AmericanJournal
ofBotany82(5): 596-606. 1995.
DIOECY AND ITS CORRELATES IN THE FLOWERING PLANTS
SUSANNE S. RENNER2 AND ROBERT
E. RICKLEFS
Institute
ofSystematic
Botany,University
ofMainz,Bentzel-Weg
2, D-55099Mainz,Germany;
and Department
ofBiology,University
ofPennsylvania,
Philadelphia,
Pennsylvania
19104-6018
Considerable
effort
has beenspentdocumenting
correlations
betweendioecyand variousecologicaland morphological
traitsforthepurposeoftesting
hypotheses
aboutconditions
thatfavordioecy.The dataanalyzedin thesestudies,withfew
exceptions,
comefromlocalfloras,
withinwhichitwaspossibleto contrast
thesubsetsofdioeciousand nondioecious
taxa
withregardto thetraitsin question.However,ifthereis a strong
to thepresenceor absenceof
phylogenetic
component
dioecy,regionalsampling
mayresultin spuriousassociations.
Here,wereport
resultsofa categorical
multivariate
analysis
ofthestrengths
ofvariousassociations
ofdioecywithothertraitsoverall flowering
plants.Familieswerescoredforpresence
ofabsenceofmonoecyor dioecy,systematic
position,numbers
ofspeciesandgenera,growth
forms,
modesofpollination
and dispersal,
and trophicstatus.Sevenpercent
ofangiosperm
geographic
distribution,
genera(959 of 13,500)containat
least some dioeciousspecies,and ;6% of angiosperm
species(14,620 of 240,000)are dioecious.The mostconsistent
associationsin thedata setrelatethepresenceofdioecyto monoecy,
windor waterpollination,
and climbing
At
growth.
boththefamilyand thegenuslevel,insectpollination
is underrepresented
amongdioeciousplants.At thefamilylevel,a
fromtheassociation
positivecorrelation
betweendioecyandwoodygrowth
resultsprimarily
betweendioecyandclimbing
growth
(whether
thetreenortheshrubgrowth
woodyorherbaceous)
becauseneither
forms
aloneareconsistently
correlated
witha family'stendency
to includedioeciousmembers.Dioecyappearsto have evolvedmostfrequently
via monoecy,
of floralsex ratiosbetweenindividualplants.Monoecyitselfis relatedto abiotic
perhapsthrough
divergent
adjustments
in theless
pollinationand climbinggrowth
as revealedby multivariate
analysis.Dioecyand monoecyare concentrated
advancedsuperorders
ofThorne(1992) and subclassesofCronquist
ofdioecyfoundin a localflora
(1988).The frequency
therefore
reflects
thelevelofdioecyin itsparticular
pool offamilies
as muchas, or morethan,localselectivefactors.
The
ofdioecywithabioticpollination
andmonoecyarerelatedto floraldevelopmental
andmorphological
positiveassociations
as is thenegativeassociationwithbirdand bat pollination;
thepositiveassociationof dioecywithclimbing
attributes,
is tentatively
foroptimalresource
Ifrapid
growth
explainedin termsofdifferential
selection
allocationto sexualfunction.
in climbersand iffruitsetat leasttemporarily
is at a premium
or requirestheproduction
inhibits
upwardgrowth
growth
ofthicker,
moreslowlygrowing
stemsto support
itmight
be advantageous
topostponefemaleness.
Iftheeffect
heavyfruits,
is strong,
thismayfavormaleplants.
Overthepast 15 yrconsiderable
effort
seeds (Bawa, 1980; Givhas beenspent fruitsand frugivore-dispersed
documenting
correlations
betweendioecyand various nish,1980;Steiner,1988;Ibarra-Manriquez
andOyama,
morphological
and ecologicaltraitsforthe purposeof 1992;butseeFox, 1985;Muenchow,1987;Thomsonand
testinghypothesesabout conditionsthatfavordioecy. Brunet,1990),smallflowers
(BawaandOpler,1975;Fox,
Ecologicalcorrelates
attracted
attention
in particular
1985;Ibarra-Manriquez
and Oyama,1992),whitetoyelbecausedioecyhas provendifficult
to explainsimplyas an
low or greenishflowers(Bawa and Opler,1975; Muenoutbreeding
mechanismin taxa lackingself-incompati- chow,1987),waterpollination
(Cox, 1988),andso-called
bility(fordiscussionsof this issue, see Charlesworth unspecializedinsectpollinators
(Bawa and Opler,1975;
and Charlesworth,
1978; Thomsonand Barrett,1981; Bawa, 1994; contraRennerand Feil, 1993).
Charlesworth,
1985;ThomsonandBrunet,1990).AtdifWhile older reportstestedthe associationsbetween
ferentspatialand hierarchicalscales,dioecyhas been dioecyand particular
attributes
morerecent
separately,
associatedwith,amongotherattributes,
windpollination oneshaveusedmultivariate
analysis,takingintoaccount
(Darwin, 1876; Kerner,1895; Sporne,1949; Stebbins, correlations
amongsome of the explanatory
variables
1951; Kaplanand Mulcahy,1971; Freeman,Harper,and themselves
(Fox, 1985;Muenchow,1987;Steiner,1988;
andOyama,1992).Someauthorshave
Ostler,1980;Muenchow,1987;Steiner,1988),monoecy Ibarra-Manriquez
(Yampolskyand Yampolsky,1922; Lewis, 1942; Wes- attemptedto incorporatephylogenetic
in
information
tergaard,
1958; McComb,1966; Lloyd,1982),perennial analysesoftheassociationofdioecywithothertraitsby
growth
andlignified
secondary
xylem,orwoodiness(Dar- lookingat thespecies,genus,and family
levelsseparately
win, 1876; Stebbins,1950; Baker, 1959; Croat, 1979; or by restricting
analysesto monophyletic
groups(Hart,
Conn,Wentworth,
and Blum, 1980; Freeman,Harper, 1985; Donoghue,1989; Cox, 1990, 1993; Lahav-Ginott
andOstler,1980;Fox, 1985;butseeSteiner,1988),fleshy and Cronk,1993).
Thedataanalyzedinthesestudies,
witha fewexceptions
1 Manuscript
allcome
analyses,
received19 May 1994;revisionaccepted23 November suchas Cox's(1990, 1993)phylogenetic
1994.
fromlocal floras.Such locallycircumscribed
data allow
The authorsthankD. Charlesworth,
P. Cox,P. Endress,
C. Freeman, oneto contrast
thesubsetsofdioeciousandnondioecious
S. Heard,J. Kohn,-J. Thomson,and K. Bawa forcomments
on the
taxawithregardto particular
ecologicaland morphologmanuscript;
and P. Berry(Onagraceae),
H.-J.Esser(Euphorbiaceae),
S.
For example,therelationships
beKnapp(Solanaceae),J.Kuijt(parasitic
angiosperms),
C. Ott(Menisper- ical traitsofinterest.
tweena particular
floralcoloror size and dioecycan be
maceae),andJ.Rohwer(Lauraceae)forinformation
on dioecyin paranalyzedonlyiffloralcolorsor sizesfortheuniverseof
ticulargroups.
2
Authorforcorrespondence.
nondioeciousspeciesare known.At present,
thisis pos596
May
1995]
RENNER AND RICKLEFS-DIOECY
IN THE FLOWERING PLANTS
597
of Thorne(1992); total
sible onlyon a local basis. No studyhas yetaddressed (1988) and the 28 superorders
plantsat large, numberofgenera(in thefamilydata set)and numberof
thecorrelatesof dioecyin theflowering
and some apparentassociationsamongdioecyand par- dioeciousspecies(in thegenusdata set);growthforms;
distribube theresultofregionalef- modesofpollinationand dispersal;geographic
ticulartraitsmay,therefore,
com- tion; and trophicstatus.Generaacceptedare thoseof
ifthereis a strongphylogenetic
fects,particularly
(1992); familiesarethoseofCronquist(1988),
ponentto thepresenceor absenceofdioecy.As longas Brummitt
theymay exceptthatin 18 cases morerecent,broaderfamilyconsuchsamplingproblemsremainunrecognized
ad hoc hypoth- ceptswereaccepted.To look at theeffects
ofdifferences
ofunnecessary
resultin theintroduction
in familialconcepts,thedata setswerealso brokendown
thatdid notplaya
eses to explainsupposedcorrelations
intothemorenarrowly
circumscribed
familiesofThorne
causal rolein theevolutionofdioecy.
Here we reportresultsof a studyin whichwe have (1992).
Dioecyandmonoecywerescoredas present
ina family
ofvariousassociations
therelativestrengths
determined
traitsacrossall flowering whenat leastone speciesin thatfamilyis dioeciousor
betweendioecyand particular
in thecase offamilieswithfew
approach,thepos- monoecious.Particularly
plants.Becausewe use a multivariate
associationsamongthetraitsthem- dioecioustaxagreatcarewastakentosearchtheliterature
sibilityoffortuitous
confirmation
of theirdioeciousstatus.
selvesis reduced.Ouranalysis,to somedegree,also takes forindependent
to Numeroustaxa(:20 familiesand ;:200 genera)listedas
bias becauseit is not restricted
care of phylogenetic
particularfamiliesthathappento dominatelocal floras includingdioeciousspeciesbyYampolskyand Yampolstriking
exampleof sky(1922) had to be removedfromthedata set,either
(see Steiner,1988,fora particularly
dioeciousplantshaveturnedout
in theCape floraof SouthAfrica).It is based becausethesupposedly
thiseffect
ofdioeciousangiosperm
polygamous,
monoecious,or gynogeneraand to be sex-changing,
on a newcompilation
and taxonomic
families,the onlyprevioussuch compilationby Yam- dioecious,or because of nomenclatural
polskyand Yampolsky(1922) beingoutdated.Systema- changes.Yampolskyand Yampolskybased theircomwithinthe pilationonEnglerandPrantl'sNatiirlichePflanzenfamilirelationships
tists'viewsof thephylogenetic
and systematic en and thevolumesof Engler'sPflanzenreich
published
angiospermsand the circumscription
placementofnumerousgenerahave changedduringthe by 1912. Theyconcludedthatout ofthetotalof 10,113
and angiosperm
972(9.6%)comprised
generathenrecognized,
past 70 yr,newcases ofdioecyhave beenreported,
manyothersmentionedby Yampolskyand Yampolsky dioeciousand/orpolygamodioecious
species.However,
haveturnedouttobe in error.In anotherpaper,thesame theirlistincludesat least 90 generasincemergedwith
ofdioecy othergenera;some,suchas Streblus,
arelistedeighttimes
data setwillbe used to studythedistribution
phy- underdifferent
in theframework
publishedangiosperm
names. There are also 43 unpublished
ofrecently
names(nominanuda),theidentity
ofwhichis obscure.
data).
logenies(Renner,unpublished
viewatthefamily
leveldioe- Severalothergenera,froma modernsystematic
weanalyzewhether
Specifically
dis- point,arecompletely
misplacedas tofamily.
Conversely,
geographic
cyis associatedwithmonoecy,particular
170 additionaldioeciousgeneraand manyadditional
windor watervs. animalpollination,fleshy
tributions,
dis- familieswereadded eitherbecauseofnewlydiscovered
vs. abiotically
animal-dispersed
fruits
and,therefore,
ofdioecyorbecauseoftaxonomic
changes,
such
forms.
Becausewelacked instances
growth
persedseeds,orparticular
modernfamilyconcepts.Our data setconwe wereunableto addressas- as narrower
data forall angiosperms
sociationsbetweendioecyand small,greenishflowers tains959 generathatincludedioeciousspecies.
Mostdioeciousgeneracompriseonlydioeciousspecies;
(Bawa and Opler, 1975; Fox, 1985; Muenchow,1987;
Ibarra-Manriquez
and Oyama,1992)andbetweendioecy however,325 ofthe959 generahavemorethanonematand pollinationby small, supposedgeneralistinsects ing system,and forthemnumbersof dioeciousspecies
fromfigures
giveninrecentliterature,
maybe a correlateof theas- hadtobe estimated
(Bawa, 1994). The former
suchas "rarelydioecious"or
belowbetweenwindpollination usuallyfloras.Statements
sociationdemonstrated
as
areoften
small "occasionallydioecious"werescoredconservatively
flowers
anddioecy,becausewind-pollinated
and lackattractive
coloration;thesecondis basedon the at least one dioeciousspecies,while"commonlydioewith cious"was scoredas 50% dioecious.Speciesnumbersare
smallnessis correlated
erroneous
ideathatpollinator
and inefficient notused in theanalyses.
relationships
pollinator-flower
unspecific
Growthformsweretakenfromflorasand accountsof
pollination(Rennerand Feil,
(in termsof outcrossing)
particularmodes of growth,such as Gentry(1991) for
1993).
are fromMabdistributions
climbers,whilegeographic
work
berley(1987),exceptwheremorerecentsystematic
MATERIALS AND METHODS
was available.Growthformwas tabulatedas presenceor
shrubs,
herbs,orclimbers
(whether
woody
This studyis based on twodata sets,one a data base absenceoftrees,
of dioeciousangiospermgeneracompiledby searching or herbaceous).
Pollinationand dispersalmodes wereassessedfrom
withspecialists(see
and by corresponding
theliterature
of the flowersand fruitsof each taxonin
theothera data base of all families descriptions
Acknowledgments),
andmonographic
sources(fordetails,see
offlowering
plants.For detailsofthesecondcompilation variousfloristic
andRenner(1994). Thegenusandthefamily Ricklefsand Renner,1994). In bothdata sets,thecateseeRicklefs
information
foreach gorieswere1) abiotic,2) biotic,and 3) variable,thelast
data bases containthe following
or dispersalpresentin
taxon: presence or absence of dioecy, presence or meaningbothtypesofpollination
In thegeneric
specieswithinthegenusorfamily.
absenceofmonoecy(in thefamilydata set);positionin different
scoredas 1)
intermsofthe11subclassesofCronquist data set,pollinationmodewas additionally
theangiosperms
598
AMERICAN JOURNAL OF BoTANY
[Vol. 82
wind,2) water,3) insects,4) bats,5) birds,6) variable, repeatedtheanalysesusingonlysmallfamilies(lessthan
or7) unknown.
Data onthepollination
whichheightens
ofmanydioecious fivegeneraperfamily),
thelikelihoodof
taxa had alreadybeen compiledin connectionwithan co-occurrence
ofthevariablesin thesamegenusor speearlierreviewof theliterature
(Rennerand Feil, 1993). cies; second,we also examinedassociationsat thegenus
A fewadditionalautecologicalstudieshave sincebeen levelwherepossible.
published(e.g.,Kato, 1993), and thereare severalsysThe statistical
significance
of each of thevariablesis
tematicreviews(Dobat and Peikert-Holle,
1985; Cox, evaluatedby a x2 withits associatedprobability.
Each
1988; Kubitzki,Rohwer,and Bittrich,1993; Webster, model has a likelihoodratio(LR) which,if significant,
1994a,b). For manyoftheremaining
genera,pollination indicatesadditionalstructure
inthedatasetnotaccounted
by eitherwindor insectscould be assessedfromfloral forbythemodel.Initialmodelsincludedno interactions.
structure,
withparticular
weightbeinggivento thepres- Nonsignificant
variablesweredeletedfromthemodeland
ence or absenceofnectaries.All fleshy
whenLR x2 values were significant,
as wellas
fruits,
interactions
were
indehiscent
largedryfruits,
werescoredas beingadapted addedbytrialand errorto arriveat a modelwitha nonforanimaldispersal.Some smalldryfruits
LR x2. Becausemonoecyis a matingsystem
scoredas abi- significant
oticallydispersedmayhave seedsinitially
dispersedbal- thatmay facilitate
the evolutionof dioecy(see below),
listically
and thenbiotically
(byants);itis unlikely,
how- thesemodelswererunbothwith(+M) andwithout
(-M)
ever,thatthisgroupintroduces
a largeerrorintothedata. monoecyas a variableto isolatetheeffects
ofecological
Wheredescriptions
offloralstructures
on dioecy.
and/orfruits
were interactions
insufficient
to assessreproductive
modes,thecondition
wasleftunscoredinthegenericdataset;all families
could
RESULTS
be scored.
For the family-level
analysis,geographicdistribution Out ofthetotalof 13,479genera(Brummitt,
1992),at
was coded as presentor absentin tropicallatitudesand least 959 (7.1%) containdioeciousspecies;if Thorne's
is
presentor absentin temperatelatitudes.The category (1992) estimateof 12,650generafortheangiosperms
is 7.6%.A conservative
estimate
in- accepted,thatpercentage
"tropical"includesall familieswhosedistributions
cludeeitherlow or highelevationsin thetropics;"tem- ofthenumberofdioeciousspeciesis 14,620or 6% ofan
plants.Of
perate"includesall familieswhosedistributions
include assumedtotalof240,000speciesofflowering
circumscribed
365 familiesof angioorborealzones-generally,
temnperate
zoneswithfrost.
The a conservatively
thefamiliesof Cronquist,1988; see
distributions
ofthedioeciousgenerawerescoredin con- sperms(essentially
siderabledetailforfuture
analysisbecausemanygenera Materialsand Methods),157 (43%) containdioecious
OfThorne's(1992) morenarrowly
defined
withvariablematingsystemsalso have theirdioecious members.
437
speciesconfinedto a particular
region.For example,in families,167 (38%) have dioeciousmembers.
In thefollowing
we first
resultsofanalysesperpresent
Asperula(Rubiaceae),the 16 Australianspeciesare didata set(Tables 1-12); this
oecious whilethe Mediterranean
speciesare hermaph- formedusingthefamily-level
is followedby resultsbased on genus-level
data (Tables
roditic.
Each variablewas scoredas 0 (absent)or 1 (present). 13 and 14).
analysesrelatingeach variableindividuWithineach of thecategoriesof variables(distribution, Contingency
in Table 1. Variablesthatare
matingsystem,pollination,
dispersal,growthform,tro- allyto dioecyarepresented
and strongly
associatedwithdioecyare,in
phic status)each familyhad to have a scoreof 1 forat significantly
oftheircorrelation,
climbleastone ofthevariablesbutcouldalso have a scoreof orderofthestrength
monoecy,
form,
bioticdispersal,
abioticpollination,
shrub
1 forall ofthem.None couldhave scoresof0 forall of inggrowth
them.For some of the analyses,the familieswerealso growthform,and tropicaldistribution.
Categoricalmodels are presentedin Table 2. The
dividedintotwogroupsbasedon numberofgenera:size
in an initialmodel(no interactions)
effects
were
= 0, fewerthan 5 genera; size = 1, 5 or more genera.
strongest
In orderto examinethe relationship
growth
form,bioticdispersal,abiotic
of dioecyto all monoecy,climbing
The individualasand tropicaldistribution.
variablessimultaneously,
categoricalmultivariate
con- pollination,
sociationof shrubbygrowthwithdioecyevidently
was
tingency
analyses(SAS Institute,
Inc., 1988,CATMOD
withother
correlation
in whichthepresenceor ab- subsumedin thismodelthrough
procedure)wereperformed
senceofdioecywas relatedto presenceor absenceofall variables.In thisanalysis,thelikelihoodratiowas sigin thedata setin
additionalstructure
indicating
the othervariablesin the data set. Categoricalmodels nificant,
A seriesofmodelswithvarious
take into accountassociationsamongthe independent theformofinteractions.
termswerethenrun.The onlysigvariablesand revealtheuniquestatistical
re- two-wayinteraction
(predictor)
interaction
was abioticpollinationx monoecy.
betweendioecyandothervariablesinthedata nificant
lationships
was includedand nonsignificant
set.Whenappliedat thetaxonomicleveloffamily,
this Whenthisinteraction
weredeletedfromthemodel,thelikelihoodratio
theassociationof traitswithintaxa effects
approachidentifies
(Table 2, model+M). Thus,sevbut does not implythata pair of associatedtraitsnec- becamenonsignificant
to thepresenceof
independently
essarilyoccursinthesamegenusorspecies.Indeeddioecy eral factorscontribute
indescending
orderofimportance:
andmonoecycannotco-occurina singlespeciesandhence dioecywithina family,
abioticpollination,
shrub
theirassociationcouldonlybe identified
bya higher-level monoecy,tropicaldistribution,
howandclimbing
form,
growth
form.In addition,
withthisapproachis thattwotraits growth
analysis.A difficulty
withabioticpollinationin conmaybe associatedbecauseeach is morelikelyto be rep- ever,monoecyinteracts
to dioecy(Table 3). When monoecywas exresentedin familieswithlargenumbersof species.We tributing
in two ways:first,
analysis(Table2,model-M),
triedto deal withthis difficulty
we cludedfromthecategorical
May
1995]
TABLE 1. Family-level relationshipof presence (in 157 families) or
absence (in 208 families)of dioecy to each of the variables.
and
of abioticpollination
tableof theeffects
3. Contingency
areincludedin
bioticdispersalon presenceofdioecy.All families
withdioecyovertotal
offamilies
theanalysis.Ratiosarenumbers
numberoffamilies.a
TABLE
Number of families
Variable absent
Categoryand
variable
Monoecy
Dioecy
absent
Dioecy
present
179
54
Variable present
Monoecy
Dioecy
present
x2a
29
103
107.6
0.000
Dioecy
absent
41
111
12
80
167
97
145
77
11.2
0.2
0.001
0.648
177
24
104
33
31
184
53
124
17.9
6.0
0.000
0.014
Dispersal
Abiotic
Biotic
55
117
59
46
153
91
98
111
5.1
26.8
0.023
0.000
Growthform
Herb
Shrub
Tree
Climber
103
119
118
157
87
59
72
72
105
89
90
51
70
98
85
85
1.2
13.9
4.2
33.8
0.264
0.000
0.039
0.000
Parasite
Size of family
203
130
149
53
5
78
8
104
1.9
30.0
0.172
0.000
X2 is
the likelihood ratio x2 value.
abioticpollinationand climbinggrowthformremained
ofdioecy.
strongcorrelates
Because,on average,largefamiliescontainmoredioecioustaxa thando smallfamilies(Table 1), thedata
weresplitintotwosetshavingnearlyequal numbersof
familiesbased on numberofgeneraperfamily(lessthan
thestronfive,and fiveor more).Amongsmallfamilies,
are monoecyand thepollination
gestindividualeffects
and dispersalvariables,withdioecyless oftenpresentin
and abioticdispersaland
familieswithbioticpollination
moreoftenpresentin familieswithabioticpollination
TABLE
Absent
p
Distribution
Tropical
Temperate
Pollination
Abiotic
Biotic
a
Abioticpollination
33/198
Absent
(17%)
21/35
Present
(60%o)
54/233
Total
(23%)
Total
Present
71/83
(86%)
32/49
(65%)
103/132
104/281
(37%)
53/84
(63%)
157/365
(43%)
(78%)
betweenmonoecyand dioecyin theabsenceof
The relationship
had LR X2= 123.4,P < 0.001,andin thepresence
abioticpollination
LR X2 = 0.2,P = 0.62.
ofabioticpollination,
a
and bioticdispersal(Table 4, butsee below).In addition,
herbsandmore
dioecyis lesslikelyinfamiliescontaining
shrubsand trees.A categorlikelyin familiescontaining
and including
effects
nonsignificant
ical modelexcluding
of monoecywithabioticpollinationhad
theinteraction
likelihood-ratio
andrevealedabioticpola nonsignificant
growth
lination,bioticdispersal,monoecy,and climbing
effects
(Table 5, Model +M).
to be the onlysignificant
contributed
bymonoecyis conMuchoftheinformation
tainedin themonoecyx abioticpollinationinteraction
(Table 6). Whenmonoecywasexcludedfromtheanalysis
(Table 5, Model -M), we couldnotfinda whollysatismodel (LR, P = 0.034), but the same variables
factory
rebioticdispersal,
climbing
growth)
(abioticpollination,
mainedsignificant.
effects
Amonglargefamilies(Table 7), the strongest
andshrubgrowth
bioticdispersal,
climbing
weremonoecy,
withabioticdispersal
forms,and tropicaldistribution,
A categorical
modelshowed
effect.
a weaknegative
exerting
to be theonlysignifmonoecyand tropicaldistribution
at thefamily
levelbetweendioecyand theindependent
2. Categorical
modelsoftherelationship
variablesin thisanalysis.
Initial model
Variable
Monoecy
Tropicaldistribution
Temperate
distribution
Abioticpollination
Bioticpolliantion
Abioticdispersal
Bioticdispersal
Herbgrowth
form
Shrubgrowth
form
Treegrowth
form
form
Climbinggrowth
Abioticpollinationx
X2
52.1
4.8
0.5
5.7
0.1
0.0
6.1
0.4
2.0
0.0
10.1
Model +M
P
0.000
0.029
0.500
0.017
0.710
0.912
0.014
0.539
0.157
0.874
0.002
X2
192.2
(143)b
Variablenotincludedin analysis.
b Degreesoffreedom
forlikelihoodratio.
0.004
Model -M
P
X2
P
27.6
11.7
0.000
0.001
5.2
0.023
8.5
0.004
39.9
0.000
10.7
0.001
8.3
0.004
36.8
0.000
26.1
monoecy interaction
Abioticpollinationx
bioticdispersal
Tropicaldistribution
x
bioticdispersal
Likelihoodratio
a
599
DIOECY IN THE FLOWERING PLANTS
RENNER AND RiCKLEFS-
19.5
(20)
0.000
0.493
-a
-
-
6.3
0.012
6.9
11.4
0.008
0.249
(10)
600
[Vol. 82
AMERICAN JOURNAL OF BOTANY
4. Relationship
ofpresence(in 53 families)
orabsence(in 130
families)ofdioecyto each ofthevariablesindependently
among
smallfamilies(<5 genera).
TABLE
6. Contingency
tableof theeffects
of abioticpollination
and
bioticdispersalon presenceof dioecy.Onlysmallfamilies(<5
genera)areincludedintheanalysis.Ratiosarenumber
ofdioecious
familiesovertotalnumberoffamilies.a
TABLE
Number of families
Variable absent
Categoryand
variable
Dioecy
absent
Monoecy
Variable present
Dioecy
present
Dioecy
absent
113
31
Monoecy
Distribution
Tropical
30
9
74
28
Temperate
Pollination
Abiotic
20
107
20
Biotic
23
Dispersal
46
Abiotic
30
Biotic
76
21
Growthform
Herb
40
75
Shrub
80
25
Tree
71
20
117
Climber
43
a x2 is thelikelihood
ratiox2.
Absent
Dioecy
present
P
x2
17
22
16.8
0.000
100
56
44
25
0.9
0.3
0.35
0.61
23
110
33
30
33.8
15.4
0.000
0.000
84
54
23
32
7.0
5.4
0.009
0.020
55
50
59
13
13
28
33
10
5.3
3.2
4.3
2.5
0.021
0.076
0.038
0.112
Present
Abioticpollination
Absent
13/114
(11%)
Present
18/30
(60%)
Total
31/144
(22%)
Total
7/13
(54%)
15/26
(58%)
22/39
(56%)
20/127
(16%)
33/56
(59%)
53/183
(29%)
a
The relationship
betweenmonoecyand dioecyin theabsenceof
abioticpollination
had LR x2 = 11.8,P < 0.001,and in thepresence
of abiotic pollination,LR x2 = 0.0, P
=
0.86.
sistentassociationsin thedata setrelatethepresenceof
tomonoecy,
abidioecywithina family
climbing
growth,
oticpollination,
andbioticdispersal;tropicaldistribution
is associatedwithdioecyonlyin largefamilies.
Becausemonoecywas suchan important
factorin asof
sociationwithdioecy,we examinedtherelationship
monoecyitselfto thedistribution
ofothervariables(excludingdioecy)withinfamilies
(Table 11).Severalfactors
icanteffects,
but therewas a stronginteraction
between had significant
associationswith monoecy:climbing
bioticdispersaland abioticpollination(Table 8, Model growth
(+), abioticpollination
(+), bioticpollination
(-),
+Ma). Climbinggrowthformwas notsignificant.
bioticdispersal(+), and temperate
distribution
(+). A
The interaction
effect
ofabioticpollinationand biotic categorical
modelofthedependence
ofmonoecyon other
dispersalin largefamiliescanbe visualizedbyexamining variablesproducedthe following
results:abioticpollithecontingency
tablerelating
presenceorabsenceofdioe- nation(x2 = 46.8, P = 0.000), climbinggrowth(36.9,
cy to combinationsof presenceand absenceof each of 0.000), temperate
distribution
(3.9, 0.049), abioticpolthesevariables(Table 9). Bioticdispersalandabioticpol- linationx bioticdispersalinteraction
(11.2,0.001),likelinationwerenot individuallysignificant
effects.
How- lihoodratio(12 df,23.4,0.025).Amongfamilies
including
ever,familieswithneitherof theseattributes
included taxawithabioticpollination,
presenceorabsenceofbiotic
fewerdioecioustaxathanfamilieswitheitheroneorboth dispersalhad no influence
on monoecy(60.9%vs. 55.3%,
of them.The same is trueof the interaction
between
abioticpollinationand monoecy(Table 10),whichalso
amonglargefamilies(?5 genera)ofpresence
makesa suitablecategorical
model(Table8,model+ Mb). TABLE 7. Relationship
(in 104 families)or absence(in 78 families)of dioecyto each of
Whenmonoecywas deletedfromthecategorical
model
thevariables.
forlargefamilies,abioticpollination,
tropicaldistribution,and climbinggrowthformweresignificant
effects,
Number of families
alongwiththeabioticpollinationx bioticdispersalinVariable present
Variable absent
teraction
(Table 8, model -M).
Categoryand
Dioecy
Dioecy
Dioecy
Dioecy
To summarizethecategorical
variable
absent
present
absent
analyses,themostconpresent
P
x2
TABLE 5. Categorical
modelsforsmallfamilies(<5 genera)of the
betweendioecyand theindependent
relationship
variablesin this
analysis.
Model +M
Variable
Monoecy
Abioticpollination
Bioticdispersal
form
Climbing
growth
Abioticpollinationx
monoecy interaction
Abioticpollinationx
form
climbing
growth
Likelihoodratio
(df)
Model -M
X2
P
6.2
0.013
13.4
7.8
4.3
0.000
0.005
0.039
4.8
0.028
15.6
(10)
0.111
x2
-
12.3
9.8
9.5
-
4.0
10.4
(4)
P
-
0.000
0.002
0.002
-
0.046
0.034
66
23
Monoecy
Distribution
11
Tropical
3
37
52
Temperate
Pollination
84
Abiotic
70
Biotic
4
10
Dispersal
29
Abiotic
9
Biotic
41
25
Growthform
47
Herb
28
34
Shrub
39
47
52
Tree
Climber
40
29
a x2 iS thelikelihood
ratiox2.
12
81
75.3
0.000
67
41
101
52
8.1
0.1
0.005
0.73
8
74
20
94
2.9
1.3
0.09
0.25
69
37
75
79
7.6
15.7
0.006
0.000
50
39
31
38
57
70
52
75
1.6
5.6
1.9
10.4
0.21
0.018
0.17
0.001
May 1995]
RENNER AND RICKLEFS-DIOECY
bemodelsforlargefamiliesoftherelationship
8. Categorical
variablesin thisanalysis.
tweendioecyand theindependent
TABLE
Variable
Monoecy
Tropicaldistribution
Abioticpollination
form
Climbinggrowth
Abioticpollinationx
Bioticdispersal
Abioticpollinationx
Monoecy interaction
Likelihoodratio
(df)
Model +Ma
Model +Mb
Model -M
x2
x2
x2
p
-
-
P
48.9 0.000
4.2 0.040
p
20.9 0.000
12.4 0.000
14.7 0.000
13.3 0.360
(12)
7.6 0.006
9.7 0.002
5.8 0.017
19.9 0.000
7.1 0.008
3.5 0.360
(5)
-
-
9.8 0.455
(10)
x2 = 0.3, P = 0.60). Amongfamilieslackingabioticpollination,presenceof bioticdispersalincreasedthelikelihood of monoecy(39.0% vs. 16.2%,x2 = 17.9, P <
0.001).
herbaceousor woody,also
whether
Climbinggrowth,
factorin association
and unexpected,
was an important,
ofthis
withdioecy,and so we examinedtherelationship
ofothervariableswithin
growthformto thedistribution
families(Table 12). Significant
associationswere:dioecy
(+), monoecy(+), bioticdis(+), tropicaldistribution
(+),
form(+), bioticpollination
persal(+), shrubgrowth
and abioticpollination(-). A categoricalmodelof the
dependenceof climbinggrowthon othervariablesprogrowth(X2= 26.5,
results:shrubby
ducedthefollowing
P = 0.000), herbaceousgrowth(21.0, 0.000),bioticdispersal(8.3, 0.004), monoecy(8.1, 0.004), abioticpolli(22 df,24.9, 0.30).
nation(5.2, 0.022), likelihood-ratio
herb x
In addition,thereweretwo stronginteractions:
shrubgrowthform(19.0, 0.000) and abioticpollination
x monoecy(6.8, 0.009).
sectionspresentresultsbased on thegeThe following
nus-leveldioecydata set. Detailed global comparisons
of the
betweenthedioeciousgeneraand theremainder
angiosperm
generawerenotfeasable.However,because
thisis thefirst
compilationofdioecyin theangiosperms
since Yampolskyand Yampolsky(1922) and Charlesofseveral
worth(1985)andbecausethedataaresuggestive
trendsamongdioecioustaxa,suchas thelikelyoverre(see below),we hopethat
ofheterotrophism
presentation
thesedataherewillstimulate
further
datacolpresenting
analyseson thegeneric
lectionand eventualmultivariate
level.
and
of abioticpollination
tableof theeffects
9. Contingency
bioticdispersalon presenceof dioecy.Onlylargefamilies(25
ofdioecious
Ratiosarenumbers
genera)areincludedintheanalysis.
familiesovertotalnumberoffamilies.
and
ofabioticpollination
tableoftheeffects
10. Contingency
monoecyon presenceof dioecy.Onlylargefamilies(25 genera)
ofdioeciousfamareincludedin theanalysis.Ratiosarenumbers
iliesovertotalnumberoffamilies.a
TABLE
Monoecy
Absent
Biotic dispersal
Abioticpollination
14/53
Absent
(26%)
11/13
Present
(85%)
25/66
Total
(38%)
Present
70/101
(69%)
9/15
(60%)
79/116
(68%)
Total
84/154
(55%)
20/28
(7 1%)
104/182
(57%)
Total
Present
Abioticpollination
84/154
64/70
20/84
Absent
(55%)
(91%)
(24%)
20/28
17/23
3/5
Present
(7 1%)
(74%)
(60%)
104/182
81/93
23/89
Total
(57%)
(87%)
(26%)
a The relationship
betweenmonecyanddioecyin theabsenceofabihad LR x2= 79.1,P < 0.001, and in thepresenceof
oticpollination
LR x2= 0.4,P = 0.54.
abioticpollination,
Dioecy and phylogeny-Dioecy is slightlymore common among dicot genera than among monocot genera
(8.2% vs. 5.1%; x2 = 30, P < 0.001). It occurs in 24 of
the 28 superordersof Thorne (Table 13) and in each of
the six dicot and five monocot subclasses of Cronquist
(1988). Because some ofCronquist'ssubclassesare poorly
the followinganalysis
definedand probablypolyphyletic,
concentrateson Thorne's superorders,which because of
theirnarrowercircumscriptionstand a betterchance of
being monophyletic.
Among the 14 dicot superordershaving > 100 genera
the distributionof dioecious generais extremelyheterogeneous (X213 = 909, P < 0.0001). In absolute numbers,
most dioecious genera are found among Thorne's Malvanae (208), his Magnolianae (134), Violanae (90), Rutanae (71), Commelinanae (62), Theanae (58), and Gentiananae (49). In relativeterms,dioecy is concentratedin
monocotyledonous Pandananae (100%), Alismatanae
(47%), and Triuridanae (25%) and the dicotyledonous
Rafflesianae(80%), Magnolianae (29%), and Malvanae
(28%). The Magnolianae and Malvanae are thus among
the most importantdioecious clades, in both relativeand
absolute terms.This is mainly due to a few dioecy-rich
families,such as the Lauraceae, Menispermaceae, Myristicaceae,and Monimiaceae in the firstsuperorderand
the Euphorbiaceae, Moraceae, and Urticaceae in the secofthepresence
11. Family-level
(in 132families)
relationships
or absence(in 233 families)ofmonoecyto eachoftheothervariables.
TABLE
TABLE
Absent
601
IN THE FLOWERING PLANTS
Variable
X2
is
Variable present
Mon- Monoecy
oecy
absent present
Mon- Monoecy
oecy
absent present
40
13
132 59
198 83
31
26
44
70
116 47
130 60
119 59
123 67
168 61
226 126
thelikelihoodratiox2value.
Tropicaldistribution
distribution
Temperate
Abioticpollination
Bioticpollination
Abioticdispersal
Bioticdispersal
form
Herbgrowth
form
Shrubgrowth
form
Treegrowth
form
Climbinggrowth
Parasitehabit
a
Variable absent
193
101
35
207
163
117
103
114
110
65
7
x2.
P
119 3.8 0.057
4.8 0.028
73
49 22.5 0.000
101 9.4 0.002
0.4 0.516
88
6.9 0.009
85
72
3.6 0.057
1.4 0.241
73
0.1 0.709
65
71 23.9 0.000
0.6 0.452
6
602
12. Family-level
ofthepresence
relationships
(in 136families)
ofclimbing
orabsence(in 229 families)
formtoeachofthe
growth
othervariables.
TABLE
Variable absent
Variable
Tropicaldistribution
Temperatedistribution
Monoecy
Dioecy
Abioticpollination
Bioticpollination
Abioticdispersal
Bioticdispersal
form
Herbgrowth
form
Shrubgrowth
Treegrowth
form
Parasitehabit
a
[Vol. 82
AMERICAN JOURNAL OF BOTANY
X2
5
76
65
51
118
10
39
39
62
45
72
132
Number of
families
Variable present
Climb- Climb- Climb- Climbers
ers
ers
ers
absent present absent present
48
115
168
157
163
47
75
124
128
133
118
220
Total
ofdioecyinThorne's(1992)superorders.
TABLE13. Distribution
ofgenerainthistablearefromThorne,whilethefamilies
numbers
as in Cronquist(1988; see Methods).
arecircumscribed
181
114
61
72
66
182
154
105
101
96
111
9
131
60
71
85
18
126
97
97
74
91
64
4
x2.
24.4
1.1
23.9
33.8
12.4
12.4
0.7
23.0
3.6
21.7
0.1
0.2
P
0.000
0.294
0.000
0.000
0.000
0.000
0.415
0.000
0.057
0.000
0.794
0.617
is the likelihood ratio x2value.
Superorder
Dicots
1 Magnolianae
2 Nymphaeanae
3 Rafflesianae
4 Caryophyllanae
5 Theanae
6 Celastranae
7 Malvanae
8 Violanae
9 Santalanae
10 Geranianae
11 Rutanae
12 Proteanae
13 Rosanae
14 Comnanae
15 Asteranae
16 Solananae
17 Loasanae
18 Myrtanae
19 Gentiananae
Dio- MonoTotal ecious ecious
34
2
3
12
40
2
20
26
9
16
23
1
39
23
6
8
1
12
0
1
9
14
1
17
13
8
4
8
1
15
16
3
2
0
14
0
1
7
10
1
12
11
6
3
8
1
14
11
2
1
0
Total
Dioecious genera
number
of
NumPercent
ber
genera
466 134
0
81
8
10
563 30
540 58
7
60
769 208
725 90
162 37
7
189
1,129 71
2
75
381 36
650 44
1,251 28
4
296
0
13
29
0
80
5
19
12
27
12
22
4
6
2
9
7
2
1
0
ond superorder.
Familieswiththehighest
concentrations
of dioeciousgenerain bothabsoluteand relativeterms
are the Menispermaceae
(100% of thegeneraare dioe1
2
3
463
3
13b
cious),Myristicaceae
(78%),Moraceae(62%),Urticaceae
2
6 2,135 49
5
23
(52%), Anacardiaceae(50%), Monimiaceae(47%), Eu8
305c 132 110 9,958 817c
Total dicots
phorbiaceae(39%), and Cucurbitaceae
(32%).
1
2 1,184 16
8
15
Lilianae
Amongthesubclasses,Cronquist(1988, pp. 263-265 20
1
0
0
2
0
0
21 Hydatellanae
and pp. 451-457) considerstheMagnoliidae,Hamamel- 22 Triuridanae
2 25
1
8
1
1
idae, and Caryophyllidae
as less advancedthantheDil- 23 Alismatanae
11
57 27 47
7
6
1
1
2
2
1
108
leniidae,Rosidae,and Asteridaeamongdicots,and the 24 Aranae
11
0
1
1
0
0
Alismatidaeand Arecidaeas relatively
moreprimitive 25 Cyclanthanae
3a
0
3 100
1
1
thattheCommelinidae,
andLiliidaeamong 26 Pandananae
Zingiberidae,
1
1
1
200 31 15
27 Arecanae
in thelessad- 28 Commelinanae
monocots.Dioecyis strongly
concentrated
5
9 1,192 62
26
6
vancedsubclasses.Also Thorne(1992,p. 244, fig.1) tries
5
60 25 22 2,765 142
Totalmonocots
to arrangehis superorders
so that"The positionofthese
7.5
365 157 132 12,723 959
plants
Totalflowering
of the phyleticshrub
stem,cross-sections
superordinal
a SomePandanaceaeare monecioussex-changers
thanconsisrather
indicatesas closelyas possiblemyinterpretation
oftheir tent
dioecists(Cox, 1982).
relationships
and theirrelativedegreeof specialization b This numberis inflatedby Cronquist'srecognition
of Punicaceae
fromtheirmoreprimitive,
archaicancestors."We have and Sonneratiaceae
fromLythraceae.
as distinct
c Including
in hissequence(Table 13) and
numbered
thesuperorders
families
thatareunassigned
byThorne:
fourofCronquist's
andPandaceae;ofthese,
Corynocarpaceae,
Barbeyaceae,
dividedthe dicotsuperorders
roughlyintotwogroups, Aextoxicaceae,
and Barbeyaaredioecious.
one relativelyless advanced (numbers1-9), the other Aextoxicon
relatively
moreadvanced(numbers10-19).As withCronin theless adquist'ssubclasses,dioecyis concentrated
Old World tropicsthan in the New as suggestedby Thox2 = 519,P < 0.0001;
vancedsuperorders
ofdicots(genera:
families:x2 = 5.4, P < 0.025). Monoeciousfamilieshave mas and LaFrankie (1993), due primarilyto the highOld
a paralleldistribution
todioeciousfamilies
(Table 13)and World diversityof such dioecy-richfamiliesas the Euin less advanceddicot phorbiaceae, Menispermaceae,and Restionaceae.
exhibita similarconcentration
superorders
(X2= 4.4,P < 0.05). Possiblereasonsforthe
Growth
genera-We have
angiosperm
formsofdioecious
concentration
of dioecyin theless advancedclades are
informationon thegrowthformsof 818 ofthe959 genera
givenin thediscussion.
Geographicdistribution
of dioeciousangiosperm
genera-Of the959 dioeciousgenera,217 occurin theneo86 are pantropical,
and
tropics,402 in thepaleotropics,
in thetemperate
zone. Thirty
149 are foundexclusively
generahave temperateand tropicalmembers.The-reto Hawaii,New
maining75 generaare mostlyrestricted
NewCaledonia,orNewSouthWales.
Zealand,Australia,
inthelargegeographic
Becausethetotalnumbers
ofgenera
regionshave notbeentabulated,it is notpossibleto calculatethedifferent
relativefrequencies
of dioecy,butit
in the
seemslikelythatdioecyis indeedmorefrequent
with dioecy. Of the 818, 198 (24%) comprise only tree
species, 157 (19%) only herbs, 128 (16%) only climbers,
and 94 (11%) only shrubs.Tree and shrubspecies occur
togetherin 195 (24%) generawith dioecy. Other combinations of growthforms,such as trees,shrubs,and herbs
(seven genera),shrubsand herbs(19 genera),shrubsand
climbers(ten genera),and so on are rare. Of the genera
with dioecy, :z551 (67%) are woody (namely those with
trees and shrubs or both growthforms,plus half those
with only climbers).In the angiospermsas a whole, 234
familiesincludingtreeand shrubgrowthformshave 7,929
genera,or 59% of the total 13,500 genera; 182 families
May 1995]
RENNER AND RICKLEFS-DIOECY
14. Genus-level
analysisoftheassociationbetween
dioecyand
pollinators.
TABLE
Number of genera
Pollinated by
Insects
Windor water
Batsor birds
With dioecy
550 (5.1%)
232 (21.0%)
4 (0.4%)
Lacking dioecy
10,317a
874
750
IN THE FLOWERING PLANTS
603
species(Porsch,1931;and personal
withbird-pollinated
plants(Table 14) it
estimate)in therestoftheflowering
pollinationare both
appearsthatinsectand vertebrate
amongdioeciousgenera.Thiswas also
underrepresented
notedby,forexample,Richards(1986);belowwediscuss
possiblereasonsforthenearabsenceof bat pollination
amongdioecists.
genera-Ofthe
angiosperm
Dispersalmodesofdioecious
data
814 dioeciousgeneraforwhichthereare sufficient
orpredomon modeofdispersal,526 (65%) areentirely
bywind,
254(31%)aredispersed
animal-dispersed,
inantly
and sixhavebothbioticand abi28 arewater-dispersed,
oticmodesofdispersal.We haveno dataon thedispersal
data set,1,782
modesof 145 genera.In thefamily-level
withwhollybioticdispersal
generabelongto 114families
and 5,362generabelongto 88 familieswithbothabiotic
havingonlyshrubsortreeshave 3,185genera,or 24% of andbioticdispersal.Takinghalfthelatterplustheformer
thetotalangiosperm
genera.Thus,between24% and 59% givesan estimateof 4,463 animal-dispersed
genera,or
ofall angiosperm
generamaybe woody,andso woodiness ;33% oftheangiosperm
total.As in thecase ofwoody
wouldappeartobe overrepresented
amongdioeciousgen- growth,
animaldispersalappearsto be overrepresented
era.In thefamily-level
analysis,
woodinessperse wasnot amongdioeciousgenera,eventhoughthiswas nota para factorbecausethetreegrowthformhad no influence ticularly
analysis.
strongfactorin thefamily-level
on thepresenceor absenceofdioecywithina familyand
theshrubgrowthformhad an effect
onlyin someofthe
DISCUSSION
analyses(butsee Materialsand Methodsfora discussion
ofthelimitations
ofa multivariate
approachatthefamily
systematic
As has oftenbeenpointedout,thescattered
level).
of dioecyin the angiosperms
suggeststhat
distribution
manytimes
thismatingsystem
hasevolvedindependently
Dioecy and trophiccondition-Ofthe 959 dioecious and possiblyfordifferent
reasons(Lewis,1942; van der
bythefact
genera,at least43 (4%) areholoparasites,
hemiparasites, Pijl, 1978;Lloyd,1982).Thisis also suggested
and
or saprophytes.
Dioecious parasitesoccurin the Bala- thatin some lineages,suchas theCaryophyllaceae
variesalmostcontinnophoraceae,
Eremolepidaceae,
Loranthaceae,
Misoden- Chenopodiaceae,
sexualexpression
ofmaleor femalefunction
draceae,Opiliaceae,Rafflesiaceae,
Santalaceae,and Vis- ually,withreadysuppression
conditions(Heslop-Harrioftheangiosperms,
caceae. Amongtheremainder
para- in responseto environmental
intheConvolvulaceae(Cus- son,1957;Freeman,McArthur,
and Harper,1984;Freesiticgeneraareconcentrated
cutoideae),Cynomoriaceae,
Hydnoraceae,
Krameriaceae, man et al., 1993), whilein otherlineages,such as the
andCucurbitaceae,
dicliny
Lennoaceae, Loranthaceae, Olacaceae, Santalaceae, Monimiaceae,Euphorbiaceae,
as
angiosperms
and is basicallyfixed.In thedicotyledonous
Scrophulariaceae
(Rhinanthoideae,
Orobanchoideae),
intheless
Rafflesiaceae
(Mitrastemonoideae),
whichtogether
may a whole,monoecyand dioecyareconcentrated
ofThorne(1992). A consequence
comprisesome 135 heterotrophic
genera(1.1% of all advancedsuperorders
ofdioeis thatfrequencies
distribution
13,500angiosperm
genera).Dioecytherefore
maybe ov- ofthisnonrandom
floras(made muchofby manyauthors)
errepresented
amongheterotrophic
plants.Thiswas also cy in particular
pool of
the level of dioecyin a particular
suggested
bya species-level
analysisofdioecyin theflora likelyreflect
ofthesoutheastern
UnitedStates(Conn,Wentworth,
and familiesas muchas, 'ormorethan,localselectivefactors.
whichof the various
the questionregarding
are Therefore,
Blum,1980); t 17% ofall theCarolinaheterotrophs
features
associatedwithdioecyplaya
dioecious.
ecomorphological
willhaveto
causalrole,and underwhichcircumstances,
Pollinationmodesofdioeciousangiosperm
genera-Of be answeredfora numberof individuallineagesbefore
the799 generawithdioeciousspeciesforwhichthereare we can extrapolatefromcommonfeaturesto common
232 (30%) are causes.
sufficient
data on themodeofpollination,
resemblancesbetween
wind-or water-pollinated,
550 (68%) arepredominantly To controlfor phylogenetic
analyzing
and 14 (2%) havewindand insectpol- membersofthesamelineage,we arecurrently
insect-pollinated,
ofrecently
linationin closelyrelatedspeciesand sometimeswithin ourdioecydatasetwithintheframework
pubdata).
a species.Threegenera,theLiliaceaeCollospermum
and lishedmolecularphylogenies
(Renner,unpublished
(letterof 16
Astelia(Dobat and Peikert-Holle,
1985) and the Bala- However,as suggested
by D. Charlesworth
betweenand similarities
nophoraceaeDactylanthus
(Webband Kelly,1993),are March 1994) the differences
buttrioecious withinlineagesshouldtendto obscuregeneralpatterns;
pollinatedbybats.Anotherbat-pollinated
apparentwe
speciesisPachycereuspringlei
(Cactaceae;Flemming,
per- so, wheregeneralpatternsare nevertheless
sonalcommunication).
Freycinetia
(Pandanaceae)is pol- can accordthemsomeweight.
betweendioecyand
linatedbybirdsand bats(Cox, 1982).Whenthesefigures Atthefamilylevel,thecorrelation
but does not
are comparedto the ,:250 generawithbat-pollinated fleshyfruits(bioticdispersal)is significant
species(Dobat and Peikert-Holle,
1985) and 500 genera accountfora largeproportionof the variationamong
a This number
ofnondioecious
generapollinated
by insectswas arfromthetotalnumberof angiosperm
rivedat by subtracting
genera
(13,500) all thedioeciousgenera(959), 750 bird-and bat-pollinated
genera,874 generain familieswithsolelywind-or water-dispersed
withvariousdispersal
members,
andan estimated
600generainfamilies
modes.Thereare;250 bat-pollinated
genera(DobatandPeikert-Holle,
1985) and 500 bird-pollinated
genera(Porsch,1931 and our ownestimate).
604
AMERICAN JOURNAL OF
BOTANY
[Vol. 82
familiesin presenceor absenceofdioecy;at thegeneric ceae, Campanulaceae,Goodeniaceae,Lobeliaceae,and
level,bioticdispersal
appearstobe overrepresented
among otherfamiliesin the Asteridaeexhibita complexsyndioecists.
Theassociation
ofdioecywithfleshy
fruits
found organization
ofmaleandfemaleorgans,
fQrexample,with
in particularfloras(see the introduction)
likelyreflects pollenfirst
beingdepositedon and thenpresented
bythe
thecombinedeffects
of local samplingand multipleas- style(secondarypollenpresentation)
or withcongenital
sociationsamongthecorrelates
themselves.
Thus,forex- and postgenital
fusionofcarpels,petals,and stamens.A
ample,acrossall angiosperms
fleshyfruitsare strongly similarsynorganization
of male and femalestructures
correlated
withthetreegrowth
form(Ricklefs
andRenner, characterizes
manyFabaceae (forfurther
examples,see
in press),whichin turnpredominates
in certaintropical van der Pijl, 1978). All thisshouldmaketheontogenic
families.
suppressionof male or femaleorgans,withoutradical
Treegrowthaloneis notassociatedwithdioecyat the alterationsin the structural
organization
of the flower,
in themoreadvancedgroupsthanin the
familylevel,whilethe shrubgrowthformhas a weak moredifficult
positiveeffect
onlyin some analyses;climbinggrowth, less advancedones.
whetherwoodyor herbaceous,by contrasthas a strong
Modem familiesthathave managedto escape from
effect
onthepresenceofdioecy(possiblymech- suchconstraints
enhancing
are,e.g.,theApiaceae,Araliaceae,and
anismsforthisassociationaresuggested
below).The sup- Asteraceae(the latterin spiteof secondarypollenpreall ofwhichhavesmallflowers
posed correlation
betweenwoodinessper se and dioecy sentation),
into
aggregated
has led variousauthors(e.g.,Lloyd,1982)to hypothesize inflorescences
and all ofwhicharecapableofsuppressing
in some flowers.
abouta particular
needforobligatory
inlong- sexualfunction
outbreeding
Theyhave andromonlived,woodyplantsdue to geneticloads. Anothersug- oeciousand gynomonoecious
species,yetrelatively
little
gestionrelateswoodinessanddioecyvia themoreintense dioecy(sixof403 generaand :z34 of3,100speciesin the
in theclimaxhabitatswherethese Apiaceae,fourof 47 generaand ;:69 of 800 speciesin
selectionforheterosis
plantsoccur(Bell, 1982). The presentanalysisprovides the Araliaceae,and 26 of 1,509 genera,and ;:526 of
littleempiricaljustification
20,000 speciesin theAsteraceae).
forthesehypotheses.
A secondcorrelateof dioecy(and monoecy)is polliDioecy is strongly
associatedwithmonoecy,abiotic
pollination,and climbinggrowth.We willnow address nationbywindorwater.Severalcausativefactors
forthe
possiblemechanisms
thesethreeassociations. associationbetweendioecyand abioticpollinationhave
underlying
The singlemostimportant
predictor
ofa group'stendency beensuggested
(Darwin,1876;Kerner,1895;vanderPijl,
to acquiredioecyis thepresenceofmonoecyin thegroup 1978; Freeman,Harper,and Ostler,1980).In wind-pol(as also foundbyYampolskyand Yampolsky,1922,and linatedplants,pollen release may requirependulous,
Lewis,1942).As pointedoutbyWestergaard
(1958),the shakingstamenswhereaspollencapturemayfavorlarge,
hydrophilous
plantshave
generaldirectionof evolutionary
changeis likelyto be erect,freestigmas.Similarly,
frommonoecyto dioecy;clearly,however,phylogenetic floralmechanisms
forthecaptureofwater-borne
pollen
interfere
withmechanisms
forthedispersal
analysesof individualexamplesare neededto support thatphysically
thisassumption.
The routefrommonoecyto dioecymay of pollen(Cox, 1988, 1991). Also,theimprecisemovebe especiallycommonbecause once a lineagehas the mentofpollenbywindorwateris likelytocausefrequent
in an her(in theabsenceofself-incompatibility)
physiological
and morphological
abilityto suppressmale selfing
in someflowers,
abioticpollinationshouldfavor
or femalefunction
Therefore,
thesubsequentstep maphrodite.
to dioecymay occurthroughdivergent
thelatterthenapparently
of unisexualflowers,
facilitating
adjustments
floralsex ratiosbetweenindividualplants(Lloyd,1972; theevolutionofdioecyfrommonoecy.Supportforsuch
McArthur
et al., 1992).It maybe easierforstrictly
comes fromrelativelyfewstudiesof
mon- an interpretation
oecious populationsto evolve dioecy(since mutations changesin breedingsystemin connectionwithchanges
mode.InAcer(Hesse,1979)andThalictrum
affecting
pollenand ovuleproduction
mustalreadyhave inpollination
occurredin theirunisexualflowers)
thanforpopulations (Kaplan and Mulcahy,1971) a switchin some species
thatproducebisexualflowers,
be theygynomonoecious, frominsecttowindpollination
accompaniedtheacquisiand dioecy;whileHesse
andromonoecious,polygamo-monoecious,gynodio- tionofdicliny,
polygamodioecy,
to have precededdiclinyin Acer,
or trioecious.Indeed,how fre- interprets
anemophily
ecious,androdioecious,
in
quentlygynodioecyhas led towarddioecy is unclear Kaplanand Mulcahyfavortheoppositeinterpretation
studiesmayeventually
andCharlesworth,
Phylogenetic
(Charlesworth
permit
1978;GouyonandCou- Thalictrum.
us toestablishtheevolutionary
vet,1987; Wellerand Sakai, 1991; Barrett,
sequenceofeventsinboth
1992).
in theless genera.In tropical,entomophilous
Whyare dioecyand monoecyconcentrated
Fagaceae,diclinyand
to a lateracquiadvanceddicotsin spiteof thefactthatveryfewofthe monoovulymayhave beenpreadaptive
mostprimitiveextantMagnoliidaeare wind-pollinated sitionofanemophily
as suggested
byvan derPijl (1978).
frombisexualto uni(Endress,1990a)? We believethatthereasonhas to do In stillothergroups,thetransition
was notassociatedwitha switchfrominwithfloralmorphological
theirab- sexualflowers
constraints,
or,rather,
sence.In primitive
floralphyllotaxis
is rel- sectsto wind,and in thesetaxa,insectpollinationmay
angiosperms,
to do withtheevolutionof dioecy,albetweenmale have something
ativelyplastic,andthereis littleintegration
forsuchan effect
and femalefloralparts(Endress,1987, 1990b). In the thoughthemechanism
(increasedselfing
more advancedgroups,by contrast,numbersof floral ratesin partsof the rangewithdifferent
pollinatorbeandstructures
haveevolved havior?)is unclear.
partsoftenarelowand fixed,
to directpollinatormovementor to concealnectar(usuThirdly,dioecyis strongly
associatedwithclimbing
orepigyny,
andzygomorphy). growth,
ofwhether
irrespective
allyvia perigyny
theplantis a woodyliana
sympetaly,
Apocynaceae,Asclepiadaceae,Brunoniaceae,Calycera- oran herbaceousvine.Familieswithclimbers,
as a group,
May 1995]
RENNER AND RICKLEFS-DIOECY
IN THE FLOWERING PLANTS
605
seemtohavea combination
offeatures
predisposing
them
LITERATURE CITED
todioecy,namelyhighincidence
ofmonoecy,
fleshy
fruits,
and tropicaldistribution.
However,thepositiveeffect
of
theclimbing
habiton a family's
likelihoodofcomprising BAKER, H. 1959. Reproductive methods as factorsin speciation in
floweringplants. Cold Spring Harbor Symposiumin Quantitative
dioeciousspeciesis independent
oftheseothervariables
Biology 24: 177-19 1.
(Table 2). We suspectdifferential
selectionforoptimal BARR=r, S. C. H. 1992. Gendervariationand theevolutionofdioecy
resourceallocationto sexualfunction
to be responsible
in Wurmbeadioica (Liliaceae). JournalofEvolutionaryBiology 5:
An increasein femalefloralallocationwith
forthiseffect.
423-444.
increasedplantsizehasbeenfoundinseveralmonoecious BAWA,K. S. 1980. Evolution of dioecy in floweringplants. Annual
Review ofEcology and Systematics11: 15-39.
climbers(Bickeland Freeman,1993). This impliesre1994. Pollination of tropicaldioecious angiosperms:a reassourcelimitations
to fruitsetbelowa certainthreshold,
sessment?No, not yet.AmericanJournalof Botany 81: 456-460.
andin Cucurbitapepo
is indeedstrongsubsequent
growth
, AND P. A. OPLER. 1975. Dioecism in tropical foresttrees.
lyinhibitedafterthefirst
fruitis produced(Nitschet al.,
Evolution 29: 167-179.
1952).Ifrapidupwardgrowth
is ata premium
inclimbers BELL, G. 1982. The masterpieceof nature.Croom Helm, London.
and if fruitset at least temporarily
inhibitsgrowthor BICKEL,A. M., AND D. C. FREEMAN. 1993. Effectsofpollen vectorand
plant geometryon floralsex ratio in monoecious plants.American
requirestheproductionof a thick,slowlygrowing
stem
Midland Naturalist 130: 239-247.
to supportheavyfruits,
itmightbe advantageous
topostR. K. 1992. Vascular plant families and genera. Royal
If the effect
pone femaleness.
is strong,thismay favor BRummITr,
Botanic Gardens, Kew.
male plants.Structural
necessitiesmayalso favorsepa- CHARLESWORTH, B., AND D. CHARLESWORTH.1978. A model forthe
rationofthesexes,withflowers
bearingfruit
better
placed
evolutionofdioecy and gynodioecy.AmericanNaturalist112: 975997.
onthicker
stemsandpollen-dispensing
flowers
onthinner,
ofdioecyand self-incompatCHARLEsWORTH,
D. 1985. Distribution
moreexposedmodules.
ibilityin angiosperms.In P. J. Greenwood and M. Slatkin [eds.],
The nearabsenceof birdand bat pollinationamong
Evolution: essays in honour of John Maynard Smith, 237-268.
dioeciousplants(Table 14) maybe explainedbythefact
Cambridge UniversityPress, Cambridge.
thatvertebrate
pollinationrequiresadaptationsoffloral CoNN,J. S., T. R. WENTWORTH, AND U. BLUM. 1980. Patternsof
whichseemsto almostprecludethe evomorphology,
dioecism in thefloraoftheCarolinas.AmericanMidland Naturalist
103: 310-315.
lutionof dicliny.First,pollinationby large-bodied
animals,suchas birdsand bats,requireslargequantitiesof Cox, P. A. 1982. Vertebratepollinationand themaintenanceofdioein Freycinetia.AmericanNaturalist 120: 65-80.
nectar(Opler,1983),whichcanbe offered
adequately
only - cism1988.
Hydrophilous pollination.Annual Review of Ecology
.
in cups,tubes,orspurstypically
formed
byconcavefloral
and Systematics19: 216-280.
receptacles
(oftenwithinferior
ovaries)and/orfusedpet1990. Pollination and the evolution of breedingsystemsin
als (sympetaly).
Secondly,pollinationby thesevectors
Pandanaceae. Annals of the Missouri Botanical Garden 77: 816840.
requiresrelatively
largequantitiesof pollen,whichare
1991. Abiotic pollination:an evolutionaryescape foranimaloftenproducedby numerousstamens(secondarypolypollinated angiosperms.Philosophical Transactions of the Royal
and secondary
andry).Inferior
ovaries,sympetaly,
polySociety of London B 333: 217-224.
oftherelatively
advancedsubclasses
andryareattributes
evolution
1993. Hydrophilouspollinationandbreedingsystem
butnearlyabsentin
Dilleniidae,Rosidae,and Asteridae,
in seagrasses:a phylogeneticapproach to the evolutionaryecology
theMagnoliidaeandHamamelidae(Cronquist,
1988;Enof Cymodoceaceae. Botanical Journalof theLinnean Society 113:
con217-226.
dress,1990b).Thusthereis a strongmorphological
straint
on vertebrate
pollination.
Indeed,ofthecirca250 CROAT, T. B. 1979. The sexualityof the Barro Colorado Island flora
(Panama). Phytologia42: 319-348.
generawithbat-pollinated
speciesknownin the angioCRoNQuIsT, A. 1988. The evolution and classificationof flowering
none
and
to
sperms(Dobat
Peikert-Holle,
1985),
belong
plants, 2d ed. Columbia UniversityPress, New York, NY.
theMagnoliidaeand Hamamelidae,while28% arein the DARWIN,C. 1876. The effectsof cross and self fertilisationin the
Rosidae,26% in theAsteridae,25% in theDilleniidae,
vegetablekingdom.JohnMurray,London.
13%inthemonocots,and 8% in theCaryophyllidae.
The DOBAT, K., ANDT. PEIKERT-HoLLE. 1985. BlutenundFledermaiuse.
Verlag von Waldemar Kramer,Frankfurt.
distributions
ofbat pollinationand dioecyin theangioDONOGHUE,M. J. 1989. Phylogeniesand the analysisof evolutionary
exclusive.
spermsare thusalmostmutually
sequences, with examples fromseed plants. Evolution 43: 1137Whiletheenvironmental
conditions
underwhichpop1156.
ulationschangebreedingsystemswill have to be ad- ENDRESS, P. K. 1987. Floral phyllotaxisand floralevolution. Botanin allianceswithrelatively
dressedexperimentally
labile
ische Jahrbiicherflir
Systematik108: 417-438.
sex expression,such as Begonia, Atriplex,or Wurmbea
etal.,,1992),theglobalanalysis
(Barrett,
1992;McArthur
famthatacrossall angiosperm
heresuggests
performed
conandclimbing
iliesmonoecy,
windpollination,
growth
favortheevolutionofdioecy.Othertraits,such
sistently
as heavy,fleshy
fruits,
mayplaya rolein certainlineages.
Wherethe ontogenetic
floraladjustmentsrequiredfor
unisexualflowersare possiblewithout
jeopardizingpollination,specializationforone sexualfunctionappears
favoredbyselectionundera widerangeofenvironmental
conditions
as is apparentfromourfinding
thatgeographic
distribution
has no strongeffect
on presenceor absence
ofdioecy.
1990a. Evolution of reproductivestructuresand functionsin
primitiveangiosperms(Magnoliidae). Memoirs of the New York
Botanical Garden 55: 5-34.
1990b. Patternsof floralconstructionin ontogenyand phylogeny.Biological Journalof theLinnean Society39: 153-175.
Fox, J. F. 1985. Incidence of dioecy in relationto growthform,pollination and dispersal. Oecologia 67: 244-249.
FREEMAN, D.
C., K. T. HARPER, AND W. K. OSTLER. 1980. Ecologyof
plantdioecyin theintermountain
regionofWesternNorthAmerica
and California.Oecologia 44: 410-417.
, E. D. McARTHuR, AND K. T. HARPER. 1984. The adaptive
significanceof sexual labilityin plants usingAtriplexcanescens as
a principalexample. Annals of the Missouri Botanical Garden 71:
265-277.
S. C. SANDERSON, AND A. R. TIEDEMANN. 1993. The
606
AMERIcAN JOURNAL OF BOTANY
influenceof topographyon male and femalefitnesscomponentsof
Atriplex
canescens.Oecologia93: 538-547.
GENmy, A. 1991. The distributionand evolution of climbingplants.
In F. E. Putz and H. A. Mooney [eds.], The biology of vines, 349. Cambridge UniversityPress, Cambridge.
GIVNISH,T. J. 1980. Ecological constraintson theevolutionofbreeding
systemsin seed plants:dioecy and dispersalin gymnosperms.Evolution34: 959-972.
GOUYON,P.-H., AND D. COUVET. 1987. A conflictbetweentwo sexes,
femalesand hermaphrodites.In S. C. Stearns[ed.], The evolution
of sex and its consequences. BirkhauserVerlag,Basel.
HART, J. A. 1985. Evolution of dioecism in Lepechinia Willd. sect.
Parviflorae(Lamiaceae). SystematicBotany 10: 147-154.
HEsLoP-HARRsoN, J. 1957. The experimentalmodificationof sex
plants.Biological ReviewsoftheCambridge
expressionin flowering
Society32: 38-90.
Philosophical
und Verteilungdes Pollenkittsin der
HESSE,H. 1979. Ultrastruktur
GattungAcer (Aceraceae). Plant Sysinsekten-und windbliutigen
tematics
and Evolution131: 277-289.
G., ANDK. OYAMA. 1992. Ecological correlates
IBARRA-MANRiQuEz,
ofreproductivetraitsofMexican rainforesttrees.AmericanJournal
of Botany 79: 383-394.
KAPLAN, S. M., AND D. L. MuLcAHY. 1971. Mode of pollinationand
floralsexualityin Thalictrum.
Evolution
25: 659-668.
gracilis(Nepenthaceae)
KATO,M. 1993. Floral biology of Nepenthes
in Sumatra.AmericanJournalof Botany 80: 924-927.
KERNER VONMARIAUN, A. 1895. Pflanzenleben,
vol. 2. Bibliographisches Institut,Leipzig.
KUBIrzKI, K., J. G. ROHWER, AND V. BrTRIucH[EDS.]. 1993. The
Berfamiliesand generaof vascular plants,vol. 2. Springer-Verlag,
lin.
LAHAv-GINoTT,S., AND Q. C. B. CRoNK. 1993. The matingsystem
ofElatostema(Urticaceae) in relationto morphology:a comparative
andEvolution186: 135-145.
study.PlantSystematics
LEWIS,D.
1942. The evolution of sex in floweringplants. Biological
Philosophical
Society17: 46-67.
ReviewoftheCambridge
[Vol. 82
NrrscH,J. P., E. B. KURz, J. L. LIVERMAN, AND F. W. WENT. 1952.
The developmentof sex expressionin cucurbitflowers.American
JournalofBotany 39: 32-43.
OPLER,P. A. 1983. Nectar productionin a tropicaLecosystem.In B.
Bentleyand T. Elias [eds.], The biology of nectaries,30-79. Columbia UniversityPress, New York, NY.
PoRscH, 0. 1931. Grellrotals Vogelblumenfarbe.Biologia Generalis
7: 647-674.
RENNER,S. S., AND J. P. FEIL. 1993. Pollinatorsof tropicaldioecious
angiosperms.AmericanJournalof Botany 80: 1100-1107.
RIcHARDs,A. J. 1986. Plant breeding systems.Allen and Unwin,
Winchester,MA.
RICKLEFS,R. E., AND S. S. RENNER. 1994. Species richnesswithin
familiesof floweringplants. Evolution 48, in press.
INc. 1988. SAS/STAT (TM) user'sguide,Release 6.03
SAS INSTITUrE,
ed. SAS Institute,Inc., Cary,NC.
K. R. 1949. A new approach to the problemof the primitive
SpoRNiE,
flower.New Phytolologist48: 259-276.
STEBBINS, G. L. 1950. Variation and evolution in plants. Columbia
UniversityPress, New York, NY.
of angiosperm
1951. Natural selectionand the differentiation
families.Evolution 5: 299-324.
K. E. 1988. Dioecism and its correlatesin the Cape floraof
STENmER,
South Africa.AmericanJournalof Botany 75: 1742-1754.
THOMAS,
S. C., AND J.V. LAFRANKIE.
1993. Sex,size,and interyear
variation in floweringamong dioecious treesof the Malayan rain
forest.Ecology 74: 1529-1537.
THOMSON, J.D., ANDS. C. H. BARRErr. 1981. Selectionforoutcrossing,
sexual selection,and the evolution of dioecy in plants. American
Naturalist 118: 443-449.
fortheevolutionofdioecy
, AND J.BRUNET. 1990. Hypotheses
in seed plants. Trendsin Ecology and Evolution 5: 11-16.
THORNE,R. F. 1992. Classificationand geographyof the flowering
plants. Botanical Review 58: 225-348.
VAN DER PuL, L. 1978. Reproductiveintegrationand sexual disharmony in floralfunctions.In A. J. Richards [ed.], The pollination
of flowersby insects,79-88. Academic Press, London.
LIOYD, D. G. 1972. Breedingsystemsin Cotula L. (Compositae, Anbiologyof the
1993. The reproductive
themideae). New Phytologist71: 1181-1194.
WEBB, C. J.,AND D. KELLY.
New Zealand flora.Trendsin Ecology and Evolution 8: 442-447.
1982. Selection of combined versus separate sexes in seed
plants. The AmericanNaturalist 120: 571-585.
WEBSTER, G. L. 1994a. Classificationof the Euphorbiaceae.Annals of
theMissouri Botanical Garden 81: 3-32.
MABBERLEY, D. J. 1987. The plant-book.CambridgeUniversityPress,
1994b. Synopsis of the genera and supragenerictaxa of EuCambridge.
S. C. SANDERSON,
phorbiaceae.Annals oftheMissouri Botanical Garden 81: 33-144.
E. D., D. C. FREEMAN,L. S. LUCKINBILL,
McARTHuR,
ANDG. L. NOLLER. 1992. Are trioecyand sexuallabilityinAtriplex WELLER, S. G., AND A. K. SAKII. 1991. The geneticbasis of male
in Schiedea (Caryophyllaceae),an endemicHawaiian genus.
canescens geneticallybased?: evidence fromclonal studies. Evosterility
Heredity67: 265-273.
lution46: 1708-1721.
in
M. 1958. The mechanismof sex determination
WESTERGAARD,
McCoMB, J. A. 1966. The sex formsof species in the flora of the
dioecious floweringplants.Advances in Genetics9: 217-281.
south-westof westernAustralia.AustralianJournalof Botany 14:
303-316.
YAMPOLSKY,
C., AND H. YAMPOLSKY.1922. Distributionof sex forms
in the phanerogamicflora.BibliothecaGenetica 3: 1-62.
MuENcHow, G. E. 1987. Is dioecy associated withfleshyfruit?Amer-
icanJournalofBotany74: 287-293.