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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
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
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).
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.
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).
12 Taxon
00 canids
01 spectacledbear
11 brownbear
01 polarbear
11 Asiaticblack bear
11 Americanblackbear
?1 sun bear
01 slothbear
01 giantpanda
8. Giantpanda(Ailuropodamelanoleuca):thisspeciesdoes nothavewinter
dormancy (84, 87). Litterweightis 0.13% of maternal
weight(74).
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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