn limbmorphologyuggest way in whichdevelopmentalndphylogeneticon-straintmay be related o one another.Among the salamanders,everalexamplesexist in whichexperimentalerturbationf limbdevelopmentproduces range fteratologies.his range oesnot ppear o beunlimited;rather,t mimics henatural ariation ccurring ithin he ineage nd doesnot exceed it (2). The generalpattern f the vertebrateimb is highlyconservative,ndclearly, xperimentsesigned operturbtsdevelopmentcanproduce nly limited ange f alternativeatterns.heseexperimentssuggest hat evelopment aybe imposingonstraintshroughouthehistoryofa lineage i.e. developmentalonstraintsead toorareactuallyquivalenttophylogeneticonstraints).urthermore,ny ineagemusthave a suite fdevelopmentalonstraintshat t does notsharewith nyotherineage. naddition,tshares suite fconstraintsithts ister roup, nd nturn hatlarger roup hares onstraintsith ts sister roup.From ower ohigherphylogeneticevels, hedevelopmentalonstraintsecomencreasinglyoreinclusive.Thehighlyonservativeature f thebasicvertebrateimbplanraises hequestion fwhetherhe nfluencefhistorys an active ra passiveone intheretentionf thisplan; notherwords, s theretentionf theplandue to

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318 MCKITRICKinertia r constraint?fhistoryffers othing ut nertian this ase, thenstasis esults rom hebasicfunctionalityfa particularauplan "if t ain'tbroke, on'tfix t"). fhistoryctivelyonstrains,hen tasismay esult romthe ifficultyf moving iadevelopmentrom particularauplan oanother(giventhe fundamentalequirementffunctionality)itworks nd it can'tchange).These reboth xtremendpossibly arrownterpretations,nd heysuggest hat heconcepts fphylogeneticnd developmentalonstraintsreoverlapping. he underlying echanisms f phylogeneticonstraintsregeneticnddevelopmentalonstraintsrfactors,ut t s possible o discussand even study ny of theseconstraints ithout eferenceo theothers.Considerably ore xperimentalndtheoreticalork s needed ointegratethese oncepts.THE CONCEPT OF KEY INNOVATIONWhereashe oncept fphylogeneticonstraintsgenerallynvoked oexplainwhy certainraitmightot ave risen rmight ot ave een ost, he onceptofkey nnovations associatedwith ttemptso explain daptive adiation(speciosity)nparticularineages 50, 56) andmay e viewed s a release romconstraint.n otherwords,phylogeneticonstraintndkey nnovationremirrormage conceptsused to erect causal hypothesesbout characterevolution. auder 47) professed hat ypothesesfthiskind re untestablebecause ll traitsreuniquentheirrigin; owever,argue therwiseelow.Raikow 83) pointed ut an importantroblemwith eginningnvestiga-tions fkey nnovationy askingwhy certainlade s so speciose: ll theworld's clade,andtheres no compellingeason o investigatenecladeoveranother. ach simply epresentssingle rbitrarilyhosennode nthecladogram f life,perhapsdiagnosedby several haractershat ffer oobvious lues to their otentialnvolvementn"adaptive" adiations. his snoreason oabandon he oncept, owever. ndoubtedlyhe rigin fsomefeatures f organisms as indeedhad an influencen theopportunityorspeciation.t s more roductiveophrase uestionsbout peciosityr ratesofevolutionntermsf historicalypothesesbout he daptive ignificanceofspecific raits,s Mitter t al (63) have donefor hytophagyninsects.Such an approachs fraught ith ifficulties.heprimarybstacles thatphylogeneticypothesesf sufficientetail nd ncludingnough nrelatedgroups isplayinghefeaturef nterestrevery are. fone does have sucha hypothesis,howingwhere nd how often he trait as arisen, ne mustthenmakecertainssumptionsbout hecomparabilityfthetrait nall ofthe groups. By definition,he several occurrences f the trait re nothomologous,o onemustmake ssumptionsbout hedegree fanalogy fthetraittself, bout he environmentshere heorganismsive that how

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PHYLOGENETIC CONSTRAINT 319thetrait, nd aboutwhetheruchcomparisonsremeaningful.he hazardsseemworth he risks.Mitter t al (63) tackled hem or n exceptionallychallengingroup f organisms,he nsecta, sing phylogeneticrameworkandassuming hat hytophagystrictlyefined)s comparablenthegroupsthat xhibit t; theywereunable o reject hehypothesishat hytophagyscausally elated o speciosity.Lauder& Liem (48) propose an alternativepproach o studying heimplicationsf evolutionaryovelties, amely o identifyhenovelty63)ratherhan he lade, nd henmake priori redictionsbout he volutionaryconsequences f possessing t.Theirhypotheticalxample nvolved singleorigin f noveltyas determinedymappingtonto n ndependentlyerivedphylogeny) nd a predictionbout increasedmorphologicalrather hannumerical) iversity ithin heclade thathas it, comparedwith he sistergroup rother utgrouphatacks t. The final tep n the pproachwas tolookfor nalogous ituationsnother lades hat ould fferndependentestsof theirhypotheses bout structuraliversity. he examples given areduplicationfgenes ompared ith uplicationf tructuraldesignlements"(i.e. biomechanicalinkages nthe aw of ray-finnedishes).Thisapproachattemptsomakehighly eneral tatementsbout volutionaryattern,uchas that tructuraliversityncreaseswhen here s an increasenthenumberof pathways vailable to achieve a certain unction. t such a level ofgenerality,hepossible onclusionsmay eemrather ninformativer eventrivial,lthoughhey rehighly onservative.hemore ecklesspproaches,such as that aken y Mitter t al (63), may ultimatelye moreuseful orrevealingess general atternsfevolutionarymportancendfor nderstand-ing therelationshipetween hylogeneticonstraintnd the iberationromsuchconstraints.CONTEXTS FOR USE OF THE CONCEPT OFPHYLOGENETIC CONSTRAINTAt leastthree lasses of contexts or heuse of thephylogeneticonstraintconcept re videntrom xaminationf he iterature.n oneclassof ontexts,constraintas beenexamined oexplain ariancenrates fevolution,s intests or hanges ver imenthe lopeof associationsmong ariables13;29) ortests fsimilaritycrossorwithin axonomicevels 8, 16, 36, 49).A second lass ofcontextss thatnwhich onstraints implied rdirectlyinvoked o explainvariationn ecological or other raits mongtaxa. Inextremeases, constraints inferredo be responsibleor nytrait hat staxonomicallyitherwidespread8, 41) or limited parthenogenesisnlizards-68). A third lass of contextsncludes tudieswhose uthors avesimply ecognized nd explored he mportancef taking hylogenynto

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320 MCKITRICKaccount n comparingifehistoryarameterscross pecies 10, 18, 20:185,27, 34, 39, 42, 43, 47). This concern eflectsheproblem f sampling rrorinmakingomparisonsmong pecies: f everal pecies n one's sample reclosely elated,hose everal peciesmayreduce o one data point. n otherwords, cological imilaritiesmong peciesmaybe due to the nheritanceofprior hylogeneticommitments,o useMoran's 65) term.A number fsubsequenttudies avefocused n this roblemndhave ttemptedo ddressitby carefullyhoosing hetaxonomicevel atwhich o make omparisons(see, e.g., 35); however, s has been pointed ut (15, 58), it is not thetaxonomicevel that s important,utrather, he evel n thephylogenytwhich he rait f interest as arisen. f the raitrose ndependentlyn twoclosely elatedpecies, hose pecies an still etreatedeparatelyor nalyticpurposes.The trick, f course, is determininghe pattern f characterevolution, hichs impossible ithout detailed hylogeneticnalysis uchas those ttemptedy a number f workers19, 25, 52, 57-59, 82). Inotherstudies, hypothesisf constraints carefullyonstructeds an alternativeooptimizationxplanations,uch as in Moran's 65) study fheteroecynaphids.Few suchexplicit ffortso study hylogeneticonstraintavebeenmade thusfar. f any progresss to be made n assessing hevalue of thisconcept,manymore uch ffortsbviouslyrenecessary.RECOMMENDATIONS ON METHODS FOR TESTINGHYPOTHESES OF PHYLOGENETIC CONSTRAINTIfoneexamines hegrowingiteraturencomparative ethodso review hestatus f theconceptof phylogeneticonstraint, striking ichotomysevident. n one branch fthis ichotomyvarietyfquantitativepproachesisbeing pplied y large roup f omparativeiologists hose undamentalresearchrogramso not nclude hegenerationfphylogeneticypotheses.Thesebiologists se several lternativesogeneratinghylogeniesopursuetheir oal ofremoving hylogeneticffectsn order o study volution:i)use phylogeniesonstructedy others; ii) use existing lassificationsndmake omparisonssing axonomicndices f various inds; iii) a combina-tion fthese wo.The atterwo pproaches, hich avebecomencreasinglysophisticated,ave apparentlypawned he greatest arietyf quantitativemethods12, 13,27, 31, 40, 43, 54).On the therranch f he ichotomyre ndividualsorwhom hylogeneticanalysis s at leastpart f thebasisoftheresearch rogram. heyuse theirphylogenies o generate r testhypothesesbout evolution singdirectcomparisons10, 14, 19, 22, 59-61, 82, 97) or statisticalests fpatternsfgains nd osses ndependentariables ith espectoan ndependentariable(25, 52, 58). For this lass ofresearchers, ethodshat mploy axonomic

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PHYLOGENETIC CONSTRAINT 321comparisonsmay seem doomed to failure, t least at the moment.Mostclassificationsre old, based on eclectic ather han ladisticmethods, ndclearly ull f many rrors hat ould eriously ias any omparativenalysisbased upon them. urthermore,ny decisions bout hetaxonomicevel atwhich o make thecomparisons ill seem contrived;f thetrait f interestaroseseveral imeswithin group f closelyrelated pecies,for xample,then t s entirelyppropriateo nclude ll those pecies nthe nalysis, venif they are congeners 58). Furthermore,uantitative ethods uch asindependentontrasts, hich re locallybutnotglobally arsimonious,retroublingo historical iologists. he actualpatternf origin nd oss of thetraitmust e thefocus fthe nalysis, ot ometaxonomiceveldetermineda priori, e it ever o carefullyhosen.For those omparativeiologists ho are not ystematists,owever,t smost rustratingo have an arsenal f nterestingypotheseso testwhennophylogeniesre available; ndeed, he omplaint as beenmade hat equiringa complete hylogenys severelympractical8), althoughtthe ame timemost workersincluding ) do recognize hat omekind of phylogenetichypothesiss imperative.Waitingfor the systematistso producethesephylogenies,f they re not yetavailable, s tiresome; he alternatives toexperiment ith uantitative ethodsor educinghebiases mposed yuseoftaxonomicriteria. he ultimatetilityfthis pproachemains obe seen.Analternativeay o tudyinghylogeneticonstraint,hich advocate ere,uses an explicitphylogenetic rameworknd the "outgroup chool" ofcomparativeiology.Ramsey& Dunbrack84) observed hat ear Ursidae)neonatesre muchsmaller hanwould be expected or hesize of the adultbear,based on aregressionf litter eight n maternal eightnother utherian ammals.By examining he metabolic equirementsf pregnancynd lactation ndthoseof hibernationr winter ormancy, hey oncluded hatcurtailinggestationnd nourishingheyoungvia lactationwas less physiologicallystressfulo a dormantnimal thannourishing fetusby metabolismfmaternal ody protein.Metabolites rom ody proteinwoulddisrupthedormancy ecause nitrogenousastesmust e eliminated,nd bearsdo noteat or void during he dormant eriod. Metabolizingmaternalipidsandtransferringhem o theyoungduring actation,n theother and,do notresultn wasteproductshat he adultbearwould need to eliminate. heimplicit uggestion ere is that, f these ursidsdid not undergowinterdormancy,hebirthweight f their oungwouldbe more n line with hattypical fotherutherians.owever, hey ite he xample f twobears hatdo nothibernate,hepolarbear (Ursus maritimus)nd thegiantpanda(Ailuropodamelanoleuca). fRamsey& Dunbrack's ypothesiss correct,onemight redict hat hese wospecieswould howhigher irthweights;

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322 MCKITRICKtheir irth eights reactually lso quite ow. Peculiaritiesf these pecies'ecology rgeographic ange re cited s possible xplanationsorwhybirthweight its he ursidpattern ather han he typical utherian attern,ndphylogeneticonstraints also mentioneds a potentialactor.nother ords,mostbearsarephysiologicallyonstrainedo have ow birthweight or hereasonsmentionedbove this hysiologicalonstraint aybe a synapomor-phy forUrsidae), nd thesetwo and other)nonhibernatingears may bephylogeneticallyonstrainedo retain heir ncestral attern.One testof the hypothesisfphylogeneticonstraintould be to showwhether ther,nonursid utherianmammalswith winter ormancy lsoshowed xceptionallyowbirth eights.f hey o,thiswould upport amsey& Dunbrack's84) hypothesisfphysiologicalonstraint,lthoughne wouldstill require phylogeneticnalysis o determine hetherherelationshipbetween he independentariable dormancy) nd the dependent ariable(smallneonate ize) was inthepredictedirection.fthey o not howthepredictedelationship,owever, hiswould uggest hatow neonateweightis simply hebears'response o winter ormancy,ndnondormantearshavethisfeature ecausethey re bears.Thismay nvolve ssumptionsorevenknowledge,f available) bout he omparabilityf physiologicalatternsndistantlyelatedrganisms;nmakinguch omparisonsemaybeintroduc-ing additional actors hat onfoundatherhan lluminateurhypotheses.The hypothesisfphylogeneticonstraintequireshatwinter ormancypreceded he volutionf ow birth eightnbears;nother ords, prematurebirth" nd hence low birthweight s an adaptation o the physiologicalrequirementsfdormancy. ne may est hese xplanationssinghistoricalevidence hat hedormancyabit s primitive ithinhebear ineage it s asynapomorphyor ears), nd that he bsence fdormancynsomebears sdue to a secondaryoss Figure a). However,fdormancys a synapomorphyonly or hose ears hat how t, nd sthereforerimitivelybsentnpandasandpolar ears, nd/orf owneonate eight receded he riginfdormancy,this wouldrefute hehypothesishatdormancyonstitutes phylogeneticconstraintnbears. twould lso refute amsey Dunbrack's84) hypothesisaboutdormancys a physiologicalonstrainteading o ow birth eight.I examined his ssueusing hypothesisfbear elationshipsrom 'Brienetal (73). Thishypothesiss actually consensus ftrees erivedromeveralmolecular ata setspublished y one or moreof the authors r by otherresearchers;hat s, the authorsnalyzed ach data set separatelynd theresultingreeswere ombined. s such, his ypothesisanonlyberegardedas tentative. evertheless,t serves o llustrateow a specific ypothesisfconstraintan be tested. took his ree s a given usinggiant andaas thesister roup o the ther ears nd canids s the utgroup; Myers, ersonalcommunication)ndthen ptimizedeonate ize andwinterormancyn thetreeusingPAUP 3.Os Phylogenetic nalysisUsingParsimony-93).Table

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PHYLOGENETIC CONSTRAINT 323pinnipedsspectacledbearbrown eara polarbearAsiatic lackbearAmerican lackbearsunbearsloth eargiant anda

2 small eonate ize

I winterormancyDossofwinterormancypinnipedsspectacledbearbrown earb L w polarbearAsiatic lackbearAmerican lackbearsunbearsloth eargiantpanda

Figure TentativehylogenyfUrsidae73), showing) distributionforiginf mallneonatesize and winter ormancyhatwouldsupport ypotheses f physiologicalndphylogeneticconstraint;) actual istributionf originf mallneonate ize andwinterormancys indicatedby PAUP (93).

1 showscharactertatesforwinter ormancynd neonate ize. Data ondormancyndbirth eightre as follows:1. spectacled ear Tremarctosrnatus):Very ittle nformations availableabout his pecies; infer,romtshabitat nddistribution80) and fromreportshat tfeeds llyear ound79), that t doesnot xhibit ormancyInformationbout ubweightss also extremelycanty; drawingfthebirth rocess na captive pectacled ear 78) showed heneonate obetiny,bout he ize ofthemother'saw;theweightfthe ubat12weekswasestimatedobe 1.5-2 kg.

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324 MCKITRICKTable 1 Matrix ftaxa and characters.Character = winter ormancy; =absent,1 = present. haracter = neo-nate ize; 0 = "average",1 = small.12 Taxon00 canids01 spectacled ear11 brown ear01 polarbear11 Asiaticblack bear11 American lack bear?1 sunbear01 slothbear01 giantpanda

2. brown ear Ursus arctos)undergoes inter ormancy81, 99). Litterweight s 0.67% of maternal eight74; thetable n (74) showingitterweight s a percentagefmaternal eightncarnivoresistsno speciesother hanbearswith percentageess than1%; percentagesutside fUrsidae ange rom .8% to 16.9%,mean= 8.02%).3. polarbear U. maritimus):oesnotundergo ormancy99). Litter eightis 0.38% ofmaternal eight74).4. Asiatic lackbear U. [Selenarctos]hibetanus):xhibits inter ormancy.Pocock 81:217) reportedhat [T]he evidence egardinghehibernationof theBlack Bear is conflicting,"ut that ndividualsiving t higheraltitudes ntered state fsemi-torporn coldweather.hismaybe the"Himalayan ear" studied y Nelson t al-71), whosedormancyabitswere similar o thoseof the American lack bear. n theformerovietUnion, his pecies"sleepsfrom ctober oMarch" 72). Schaller t al(87) reportedhatAsiaticblack bears hibernate"nChina. nformationon birth eights not vailable.5. American lack bear U. americanus): ndergoes inter ormancy99).Litterweights 0.73% of maternal eight74).6. Malayan un bear (U. [Helarctos]malayanus:No informationn dor-mancy. athe 21) reportedhebirth eightfa cub born ncaptivitys325 g, andthat fa captive emalewhichmayhavebeen themotherfthat ub) as 50.135kg. The litter eights thereforenferredo be about.65% ofmaternal eight.7. sloth ear Melursus rsinus): rom tsdistributionntropicalndia andreportshat thasnoparticularreedingeason 7:446, 81:200), inferredthat his peciesdoes notundergo ormancy.nformationn birth eightis not vailable.

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PHYLOGENETIC CONSTRAINT 3258. Giantpanda Ailuropodamelanoleuca): his peciesdoes nothavewinterdormancy84, 87). Litterweights 0.13% of maternal eight74).

I coded all bear species s having mallneonate ize, despite he ackofinformationor fewspecies.This assumptions of criticalmportanceortestinghehypothesesnd maybe incorrect.The most arsimoniousypothesisorneonate ize and winterormancy,regardlessf optimization ethod,s that mallneonate ize s a synapomor-phyforbears,butthatwinter ormancyroseonce, after heevolution fsmall ize, and was subsequentlyost npolarbears ndsloth ears Figurelb). Therefore,hehypothesishat mallneonateize arose s an adaptationtothephysiologicalequirementsfwinter ormancys not upported. iventhepatternforigin fthese wo haracters,he uggestionhat mallneonatesize is dependentnwinter ormancys not upported.hus,phylogeneticconstraintoes not explain he relationshipetweenwinter ormancyndneonate size in bears, and Ramsey & Dunbrack's 84) hypothesis fphysiologicalonstraints refuted.There s much obe earned bout he etails fbear hysiology,ife istory,and evolution. or example, he fossilrecord hows ursids ppearingnmid-MioceneoRecent epositsnEurope,North merica, nd Asia,butnofossil rsids ppear nSouthAmerica ntil hePleistocene91; Martin 53]noted hefirst ppearance f fossilTremarctos as in the ate Pliocene ndthat remarctinesusthave originatednAsia). It is possible hatno bearswerenSouthAmerica efore he leistocenendpossibly remarctosrnatusis more ecentlyerivedhan s suggested y thephylogenyf O'Brienet al(73). Furthermore,f the ommon ncestorf all modern ears xperiencedtemperater arctic limates, hen ossiblyt underwenteasonaldormancyand the bsence fdormancyn somemodernpecies s, infact, secondaryconditionhowever, iant andas ive n temperatelimate nddo not xhibitdormancy,o thisnference ay eflawed). espite hese otentialroblemsdue to gaps in information,his xample hould erve o illustrateowanoutgroup pproachhas the potential o illuminateur understandingfevolutionaryatternsndprocesses, ncluding hylogeneticonstraint.ereis a case inwhich hylogeneticonstraintas invokedoexplain deviationfrom patternhat s itself deviation rom pattern;ntheory,t spossibletotest or hylogeneticonstraintnthis ase and at the ame ime otest hehypothesishat hysiologicalonstraintsave ed to theevolutionf smallneonate ize in bears. Neither ypothesiss supported.n thiscase, nostatisticalests re required o testsignificancef characterssociations;simple nspectionfthe ladogrameveals hathe xpected elationshipoesnot ccur 14-15).Whenwe havefinishedesting ypothesesfphylogeneticonstraintn

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326 MCKITRICKthismanner, e must sk: if a hypothesisf constraints supported,re theorganisms nable o lose or gain thetrait n question, r have they implynotdone t yet? n one sense,hypothesesf constraintre really ypothesesabout ates f evolution29), becausewe cannot eally now hat omethingis constrainednlesswe can see itsfuture; e cannot aythat omethingillnothappen except erhaps n a biomechanicalngineeringense),only hatit has nothappened.If we testhypothesesf constraintnddeterminehat hylogeneticistorymaybe an importantactorn explaining hy n observed atternoesnotfit he xpected atternasedon predictionsf adaptive ypotheses, e mayin some nstances e able to predict he ikelihood f eventual hange o theexpected atternf uch n exercise eemsuseful. he nstancesnwhich hiscould be usefulmay be limited o phenomena uch as gene productsndbiochemical athways, here ctual onstraintsan reasonably e hypothe-sized and studied, nd developmental nd functional athways,wherepredictionsan be made about he mechanical nd structuralikelihood fmoving rom tateA to state or simplywayfromtateA. Thesepredictionshave their imits, owever, s even engineers re not always uccessfultdetermininghetherheir lueprints ill translatento uccessfulunctionalstructures-(e.g. overcraftsereoriginally esigned o be flyingaucers:thefailure f theflying aucer eft s with hehovercraft).tudiesdemon-stratingransitionrobabilitiesasedon thepast 46) areuseful or lluminat-ing rates f evolution ut may say nothingboutwhether transitionanoccur. believe hatwe can test volutionaryypothesesndreject onstraintas a confoundingactor r confirmt as a possible roximatexplanationoranunanticipatedesult. rom biomechanicalr biochemicalerspectiveemayalso be able to explainwhy,given ertain onditions, e shouldnotexpect certaintructuralr chemical utcome,nd we cantherebydentifythe ctual onstraint.eyond hat, owever, eprobablyannot o. Forthepresent,o test he imits fthe xplanatoryower fphylogeneticonstraint,I advocate the exploration f the concept using detailed phylogenetichypotheseshat ocus n the ctual otentialonstraints,s well s the ecklessformulationf hypotheses bout the evolution f correlated haracters.Certainly,f we are timid boutproposingausal correlationsn characterevolution, e will imit uropportunitieso understandhe llusory onceptofconstraint.CONCLUSIONInreviewinghe oncept f phylogeneticonstraint,havetaken utilitarianapproach hat eeks to explore hemeaning f theconcept ndto testforoccurrencesfconstraintn thehistoryf ineages.A historicalpproachhat

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PHYLOGENETIC ONSTRAINT 327framesxplicit ypothesesbout he elationshipsmong volving haracterswithin phylogeneticontext19, 14, 25, 47, 52, 58, 59, 97) can lead tobetter nderstandingf constraintnd of theevolutionaryistory f thelineage.To understandhenature f suchconstraintshemselves, mecha-nisticpproach hat eeks o dentifyhe nderlyingenetic nddevelopmental"limits o design"will be necessary. uch a goalwill require n integrationofstructural,unctional,nd genetic pproachesothe tudyfevolution6,96) and should ead to productiveollaborationsmong developmentalbiologists, unctional orphologists,uantitativend molecular eneticists,andphylogeneticystematists.hesecollaborativefforts ill beamong hemost roductivereasof researchn evolutionaryiology n thenext ecade.ACKNOWLEDGMENTSI havebenefited reatly rom iscussionswithVernFath,PhilGingerich,JohnGittleman, rianHall, David Ligon, Dan McShea, ShawnMeagher,CharlesMitter, erdMuller, hilMyers,GunterWagner, eterWimberger,andMiriam elditch. ed Garland, odyHey,NancyMoran,Dan McShea,PhilMyers, ndPeterWimbergeread earlier raftsf themanuscriptndofferedmanyvaluable uggestions,orwhich amgrateful. thank ohnFlynn or iscussing ithmehis viewson carnivorehylogeny.This researchwas supportedy grant SR-9006208from he NationalScienceFoundation.LiteratureCited

1. Alberch, . 1985. Developmentalon-straints: hy St. Bernards ftenhavean extradigit and poodlesneverdo.Am.Nat. 126:430-332. Alberch, , Gale, E. 1983. Size de-pendency uring he developmentfthe mphibian oot.Colchicine nduceddigital oss and reduction. .Embryol.Exp. Morphol.76:177-973. Alexander D. 1989. Evolution f thehumanpsyche. n TheHumanRevo-lution, d. P Mellars,C Stringer,p.455-513. Edinburgh: niv.EdinburghPress4. AndersonDJ, Stoyan NC, RicklefsRE. 1987. Why rethere oviviparousbirds?A comment. m.Nat. 130:941-475. Antonovics,J, van TienderenPH.1991. Ontoecogenophyloconstraints?The chaos of constrainterminology.Trends col. Evol. 6:166-686. Arnold J. 1993. Constraintsn phe-notypic volution. m.Nat. 140:S85-107

7. Asdell SA. 1946. Patterns f Mam-malianReproduction.thaca,NY: Cor-nell Univ. Press8. Bell, G. 1989.A comparative ethod.Am. Nat. 133:553-719. Blackburn G, EvansHE. 1986. Whyare thereno viviparous irds?Am.Nat. 128:165-9010. Brooks DR, McLennanDA. 1991.Phylogeny,cology, nd Behavior:AResearch rogramnComparativei-ology. Chicago:Univ. Chicago Press11. Burger,R. 1986. Constraintsor theevolution ffunctionallyoupled har-acters:A nonlinearnalysis f a phe-notypicmodel. Evolution 0:182-9312. Burghardt M, Gittleman L. 1990.Comparativeehavior ndphylogeneticanalyses:New wine, old bottles. nInterpretationnd Explanationn theStudy of AnimalBehavior, ed. MBekoff,D Jamieson, p. 192-225.Boulder,Colo: Westview13. Burt,A. 1989. Comparativemethodsusing hylogeneticallyndependenton-

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