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

Author(s): Mary C. McKitrick

Source: Annual Review of Ecology and Systematics, Vol. 24 (1993), pp. 307-330
Published by: Annual Reviews
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Annu.Rev. Ecol. Syst.1993. 24:307-330
(? 1993 byAnnualReviewsInc. All rightsreserved
Copyright

PHYLOGENETIC CONSTRAINT
IN EVOLUTIONARY THEORY:
Has It AnyExplanatory
Power?
MaryC. McKitrick
Museumof Zoology,University
of Michigan,AnnArbor,Michigan48109

KEY WORDS: constraint,

phylogeny,
evolutionary
theory

Abstract
The notionofconstraints is a centralone in evolutionary
biology.Thatlimits
mayexistin thepatterns resulting fromdiverseevolutionary processes,and
thepossibilitythattheselimitscan be discoveredandexplainedmechanistic-
ally, suggeststhatmuch of evolutionmay be interpretable throughan
integratedtheoryof constraint. Phylogenetic constraint
has been invokedin
a varietyof contextsbutas yetthereis no consensuson itsdefinition. It is
definedhere as any resultor componentof the phylogenetic historyof a
lineage thatpreventsan anticipatedcourse of evolutionin thatlineage.
Hypothesesof constraint can be testedwithina phylogenetic framework;
understanding thenature of theconstraints themselves willrequirea mecha-
nisticapproachthatidentifies thegeneticand developmental components of
"limitsto design."

INTRODUCTION
The conceptof constrainthas been invokedin a varietyof contextsin the
evolutionary to explainevolutionary
literature, patternsand as a counterto
or optimality
adaptationist arguments (32, 39, 45), althoughone authorhas
termedit "an argument of lastresort"(3:461). The literature
reflectsmuch
confusionaboutthe meaningof constraint (5); my goal here is to define
phylogenetic constraint
and to examineits use in evolutionary biology.
Wimsatt& Schank (100:234-35) assertedthat"notionsof evolutionary
progressor changeareproductively discussedin termsof thecloselyrelated
307
0066-4162/93/1120-0307$05.00
308 MCKITRICK

notionof an evolutionary Although

constraint...." I do notclaimtoresolvethe
questionposed in thetitleof thispaper,I do wishto exploreit, to invitea
morerigorousexamination of the meaningand use of the conceptand to
determine whetherthisconceptcan be harnessedto help us revealgreater
detailin theevolutionary patterns we attempt to study.Otherauthorshave
advocateduse of the phylogenetic methodforexploringthe relationship
betweenadaptation andhistorical (10, 14, 19, 24, 25, 27, 52, 58, 59,
effects
97, 98). I wish also to urgea phylogenetic approachto testinghypotheses
formulated specifically to implicateor identify phylogenetic constraintin an
evolutionary system.
In thelastdecade, a "nullmovement" has arisenin evolutionary biology
thathas offered a restrainton a possibleexcessof deterministic explanations
forall evolutionary patterns.This movement advocatestheprominence of
stochasticfactorsin evolution,evenwhenobservedpatterns seemto indicate
a coherent,nonrandom cause. A pivotalpaperin the development of the
movement is thatof Gould & Lewontin(39), in whichtheauthorscaution
againstassumptions of adaptationwhenthehistory of a lineagemayoffer
obvious cues to the statusquo. This paper fueleddiscussionin many
directions.Slowinski& Guyer(90) suggesteda rigorous quantitative method
fordetermining whether of
patterns speciation within clades, compared with
theirsisterclades, deviate from thoseexpectedby chance. The authors said
thatrejectingthenullmodelbythismethod "establishes onlythatdeterministic
diversityevolutionoccurs,notwhether individualphylogenies requiredeter-
ministicexplanations; we willprobablyneverknowwhether theradiation of
anolinelizardsrepresents nonrandom evolution"(p. 916).
Despite the startling realismof such views, the futureof evolutionary
biologyneed notbe seen as a bleak one. Of coursethetruthabouthistory
cannotever be known,but we need not becomenihilistsas a result.The
possibilityof excess existsin anyintellectual wave, and althoughan excess
of"nullness"is notyetapparent, thedangerofitcanbe anticipated (as warned
in 76). The conceptofphylogenetic constraintin someofitsusagesdescends
fromthenullmovement andis notyetwelldeveloped.Itshouldnotbe invoked
as an ultimate explanation. Suchinvocations wouldbe analogoustoSlowinski
& Guyer's(90) exampleof a seriesof coin tosses:We do notrequirean
explanationforthepattern we see becauseit is due to chance,even though
theresultof each coin toss has an ultimatecause thatwe do notbotherto
study.In otherwords,it is not enoughto discoverthattheoccurrenceor
absenceof a certaintraitis relatedto itsretention in a commonancestor,and
to christenthisretention a constraint;thisdiscovery merelyallowsus to shift
ourattention to theappropriate hierarchicallevel.
Thereis moreto be learnedabouttheevolutionary patterns we studyeven
afterwe haveoffered explanations basedon constraint, andI suggesthowto
 PHYLOGENETIC CONSTRAINT 309

proceedtowardthisgoal. I beginby reviewingsome of the literature on

constraint;thisincludespapersthat(i) directlyrefer tophylogenetic constraint;
(ii) implya conceptof phylogenetic constraint;(iii) discussphylogenetic or
"taxonomic"effects;(iv) discusscomparative methods;(v) referto limitsto
diversity;or (vi) referto a notionof keyinnovations (theflipside of limits
to diversity).I also briefly
exploretherelationship ofphylogenetic constraint
tootherconceptsofconstraint suchas thatusedbydevelopmental evolutionary
biologists.Takentogether, thisliterature
is vastandcannotbe dealtwithhere
without losingthefocusofthispaper.I offertherefore a preemptive apology
fornotcitingall relevant andimportant works.In somesense,all evolutionary
studiesimplicate phylogeneticconstraint,
andreviewing thetopicis liketrying
to catcha greasedpig.

DEFINITIONS OF PHYLOGENETIC CONSTRAINT

Derrickson & Ricklefs(23) pointoutthatmanybiologistsconfusephyloge-
neticconstraint withphylogenetic effect;thelatteris thetendency of closely
relatedorganismsto be similardue to theirsharedhistory.They define
phylogenetic constraint as "changesin diversification of a clade,"or "differ-
ences in theevolutionary interactionbetweenphenotype and environment."
Derrickson& Ricklefsproposea methodof identifying constraint using
multivariate analysisto locatechangesin slope of quantitative traitswithin
and amongtaxa. Such a definition of constraint seemsto referto theresult
of constraint rather thanto theactualphenomenon or itscause. Constraint in
generalis a checkon an expectedactionor lackof action,andthusitimplies
the absence of an anticipatedoutcome.Phylogenetic constraintlikewise
impliesthe absence of an anticipatedcourse of evolution,such as, for
example,the failureof birdsto evolve viviparity (4, 9). I would define
phylogenetic constraint, therefore,as anyresultor component of thephylo-
genetichistory of a lineagethatpreventsan anticipated courseof evolution
in that lineage. This definitionis relatedto the "local" developmental
constraints of MaynardSmithet al (55), i.e. themechanisms of constraints
are examinedat thedevelopmental level, and local, as opposedto universal
or global,constraints areconsidered to be thoseapplyingto a "limitedrange
of taxa." It is also similarto Ligon's (51) use of phylogenetic constraint to
mean"thatcertainevolutionary pathwaysare notlikelyto be followedby a
speciesor groupof relatedspecies,as a resultof priorevolutionary history.
In short,yesterday's adaptationmaybe today'sconstraint."
Thisviewmeans,of course,thata researcher hadto askthequestion,why
have birdsneverevolvedviviparity? Althoughmostof theanswersto this
questionhave focusedon physiology, it is a factthattheancestorsof birds
were,likebirds,oviparous.Thustheproximate answerto thequestionmay
310 MCKITRICK

be simplythatbirdshavenotdivergedfromtheirancestors(theyare forever
"constrained" phylogenetically).The morenearlyultimateanswerwouldbe
thatfor a specificreason (namely,the actual constraint,) theyhave not
divergedfromtheirancestors yet(theyaretemporarily constrained; i.e. they
mustovercomephylogenetic inertia).In otherwordstheabsenceofviviparity
withinAves is a matter of variationin ratesof evolution(see, e.g., 29, 90).
Mammals,theonlyotherclade of warm-blooded organisms,are primarily
viviparous,and forsomereasontheyachievedthisaheadof thebirds.Why
theymanagedthisbeforebirdscould be forphysiologicalreasons(avian
physiology is delayingtheachievement of viviparity)
or foranynumberof
otherreasons.Derrickson& Ricklefs(23) were correctin surmising that
constraint will manifestitselfin variationin ratesof characterevolution;
however,reconstructing ancestralstatesat thenodesof a phylogenetic tree
will be a moreaccurateindicatorof such a manifestation thanany method
relyingon a taxonomichierarchy. By analogy,thelengthof timeone must
waitbeforeone can spell theword"quagmire"in a gameof Scrabblewill
certainlydependontheletters onereceivesattheoutsetofthegame.Similarly,
dependingon thestarting materials,twolineagesmaydiffer in thelengthof
timeit takesthemto reacha certainresultsuch as a flipper(to choose an
exampleof a typeof structure thathas evolvedin morethanone lineage-
obviouslywe cannotuse an exampleof a structure in one lineagethatwill
eventually be evolvedindependently in another).As a reflection ofevolution-
aryhistory, theScrabbleanalogyis quiteimperfect, however, becausewhereas
we mightsettheproduction of"quagmire"as a goal attheoutsetofthegame,
thelineagehas no specificgoals (45). In our studyof constraint, however,
theanalogyis a goodone,becauseitis theresearcher whomustinvent possible
endpoints fora lineagein orderto studyevolutionin thisway.Thisbringsus
back to the questionof the usefulnessof the conceptof constraintin
evolutionary biology.Can we learnanything bystudying thosephenomena-
namelyconstraints-that prevent or delayan anticipated result?I believethat
we can, althoughthereare limitsto whatwe can learn.
In the followingreview of the literature, I treatstudiesthat equate
phylogenetic effectandphylogenetic constraint, as wellas studiesthatappear
to be using"phylogenetic constraint" in themannerI envision(above) to be
moremeaningful. The distinctionbetweenconstraint and effectis discussed
furtherin a latersection(below).

THE AUTOCORRELATION FAMILY OF COMPARATIVE

METHODS FOR REVEALING CONSTRAINT
Cheverudet al (16) attempted
to definephylogenetic in a quantita-
constraint
tivemanner,usinga maximum-likelihood methodanalogoustothecovariance
analysisforapportioning varianceamongrelativesintoenvironmental and
 PHYLOGENETIC CONSTRAINT 311

geneticcomponents. In thismethod,groupsof speciesarethecounterpart to

familial(e.g. sibling)groups.The morecloselya traittracksphylogeny, the
higherwill be thephylogenetic autocorrelation (p) forthattrait.
coefficient
As yet,thereis no empiricalbasis fortestingthisrelationship.Gittleman &
Kot (36) attempted to improvethemethodof Cheverudet al (16) and apply
it to bodyweightin carnivores and clutchsize in birds.Grafen(40) used a
kindof autocorrelation method,the phylogenetic regression,
to deal with
phylogenetic effect.Forthemostpart,applications ofautocorrelation
methods
have left considerableroom for errorin theiruse of poorly resolved
phylogenies,althoughthe methodsmay have potentialif used in a more
explicitlyhistoricalcontext(30).

VARIATIONS ON INDEPENDENT CONTRASTS

Felsenstein (27) presenteda methodfordealingstatistically withthenon-in-
dependenceof closelyrelatedorganismsin analysesof causal relationships
among phenotypicand/orenvironmental variables.Previousauthorshad
pointedouttheproblemof non-independence (17, 33, 85) buthad attempted
todealwithitbyshifting theirattention
totaxonomic levelshigher thanspecies
suchas generaor families.The independent contrasts method(27) has been
discussedextensively and furtherdevelopedby subsequentauthors(13, 29,
31, 37, 43); numerous workers haveusedvariations on thismethodtoexplore
constraint(below).
Lessios (49) used a variantof independent contraststo comparesize
measuresin pairsof sister(geminate)speciesoccurring in differentenviron-
ments.Lessios proposedthatenvironmental factorsinfluenceegg size in
echinoderms,and comparedgeminateswith an Atlanticand a Pacific
representative.Six of sevencomparisons showedthatthePacificrepresenta-
tiveshad smallereggs. This methodsuggeststhatdifferences in thetraitof
interestmayhave arisensubsequentto divergence of terminal speciespairs
fromthecommonancestor.Thus,phylogenetic constraint (or effect)should
affecteachspeciesoftheterminal pairequally,anddifferences withinterminal
pairs in the traitof interestcan reasonablybe attributed to ecological
differences. This methodis mostlikelyto be applicableto measuresof size
(orotherquantifiable features)ina homologousstructure interminal branches
of a lineage.Lessios (49) pointedout thatno lineage-independent egg size
characteristicsexistedforthetwooceans,indicating thategg morphology is
notinfinitely malleablebytheenvironment; in otherwords,egg morphology
is constrained.Whetherthisconstraint can be identified as phylogenetic,
developmental, orotheris opentoquestion.Thatis, limitstoeggmorphology
mayhaveless to do withhistory thanwithstructural, physiological, or other
requirements of being an egg in general(ratherthanbeingthe egg of an
echinoderm).
312 MCKITRICK

A similarapproachwas suggestedby M0ller& Birkhead(64), who did

pairwisecomparisons of conspecific populations.Althoughthemaintenance
of traitsmay be studiedby makingthesepairwisecomparisons, questions
abouttheoriginor loss of features at internalratherthanjustterminal nodes,
andparticularly features thatarecomplex(e.g. suitesoflifehistory traitssuch
as heteroecy in aphids;see below) are notapproachable by suchmethods.
In thequantitative studiesdescribedabove,theauthorseither(i) compared
closelyrelatedspeciesto determine therelativeroleofhistory andecologyin
species'traits;or(ii) examinedlargerlineagestoassessthehistorical "burden"
of a traitwhosecurrent adaptivesignificance theywishedto examine.The
questionsaskedinmanyevolutionary studiesareoftenmoregeneralthanthose
addressedby such quantitative approaches.For example,we may wish to
understand whyprimates exhibitsexualsize dimorphism, anda phylogenetic
methodwould be more appropriate thansome of the statisticalmethods
discussed.We mightapproachour questionby firstexamininga detailed
phylogenetic hypothesis fortheprimates anddetermining thepattern oforigin
(and loss) of size dimorphism. If we foundthat,forexample,dimorphism
arosetwice,we wouldthenhavetwodatapoints(twolineageswhosecommon
ancestorwas notdimorphic) to compare.(We do need at leasttwo in order
to testcertainhypotheses aboutthesignificance ofthetraitofinterestbecause
onlyindependent origins(analogies)can be used to testsuch hypotheses.)
This analysiswouldtellus at a coarseleveltheeffects of phylogeny: within
each of thosetwolineages,theproximate (and mostconservative) answerto
thequestion,"Whydo theseprimatesexhibitsize dimorphism?" wouldbe,
"becausetheirancestorsdid." However,we are now in a positionto pursue
theultimateanswersby comparingtherolesof selectionand chancein the
separateoriginsof thetraitin thesetwolineages(10, 47, 59), andto identify
candidatesforphylogenetic constraint. If the traitarose only once in the
primates, however,ourecologicalcomparisons wouldhavetobe amongmore
distantlyrelatedgroups;thiswouldintroduce thepossibilityof errorin our
attempts to drawgeneralconclusionsabouttheevolution ofthistrait,because
we wouldhaveto makemoreassumptions abouttheprecisionof theanalogy
(similarityof thetrait)in thedifferent groupsin whichit arose.Mostof the
studiesreviewedhere seek to test optimization hypothesesand explain
deviationsfrompredictions as phylogenetic or theyexplorethe
constraint,
roleof certainfeatures in limitingor promoting withinclades.
diversity

CONSTRAINTS ON ECOLOGICAL PATTERNS AND LIFE

HISTORY PARAMETERS
Ryan& Brenowitz(86) examineda studyby Morton(69-70) in whichthe
acousticalcharacteristics influence
of habitatswereproposedas an important
on theevolutionof birdsongfrequencies. Ryan& Brenowitz(86) suggested
 PHYLOGENETIC CONSTRAINT 313

thatbodysize, whichmaybe relatedto phylogeny, constrains songfrequency

andthatthismayobscuretheroleofhabitatinsongevolution.Possiblycertain
habitatsaredominated bybirdsof a singlelineage(and therefore of a certain
size), andthiscouldresultin a spuriousrelationship betweenhabitatandsong
frequency.In otherwords,phylogenymay constrainsize, whichin turn
constrains therelationship of songfrequency to habitatcharacteristics. Ryan
& Brenowitz (86) founda significant relationship betweenbodysize andsong
frequency amongbirdspecieslivingin thesame habitat.Theyalso founda
significant relationshipbetweenthesetwovariableswithintwomonophyletic
groups(suboscinesand oscines)and one paraphyletic group(nonpasserines)
of birds;theregressions weresignificantly different forthesethreegroups.
The authorsconcludedfromtheseresultsthatphylogeny influences bodysize
and thatbodysize influences song frequency. However,once theyfactored
outbodysize, theyfoundthata relationship betweenbirdsongfrequency and
habitattype remained.In otherwords, phylogenyhas not completely
constrained theadjustment of songfrequency to habitatin thiscase. Similar
conclusions werereachedbyMiles& Dunham(62), whoexaminedlifehistory
patterns in iguanidlizardsand attempted to separatephylogenetic effects and
ecologicalresponse.Phylogenetic effectswereidentified usingtheautocorre-
lationmethodandthenremoved,andtheremaining variation washypothesized
to reflectadaptation.
Gittleman (34) studiedallometric and phylogenetic effectson lifehistory
variablesin themammalian orderCarnivoraand foundthatlifehistory traits
werepositively correlatedwithbodyweightandbrainweight.The slopesof
theserelationships werenotsignificantly different amongfamilies,whichled
Gittleman (34) to concludethatthefamilyis theappropriate taxonomiclevel
forexamining ecologicalcorrelates withlifehistory traits.However,associ-
ationsamongtraitswithinfamiliesdid notshowconsistent (or interpretable)
patterns.For example,withinthe Canidae, gestationlengthis longerin
omnivores thanin carnivores, butno suchdietarypattern is evidentin other
familiesof Carnivora.Forest-dwelling felidshave heavierlitters thanwood-
land speciesof felids.Significant differences in mostlifehistoryvariables
werefoundbetweenfamilies,evenaftersize effects wereremoved.No clear
trendswereevidentin thisahistorical analysis,however,andGittleman (34)
was notable to suggestwhatrole phylogenetic historymayhave playedin
theevolutionof lifehistory traitsin thisgroupof mammals.
Stearns(92) attempted to controlforphylogeny in his studyof lifehistory
variationin reptiles,usingmultivariate analysesand comparisons of lizards
in different ordersand families.This studywas criticizedby Vitt& Seigel
(94) and by Hedges(44) forthefollowing reasons:Hedges(44) pointedout
thatthephylogenetic comparisons shouldhavebeenmadebetweentaxathat
weremoresimilarecologicallythanthoseusedbyStearns(92). He emphasized
thegreatdifficulty of isolatingtheeffectsof phylogeny on lifehistory traits
314 MCKITRICK

and suggestedthatcomparisons betweenconvergent groupsmighthavebeen

moremeaningful. Thisis true,although again,thisinvolvesjudgments about
thedegreeandprecisionofthesimilarity oftheanalogoustraits;i.e. aretraits
thatare convergently similarreallysimilarenoughto make worthwhile
comparisons? Despitethehazardsof misjudging thecomparability ofconver-
genttraits,suchrisksare worthtaking,as Mitteret al (63) have done (see
below).
Effortssuch as those alreadydescribedto examinesimultaneously the
coincidenceof ecologicalfactorsand phylogenetic history are a tremendous
advancein boththeecologicaland thephylogenetic literature. Muchof this
literature,however,examinesphylogenetic effector taxonomicsimilarity,
and it eitherdoes notdirectly addresstheissueof phylogenetic constraintor
doesnotdistinguish thatphenomenon fromeffect. Derrickson & Ricklefs(23)
and Burt(13) suggestedthatmethodssuchas thoseof Cheverudet al (16)
assess "taxonomic"(phylogenetic) similarity ratherthanphylogenetic con-
straintin the evolutionof relationships among variables. Phylogenetic
constraint is definedin thispaperas thefailureof an anticipated resultdue
to history, thatis, due to theretention of features thatforsomereasonlimit
or divertevolutionary pathways.Taxonomicsimilarity is the sharingof
apomorphies or retention of plesiomorphies thatde factoresultin thetaxa
beingsimilar,butthissimilarity does notnecessarily implicate anyparticular
traitin constraint (althoughitcould). Attempts to "factorout"thissimilarity
are usuallymadein thecontextof studying adaptation andthecorrelation of
characters. In suchcases theresearcher wishesto reducethedatapointsto
an appropriate number, namely,thenumber oftimesthetrait ofia(eres(arose.
The confusionof phylogenetic constraint and effectmay also stemfrom
differing viewsaboutwhether "constraint" is an activeor a passivecondition
in thehistory of a lineage(see further discussionof thelatterin thesection
on developmental constraint, below).
Moritzet al (68) performed a phylogenetic analysisof Cnemidophorus to
studyhistorical patternsoftheoriginofparthenogenesis. Theysuggested that
because trueparthenogenesis amongvertebrates is limitedto "reptiles,"a
phylogeneticconstraintmust be operative.In otherwords, nonreptiles
somehowface an obstacle (constraint) to the originof parthenogenesis,
whereasreptilesare releasedfromthatobstacle.Moritzet al werenotable
to discoverwhy this shouldbe the case, althoughtheydid findthatin
Cnemidophorus at least, a certainlevel of geneticdivergencebetween
hybridizing specieswas necessaryin orderforparthenogenetic offspringto
result.Theuse oftheconceptofconstraint inthiscase is meanttocall attention
to the phylogenetic restriction of a particularevolutionary phenomenon
(parthenogenesis) to one lineagein whichitevolvedseveraltimes.In effect,
theuse oftheconceptpointsoutthatbecauseparthenogenesis is limited,there
 PHYLOGENETIC CONSTRAINT 315

mustbe a constraint. This is simplydescriptive and thushas no explanatory

power.
In some cases, an actual candidatefor the constraint itselfhas been
proposed.Parker(77) observeda decreasein frequency of disease-resistant
lineagesof thelegumeAmphicarpabracteatadespitethepersistence of its
pathogenSynchytrium decipiens.He suggestedthatthe plants' systemof
self-pollination constrainstheincreaseor maintenance of diseaseresistance,
becauseselectionon traitslinkedwithgenesfordiseaseresistance mayresult
in nonadaptivechangein the latter.(This may be a geneticratherthana
phylogenetic constraint,
however,iftheself-pollination systemis notpresent
in the closest relativesof Amphicarpabracteata;discussionof genetic
constraintis beyondthescope of thispaper;fora reviewsee 6.) Futuyma's
analysis(28) of speciationand hostplantshiftsin theleafbeetlesOphraella
indicatedthatdivergenceof hostplantspecieslongprecededspeciationand
hostshiftsby thebeetles.Such earlydivergence is in contrast to predictions
of classicalparasitology thatspeciationin hostsandtheirparasitesshouldbe
congruent (26 in 28). Futuyma(28) did notinterpret thislack of correspon-
dencebetweenhostshifts bybeetlesandhostplantspeciationas evidencefor
constraint (host shiftswere, afterall, eventuallyachieved); instead,he
suggestedthatnovel host plantchemistries represent obstaclesthatmay
eventually be overcomebytheinsects.In otherwords,"constraints" arelimits
to ratesofchangein Ophraellarather thanto changeitself(see, forexample,
11, 29).
Numerousauthors(19, 47, 88, 89, 97) have advocatedthe use of
phylogenies to testhypotheses ofconstraintortransformation versushypoth-
esesofoptimization, adaptation,orequilibrium [seeLauder(47) fordiscussion
of transformation versusequilibriumanalyses].In whatwas amongthefirst
attemptsby an ecologistto use a phylogenetic framework to evaluate
hypotheses of ecologicaloptimization versusphylogenetic constraint,Moran
(65-66) examinedtheevolution ofhost-plantalternation (heteroecy) in aphids
(Aphidoidea).She examinedpossiblepatterns of originof heteroecy on a
phylogeny of the group,optimizing thecharacters usingdeterminations of
homologybased on analysis of associated life historycharacters.She
concludedthatheteroecy evolvedseveraltimesindependently in aphids,on
the basis thatthe natureof the cycle betweensexual and parthenogenetic
phases differsamong heteroeciousspecies; the cycles (and therefore
heteroecy) areprobablynothomologous.In addition,thefossilandphyloge-
neticevidencesuggeststhatheteroecy is derivedinaphids.Becauseheteroecy
is fairly
commonamongaphidsbutrareamongherbivorous insectsingeneral,
Moransuggestedthatsome featureof aphidsmustpredisposethemto the
evolutionof heteroecy. She examinedvariousadaptational hypotheses about
theevolutionofthistrait,butnoneseemstotakeall theevidenceintoaccount
316 MCKITRICK

satisfactorily.As an alternative,
she proposeda hypothesis based on con-
straint,
whichstatesthattheearlyspringgeneration was somehowless able
toswitchhostseventhoughswitching toa herbaceous hostmight bringgreater
nutritionalrewardsthanremaining on theancestralwoodywinterhost.
Whyshouldtheearlyspringformsbe constrained? Morannotedthatthe
firstspringgenerationon the winterhost is usuallythe "fundatrix," a
parthenogenetic femalewhichinheteroecious speciesis apparently specialized
forextraordinary fecundity,withpoorlydevelopedlimbsand senseorgans.
In autoeciousaphids,on theotherhand,thefundatrix is verysimilarto other
parthenogenetic females. When nutritionally superiorherbaceousplants
appeared(thishappenedlaterin evolutionary timethantheappearanceof
woodyplants),somegenerations of aphidswereable to switchhosts,butthe
specialized fundatrix could not. The species as a whole was therefore
committed to theancestralplantforpartof its lifecycle(i.e. constrained),
and thenewhostwas used fortherestof thelifecycle.
In ordertotesttheconstraint hypothesis effectively,we wouldneedtohave
a detailedphylogeny of theAphidoidea,showingthepattern oforigin/loss of
bothheteroecy and autoecyin Aphidoidea,and whereon thatphylogeny the
existenceof specializedfundatrices arose in thegroup.It is notenoughto
show that the occurrenceof specialized fundatrices and heteroecyare
correlated;we mustshowthattheyare causallycorrelated (25, 52, 58, 59).
This wouldrequirethatspecializedfundatrices evolvedpriorto theoriginof
heteroecy.In one lineageof aphids,theAphidinae,secondaryautoecyhas
evolvedandthespecializedfundatrix morphhas beenlost(67). By inference,
in theaphidsthatretaintheassociationwiththeprimitive (woody)hostplant,
thetraitsofthespecializedfundatrixmorphmayindeedconstitute a constraint.
Constructing detailedphylogenetic hypothesesand examiningpatternsof
transformation in theecologicalor otherparameters of interest withinthat
phylogenetic framework arekeyto understanding theroleof phylogeny as a
constraining influencein character
evolution.

RELATIONSHIP BETWEEN PHYLOGENETIC AND

DEVELOPMENTAL CONSTRAINT
Although Gould(38) correctly pointedoutthatontogeny is themilieuthrough
whichhistoricalconstraint is expressed,phylogenetic and developmental
constraintare overlappingbut not identicalconcepts.Developmentalcon-
strainthas been definedas "a bias on theproduction of variantphenotypes
or a limitation
on phenotypic variabilitycausedby thestructure, character,
composition, ordynamics ofthedevelopmental system"(55; see also73, 95).
In otherwords,development is a seriesof branchingeventsthatmay be
stronglyconstrained;theresulting species-orlineage-specific
patternsarethe
 PHYLOGENETIC CONSTRAINT 317

resultoftheaveraging ofnumerous suchevents.Theconcepthasnotyetbeen

well-integrated witha conceptof phylogenetic constraint (butsee 47). These
twotypesof constraint are intimatelyrelated,as can be illustrated usingthe
simpleexampleemployedby Alberch(1) to clarifytheconceptof develop-
mentalconstraint.Several large domesticcanine breeds show a strong
tendencyto developa sixthtoe, whereassmallerbreedssuch as miniature
poodlesneverdo. Alberch(1) explainedthisin termsof thegreaternumber
ofcells in thelargerlimbbudofthelargerbreeds.Lackingthenecessary cell
mass, smallerbreedsare simplyunableto producethisextratoe. In other
words,size presentsa simpledevelopmental constraint; correspondingly,
phylogeny maypresenttheinitialconstraint of size (it shouldbe notedthat
largesize is independently derivednumerous timesin thisexample).
Osteret al (75) pointedout theremarkable uniformity of vertebratelimb
morphology throughout a vastexpanseoftime.Theysuggested that"historical
inertia"was an inadequateexplanation, referringto thephenomenon instead
as resultingfrom"historically conservedmechanisms of morphogenesis" (p.
874). Thesealternatives suggestan important distinction betweenpassiveand
activehistoricalinfluences (see below). Althoughtheauthorsprobablydid
notintenda scenarioof balancingselection,thegeneralized limbplancould
be viewedas an optimalone, and theretention of thislimbplan imposes
limits(a bias or constraint)on thevariantsthatcan be generated fromit (see
96 forfurther discussionof theselimits).
Observationsof naturaland experimentally inducedvariationin limb
morphology suggesta way in whichdevelopmental and phylogenetic con-
straintmay be relatedto one another.Amongthe salamanders,several
examplesexist in whichexperimental perturbation of limb development
producesa rangeof teratologies. Thisrangedoes notappearto be unlimited;
rather,it mimicsthenaturalvariation occurring withinthelineageand does
not exceed it (2). The generalpatternof the vertebrate limb is highly
conservative, and clearly,experiments designedto perturb its development
can produceonlya limitedrangeof alternative patterns. These experiments
suggestthatdevelopment maybe imposingconstraints throughout thehistory
of a lineage(i.e. developmental lead to or areactuallyequivalent
constraints
to phylogenetic constraints).Furthermore, anylineagemusthave a suiteof
developmental constraintsthatit does notsharewithanyotherlineage.In
addition,it sharesa suiteof constraints withitssistergroup,and in turnthat
largergroupsharesconstraints withits sistergroup.Fromlowerto higher
phylogenetic levels,thedevelopmental constraintsbecomeincreasingly more
inclusive.
The highlyconservative natureof thebasic vertebratelimbplanraisesthe
questionof whether theinfluence of historyis an activeor a passiveone in
theretentionof thisplan; in otherwords,is theretention of theplan due to
318 MCKITRICK

inertiaor constraint?If historyoffersnothingbutinertiain thiscase, then

stasisresultsfromthebasic functionality of a particular
Bauplan("if it ain't
broke,don'tfixit"). Ifhistoryactivelyconstrains,thenstasismayresultfrom
thedifficultyofmovingvia development froma particular Bauplantoanother
(giventhefundamental requirementof functionality)(it worksand it can't
change).Thesearebothextreme andpossiblynarrow interpretations,
andthey
suggestthattheconceptsof phylogenetic and developmental constraints are
overlapping.The underlying mechanismsof phylogenetic constraints are
geneticanddevelopmental constraintsor factors,butitis possibleto discuss
and even studyany of theseconstraints withoutreference to the others.
Considerably moreexperimental and theoreticalworkis neededto integrate
theseconcepts.

THE CONCEPT OF KEY INNOVATION

Whereastheconceptofphylogenetic constraintis generallyinvokedtoexplain
whya certain traitmight nothavearisenormight nothavebeenlost,theconcept
of key innovation is associatedwithattempts to explainadaptiveradiation
(speciosity)inparticularlineages(50, 56) andmaybe viewedas a releasefrom
constraint.In otherwords,phylogenetic constraintand key innovation are
mirrorimage conceptsused to erect causal hypothesesabout character
evolution.Lauder(47) professedthathypotheses of thiskindare untestable
becauseall traitsareuniqueintheirorigin;however,I argueotherwise below.
Raikow(83) pointedout an important problemwithbeginning investiga-
tionsof keyinnovation by askingwhya certainclade is so speciose:all the
world'sa clade, and thereis no compellingreasonto investigate one clade
overanother.Each simplyrepresents a singlearbitrarilychosennodein the
cladogramof life, perhapsdiagnosedby severalcharactersthatofferno
obviousclues to theirpotentialinvolvement in "adaptive"radiations.This is
no reasonto abandontheconcept,however.Undoubtedly theoriginof some
featuresof organismshas indeedhad an influenceon the opportunity for
speciation.It is moreproductive to phrasequestionsaboutspeciosity or rates
of evolutionin termsof historical hypotheses abouttheadaptivesignificance
of specifictraits,as Mitteret al (63) havedoneforphytophagy in insects.
Such an approachis fraught withdifficulties. The primary obstacleis that
phylogenetic hypotheses of sufficient detailand includingenoughunrelated
groupsdisplaying thefeatureof interest are veryrare.If one does have such
a hypothesis, showingwhereand how oftenthetraithas arisen,one must
thenmakecertainassumptions aboutthecomparability of thetraitin all of
the groups. By definition,the several occurrencesof the traitare not
homologous,so one mustmakeassumptions aboutthedegreeof analogyof
thetraititself,abouttheenvironments wheretheorganismslive thatshow
 PHYLOGENETIC CONSTRAINT 319

thetrait,and aboutwhether suchcomparisons are meaningful.The hazards

seem worththe risks.Mitteret al (63) tackledthemforan exceptionally
challenging groupoforganisms, theInsecta,usinga phylogenetic framework
and assumingthatphytophagy defined)is comparablein thegroups
(strictly
thatexhibitit; theywereunableto rejectthehypothesis thatphytophagy is
causallyrelatedto speciosity.
Lauder & Liem (48) proposean alternative approachto studyingthe
implications of evolutionary novelties,namelyto identify thenovelty(63)
rather thantheclade,andthenmakea prioripredictions abouttheevolutionary
consequencesof possessingit. Theirhypothetical exampleinvolveda single
originofa novelty (as determinedbymapping itontoanindependently derived
phylogeny)and a predictionabout increasedmorphological (ratherthan
numerical)diversity withinthe clade thathas it, comparedwiththe sister
groupor otheroutgroupthatlacks it. The finalstepin theapproachwas to
lookforanalogoussituations inothercladesthatcouldofferindependent tests
of theirhypothesesabout structural diversity.The examplesgiven are
duplication ofgenescompared withduplication "designelements"
ofstructural
(i.e. biomechanical linkagesin thejaw of ray-finned fishes).This approach
attempts to makehighlygeneralstatements aboutevolutionary pattern,such
as thatstructural diversityincreaseswhenthereis an increasein thenumber
of pathwaysavailable to achieve a certainfunction.At such a level of
generality, thepossibleconclusionsmayseemratheruninformative or even
trivial,although theyarehighlyconservative. The morerecklessapproaches,
such as thattakenby Mitteret al (63), mayultimately be moreusefulfor
revealingless generalpatterns ofevolutionary importance andforunderstand-
ing therelationship betweenphylogenetic constraintand theliberationfrom
suchconstraints.

CONTEXTS FOR USE OF THE CONCEPT OF

PHYLOGENETIC CONSTRAINT
At leastthreeclasses of contextsfortheuse of thephylogenetic constraint
conceptareevidentfromexamination oftheliterature.
In oneclassofcontexts,
constrainthas beenexaminedto explainvariancein ratesof evolution,as in
testsforchangesovertimein theslopeof associationsamongvariables(13;
29) or testsof similarity
acrossor withintaxonomiclevels(8, 16, 36, 49).
A secondclass of contextsis thatin whichconstraintis impliedor directly
invokedto explainvariationin ecologicalor othertraitsamongtaxa. In
extremecases, constraint is inferred
to be responsibleforany traitthatis
taxonomicallyeitherwidespread(8, 41) or limited(parthenogenesis in
lizards-68). A thirdclass of contextsincludesstudieswhoseauthorshave
simplyrecognizedand exploredthe importance of takingphylogenyinto
320 MCKITRICK

accountin comparing lifehistoryparameters acrossspecies(10, 18, 20:185,

27, 34, 39, 42, 43, 47). Thisconcernreflects theproblemof samplingerror
in makingcomparisons amongspecies:ifseveralspeciesin one's sampleare
closelyrelated,thoseseveralspeciesmayreduceto one datapoint.In other
words,ecologicalsimilarities amongspeciesmaybe due to theinheritance
of priorphylogenetic commitments, to use Moran's(65) term.A numberof
subsequent studieshavefocusedonthisproblemandhaveattempted toaddress
it by carefullychoosingthetaxonomiclevel at whichto makecomparisons
(see, e.g., 35); however,as has been pointedout (15, 58), it is not the
taxonomiclevel thatis important, butrather,thelevel in thephylogeny at
whichthetraitof interest has arisen.If thetraitaroseindependently in two
closelyrelatedspecies,thosespeciescanstillbe treated separately foranalytic
purposes.The trick,of course, is determining the patternof character
evolution,whichis impossiblewithout a detailedphylogenetic analysissuch
as thoseattempted by a numberof workers (19, 25, 52, 57-59, 82). In other
studies,a hypothesis is carefully
of constraint constructedas an alternative
to
optimization explanations,such as in Moran's (65) studyof heteroecyin
aphids.Few suchexplicitefforts to studyphylogenetic constraint havebeen
made thusfar.If anyprogressis to be made in assessingthevalue of this
concept,manymoresuchefforts obviouslyare necessary.

RECOMMENDATIONS ON METHODS FOR TESTING

HYPOTHESES OF PHYLOGENETIC CONSTRAINT
If one examinesthegrowingliterature on comparative methods to reviewthe
statusof the conceptof phylogenetic constraint, a striking dichotomyis
evident.On one branchofthisdichotomy a varietyofquantitativeapproaches
is beingappliedbya largegroupofcomparative biologists whosefundamental
researchprograms do notincludethegeneration ofphylogenetic hypotheses.
Thesebiologistsuse severalalternatives to generating phylogenies to pursue
theirgoal of removingphylogenetic effectsin orderto studyevolution:(i)
use phylogeniesconstructed by others;(ii) use existingclassificationsand
makecomparisons usingtaxonomicindicesofvariouskinds;(iii) a combina-
tionofthesetwo.The lattertwoapproaches, whichhavebecomeincreasingly
sophisticated, have apparently spawnedthegreatestvarietyof quantitative
methods(12, 13, 27, 31, 40, 43, 54).
On theotherbranchofthedichotomy areindividuals forwhomphylogenetic
analysisis at leastpartof thebasis of theresearchprogram.Theyuse their
phylogeniesto generateor test hypothesesabout evolutionusing direct
comparisons testsofpatterns
(10, 14, 19, 22, 59-61, 82, 97) or statistical of
gainsandlossesindependent variableswithrespecttoanindependent variable
(25, 52, 58). For thisclass of researchers, methodsthatemploytaxonomic
 PHYLOGENETIC CONSTRAINT 321

comparisonsmay seem doomedto failure,at least at the moment.Most

classifications are old, based on eclecticratherthancladisticmethods,and
clearlyfullof manyerrorsthatcouldseriously bias anycomparative analysis
based uponthem.Furthermore, anydecisionsaboutthetaxonomiclevel at
whichto makethecomparisonswill seem contrived; if thetraitof interest
arose severaltimeswithina groupof closelyrelatedspecies,forexample,
thenitis entirely appropriate to includeall thosespeciesin theanalysis,even
if they are congeners(58). Furthermore, quantitative methodssuch as
independent contrasts, whichare locallybutnotgloballyparsimonious, are
troubling to historicalbiologists.The actualpattern of originand loss of the
traitmustbe thefocusof theanalysis,notsometaxonomicleveldetermined
a priori,be it everso carefully chosen.
For thosecomparative biologistswho are notsystematists, however,it is
mostfrustrating to have an arsenalof interesting hypotheses to testwhenno
phylogenies areavailable;indeed,thecomplaint has beenmadethatrequiring
a completephylogeny is severelyimpractical (8), althoughat thesametime
mostworkers(including8) do recognizethatsome kindof phylogenetic
hypothesisis imperative.Waitingfor the systematists to producethese
phylogenies, if theyare notyetavailable,is tiresome;thealternative is to
experiment withquantitative methodsforreducing thebiasesimposedbyuse
oftaxonomic criteria.The ultimate ofthisapproachremainstobe seen.
utility
An alternative waytostudying phylogenetic constraint,whichI advocatehere,
uses an explicitphylogenetic framework and the "outgroupschool" of
comparative biology.
Ramsey& Dunbrack(84) observedthatbear(Ursidae)neonatesaremuch
smallerthanwould be expectedforthe size of theadultbear,based on a
regression of litterweighton maternalweightin othereutherian mammals.
By examiningthe metabolicrequirements of pregnancy and lactationand
those of hibernation or winterdormancy,theyconcludedthatcurtailing
gestationand nourishing the youngvia lactationwas less physiologically
stressfulto a dormantanimal thannourishing a fetusby metabolismof
maternalbody protein.Metabolitesfrombody proteinwould disruptthe
dormancy becausenitrogenous wastesmustbe eliminated, and bearsdo not
eat or void duringthe dormantperiod.Metabolizingmaternallipids and
transferring themto theyoungduringlactation,on theotherhand,do not
resultin wasteproductsthatthe adultbear would need to eliminate.The
implicitsuggestionhere is that,if these ursidsdid not undergowinter
dormancy, thebirthweightof theiryoungwouldbe morein line withthat
typicalof othereutherians. However,theycitetheexampleof twobearsthat
do not hibernate,the polar bear (Ursus maritimus) and the giantpanda
(Ailuropodamelanoleuca).If Ramsey& Dunbrack'shypothesis is correct,
one mightpredictthatthesetwo specieswouldshowhigherbirthweights;
322 MCKITRICK

theirbirthweightsare actuallyalso quitelow. Peculiarities of thesespecies'

ecologyor geographic rangeare citedas possibleexplanations forwhybirth
weightfitsthe ursidpatternratherthanthe typicaleutherian pattern,and
phylogenetic constraint is also mentioned as a potentialfactor.In otherwords,
mostbearsare physiologically constrained to have low birthweightforthe
reasonsmentioned above (thisphysiological constraint maybe a synapomor-
phyforUrsidae),and thesetwo (and other)nonhibernating bearsmay be
phylogenetically constrained to retaintheirancestral pattern.
One testof the hypothesis of phylogenetic constraint wouldbe to show
whetherother,nonursideutherianmammalswith winterdormancyalso
showedexceptionally lowbirth weights.Iftheydo,thiswouldsupport Ramsey
& Dunbrack's(84) hypothesis ofphysiological constraint,although onewould
stillrequirea phylogenetic analysisto determine whetherthe relationship
betweenthe independent variable(dormancy)and the dependentvariable
(smallneonatesize) was in thepredicted direction. If theydo notshowthe
predicted relationship, however,thiswouldsuggestthatlow neonateweight
is simplythebears'responseto winter dormancy, andnondormant bearshave
thisfeaturebecausetheyare bears.This mayinvolveassumptions (or even
knowledge,if available)aboutthecomparability of physiological patternsin
distantlyrelatedorganisms; in makingsuchcomparisons we maybe introduc-
ingadditionalfactorsthatconfound rather thanilluminate ourhypotheses.
The hypothesis of phylogenetic constraint requiresthatwinterdormancy
precededtheevolution oflowbirth weightinbears;inotherwords,"premature
birth"and hence low birthweightis an adaptationto the physiological
requirements of dormancy.One maytesttheseexplanations usinghistorical
evidencethatthedormancy habitis primitive withinthebearlineage(it is a
synapomorphy forbears),andthattheabsenceof dormancy in somebearsis
dueto a secondary loss (Figurela). However,ifdormancy is a synapomorphy
onlyforthosebearsthatshowit,andis therefore primitively absentinpandas
andpolarbears,and/or iflow neonateweightprecededtheoriginofdormancy,
thiswould refutethe hypothesis thatdormancyconstitutes a phylogenetic
constraint inbears.It wouldalso refute Ramsey& Dunbrack's(84) hypothesis
aboutdormancy as a physiological constraint leadingto low birthweight.
I examinedthisissueusinga hypothesis ofbearrelationships fromO'Brien
etal (73). Thishypothesis is actuallya consensusoftreesderivedfromseveral
moleculardata sets publishedby one or moreof the authorsor by other
researchers; thatis, the authorsanalyzedeach data set separatelyand the
resulting treeswerecombined.As such,thishypothesis can onlybe regarded
as tentative. Nevertheless, it servesto illustrate how a specifichypothesis of
constraint can be tested.I tookthistreeas a given(usinggiantpandaas the
sistergroupto theotherbearsand canidsas theoutgroup; P Myers,personal
communication) andthenoptimized neonatesize andwinter dormancy on the
treeusingPAUP 3.Os (Phylogenetic AnalysisUsingParsimony-93).Table
 PHYLOGENETIC CONSTRAINT 323

pinnipeds
spectacledbear
brownbear
a polarbear
Asiaticblackbear
Americanblackbear
sun bear
slothbear
giantpanda

2 smallneonatesize

I winter
dormancy

D
loss ofwinter
dormancy

pinnipeds
spectacledbear
brownbear
b L w polarbear
Asiaticblackbear
Americanblackbear
sun bear
slothbear
giantpanda
FigureI Tentative phylogeny ofUrsidae(73), showinga) distribution
oforiginofsmallneonate
size and winterdormancythatwould supporthypotheses of physiologicaland phylogenetic
constraint;
b) actualdistribution
oforiginofsmallneonatesize andwinter dormancy as indicated
by PAUP (93).

1 shows characterstatesforwinterdormancyand neonatesize. Data on

dormancy and birthweightare as follows:

1. spectacledbear (Tremarctos ornatus):Verylittleinformationis available

aboutthisspecies;I infer, fromitshabitatand distribution
(80) and from
reportsthatit feedsall yearround(79), thatitdoes notexhibitdormancy
Information aboutcub weightsis also extremely scanty;a drawingof the
birthprocessin a captivespectacledbear (78) showedtheneonateto be
tiny,aboutthesize ofthemother's paw; theweightofthecub at 12 weeks
was estimated to be 1.5-2 kg.
324 MCKITRICK

Table 1 Matrixof taxa and characters.

Character1 = winterdormancy; 0 =
absent,1 = present.Character2 = neo-
natesize; 0 = "average",1 = small.

12 Taxon

00 canids
01 spectacledbear
11 brownbear
01 polarbear
11 Asiaticblack bear
11 Americanblackbear
?1 sun bear
01 slothbear
01 giantpanda

2. brownbear (Ursus arctos) undergoeswinterdormancy(81, 99). Litter

weightis 0.67% of maternal weight(74; thetablein (74) showinglitter
weightas a percentage of maternalweightin carnivores listsno species
otherthanbearswitha percentage less than1%; percentages outsideof
Ursidaerangefrom1.8% to 16.9%, mean= 8.02%).
3. polarbear(U. maritimus): does notundergodormancy (99). Litterweight
is 0.38% of maternal weight(74).
4. Asiaticblackbear(U. [Selenarctos]thibetanus): exhibitswinter dormancy.
Pocock (81:217) reported that"[T]he evidenceregarding thehibernation
of the Black Bear is conflicting," but thatindividualslivingat higher
altitudesentereda stateof semi-torpor in cold weather. This maybe the
"Himalayanbear"(studiedbyNelsonet al-71), whosedormancy habits
were similarto thoseof theAmericanblack bear.In theformer Soviet
Union,thisspecies"sleeps fromOctoberto March"(72). Schalleret al
(87) reportedthatAsiaticblackbears"hibernate" in China. Information
on birthweightis notavailable.
5. Americanblack bear (U. americanus):undergoeswinterdormancy (99).
Litterweightis 0.73% of maternal weight(74).
6. Malayansun bear (U. [Helarctos]malayanus:No information on dor-
mancy.Dathe (21) reported thebirthweightof a cub bornin captivity as
325 g, and thatof a captivefemale(whichmayhavebeenthemotherof
thatcub) as 50.135 kg. The litterweightis thereforeinferred to be about
.65% of maternal weight.
7. slothbear (Melursusursinus):Fromits distribution in tropicalIndia and
reports breedingseason(7:446, 81:200),I inferred
thatithas no particular
thatthisspeciesdoes notundergodormancy. Information on birthweight
is notavailable.
 PHYLOGENETIC CONSTRAINT 325

8. Giantpanda(Ailuropodamelanoleuca):thisspeciesdoes nothavewinter
dormancy (84, 87). Litterweightis 0.13% of maternal
weight(74).

I coded all bear speciesas havingsmallneonatesize, despitethelack of

information fora fewspecies.This assumption is of criticalimportance for
testingthehypotheses and maybe incorrect.
The mostparsimonious hypothesis forneonatesize and winterdormancy,
regardless of optimization method,is thatsmallneonatesize is a synapomor-
phyforbears,butthatwinterdormancy arose once, aftertheevolutionof
smallsize, and was subsequently lostin polarbearsand slothbears(Figure
lb). Therefore, thehypothesis thatsmallneonatesize aroseas an adaptation
tothephysiological requirements ofwinter dormancy is notsupported. Given
thepattern oforiginofthesetwocharacters, thesuggestion thatsmallneonate
size is dependent on winterdormancy is notsupported. Thus,phylogenetic
constraint does not explainthe relationship betweenwinterdormancyand
neonate size in bears, and Ramsey & Dunbrack's(84) hypothesisof
physiological constraint is refuted.
Thereis muchtobe learnedaboutthedetailsofbearphysiology, lifehistory,
and evolution.For example,the fossilrecordshows ursidsappearingin
mid-Miocene to Recentdepositsin Europe,NorthAmerica,andAsia, butno
fossilursidsappearin SouthAmericauntilthePleistocene(91; Martin[53]
notedthefirstappearanceof fossilTremarctos was in thelatePlioceneand
thattremarctines musthave originated in Asia). It is possiblethatno bears
wereinSouthAmericabeforethePleistocene andpossiblyTremarctos ornatus
is morerecently derivedthanis suggested bythephylogeny of O'Brienet al
(73). Furthermore, ifthecommonancestorof all modernbearsexperienced
temperate or arcticclimates,thenpossiblyit underwent seasonaldormancy
andtheabsenceof dormancy in somemodernspeciesis, in fact,a secondary
condition (however,giantpandasliveina temperate climateanddo notexhibit
dormancy, so thisinference maybe flawed).Despitethesepotential problems
due to gaps in information, thisexampleshouldserveto illustrate how an
outgroupapproachhas the potentialto illuminateour understanding of
evolutionary patterns and processes,including phylogenetic constraint.Here
is a case in whichphylogenetic constraintwas invokedto explaina deviation
froma pattern thatis itselfa deviationfroma pattern; in theory,itis possible
to testforphylogenetic constraint in thiscase andat thesametimeto testthe
hypothesis thatphysiological constraints have led to theevolutionof small
neonatesize in bears. Neitherhypothesisis supported.In this case, no
statisticaltestsare requiredto testsignificance of characterassociations;
simpleinspection ofthecladogram revealsthattheexpectedrelationship does
notoccur(14-15).
Whenwe have finishedtestinghypotheses of phylogenetic constraintin
326 MCKITRICK

thismanner,we mustask: if a hypothesis of constraintis supported, are the

organismsunableto lose or gain thetraitin question,or have theysimply
notdone it yet?In one sense,hypotheses of constraint
arereallyhypotheses
aboutratesof evolution(29), becausewe cannotreallyknowthatsomething
is constrained unlesswe can see itsfuture; we cannotsaythatsomething will
nothappen(exceptperhapsin a biomechanical engineering sense),onlythat
it has nothappened.
If we testhypotheses ofconstraint anddetermine thatphylogenetic history
maybe an important factorin explainingwhyan observedpattern does not
fittheexpectedpattern basedon predictions of adaptivehypotheses, we may
in someinstancesbe able to predictthelikelihoodof eventualchangeto the
expectedpattern ifsuchan exerciseseemsuseful.The instancesinwhichthis
could be usefulmay be limitedto phenomenasuch as gene productsand
biochemicalpathways,whereactualconstraints can reasonablybe hypothe-
sized and studied,and developmentaland functionalpathways,where
predictions can be made aboutthe mechanicaland structural likelihoodof
movingfromstateA tostateB orsimplyawayfromstateA. Thesepredictions
have theirlimits,however,as even engineersare notalwayssuccessfulat
determining whethertheirblueprints will translateintosuccessfulfunctional
structures-(e.g.hovercrafts wereoriginally designedto be flyingsaucers:
thefailureof theflyingsaucerleftus withthehovercraft). Studiesdemon-
stratingtransition basedon thepast(46) areusefulforilluminat-
probabilities
ing ratesof evolutionbutmay say nothingaboutwhethera transition can
occur.I believethatwe can testevolutionary hypotheses andrejectconstraint
as a confounding factoror confirm it as a possibleproximate explanation for
an unanticipated result.Froma biomechanical orbiochemical perspective we
may also be able to explainwhy,givencertainconditions, we shouldnot
expecta certainstructural or chemicaloutcome,andwe can thereby identify
theactualconstraint. Beyondthat,however,we probablycannotgo. Forthe
present, to testthelimitsoftheexplanatory powerofphylogenetic constraint,
I advocate the explorationof the conceptusing detailedphylogenetic
hypotheses thatfocuson theactualpotential constraints,
as wellas thereckless
formulation of hypothesesabout the evolutionof correlatedcharacters.
Certainly,if we are timidaboutproposingcausal correlations in character
evolution,we will limitouropportunities to understand theillusoryconcept
of constraint.

CONCLUSION
In reviewingtheconceptofphylogenetic I havetakena utilitarian
constraint,
approachthatseeks to explorethe meaningof theconceptand to testfor
occurrencesofconstraint oflineages.A historical
in thehistory approachthat
 PHYLOGENETICCONSTRAINT 327

framesexplicithypotheses abouttherelationships
amongevolvingcharacters
withina phylogenetic context(19, 14, 25, 47, 52, 58, 59, 97) can lead to
betterunderstanding of constraintand of the evolutionary historyof the
lineage.To understand thenatureof suchconstraints themselves, a mecha-
nisticapproachthatseekstoidentifytheunderlying geneticanddevelopmental
"limitsto design"will be necessary.Such a goal will requirean integration
of structural,
functional,andgeneticapproachesto thestudyofevolution(6,
96) and should lead to productivecollaborationsamong developmental
biologists,functional
morphologists, quantitativeand moleculargeneticists,
and phylogeneticsystematists.Thesecollaborative effortswillbe amongthe
mostproductive areasofresearchin evolutionary biologyin thenextdecade.

ACKNOWLEDGMENTS

I have benefited
greatlyfromdiscussionswithVernFath,Phil Gingerich,
JohnGittleman, BrianHall, David Ligon, Dan McShea, ShawnMeagher,
CharlesMitter,GerdMuller,PhilMyers,GunterWagner,PeterWimberger,
and MiriamZelditch.Ted Garland,JodyHey, NancyMoran,Dan McShea,
Phil Myers,and PeterWimberger readearlierdraftsof themanuscript
and
offeredmanyvaluablesuggestions, forwhichI am grateful.I thankJohn
Flynnfordiscussingwithme his viewson carnivore
phylogeny.
This researchwas supportedby grantBSR-9006208 fromthe National
ScienceFoundation.

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