Angiosperm Fleshy Fruits and Seed Dispersers: A Comparative Analysis of... Constraints in Plant-Animal Interactions

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Angiosperm Fleshy Fruits and Seed Dispersers: A Comparative Analysis of Adaptation and
Constraints in Plant-Animal Interactions
Author(s): Pedro Jordano
Reviewed work(s):
Source: The American Naturalist, Vol. 145, No. 2 (Feb., 1995), pp. 163-191
Published by: The University of Chicago Press for The American Society of Naturalists
Stable URL: http://www.jstor.org/stable/2463122 .
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Vol. 145,No. 2
Naturalist
The American
February1995
ANGIOSPERM FLESHY FRUITS AND SEED DISPERSERS:
A COMPARATIVE ANALYSIS OF ADAPTATION AND
CONSTRAINTS IN PLANT-ANIMALINTERACTIONS
PEDRO JORDANO*
Estaci6nBiol6gicade Doniana,CSIC, Apdo. 1056,E-41080,Sevilla,Spain
August24, 1993;RevisedMarch28, 1994;AcceptedMarch31, 1994
Submitted
in phenotypic
traitsofangiosperm
fleshy
fruits
has beenexplainedas the
Abstract.-Variation
available
By analyzing
theinformation
to theirmutualistic
seeddispersers.
resultofadaptations
ofevolutionary
species,I assessthehypothesis
on fleshy
of910angiosperm
fruit
characteristics
traitsand typeof seed disperser(birds,mammals,and
associationbetweenfruitphenotypic
nullhypotheses
about
and quantitatively
alternative
mixeddispersers)
and addressexplicitly
affinity
amongplanttaxa is accountedforby comparative
phylogenetic
effects.Phylogenetic
contrasts.
autocorrelation,
and independent
methodsincluding
nestedANOVA, phylogenetic
effects
downto genuslevelexplain
phylogenetic
Averaging
overthe 16 fruittraitsexamined,
reaching
are strong
amongcloserelatives,
autocorrelations
61% oftotalvariance.Phylogenetic
contrast
significance
for 11 of the 16 fruittraitsexamined.Whenassessed by independent
evolutionbetweentypeof disperserand fruittraitsis confinedto fruit
methods,correlated
for
in othertraitsvanishafteraccounting
amongdispersalsyndromes
diameter.Differences
arenotentirely
interTheseanalysesrevealthatseeddispersalsyndromes
effects.
phylogenetic
can be assessed
to seed dispersers.
Theirstatusas exaptations
pretableas current
adaptations
studiesofnaturalselectionon fruitsize and rigorouscomparative
by combining
experimental
hypotheses.
and cladistictestsofadaptational
Plantadaptationsto one or a fewseed dispersersare rarein nature,butrelasetsoffruit
knownas syndromes
(Ridley
morphologies
integrated
tivelyinvariant,
and interpreted
as
1930; van der Pijl 1982;Janson1983)have been identified
environment"
(Howe
reflecting
broad adaptationsto the "disperser/dispersal
is theasinterpretation
1986;Fleminget al. 1993).Centralto thisadaptationist
is themain
accruesto bothparts,and thisbenefit
thata mutualbenefit
sumption
Recentstudieschallengethis
thecoevolutionoftheinteraction.
factorimpelling
coevolution.Geneticconlimitations
to plant-seed
disperser
viewbydiscovering
andhistory
straints
(Herrera1986,1992a;Janson1992),
(Howe 1984),phylogeny
oftheinteractions
(Jordano1987c),andextensivevariaandasymmetry
diversity
themselves(Howe 1983; Wheelwright
tionin the outcomeof the interactions
as the mainobstaclesfortheevolutionof tight,co1988)have been identified
the
A centralissue relevantto thisquestionis therefore
evolvedrelationships.
of "constraints"(McKitrick1993) and
estimationof the relativemagnitudes
mutualisms.
"specificadaptations"in theevolutionofplant-frugivore
*E-mail:jordano@cica.es.
Am. Nat. 1995. Vol. 145, pp. 163-191.
? 1995 by The Universityof Chicago. 0003-0147/95/4502-0001$02.00.
All rightsreserved.
164
THE AMERICANNATURALIST
are important
in
Previousstudieshave suggested
thatphylogenetic
constraints
plants(see, e.g., Lechowicz 1984;Hodgsonand Mackey 1986; Kochmerand
Handel 1986;Herrera1987,1992b;Baldwinand Schultz1988;Michaelset al.
1988;Donoghue1989;Stratton1989;Willsonet al. 1989;Gorchov1990;Mazer
1990;Willsonand Whelan1990;Chazdon 1991; Lee et al. 1991; Schupp and
Feener 1991;Bremerand Eriksson1992;Fischerand Chapman1993),butfew
have attempted
to considertheireffectsexplicitlyand quantitatively
(but see
Janson1992).A comparative
approach(Pageland Harvey1988)is indispensable
thatis attributable
to commonancestry
fromsimilarfordistinguishing
similarity
ityattributable
to paralleland convergent
evolutionary
change.The latteris expected amongplantssharingthe same major seed dispersersif evolutionary
traitsis attributable
tocoevolvedselectivepressuresbyfrugivores.
changeinfruit
arenotnecessarily
Notethatbothtypesofeffects
mutually
exclusive,as phylogetraitsbutset
do notpreventnaturalselectionactingon phenotypic
neticeffects
a rigidpatternof covariationamongcharacters.
limitsto itsactionby imposing
A wholesetofrecently
developedcomparative
methods(Felsenstein1985;Pagel
and Harvey1988,1989;Grafen1989;HarveyandPagel 1991;Harveyand Purvis
1991;MartinsandGarland1991;Garlandetal. 1992,1993)can be usedforassessingtheevolutionary
associationamongquantitative
charactersbut,as faras I
know,haveneverbeenusedwithplantdata.HereI adoptan explicitly
comparativeapproachto testforevolutionary
associationsbetweenfruittraitsand seed
disperser
types.
My objectivein thisarticleis to answerthefollowing
questions.First,what
fruits
fraction
oftotalphenotypic
variancein angiosperm
fleshy
can be explained
by sharedancestry?Residualvariationis likelythe resultof selectiveforces
sensustricto)
one ofthepoten(adaptations,
(GouldandVrba1982)andcertainly
tialmajorforcesis thatexertedbyfrugivores.
Second,are fleshyfruitcharacternutrient
in thepulppreisticssuch as fruitdesignand particular
combinations
dictablyassociatedwithseed dispersalby particularfrugivore
groupswhen
phylogenetic
affinity
amongplanttaxa is accountedfor?If phylogenetic
affinity
of totalphenotypic
variancein fruittraits,we might
explainsa largefraction
forevolutionary
modification
offruitstructure
as sugexpectsevereconstraints
gestedby Herrera(1986,1992a)and Wheelwright
(1988).Boththebroadset of
plantdata consideredand thegeneralcategoriesof dispersertypesimposedby
the availableinformation
set limitations
to thisanalysis.However,its validity
stemsinidentifying
generaltrends(androbustmethodsto assess them)thatbear
on theimportant
clade-wideassociationbetween
questionof theevolutionary,
fruitcharacters
and seed dispersertypes.
angiosperm
fleshy
ADAPTIVE
HYPOTHESES
AND PREDICTIONS
The last two decadesof studieson thedispersalecologyof animal-dispersed
plantshave centeredin adaptiveexplanationsof the enormousmorphological
variationin fruittypesand frugivore
behaviors(see reviewsin Howe 1986;Jordano 1992).A strictly
statesthatfleshyfruitphenotypic
adaptationist
hypothesis
variationis exclusivelytheresultof a plant'sadaptationto its seed dispersers
PHYLOGENETICCONSTRAINTS
IN FLESHY FRUITS
165
(Snow 1971;McKey 1975;Janson1983).The earliersurveysof Ridley(1930),
Turcek(1961,1967),and van derPiji (1982),providing
correlative
evidencefor
thehypothesis,
have been largelysupported
by moreexhaustivestudies(Snow
1981;Janson1983;Wheelwright
et al. 1984;Gauthier-Hion
et al. 1985;O'Dowd
and Gill 1986;Debusscheet al. 1987;Herrera1987,1989;Debussche 1988;Debusscheand Isenmann1989;Willson1991,1993).
Ideally,supportfortheadaptivehypothesis
wouldcome fromdetailedmeasuresofnaturalselectionon fruit
traitsin thefield.Bothexperimental
studiesin
captivity
and fieldobservations
have foundpositivecorrelations
betweengape
widthoffrugivorous
birdsand maximum
diameter
ofthefruits
ingested(Wheelwright
1985;Piper1986;Jordano1987b;DebusscheandIsenmann1989;Lambert
1989;also see Fleming1988),whichsuggeststhatindividual
plantsmaydifferentiallydisperseseedson thebasisoffruit,
seed size,or seed load variation(Howe
and Vande Kerckhove1980,1981;Herrera1981,1984;Howe 1981;Piper1986;
Jordano1987a;Obeso 1988;Wheelwright
1993;butsee Flemingetal. 1985;Foster
1990).Fieldevidencefordifferential
fruit
removalfromindividual
cropsmediated
in pulpnutrient
by differences
qualityis, however,scanty(Manasse and Howe
1983;Piper1986;Jordano1987a,1989;Herrera1988;Foster1990).In addition,
mostofthesestudieshave shownthattheselectivepatterns
by frugivores
were
whichaddedinconsistency
in
subjectto extremespatialand temporalvariation,
theirstrength,
and persistence.
direction,
inpreferandso forth,
differ
To theextentthatbirds,bats,nonflying
mammals,
fruit
ence patterns
fordifferent
traits,theabove selectionpressuresmighttransstudiesacross
late intothedifferences
betweensyndromes
foundin correlative
can
species (see Howe 1986,pp. 150-155;Fleminget al. 1993).The following
thusbe predictedunderthepresence(or greatinfluence)
of dispersal/disperser
selectiveeffects:
1. Species in different
disperser/dispersal
categoriesshoulddifferin overall
fruit
morphology
orparticular
traitswhenphylogenetic
effects
are controlled
for.
after
reductions
Thevarianceexplainedbydisperser
typewillnotshowsignificant
withnonsignificant
resultsfor
forphylogenetic
effects.
controlling
This,together
methods(autocoreffects
whenestimated
phylogenetic
byadequatecomparative
will suggestthe absence of phylogenetic
conrelation,independent
contrasts),
whichwouldadd supportto
in fruitmorphology
and pulpcomposition,
straints
theadaptivehypothesis.
2. Considera gradient
ofvariationin thecomposition
of thedisperserassemorpredominantly,
blageamonga setofspecies,fromthosedispersedexclusively,
of birdsand mammals
by birds,throughthose showinga similarimportance
(mixeddispersal),and then,at theotherextreme,thosedispersedexclusively,
orpredominantly,
bymammals.Ideallyeach specieswouldfallsomewhere
along
ofbirdsand mammalsin, say,
thegradient
on therelativeimportance
depending
number
ofvisitsto theplants,totalfruit
removal,or numberofestablishedseedthem.
The adaptivehypothesispredicts
from
seed
recruited
lings
dispersedby
thatcan be summatrends
of
for
fruit
traits
variation
particular
alongthisgradient
relative
of
rizedas follows:overallfruit
seed
size,
number,
yield pulp,nonstructuand fiberwouldtendto increasefrom"bird" to "mixed" to
ral carbohydrates,
166
THE AMERICANNATURALIST
"mammal"dispersertypes.Individualseed size, energycontentper gramof
pulp,lipids,and protein,
wouldshowa decreasealongthisgradient.
METHODS
Data
on traitsof angiosperm
Quantitative
information
fleshyfruits(910 species in
392 generaand 94 families)was compiledfrombothpublishedand unpublished
familieswiththisfruittype.
sourcesincluding
data on 42% of the angiosperm
materialcomes fromcollections(C. M. Herreraand P. Jordano,
Unpublished
unpublished
data)for42 speciesinCostaRica and severalMediterranean
species
not includedin Herrera'spublishedstudy(1987). The data include92 North
American
species,46 NorthEuropean,86 Mediterranean
(Europe),277Neotropical, and409Paleotropical
(244African,165Indo-Malayan-Australian).
Copies of
thedata set are availablefromme uponrequest(also see Jordano1992).Fruit
size (lengthand diameter),
freshfruitmass, drymass of seed(s) per fruit,dry
individual
seed drymass,numberof seeds perfruit,and
massofpulpperfruit,
relativecontentofdrypulpwithrespectto freshmassofthewholefruit(relative
ofwater,proportions
yield)wereconsidered"designtraits."Proportion
oflipids,
andacid-detergent
fiberwithrespectto
solublecarbohydrates,
protein,
minerals,
drymass of pulp,as well as theenergycontentper gramof drymass of pulp,
wereconsidered"nutrient
content"traits.Figandthetotalenergycontent/fruit
uresforrelativeyieldof pulp,totalenergyperfruit,and totalenergyper gram
thesevariablesfromraw
of pulpwerecomputedwhennecessaryforestimating
data.
theanalyticalmethodsused in thearticlessurveyedwereobviously
Although
varied,mostauthorsfollowedthemethodsoutlinedbytheAssociationofOfficial
Chemists(1975).Lipidswereobtainedinmostcases withmicrosoxhlet
Analytical
content
extraction
andprotein
bymicro-Kjeldahl
analysis.Whenstudiesreported
totalnitrogen
(N), I used N x 6.25 as an estimateof crudeproteincontent.
Studiesreporting
analysesofthewholefruit
(i.e., including
seeds)wereexcluded.
Ideally,each species shouldbe characterized
of
by the relativeproportions
totalvisitsor fruitsremovedby each majorfrugivore
group,correctedby their
in termsof seedlingsrecruited
effectiveness
fromthe seeds removed(Murray
is lackingformostspecies,and I
1988;Schupp1993).This typeof information
to assignthemto threebroad categoriesalong a gradientbetween
attempted
speciestotally,or mostly,dispersedby birdsto speciestypicallydispersedby
mammalsalone. Dispersertypecategoriesused as classificatory
criteriawere
dispersalpredominantly
by birds,mixed(birdsand mammals),and mammals
Previousstudieshaveemphasizeddifferences
(primates,
bats,ungulates).
among
thesebroadcategories(Ridley1930;Janson1983;Howe 1986;Fischerand Chapman1993),and I used themin theanalyses.These generalcategoriespose obvious limitations
to thepresentanalysisbut,on theotherhand,solvethepotential
finer"ad hoc" syndromes
of establishing
whenappropriate
shortcomings
informationis lackingformosttaxa(see table1 inFischerandChapman1993).Species
wereassignedto thethreecategorieson thebasisofpublishedinformation
inthe
PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS
167
originalarticles,generaltreatments
(Ridley1930;Turcek1961,1967;Croat1978;
van Roosmalen1985; Snowand Snow 1988;Willson1991,1993),personalcommentsoftheauthors,and personalobservations
(C. M. Herreraand P. Jordano,
unpublished
data) forMediterranean
and Europeanspecies and some Central
Americantaxa. Assignments
werebased mostlyon qualitativeassessmentsof
thefrequency
offeedingrecords,importance
offruits
in thediet,and frequency
ofreferences
withpositiverecordsoffeeding
by different
frugivore
types.Informationaboutcongeneric
speciestogether
withfruit
morphology
(see Janson1983,
1992)was used in a fewcases. The robustness
ofthesecriteriavariedobviously
accordingwiththequalityofthebackground
information
we presently
have for
different
plant-disperser
systems.The categoriestherefore
are rough,and future
analysesmight
showtheyhaveto be reassigned
forsometaxa,butI am confident
thatthegeneralconclusionsofthepresentanalysiswillhold.Thus,preliminary
analyseswithdata subsetswithgreaterresolution
ofdispersertypes(Mediterranean,NorthAmerican,
andsomeNeotropical
sets)didnotrevealthatpartitioning
thedispersaltypesintoadditional
categories(i.e., largeand smallbirds,batsand
nonflying
mammals)wouldalterthemainconclusions.
Use of TaxonomicInformation
I performed
theanalysisusingtheclassification
systemofCronquist(1981)and
estimated
effectsand relatedness
phylogenetic
usingthetaxonomicrelationship
caveatmustbe madethat
amongthe910 speciesin thedata set. The important
a moreexplicitly
is tobe preferred
forfuture
arrangement
reanalyses
phylogenetic
informaofthisdataset.Morelocalanalyses,nowpossiblewiththephylogenetic
thepowerofcomparationforcertaintaxa,havea greatpotential
forincreasing
tivetests(see, e.g., Erikssonand Bremer1991;Bremerand Eriksson1992)if
combinedwithgreater
ofthedisperser
resolution
types,andtheywillbe thegoal
of subsequentarticles.
A phylogenetic
classification
system(Sporne1956)is an estimateof a phylogButtheconcluenythatcan be usedto allowanalyseswithavailableinformation.
sionsdrawnneedto be reassessedwhenmorerefined
information
phylogenetic
becomesavailable.Miles and Dunham(1993)providean updateddiscussionof
in comparative
in choosinga well-supported
the problemsinherent
phylogeny
when
insteadof
inherent
taxonomies
studiesand thepotential
weaknesses
using
al. 1992).
and
Gauthier
Garland
et
trees
see
de
phylogenetic (also
Querioz
1992;
Statistical Analyses
Nested ANOVA and autocorrelationmnethods.-Analyseswere performedon
and angular
variables(naturallogsforweightsandlineardimensions
transformed
The variancecomponents,as a percentage
transformations
forproportions).
of totalvarianceforeach taxonomiclevel,wereestimatedwithNESTED and
ofthe
VARCOMPprocedures
(SAS Institute
1988)and are used as a description
and theirconsistency
patternsofvariancepartitioning
amongtraits.Taxonomic
as nestedrandom
andgenus)werespecified
levels(class,subclass,order,family,
effectswithineach higherlevel,withclass effectbeingfixed(Bell 1989).Howlevelsfortheseeffects,as thenominaldeever,I did notestimatesignificance
168
THE AMERICAN NATURALIST
of the data, and the
greesof freedomare lackingbecause of nonindependence
nestedANOVA is heavilyunbalanced.
autocorrelation
method(Cheverudand Dow 1985;Cheverud
The phylogenetic
and Kot 1990)partitions
thetotalphenotypic
varianceof
et al. 1985;Gittleman
ofspeciesintoa component
attributable
to theirphylogea traitacrossa number
inand a specificcomponent
notattributable
to phylogenetic
neticrelationships
coefficients
and proportional
varianceaccountedfor
heritance.Autocorrelation
wereestimated
autocorrelation
byphylogeny
bya network
model,y = p Wy + e,
and Kot (1990).
usingthemethoddescribedin detailby Gittleman
theextentto whichthephenoautocorrelation
The phylogenetic
p, measuring
thephylogeny,
is estimatedby Wy,
typictraitvalues (y) correlatethroughout
in a traity amongspecies
ofthetotalvariation
representing
a linearcombination
or taxonomic
relatedness
weighedbytheirphylogenetic
(matrixW). A maximum
likelihoodprocedurewas used to estimatep and R2, thevarianceexplainedby
themodel.Higherp valuesindicatethatthemorerelatedspeciestendto be more
similar.I used Moran'sI statistic(Moran1950)to estimateautocorrelation;
at
traitofa specieswitha weighted
anylevel,I comparedthephenotypic
averageof
The weights(wij)are functions
ofthetaxonomic
thetraitovera setofneighbors.
relatedness
ofthespeciesincludedin theanalysisto each other.I used a hierarchicaldistance(one forcongenericspecies,twoforconfamilial
species,and so
on up to fiveforspeciesin thesameclass). To improvemodelfitI used thegrid
searchprocedurefora maximumlikelihoodestimatordescribedby Gittleman
and Kot (1990)to derivewijvalues:wij= I1dU7,wheredijis thedistancebetween
indexobtainedby maximum
likelispeciesi andj, and a( is a variable-weighting
function
ofphylogehoodestimation.
By thismethod,theformofthedecreasing
values(wij)whenincreasing
distanceneednotbe
neticconnectivity
phylogenetic
assumeda priori,as intheCheverudet al. (1985)method.Alldatawerestandardized to meanzero and unitvariancepriorto the analysis.Residualsfromthe
Gittleman
and Kot
modelweretestedforindependence
autoregressive
following
(1990).
Independentcontrastsmethods.-I addressed the hypothesisof functionalas-
sociation(correlated
and dispersalsyndrome
evolution)betweenfruitcharacters
contrasts
methods(Felsenstein1985;Burt1989).I used the
byusingindependent
Contrasts(CAIC) package,version1.2,
Comparative
Analysisby Independent
whichimplements
a variety
developedby A. Purvis(1991),OxfordUniversity,
and discretevariables(Garlandet al. 1992).I report
of methodsforcontinuous
heretheresultsobtainedwiththepunctuational
changeassumption
(equal, fixed
branchlengths),because analyseswiththe gradualisticassumption(variable
consistent.
The evolutionary
branchlengths)
werehighly
correlation
betweentwo
charactersis testedby assessingthe relationship
betweencontrastson the X
variable(e.g.,disperser
predictor
type)andcontrasts
on theY-dependent
variable
(e.g., fruitdiameter)
(Harveyand Pagel 1991).If a positiverelationship
between
thetwotraitsexists,itwillshowup,whenthecontrasts
are plotted,as a positive
least squaresregression
slope acrosstaxa. I testedthisrelationship
by ordinary
withcontrasts
theorigin,
standardized
through
usingbranchlengthsofthephyloI useda binomialtestto assess theprobability
ofgetting
genetictree.In addition,
PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS
169
an equal number
ofpositiveandnegative
ofpositivecontrasts;
a givenproportion
relationship
beof no evolutionary
contrasts
are expectedunderthehypothesis
tweenthetraitsexamined.HarveyandPagel(1991)andPageland Harvey(1992)
and addresstheproblemofunregivedetailsforthecalculationofthecontrasts
solvednodes,an issue forwhichthereis no optimalsolutionyet.The method
nodesuses valuesoftheX variableto split
at multiple
usedto resolvepolytomies
thetaxa (congeners)intotwogroups,above and belowthemeanofX, yielding
is computedas thediffertwosubnodesforthemultiple
node.The linearcontrast
subnodes(Purvis1991).
ence betweenvaluesoftheserecomputed
I codeddispersertypeas a categoricalvariablewiththreelevels:birds,value
the outputforthe
of one; mixed,two; and mammals,three.I theninterpret
traits(e.g., fruitdiameteror
relationships
betweencontrastson thecontinuous
on thisvariableas a difference
in proporlipidcontentofthepulp)and contrasts
in the continuous
tionsof each dispersercategoryassociatedwithdifferences
trait.The rationaleforthisprocedurefollowslogicdevelopedby Fleminget al.
ofdispersertypes
(1993).Supposeeach speciesis locatedalongan idealgradient
dispersedby birds,
betweenan extremewithspeciestotally,or predominantly,
dispersedby mammals.
and anotherone withspeciestotally,or predominantly,
Species withmixedseed dispersalwouldbe closerto one or theotherextreme
depending
on theirrelativerelianceon birdsand mammalsforfruitremovaland
between,say, fruitsize
seed dispersal.Thus, positiveand linearrelationships
increasesin
wouldmeanthatevolutionary
contrasts
and disperser
typecontrasts
of
changesto a greaterproportion
fruitsize are associatedwithevolutionary
ofmammal
be illustrated
bya greaterproportion
mammalian
dispersalthatmight
orbya greater
coterieofthetaxainvolvedinthecontrast
speciesinthedisperser
ofseedsdispersedbymammals(PagelandHarvey1988;Harvey
totalproportion
and Pagel 1991).
stated.Probaaregivenas meanand 1 SD, unlessotherwise
Summary
statistics
bilitylevelswerefixedat .05. However,in mostinstancesI used a Bonferroniacrossgroupsare tablewise
P level of .0031,sincemostcomparisons
corrected
testsforthe16fruittraitsconsideredhere(P =
and involveseparateunivariate
.05/16)(Rice 1989).
RESULTS
General Trendsof Variation
A factoranalysis of the correlationmatrix(across species) between fruittraits
revealsthatfivesignificant
componentsaccountfor77.3% of totalvariation,
amongtraits(table 1). Families
patternof covariation
whichindicatesa distinct
ofspeciesvalueson thespace defined
distributions
showlargelynonoverlapping
structure
(fig.1), and familyeffectsaccountedfora 27.49%
by thiscomponent
of totalvariationon principalcomponent(PC) 1 and 8.48% forPC 2. Note
tests(ANOVA, MANOVA) forthesedifferences
thatconventional
parametric
becausespeciesare
estimates,
wouldyieldinvalidP valuesandbiasedparameter
not phylogenetically
independent,and the nominaldegrees of freedomwould be
170
THE AMERICAN NATURALIST
TABLE 1
RESULTS OF A FACTOR ANALYSIS OF ANGIOSPERM FLESHY FRUIT TRAITS BASED ON THE CORRELATION
MATRICES OF BOTH ORIGINAL VARIABLES AND INDEPENDENT CONTRASTS
FruitTrait
Fruitlength
Fruitdiameter
Fruitfreshmass
Pulp drymass
Seed(s) drymass/fruit
Numberof seeds/fruit
Seed drymass
Relative yield of pulp
Energycontent/gpulp
PC I
.4227
.8952
.4110
.8506
.4379
.9320
.4018
.8776
.3662
.8043
. . .
. ...
. . .
.4554
. . .
* . .
...
PC 2
PC 3
...
. . .
...
...
. . .
...
. . .
...
. . .
. . .
. . .
. . .
. ..
. . .
. . .
. . .
. . .
-.2983
Water in pulp (%)
.3619
.8764
...
.7603
. . .
. . .
. .
Lipids
. . .
. ..
. . .
.2674
. ..
. . .
Energycontent/fruit
Protein
Nonstructuralcarbohydrates
Minerals
Fiber
Eigenvalues
% Variance
* . .
. . .
...
. . .
. . .
...
5.31
4.93
33.22
30.83
-
.8118
.8216
. . .
.3747
...
2.74
2.20
17.11
13.75
PC 4
... ....
. .. ..
. .
... ....
. . .
. .. ..
... ....
. .. ..
... ..
. ..
...
. . .
...
. . .
. . .
. . .
. . .
. ..
. . .
. . .
.5878
.6608
. . .
. . .
.2581
.3223
-.4858
-.7645
. . .
. . ...
. . ..
...
.9170
. . .
-.7066
...
...
. ..
. . .
. ..
. . ...
.
. ..
. . .
. ..
- .6427
. . .
. . .
. ..
. . .
.4571
.5968
1.61
1.71
10.09
10.66
PC 5
. .
. .
. .
.
.7328
.. .
-.6140
.3024
- .3888
...
.4579
...
.8710
....
- .6088
-
.3563
...
1.41
1.56
8.82
9.77
1.29
1.20
8.05
7.49
NOTE.-Varimax rotationmethodwithprincipalcomponentextractionwas used on both the correlationmatrixforall species in the sample withpairwisedeletionof missingvalues (originalvariables,
values not in italic) and the correlationmatrixfor independentcontrastsin each variable (values in
italic). Figures show correlationsof each variable witheach principalcomponent(PC 1-PC 5). Only
these fivecomponents,witheigenvalues >1.0, were considered significant
(Legendre and Legendre
1979). Loadings < 10.251are omitted.
I repeatedtheprincipal
incorrect.
components
analysis(PCA) on the
Therefore,
matrix
correlation
obtainedfortheindependent
contrasts.
Resultswerehighly
consistentwiththepattern
obtainedfromthepreviousanalysis(table1), as expected
fromthesignificant
consistencybetweenthetwo matrices(r = 0.8057, t = 7.24, P
< .0001;Manteltestwithrandomization,
n = 1,000)(LegendreandLegendre1979).
Because of the strongcovariationamongall size variables,taxa witheither
PHYLOGENETIC
CONSTRAINTS IN FLESHY
2-
FRUITS
171
Lauraceae
,1/~~~~~~~~~~~~~Sml'lacaceae
1
Viscaceae
0
Ericaceae
Rosaceae
Ebenaceae
-12-
myrtaceae
\
Caprifoliaceae -----
oraceae
Oleaceae
- -- - - - ---
----
2Pa/mae
Celastraceae
,acourtiaceae
Rhamnaceae
Palmae
0 AnacardiaceaeRuica
racea
ubiaceae
Rutaceae
Sapotaceae
Rhamnaceae
flacourtiaceae
m
O
AralilveaemsolanDC@aE
1
;Mliacea
2Myristicaceae
ci
~ ~
-1
ibr hw
0ipid cotetan
for
. oftoAraliaceae
y
C
f
-2
-1
P
Solanaceae
Liliaceae
-3
Vitaceae
~ihostvelado
~ ~
0
1
2
3
Verbenaceae
C,annntrcurlaboyraeCucurbitaceae
e
MelastoV (ceae
-3
PC 1
-2
-1
0
1
2
3
FIG. 1.-Relative locationsofangiosperm
twoprincipal
on thefirst
species,byfamilies,
offleshy
fruitcharacteristics.
components
ellipses(P = .900)are plotted
Equal frequency
foreach family.
These ellipsesare thecontourlinesencompassing
90% of thedata points
Fruit-size-related
variableshavehighpositiveloadson PC 1, both
(species)foreachfamily.
lipidcontentand fibershowhighpositiveloads on PC 2, and nonstructural
carbohydrates
and energycontent
pergramofpulphavenegativeloadson it(table1). Bothaxes account
for50.3%oftotalvariance.
fruits(e.g., Moraceae) or large,drupaceous,or few-seeded
large,multiseeded
fruits(e.g., Lauraceae,Rutaceae,Sapotaceae,someRosaceae) scorehighon a
associatedwithoverallfruitsize (fig.1). Small-fruited
first
taxa,notacomponent
bly Caprifoliaceae(Sambucus), Loranthaceae(Cladocolea), Viscaceae (Dendrophtora), Thymelaeaceae(Daphne), Melastomataceae(Miconia), and some
Rubiaceae(Nertera,Putoria,Relbunium)
scorelow on it. Onlythefirstand fifth
172
THE AMERICAN NATURALIST
whichdepictthetrade-off
betweenindividualseed mass and seed
components,
numberperfruit,
involvelargeloads of"morphological"
traits.The components
2, 3, and4 involvepulp"nutritional"
traits(table1). Thus,PC 2 is interpretable
Taxa
betweenlipidsand nonstructural
bythestrongdissociation
carbohydrates.
withlipid-rich
and relatively
fibrouspulp score highon it (mostPalmae, Lauraceae, Myristicaceae,
some Anacardiaceae,and Celastraceae).Fruitsrichin
soluble carbohydrates,such as Mimusops, Sideroxylon(Sapotaceae), Pancovia,
Paullinia (Sapindaceae), Dictyophleba, Lacmellea (Apocynaceae), and most
andCapriMelastomataceae,
Rhamnaceae,
Flacourtiaceae,
Rosaceae,Myrtaceae,
foliaceaeshownegativescoreson PC 2 (fig.1).
theinverserelationship
across species
The thirdcomponent
(PC 3) illustrates
betweenrelativeyieldof pulp,energycontentperfruitand fiber,on one hand,
and pulp watercontenton the other(table 1). The watery,succulentfruitsof
Liliaceae (Clintonia,Dianella, Paris), Ranunculaceae (Actaea), some Rubiaceae
(Coprosma, Coussarea), and Empetraceae (Empetrum)species score negatively
richinminerals.Taxa with
on thisaxis. These specieshaverelatively
largefruits
relatively
dry,fibrous,
and pulpyfruitstypically
yielda highamountof energy
and show highpositive
of themajororganiccomponent,
per fruit,irrespective
scores on this PC 3; they include Crataegus, Hesperomeles, Sorbus and Pyrus
(Rosaceae), Arbutusand Arctostaphylos(Ericaceae), Elaeocarpus and Muntingia
(Elaeocarpaceae),Ziziphus(Rhamnaceae),and someAnnonaceae.
Finally,specieswithhighproteinand mineralcontentsshownegativescores
on PC 4 (EkebergiaandsomeTrichilia,
Meliaceae;Ximenia,Olacaceae; Zingibershowhighcontent
aceae, and mostPiperaceae).In addition,taxa thattypically
inthepulpscorenegatively
on thisaxis,andtheseinclude
ofnonprotein
nitrogen
Ruscus, Ripogonum (Liliaceae); Bryonia, Citrullus,Coccinia (Cucurbitaceae);
Tamus(Dioscoreaceae);and Mandragora(Solanaceae).
Phylogeneticand AdaptiveEffectsin FruitPhenotypicVariance
Phylogenetic variance components.-Partitioning of phenotypic variation
amonghighercategoriesintheLinneanhierarchy
(fig.2) suggestshighsimilarity
in fruittraitsamongclose phylogenetic
relatives.On theaverage,phylogenetic
effects
downto genuslevelexplain61% oftotalphenotypic
varianceinthetraits
examined.All thetestsrevealedlargeeffects
ofthenestedtaxonomichierarchy
on the16fruit
from26.1% (relativeyield
traits,withexplainedvariancesranging
of pulp)to 89.2% (numberof seeds per fruit).For 13 of 16 traits,the variance
explainedby thenestedmodelaccountedformorethan30.0% oftotalvariance.
The intraclasscorrelation
less
coefficients
up to theordinallevelweregenerally
than0.15, whichindicatesthata negligible
fractionof totalvariancewas acinthissample.Onlyseed(s) dry
countedforbyclass, subclass,and ordereffects
individualseed drymass,and mineralsshowedrelatively
largesubmass/fruit,
class and ordereffects,withintraclasscorrelationsbetween0.20 and 0.30
(fig.2).
were large for most formand designtraits
Familyintraclasscorrelations
(fig.2), especiallyfruit,
pulp,and seed(s)masses,individual
seed mass,and seed
numberper fruit.This patterncontrastswiththe smallerfamilialeffectsand
PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS
M Class
1 Subclass M Order M Family
E
173
Genus FWithin genus
100
(D
<
LI
Q
/
0
Formanddesign
Fruit
trait
Nutrient
content
levels(class to
FIG. 2.-Percentagesof totaltraitvarianceaccountedforby taxonomic
classification
systemin a nestedANOVA ofangiogenus)ofCronquist
(1981)phylogenetic
Fruittraits
aregrouped
in"formanddesign,"orstructural,
spermfleshy
fruit
characteristics.
length;DIAM,
andnutrient
content
characteristics.
Abbreviations
fortraitsareLENG, fruit
fruit
diameter;
FRFM,fruit
freshmass;PDM, pulpdrymass;8DM, drymassofseed(s)per
RY, relative
fruit;SEEDM, drymassofindividual
seed; SEEDS, number
ofseedsperfruit;
yieldof pulp(100 PDM/FRFM);PCW,percentage
watercontent;KJFR,energycontent
contentsare givenas
(kJ)per fruit;KJG,energycontentpergramof drypulp.Nutrient
proportions
relativeto pulpdrymass:LIP, lipids;PRO, protein;
NSC, nonstructural
carbohydrates;
ASH, minerals;
FIB, fiber.
greatergenericeffectsexhibitedby nutrient
traits(fig.2). Excludingthe conforfamily
structed
variatesRY, KJFR,and KJG,averageintraclasscorrelations
higherthanthosefornutriamongformand designtraits(0.459)are significantly
all taxonomiclevelsdown
entcontenttraits(0.209;t = 2.27, P = .04). Including
to genus,the differences
betweenthe two groupsof traitsare onlymarginally
forgenus,0.697 and 0.523, respecsignificant
(averageintraclasscorrelations
thetwogroupsoftraitsdiffer
inthetypes
tively;t = 1.77,P = .105).Therefore,
of phylogenetic
effectsbut onlymarginally
in the overallmagnitudeof these
effects.
Phylogenetic and specificcomponents:an autocorrelationmodel.-By fitting
theautoregressive
model,significant
autocorrelations
wereobtainedfor11ofthe
on
16fruittraitsexamined(table2). Thisindicatesa generaleffectofphylogeny
As estimated
byR2,sizable
mostphenotypic
variation
ofangiosperm
fleshy
fruits.
significant
fractions
of totalvariancein fruitand seed masses,fruitseediness,
(taenergyreward/fruit,
and lipidcontentcan be accountedforby phylogeny
showsignificant
ble2). Fruitdimensions,
pulpwatercontent,
andprotein
phyloge-
174
THE AMERICAN NATURALIST
TABLE 2
PHYLOGENETIC
AUTOCORRELATION
COEFFICIENTS
(p), ASSOCIATED
SE, R2, ANDSAMPLESIZE, FOR
ANGIOSPERM
FLESHYFRUITTRAITS
FruitTrait
Fruitlength
Fruitdiameter
Fruitfreshmass
Pulp drymass
Seed(s) drymass/fruit
Number of seeds/fruit
Seed drymass
Relative yield of pulp
Energycontent/gpulp
Energycontent/fruit
Water in pulp (%)
Lipids
Protein
Nonstructuralcarbohydrates
Minerals
Fiber
n
504
597
428
376
263
320
194
370
453
233
506
495
561
462
264
232
a
1.00
3.30
1.00
1.40
1.00
1.30
3.00
7.00
.10
1.10
4.00
1.20
8.00
.001
.20
7.00
p
P
SE(r)
R2
.24
.24
.46
.42
.38
.34
.44
.10
.16
.37
.21
.41
.14
.15
.06
.03
*
*
*
*
*
*
*
.043
.043
.041
.045
.055
.051
.059
.052
.046
.058
.043
.039
.042
.046
.062
.066
7.65
8.29
29.68
25.67
21.76
16.80
31.56
2.16
3.46
21.67
7.12
23.12
4.03
3.04
.55
.14
NS
NS
*
*
*
*
NS
NS
NS
Coefficienta is a
NOTE.-Variable n, numberof species; P, probabilitylevel; NS, nonsignificant.
maximumlikelihoodestimateof the variable weightingindex used to obtain phylogeneticdistances
(see text); R2 is the totalamountof variation(%) explained by the phylogeny.Asterisksmarksignificant values forthe Bonferroni-corrected
probabilitylevel P < .05/16 = .003.
neticcomponents,
buttheseaccountformuchlowerfractions
oftotalphenotypic
variance.Finally,relativeyieldof pulp,mass-specific
energycontent,soluble
and fibershownegligible
effects(table2).
carbohydrates,
minerals,
phylogenetic
forfruit
traitscomputedaccording
Figure3 showsthetaxonomic
correlograms
to Gittleman
and Kot (1990).These values of Moran'sI depictthecorrelations
betweentraitvaluesandweighted
averagesofthesevaluesoversetsoftaxonomic
neighbors.
The correlograms
locate wherethetaxonomiceffectsshow up and,
if the way phylogenetic
autocorrelations
moreimportantly,
changewithtaxonomicdistanceis consistent
acrosstraits.A patternthatemergesfromfigure3
withstrongautocorrelations
is thatmostfruit
traitsshowdecayingcorrelograms,
betweenclose taxonomic
relativesthatdecreasewhenone proceedsup theLinnean hierarchy.
The decayingof I values is steeperfordesigntraitsthanfor
nutrient
traits,whichadds supportto the resultsreportedabove fromnested
ANOVA.
EvolutionaryAssociations betweenFruitPhenotypicVariationand
Type of Seed Disperser
Patterns of variation associated with seed dispersal syndromes.-A central
issue in thisstudyis whether
differences
betweenseed dispersalsyndromes
are
betweenspecies are controlled
supportedwhenthe phylogenetic
relationships
for.To an unknowndegree,thesedifferences
mayarise fromthe association
between phylogenyand fruitcharacteristics,because individualspecies are not
datapoints.
independent
CONSTRAINTS IN FLESHY
PHYLOGENETIC
FRUITS
175
Nutrients
Design
* LENG +DIAM A FRFM T PDM
* SDM ESEEDS XSEEDM D RY
* KJG + KJFR A PCW T LIP
* PRO * NSC X ASH U FIB
0.8
0.6
0.2
-0.2
-0.4
GEN FAM ORD
SCL
CL
GEN FAM ORD
SCL
CL
Taxonomiclevel
fordesignand nutrient
FIG. 3.-Phylogenetic
contenttraits(abbreviations
correlograms
as in fig.2) of angiosperm
fleshyfruits.Values of Moran'sI statisticat variousnested
order,subclass,and class,alongtheabscissa)are plotted
taxonomic
levels(genus,family,
I values('max)forcomparison
foreachfruit
trait.Moran'sI valueswererescaledbymaximum
correlations
showhow phylogenetic
and Kot 1990).Correlograms
acrosstraits(Gittleman
hierarchy.
changealongthenestedtaxonomic
are consumedand seeds
specieswhosefruits
similarity,
Ignoring
phylogenetic
differin mostfruittraits
frugivores
typesof vertebrate
dispersedby different
observableconfirm
examined(tables3 and4), andthegeneraltrendsofvariation
thosefoundin previousstudieswithsmallerdata sets. First,averagefruitsize,
increasesfrom
eitherbythelength,
diameter,
orfreshmassofthefruit,
estimated
valuesfor
species,withintermediate
speciesto mammal-dispersed
bird-dispersed
taxa withmixeddispersal.Second,thetotalenergyrewardper fruitincreases,
ina paralleltrend,frombird-to mammal-dispersed
species,a resultofthestrong
size anddrymassofpulpperfruit.
Third,
correlation
acrossspeciesbetweenfruit
energycontentsthan
speciesshowhigherlipidand mass-specific
bird-dispersed
species.
mixed-and mammal-dispersed
Controllingphylogeneticvariation.-Comparisons across species in fruittraits
associationsbetweentraitvalues
have beenroutinely
used to inferevolutionary
in table3, and
is illustrated
and typeofseed disperser.Thistypeofcomparison
thestatistical
of theANOVA testsamongseed dispersergroupsis
significance
intypeofseed disperserdiffer
intable4. Groupsofspeciesdiffering
summarized
in nineofthe16fruit
accounts
traitsexamined.However,thiseffect
significantly
forless than20% ofvarianceofanytrait(table4).
affinities
among
If thesedifferences
are mainlytheresultof thephylogenetic
forthe influenceof shared
species,thentheywould vanishwhencontrolling
176
THE AMERICAN NATURALIST
TABLE 3
SUMMARY STATISTICS FOR FRUIT TRAITS OF ANGIOSPERM SPECIES DISPERSED
VERTEBRATE FRUGIVORES
BIRDS
FRUIT TRAIT
Fruit length
Fruit diameter
MIXED*
Mean
SD
n
Mean
11.88
7.22
266
14.70
10.21
5.37
Fruitfreshmass
1.485
4.792
Pulp drymass
.144
.303
.406
Seed(s) drymass/fruit .185
Numberof seeds/fruit 8.9
32.5
Seed drymass
0.1097
.4753
Relative yield of pulp 13.65
6.84
Energy content/g
pulp
Energy content/fruit
Water in pulp (%)
Lipids
Protein
Nonstructural
carbohydrates
Minerals
Fiber
BY DIFFERENT
332
13.20
SD
7.96
MAMMALS
n
Mean
192 29.28
7.32
217 23.56
5.56
173
14.64
221
15.38
71.82
.149
.063
16.02
.171
.046
259
228
264
73.57
.070
.057
14.46
.125
.041
203
207
231
72.29
.082
.051
.540
.055
.130
.270
.038
.099
204
121
98
.565
.047
.170
.273
.028
.110
197
.597
.047
.150
2.18
4.49
SD
n
22.75
46
18.56 48
264
1.881
3.469 134 5.611
15.898
.274
.465 119
.637
.842
238
172
.163
.227
76
.310
.428
203 106.9
494.1
93
8.3
20.1
.5532 14.738
123
.0803
.1655 58
8.70
234
16.68
117 20.04
12.05
5.70
17.87
TYPES OF
159
4.02
6.04
63 16.99
111
103
5.13
16.35
30
19
15
24
13
19
59
11
16.30 44
.138 60
.035 66
.251 61
.036 32
.127 31
masses in grams,energycontentsin kilojoules, and values
NOTE.-Lengths are givenin millimeters
for lipids to fiber are proportions relative to dry mass of pulp.
* Seeds dispersed by birds and mammals.
In thissituation,
I wouldalso expectlargereductions
inR2valueswhen
ancestry.
It is possibleto perform
effects
are subtracted.
suchtestswiththe
phylogenetic
thedifferences
betweendispersalsyndromes
on
autoregressive
model,bytesting
thespecificvalues,S, whichrepresent
residualvariation.The mainassumption
is thatthisresidualdepictstheindependent
evolutionofeach species.Thus,
S = T - pWy,
whereT is thetotalphenotypic
value,represented
bythey vector(Cheverudand
Dow 1985;Cheverudet al. 1985).I rantheANOVA testsforeach traitagainon
theseS valuesin orderto testfordifferences
betweenseed dispersertypescontrolling
forphylogenetic
effects.Table 4 showsthatthe numberof traitswith
differences
significant
decreasedfromnineto six. In addition,R2 values were
reduced,on the average,32% of the initialvalues explainedwhenusingtotal
phenotypic
variation.
Traitsstillshowingsignificant
betweentypesof
differences
seed disperserwhencontrolling
forphylogenetic
effectswere fruitlengthand
diameter,
fruitand pulpmasses,energycontent/fruit,
and lipids.The variance
accountedforby thismodelwas extremely
low forlipids(4.8%), freshfruit
mass (3.2%), and pulp drymass (6.8%), whichindicatesthatsizable variation
attributable
to majorseed dispersers
is reallypresentonlyin fruitsize and total
content/fruit
energetic
(largelya correlateoffruitsize).
PHYLOGENETIC
CONSTRAINTS IN FLESHY
FRUITS
177
TABLE 4
SIGNIFICANCEOF THE DIFFERENCESIN FRUIT TRAITS AMONGSPECIES PREDOMINANTLYDISPERSED BY
BIRDS (B), MAMMALS(Mm-BATS, UNGULATES,PRIMATES),AND WITH MIXED SEED
DISPERSAL BY BOTH GROUPS OF FRUGIVOROUSVERTEBRATES(Mx)
TOTAL PHENOTYPIC
VARIATION
FRUIT TRAITS (df)
Fruitlength(2, 503)
Fruitdiameter(2, 596)
Fruitfreshmass (2, 429)
Relative yield of pulp (2, 371)
Pulp drymass (2, 377)
Seed(s) drymass/fruit
(2, 264)
Number of seeds/fruit
(2, 322)
Seed drymass (2, 193)
Energycontent/gpulp (2, 455)
Energycontent/fruit
(2, 234)
Water in pulp (%) (2, 508)
Lipids (2, 497)
Protein(2, 563)
Nonstructuralcarbohydrates
(2, 464)
Minerals (2, 263)
Fiber (2, 231)
PHYLOGENETICVARIATION
CONTROLLED
F
R2
B Mx Mm
44.61*
49.61*
19.83*
6.94*
25.18*
15.1
14.3
8.5
3.6
11.9
2.7
5.2
2.0
4.6
19.4
.2
7.9
.9
A
A
A
A
A
A
A
A
A
A
A
A
A
B
B
B
B
B
A
B
A
B
B
A
B
A
C
C
C
B
B
A
A
A
AB
C
A
B
A
.5 A
1.3 A
3.39NS 2.9 A
A
A
B
A
A
B
3.63NS
8.7 1*
1.98NS
10.80*
27.67*
.62NS
21.16*
2.62NS
1.13NS
1.76NS
F
R2
B Mx Mm
1.33NS
A B
A B
A AB
A B
A B
A A
A A
A A
A B
A A
.1 A A
4.8 A B
.5 A A
1.36NS
2.22NS
3.14NS
.6 A
1.7 A
2.7 A
13.6
12.3
3.2
6.98NS
2.6
4.94Ns
13.67*
6.8
2.1
2.77NS
1.4
2.35NS
1.1
1.06NS
6.91NS
2.9
19.83* 14.6
39.33*
41.40*
.33NS
12.62*
A
A
A
C
C
B
AB
B
A
A
A
AB
B
A
B
A
A
A
A
NOTE.-Separate ANOVA tests were carriedout on the total phenotypicvariance and on residual
variance aftercontrollingforphylogeneticeffectsby means of an autocorrelationmethod(see text).
R2 is the percentageof variationexplainedby the model (dispersercategories). Entrieswithdifferent
lettersindicate significant
differences(Scheffea posterioritest,P < .05) between the means of each
traitvariable. NS, Not significant.
* P < .003, Bonferroni-corrected
significancelevel (P = .05/16 = .003).
Independent
contrastsanalysis.-The angiosperm
classification
phylogenetic
of Cronquist(1981)providesa totalof 541 nodesforthe910 speciesin thedata
witha bifurcating
of
set, 59.5% of themaximum
possibleresolution
phylogeny
909 nodes.The numberofnodesavailablefora giventraitis reduced,however,
valuesandbythefactthatvariation
fortypeofseed disperser
becauseofmissing
is absentat a numberof nodes (contrastswithvalue zero), especiallygeneric
nodes.Mostcongenerssharethesametypeofseed dispersalagent,as expected
fruitmorphology
and pulpcomposition
by theconservative
shownat thistaxonomiclevel(fig.2).
theresultsofbothregression
theoriginand sign
Table 5 summarizes
through
and thelatterare plottedin figure4. Each
testson thecontrastscomparisons,
ofthetypeof seed disindicatesan independent
pointin thisfigure
comparison
in
the
in traitvalue
a
taxon
perser given
plottedagainst independent
comparison
forthattaxon.Contrastsin typeof seed disperser(independent
variable)are
as an
forcedto be positive,and theirvalues alongtheX-axisare interpretable
in
of
mammals
the
of
each
taxon
increasing
importance
dispersal
(see Methods).
178
THE AMERICAN NATURALIST
TABLE 5
SUMMARY
OF THEANALYSIS
OF THERELATIONSHIPS
BETWEEN
DISPERSER-TYPE
CONTRASTS
ANDFRUIT
TRAITCONTRASTS
FORANGIOSPERM
SPECIES
NUMBEROF CONTRASTS
FRUITTRAIT
df
SLOPE
Positive
Negative
Fruitlength
Fruitdiameter
Fruitfreshmass
Pulp drymass
Seed(s) drymass/fruit
Seed drymass
Numberof seeds/fruit
Relative yield of pulp
Energycontent/fruit
Energycontent/gpulp
Water in pulp (%)
Lipids
Protein
Nonstructuralcarbohydrates
Minerals
Fiber
164
183
50
138
104
83
114
137
100
154
165
163
174
157
114
99
.1278*
.1183*
92
107
86
73
60
47
35
73
59
68
84
68
92
85
54
45
67
71
64
65
42
35
38
64
41
86
80
95
78
71
55
49
.2145NS
.3124*
136INS
.3144NS
- 9248NS
0545NS
.3553*
-.0464NS
.0348NS
- .0727*
-.0124NS
-
.0207NS
0162NS
0019NS
BINOMIAL
P
.075
.01
NS
NS
NS
NS
NS
NS
NS
NS
NS
.10
NS
NS
NS
NS
NOTE.-For each trait,separate regressionsthroughthe originwere calculated between dispersertype contrastsand fruittraitcontrasts.NS, Not significant.Bonferroni-corrected
significancelevels
are given forslopes. Binomialprobabilitiesare the P levels forthe binomialtest on an equal number
of positiveand negativecontrastsforeach trait.Constrastsequal to zero forthe typeof seed disperser
were excluded fromcalculationof the regressionslopes and binomialP.
* P < .05/16 = .0031.
I omittedthosetaxa thatwereinternally
homogeneouswithregardto typeof
seed disperser.Independent
contrastsforthe traitvalues (Y variable)can be
indicates
zero,positive,or negative.Each pairofpositiveX-Y valuestherefore
an independent
instancein whicha changeformixedor mammal
evolutionary
dispersal(i.e., an increasein therelativeimportance
of mammalsas dispersers
ofa taxon)has beenassociatedwitha positivechangein thetraitvalue (i.e., an
increasein fruitor seed size, pulpmass,or amountof a givennutrient).
withthose
Resultsoftheindependent
contrasts
analyses(table5) areconsistent
methods(table4). The prevailing
obtainedusingtheautoregressive
illuspattern
4 is thatevolutionary
and typeof
tratedbyfigure
changesinfruitcharacteristics
seed disperser
havebeenlargelyindependent.
formand designvariAmongfruit
anddrymassofpulpshoweda significant
trend
ablesonlyfruit
length,
diameter,
of syndromes(fig.4A).
to increasealong the bird-mixed-mammal
continuum
Amongnutrient
contenttraits,onlyenergycontentper fruitand lipidcontent
showedsignificant
trends(table 5; fig.4B), but the correlation
forlipidswas
negative.The correlation
of energycontent/fruit
is a side effectof the strong
covariation
betweenthisderivedvariableandfruitsize. Obviously,largerfruits,
witha greateramountof pulp,also yielda greateramountof energyper fruit.
betweendisperser
andenergycontent/
Thus,thepartialcorrelation
typecontrasts
fruitcontrasts
is only0.001afterfruitsize effects
are removed(bypartialing
out
PHYLOGENETICCONSTRAINTS
IN FLESHY FRUITS
179
fruitdiameter).Therefore,
theonlyevolutionary
correlations
evidencedby the
independent
contrastanalysisinvolvefruitsize and lipidcontent.
The negativecorrelation
betweenlipidcontentcontrastsand dispersertype
contrasts
(table5; fig.4B) indicatesthathighlipidcontentis evolutionarily
associatedwithavianseed dispersalanddecreasesamongtaxawithmammaldispersal.
However,R' is verysmallforthistrait(5.6%),andthecorrelation
vanisheswhen
controlling
the influence
of threeoutliers(thethreebottomdata pointsin the
panelforlipids,fig.4B). These contrasts
correspond
to thegenusAglaia (Meliaceae), andfamilies
AnacardiaceaeandApocynaceae,whichshowrelatively
large
amountsoflipidsin thepulpbutwithextremevariationamongspeciesdiffering
indisperser
type.AmongApocynaceae,specieswithmixeddispersalshowmuch
higherlipidcontent(0.34 + 0.09, n = 3; generaStemmadeniaand Tabernaemontana) thanthose dispersedby mammals(e.g., genera Lacmellea, Thevetia,Landolphia; 0.044 + 0.063, n = 6). The same trendoccurs in Anacardiaceae, where
bird-dispersed
Pistacia, Rhus, and Harpehyllum
show averageproportions
of
lipids(0.378 + 0.07,n = 6) wellabove specieswithmixeddisperserssuchas in
genera Spondias, Pseudospondias, Tapirira, Trichoscypha, and Sclerocarya
(0.025 + 0.07, n = 6). Finally,the same extremetrendexistsamongAglaia,
withlipidcontentof0.492 + 0.09,n = 3, in bird-and mixed-dispersed
taxa and
0.089 + 0.059,n = 3, amongmammal-dispersed
species.
As indicatedby the binomialtests(table5), thereis evidenceonlyfortaxa
withgreaterproportions
of mammal-dispersed
speciesto showlargerfruits;the
forfruitlength.
signtestsare significant
onlyforfruitdiameterand, marginally,
The resultstherefore
indicatethatcorrelatedevolutionbetweentypeof seed
is largelyconfinedto fruit
characteristics
disperserand fleshyfruitphenotypic
size, especiallytheexternaldimensions.
Pairwise comparisonsamong congeners.-I carriedout a furthertest to see if
thetrendsshownin tables4 and 5 andfigure
4 holdwhencloselyrelatedspecies
in typeof seed disperserare compared.I selectedthosegenerain the
differing
intypeofseeddisperser.For each genus,
datasetforwhichseveralspeciesdiffer
I averagedtraitvalues across species sharingthe typeof seed disperserand
comparedthesemeansamongdisperser
categories(Wanntorp
1983).I talliedthe
numberof generashowingincreasesor decreasesin averagetraitvalues when
congenersdispersedby birdsare comparedwiththosedispersedby birdsand
mammals(mixeddispersal)and/orthosethatare mammaldispersed.Each comto a signtestunderthe
observation
parisonwithina genusadds an independent
nullhypothesis
shouldgo in the
thatequal numberofwithin-genus
comparisons
samedirection.
trendforlarger
The pairwisecomparisons(table6) revealonlya significant
fruits(greaterdiameterand, marginally,
greaterlength)to occuramongmixedor mammal-dispersed
species(signtests,P = .053and P = .115,respectively).
resultsin
For theothertraitsthatshowedsignificant,
or marginally
significant,
trendis evidentin the
theautocorrelation
and contrasts
analyses,no significant
within-genus
pairwisecomparisons(table6). To sum up, onlyfruitsize (fruit
fruitlength)showcorrelatedevolutionwithtypeof
diameterand, marginally,
whenphylogenetic
are controlled
for.
seed disperser
effects
THE AMERICAN NATURALIST
180
0.4
f0.4
A0.2
0.2
0
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0
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0 0
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00
ui lnt
tF
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0
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--
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hlgntccassioficto
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(1981).A,~~~
Morhoogia an eintat;B
upwtrcnetadntinris
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amog-dffren-taa-ithn-echhiger-od-ofth
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ereds
idsper
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FIG, 4.-Plotsg
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sowensnonsfuttraituvalue
PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS
181
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varia.Tiona
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morphologicaladdsg
upallvaration,
amongspecieswouldspan mostof thisspace. The oppositetrendwas found,
and different
familiesand generatendedto clusterat particularcombinations
of PC values, showinghighlysignificant
differences
in thesevariates(also see
Gauthier-Hion
et al. 1985;Herrera1987).A similarresultconcerning
flowering
timeand phenologicalvariationwas obtainedby Kochmerand Handel (1986).
This outcometherefore
variationis largelyan
suggeststhatfruitmorphological
C)
C#4)
c
C#4)U))
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PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS
183
in this
ofhighertaxonomiclevels(family,
stableproperty
and relatively
intrinsic
case).
offruit"form"and "design"charThe analysisrevealeda markeddecoupling
evidentalso whenanaa pattern
contentcharacteristics,
and nutrient
acteristics
ofcovariation
In fact,theonlypattern
matrix
on contrasts.
lyzingthecorrelation
traitswas thatfibrousfruitstendto yielda greater
amongdesignand nutrient
variation
in thesetwomaincomporelativeamountofpulpperfruit.Otherwise,
Figure1 shows thatsome families
is independent.
nentsof fruitmorphology
spannedgreatvariationalongPC 1 whileshowinga narrowrangeof scoreson
Rutaceae,
horizontally,
e.g., Melastomataceae,
ellipsesoriented
PC 2 (confidence
Rubiaceae,Ebenaceae, Rhamnaceae).Othersshow the oppositetrend(confie.g., Lauraceae,Smilacaceae,Ericaceae,Paldenceellipsesorientedvertically,
(size
Meliaceae,Vitaceae).Thefactthatthesetwogradients
mae,Flacourtiaceae,
infleshy
oftotalvariation
explainone-half
andlipid-soluble
carbohydrate
content)
meansthattheyare twomajorlinesoffamilialdiversification
fruit
characteristics
withinhighertaxa
and revealsthatvariationin fruitformand pulpcomposition
is boundedby constraints.
The precedingresultis notunexpected.Studiesby Sporne(1956, 1976)and
reproof angiosperm
Stebbins(1951),forexample,indicatethatcharacteristics
co-varywithinhighertaxa,sincefloral,carpel,seed, andfruit
ductivestructures
path(Primack
associatedandconnectedalongan ontogenetic
traitsareultimately
designmostlikelyarisefromdevelopsize andinternal
onfruit
1987).Constraints
of floralparts,espearrangement
imposedby the particular
mentallimitations
On theotherhand,PCA loadingsforthe
of thegynoecium.
ciallythestructure
expressionof nutrient
ofthepulpsuggestthatconservative
organicconstituents
taxamight
be attributable
to allocationpatterns
among
within
higher
composition
of majorcompathways.In addition,certaincombinations
majorbiosynthetic
pounds (e.g., highwaterand lipid content,or low waterand high solublebe simplyincompatible
froma metabolicor physiocontent)might
carbohydrate
parts of the flowerand fruitare highly
logical perspective.That different
and showcorrelatedevolutionwas proposedby Vavilov(1922) and
integrated
by Sporne(1956).These are relevantpointsto a
thenestablishedmoreformally
rigorousanalysisoffruitand flowerevolutionin relationto seed dispersersand
partsof
A highlystructured
patternof covariationamongdifferent
pollinators.
theactionofnaturalselectionamongcoevolving
does notprevent
thephenotype
evolutionary
change.
butitimposeslimitson theresulting
partners,
PhylogeneticConstraintson Seed Dispersal Syndromes
fruitmorphology
and seed dispersalagents
Previousworkon comparative
to the adaptationist
hypothesisor, if the potential
largelyignoredalternatives
(Herrera1986;Desourcesof variationwas acknowledged
effectof alternative
et
al.
1991),no explicit
busscheet al. 1987;Willsonet al. 1989;French1991;Lee
How
is adaptationto
was attempted.
of its significance
important
quantification
or
for
fruitvariationnotaccounted by phylogeny
seed dispersersin explaining
randomeffects?
The nestedANOVA analysisshowedthatan averageof 61% of totalpheno-
184
THE AMERICAN NATURALIST
in anyangiosperm
fruit
traitcan be accountedforby taxotypicvariation
fleshy
nomicaffiliation
downto genus.Seed size and seed numberperfruitshowedthe
highestphylogenetic
variancecomponentvalues,as expectedfromtheirclose
relationto flowerand carpellarstructure.
Familyeffectswere largeformost
traits.These, in contrast,showed
designtraitsand smallerforpulp nutrient
greatergenericvariancecomponentvalues, whichthusadds evidenceto the
ofthisstudy(also see Herrera1987)ofa decoupling
ofthetwogroupsof
finding
traits.Janson(1992)reporteda stronginvariancein thekindsof dispersalsyna resultof
dromesevolvedwithinhighertaxa (generaand families),apparently
or low adaptivevalue
fixeddevelopmental
and ontogenetic
relatively
programs
To someextent,phylointermediate
oftransitional,
forms,betweensyndromes.
comestimatetherelativesize of "plesiomorphic"
geneticvariancecomponents
available for speciesponentsof the phenotype.Littlevariationis therefore
specificresponsesto selectionby seed dispersers,since the potentialfor
withina givenhighertaxa (e.g., genus)is "nested" withinthis
diversification
largecomponent
ofdescent.Thus,interactions
withseed dispersers
wereprobaforangiosperm
blyrelevantin shapingthemajorlinesofdiversification
families
and genera,butwe mightexpectverylow evolutionary
responseamongcongeMorelocal analyses,witha taxonomicscope
nericspeciesto thesemutualists.
thantheone used here,can obtaingreaterresolution
forthedefinition
narrower
of dispersertypes,hencemorepowerto testadaptivetrendswithina rigorous
framework.
phylogenetic
of the 16 traitsexaminedheredescribea
The phylogenetic
autocorrelograms
withascendingtaxonomichierarchy.
of phenotypic
decayingfunction
similarity
Theyfurther
indicatea highlystructured
pattern
ofvariationrelatedto phylogeofdecreasing
with
neticaffinity.
Thereis a muchsteepergradient
autocorrelation
levelfordesigntraitsthanforpulpnutrient
contenttraits.
increasing
taxonomic
effectsare expectedto be relevantin complexanatomical
Since phylogenetic
structures
or physiological
suitesof traits
processesthatevolve as integrated
(Stebbins1974),thesewill show up moreclearlyin fruitformand structure,
attributes
offamilies(Cronquist1981).The autoregresconsideredcharacteristic
in fruitdesignthanin pulp nutrient
sive patternis stronger
content,and the
formergroupof traitsshowsmorehomogeneouscorrelograms
(fig.3), which
supportsthisview.
werehighly
autocorrelation
coefficients
for11ofthe16
Phylogenetic
significant
traitsexamined,whichindicatesthata sizablefraction
ofphenotypic
phenotypic
variancecan be accountedforwhenconsidering
all phylogenetic
simultaneously
relatednessamongspecies. Phylogenetic
effectsare important
for two main
groupsof traits,namelyfruitand seed mass and fruitseedinessamongdesign
traitsand energycontentperfruit
andlipidsamongnutrient
contenttraits.Other
butlowerR2 values(e.g., fruitdimentraitsshowedsignificant
autocorrelations
sions,pulpwatercontent,
protein).Futurestudiesshouldtherefore
payattention
to othereffects
notexaminedhere(growth
form,fruitaccessibility,
and color),
butsomeanalysessuggesta sizablephylogenetic
in them(see, e.g.,
component
Hodgsonand Mackey1986;Willsonand Whelan1990;Chazdon 1991;Fischer
and Chapman1993).Whenusingoriginaldata, significant
between
differences
PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS
185
betweensynsyndromes
were obtainedfornineof the 16 traits.Differences
and
dromesin fruitlengthand diameter,pulp drymass, energycontent/fruit,
forlipidsand pulp mass
of determination
lipidsremained,and the coefficients
relatednesswas accountedfor.
halvedwhenphylogenetic
were approximately
among
addressedin thisstudy(i.e., differences
Therefore,
the firstprediction
forphylogenetic
effects)is supported
syndromes
shouldremainaftercontrolling
of strict
ofthetraitsexamined.However,thefraction
onlyin partfora minority
small(? 15%).
exhibited
bythesetraitswas extremely
sense"adaptive"variation
Dispersal SyndromesRevisited
traitsandmajorseed dispersassociationsbetweenfruit
Present-day
functional
ers do notnecessarily
implytheircoevolutionas a causal process.All theabove
are notinterpretable
onlyin
indicatethatdispersalsyndromes
analysesstrongly
a significant
histermsofcurrent
adaptationto seed dispersersand demonstrate
fleshy
variationamongangiosperm
phenotypic
toriccomponentin present-day
fruits
(also see BremenandEriksson1992;Herrera1992a;Fischerand Chapman
varianceaccountedforby highernodes was "subtracted"in
1993).Phenotypic
becauseitillustrates
theplesiothepreviousanalysesandconsidered
nonadaptive
are probablya
morphicload of thetraits.However,fleshyfruitplesiomorphies
and shouldbe incorporated
to pastmutualistic
interactions
resultof adaptations
in a comparative
analysis.
contrastsrevealedtwo strongpatterns.First,a
The analysisby independent
fruit
betweenseed dispersaltypeand mostfleshy
correlation
lackofevolutionary
fruitlengthand pulp lipid
traits;in fact,onlyfruitdiameterand, marginally,
withtypeof seed disperser.The results
contentshoweda trendforcovariation
withand supportedthoseof the two previous
weretherefore
highlyconsistent
showeda significant
asespeciallydiameter,
analyses.Second,fruitdimensions,
to increasewithincreasing
participation
sociationwithtypeofdisperser,
tending
of crossof mammalsamongthedispersalagents.This supportsearlierfindings
et al. 1985;
speciesstudiesshowingthesametrend(Janson1983;Gauthier-Hion
Dowsett-Lemaire
1988;Debusscheand Isenmann1989; Herrera1989; Willson
of significant
withthefinding
phylogenetic
1993).Thisresultis notincompatible
forevolutionary
infruit
Thepointisthatthepossibilities
effects
dimensions.
change
inthesetraitsaretightly
boundedbythebauplaninherited
byeach species.
The evidencefromthe analysisof contrastsand the pairwisecomparisons
increasesin fruitsize (diameterand, marginally,
demonstrated
thatevolutionary
associatedwithmixedand mammaldispersal.Studies
length)are significantly
but
on fruitsize are numerous,
showinga potentialselectiveeffectoffrugivores
to demonstrate
conditions
fewhave addressedboththenecessaryand sufficient
theoperationof naturalselection(Schupp1993;Wheelwright
1993).In contrast
selectionon fruitsize has immediate
implications
to otherfruittraits,frugivore
becauseoftheassociationamongfruitsize,
on keyaspectsofplantdemography,
and successfulseedling
seed size, and seedlingvigor;germination
probability;
selectivepressures
I wouldexpectthattheeffects
ofpresent-day
establishment.
causal processes
constraints
as contributing
and phylogenetic
or developmental
infuturestudieson
couldbe dissectedmorefinely
coevolution
to plant-disperser
186
THE AMERICANNATURALIST
particular
speciesgroups(e.g., diversified
taxa suchas Solanum,or Rubiaceae)
in whichcomparative
data and well-established
can be combined
phylogenies
withdetailedecologicalexperiments
(Bremerand Eriksson1992).In addition,
generaltrendssuchas thosedescribedin thepresentstudyforthewholeangiospermclade couldbe testedin smallersubsetsoftheclade (E. Martins,personal
Futurestudiesshouldaddresstheshortcomings
communication).
imposedbythe
characteristics
of thelargedata base used hereand take advantageof the new
ofwell-established
comparative
methodsand availability
combined
phylogenies,
withrigorousfieldstudiesoffrugivore
activity.
Allthefruit
traitsexaminedshowimportant
effects
andextremely
phylogenetic
low potentialforcoevolutionary
species-specific
adaptationto seed dispersers,
probablybecause of constraints
and integration
imposedby development
with
structures.
A recentmodelfortheevolutionofspecialpredispersal
reproductive
ized seed dispersalamongvertebrate-dispersed
plantspredicteda centralroleof
andrapidpunctuated
conservatism
evolutioninfruit
phylogenetic
traits(Fleming
et al. 1993),and theresultsof thepresentanalysisstrongly
supportthisview.
But thisis a complicatedsituation.The hypothesis
thatfruittraitsevolvedas
to seed dispersers
butare nowmaintained
adaptations
otherthan
by something
selectionis hardtofalsify
(Howe 1985),butitis probablycorrectformostindividual fruit
traits.The idea ofphylogenetic
inertiaand/ordevelopmental
constraints
implicitly
recognizesthattheoriginand maintenance
ofadaptationsto seed disdifficult
to test(Coddington
persersare decoupled,whichmakesthehypothesis
1988;McKitrick1993).The presentanalysissuggeststhatnaturalselectionmight
notbe involvedin maintaining
adaptationsto seed dispersers,
at leastformost
fruitphenotypic
evolutionwithtypeof seed disperser
traits,and thatcorrelated
is, at best,onlyevidentforfruitdiameter.To the extentthatthe patternsof
covariationbetweenfruittraitsand dispersertypeare epiphenomena
of other
selectivepressures,suchas flowerdesign,pollinator-derived
or physioeffects,
on fruitdesign(Cipolliniand Levey 1991; Herrera1992b),
logicalconstraints
are to be consideredas exaptations(Gouldand Vrba
fleshyfruitcharacteristics
1982)to theirpresent-day
seed dispersers.
The presentstudyand otherrecentanalyses(Bremerand Eriksson1992;Herrera 1992a, 1992b;Janson1992;Fischerand Chapman1993)demonstrate
the
need to addressthehistoriccomponent
of plant-disperser
interactions
by using
bothrigorous
methodsandsoundexperimental
evidenceforecologicomparative
cal effects.
theseare keyaspectsforunderstanding
Although
themechanisms
of
plant-seeddisperser(also pollinator)
coevolutionabove the species level, they
wouldbe difficult
to integrate.
Recentevidenceof multiple
typesof constraints
on coevolution
andOrians1982;Howe 1984;Herrera1986;Jordano
(Wheelwright
1987c;Wheelwright
1988;Janson1992;presentstudy)argueagainsta singleforto represent
mulation
all contributing
causalfactorsadequately.Thisis a general
issue in evolutionary
biologytoday,not specificto the studyof plant-disperser
coevolution.A majorproblemis thelack ofa commoncurrency
to measurethe
effectsof contributing
causal processes,and probablytheonlyalternative
will
be a piecemealapproachto integration
(Mitchell1992).Thisexplicitly
recognizes
theplurality
ofcausalprocesses(present-day
selection,phylogenetic
oneffects,
PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS
187
togenetic
constraints,
and randomvariation)
and thesingularity
oftheparticular
combination
ofeffects
and theirsignificance
in each particular
situation.
ACKNOWLEDGMENTS
I thankC. M. Herreraand L. Lopez Soria fortheircontinuoussupportand
valuablediscussionsand mywifeMyriamforessentialhelpin data preparation;
all of themwereextremely
patientduringthelonggestationof thisproject.M.
withtheanalysesofmostfruitsamplesofCosta Rican
Carrionhelpeduntiringly
species.Chemicalanalysesof somefruitspecieswereperformed
by B. Garcia
and A. Garcia,Centrode Edafologiay BiologiaAplicada,Consejo Superiorde
Investigaciones
Cientificas,
Salamanca.Unpublished
information
was kindlysupplied by F. H. J. Cromeand C. M. Herrera;the latter,L. Lopez-Soria,D.
Levey,T. Garland,Jr.,T. Evans,E. Martins,
T. H. Fleming,
andtwoanonymous
reviewers
offered
usefulcomments
to themanuscript;
J.M. CheverudandM. F.
Willsonmade helpfulsuggestions
to earlierdrafts,but theydo notnecessarily
H. Luh, and
agreewithmyinterpretations.
J. M. Cheverud,J. L. Gittleman,
A. Purviskindlyprovidedcopies of theirstatistical
packagesand programs
for
comparative
analyses.A. Purvisand H. Luh gave excellentadvice and very
helpfulassistancewiththeanalysis.My father,D. JordanoBarea, clarified
my
doubtswithSAS IML programming
and alwaysoffered
thoughtful
suggestions.
timeand facilities
werekindlyprovidedby theCentrode Informaitica
Computer
de Andalucia.Financialsupportwas fromtheSpanishDireccionGenCientifica
eralde Investigacion
Cientifica
y Tecnica,projectsPB-87-0452and PB-91-0114,
and theConsejeriade Educaciony Ciencia,Juntade Andalucia.
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