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Dioecy and Its Correlates in the Flowering Plants

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Dioecy and Its Correlates in the Flowering Plants AmericanJournal of Botany 82(5): 596-606. 1995. DIOECY AND ITS CORRELATES IN THE FLOWERING PLANTS SUSANNE S. RENNER2 AND ROBERT E. RICKLEFS Instituteof SystematicBotany, University of Mainz, Bentzel-Weg 2, D-55099 Mainz,Germany; and Departmentof Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6018 Considerableeffort has beenspent documenting correlations between dioecy and variousecological and morphological traitsfor the purpose of testing hypotheses about conditions that favor dioecy. The dataanalyzed in thesestudies, with few exceptions,come from local floras,within which it was possibleto contrastthe subsets of dioecious and nondioecioustaxa withregard to thetraits in question.However, if there is a strongphylogenetic component to thepresence or absenceof dioecy,regional sampling may result in spuriousassociations. Here, we reportresults of a categoricalmultivariate analysis ofthe strengths ofvarious associations of dioecy with other traits over all floweringplants. Families were scored for presence ofabsence of monoecy or dioecy,systematic position, numbers of speciesand genera,growth forms, modes of pollination and dispersal,geographic distribution, and trophicstatus. Seven percent of angiospermgenera (959 of 13,500)contain at least some dioeciousspecies, and ;6% of angiospermspecies (14,620 of 240,000) are dioecious.The mostconsistent associationsin thedata setrelate the presence of dioecyto monoecy,wind or waterpollination, and climbinggrowth. At boththe family and thegenus level, insect pollination is underrepresentedamong dioecious plants. At thefamily level, a positivecorrelation between dioecy and woodygrowth results primarily from the association between dioecy and climbing growth(whether woody or herbaceous)because neither the tree nor the shrub growth forms alone are consistently correlated witha family'stendency to includedioecious members. Dioecy appears to have evolvedmost frequently via monoecy, perhapsthrough divergent adjustments of floralsex ratiosbetween individual plants. Monoecy itself is relatedto abiotic pollinationand climbinggrowth as revealedby multivariateanalysis. Dioecy and monoecyare concentratedin theless advancedsuperorders of Thorne (1992) and subclassesof Cronquist (1988). The frequencyof dioecy found in a local flora thereforereflects the level of dioecy in itsparticular pool offamilies as muchas, or morethan, local selectivefactors. The positiveassociations of dioecy with abiotic pollination and monoecyare related to floraldevelopmental and morphological attributes,as is thenegative association with bird and bat pollination;the positive association of dioecywith climbing growthis tentativelyexplained in termsof differential selection for optimal resource allocation to sexualfunction. If rapid upwardgrowth is at a premiumin climbersand iffruit set at leasttemporarily inhibits growth or requiresthe production ofthicker, more slowly growing stems to supportheavy fruits, it mightbe advantageousto postponefemaleness. Ifthe effect is strong,this may favor male plants. Over thepast 15 yrconsiderable effort has been spent fruitsand frugivore-dispersedseeds (Bawa, 1980; Giv- documentingcorrelations between dioecy and various nish,1980; Steiner, 1988; Ibarra-Manriquez and Oyama, morphologicaland ecologicaltraits for the purposeof 1992;but see Fox, 1985;Muenchow, 1987; Thomson and testinghypotheses about conditionsthat favor dioecy. Brunet,1990), small flowers (Bawa and Opler,1975; Fox, Ecologicalcorrelates attracted attention in particularbe- 1985;Ibarra-Manriquez and Oyama,1992), white to yel- cause dioecyhas provendifficult to explainsimply as an low or greenishflowers (Bawa and Opler,1975; Muen- outbreedingmechanism in taxa lackingself-incompati- chow,1987), water pollination (Cox, 1988),and so-called bility(for discussionsof this issue, see Charlesworth unspecializedinsect pollinators (Bawa and Opler,1975; and Charlesworth,1978; Thomsonand Barrett,1981; Bawa, 1994; contraRenner and Feil, 1993). Charlesworth,1985; Thomson and Brunet,1990). At dif- While older reportstested the associationsbetween ferentspatial and hierarchicalscales, dioecyhas been dioecyand particularattributes separately, more recent associatedwith, among other attributes, wind pollination oneshave used multivariateanalysis, taking into account (Darwin, 1876; Kerner,1895; Sporne,1949; Stebbins, correlationsamong some of the explanatoryvariables 1951; Kaplanand Mulcahy,197 1; Freeman,Harper, and themselves(Fox, 1985; Muenchow,1987; Steiner,1988; Ostler,1980; Muenchow, 1987; Steiner,1988), monoecy Ibarra-Manriquezand Oyama,1992). Some authors have (Yampolskyand Yampolsky,1922; Lewis, 1942; Wes- attemptedto incorporatephylogenetic information in tergaard,1958; McComb,1966; Lloyd,1982), perennial analysesof the association of dioecy with other traits by growthand lignified secondary xylem, or woodiness (Dar- lookingat thespecies, genus, and familylevels separately win, 1876; Stebbins,1950; Baker, 1959; Croat, 1979; or by restrictinganalyses to monophyleticgroups (Hart, Conn, Wentworth,and Blum, 1980; Freeman,Harper, 1985; Donoghue,1989; Cox, 1990, 1993; Lahav-Ginott and Ostler,1980; Fox, 1985;but see Steiner,1988), fleshy and Cronk,1993). Thedata analyzed in these studies, with a fewexceptions 1 Manuscriptreceived 19 May 1994;revision accepted 23 November suchas Cox's (1990, 1993)phylogenetic analyses, all come 1994. fromlocal floras.Such locallycircumscribed data allow The authorsthank D. Charlesworth,P. Cox, P. Endress,C. Freeman, one to contrastthe subsets of dioecious and nondioecious S. Heard,J. Kohn,-J. Thomson,and K. Bawa forcomments on the taxawith regard to particularecological and morpholog- manuscript;and P. Berry(Onagraceae), H.-J. Esser (Euphorbiaceae), S. Knapp(Solanaceae), J. Kuijt (parasitic angiosperms), C. Ott(Menisper- ical traitsof interest.For example,the relationships be- maceae),and J.Rohwer (Lauraceae) for information on dioecyin par- tweena particularfloral color or size and dioecycan be ticulargroups. analyzedonly if floral colors or sizes forthe universe of 2 Authorfor correspondence. nondioeciousspecies are known.At present,this is pos- 596 May 1995] RENNER AND RICKLEFS-DIOECY IN THE FLOWERING PLANTS 597 sible onlyon a local basis. No studyhas yetaddressed (1988) and the 28 superordersof Thorne(1992); total the correlatesof dioecyin the floweringplants at large, numberof genera (in thefamily data set)and numberof and some apparentassociations among dioecy and par- dioeciousspecies (in thegenus data set);growth forms; ticulartraits may, therefore, be theresult of regionalef- modesof pollinationand dispersal;geographic distribu- fects,particularly if thereis a strongphylogenetic com- tion; and trophicstatus. Genera accepted are those of ponentto thepresence or absenceof dioecy.As longas Brummitt(1992); familiesare those of Cronquist (1988), suchsampling problems remain unrecognized they may exceptthat in 18 cases morerecent, broader family con- resultin theintroduction of unnecessary ad hoc hypoth- ceptswere accepted. To look at theeffects of differences eses to explainsupposed correlations that did notplay a in familialconcepts, the data setswere also brokendown causal rolein theevolution of dioecy. intothe more narrowly circumscribed families of Thorne Here we reportresults of a studyin whichwe have (1992). determinedthe relative strengths of various associations Dioecyand monoecywere scored as presentin a family betweendioecy and particulartraits across all flowering whenat least one speciesin thatfamily is dioeciousor plants.Because we use a multivariateapproach, the pos- monoecious.Particularly in thecase offamilies with few sibilityof fortuitous associations among the traits them- dioecioustaxa great care was taken to searchthe literature selvesis reduced.Our analysis, to somedegree, also takes forindependent confirmation of theirdioecious status. care of phylogeneticbias because it is not restrictedto Numeroustaxa (:20 familiesand ;:200 genera)listed as particularfamilies that happen to dominatelocal floras includingdioecious species by Yampolskyand Yampol- (see Steiner,1988, for a particularlystriking example of sky(1922) had to be removedfrom the data set,either thiseffect in theCape floraof SouthAfrica). It is based becausethe supposedly dioecious plants have turnedout on a newcompilation of dioecious angiosperm genera and to be sex-changing,polygamous, monoecious, or gyno- families,the onlyprevious such compilationby Yam- dioecious,or because of nomenclaturaland taxonomic polskyand Yampolsky(1922) beingoutdated. Systema- changes.Yampolsky and Yampolskybased theircom- tists'views of the phylogeneticrelationships within the pilationon Englerand Prantl's NatiirlichePflanzenfamili- angiospermsand the circumscriptionand systematic en and thevolumes of Engler'sPflanzenreich published placementof numerous genera have changedduring the by 1912. Theyconcluded that out ofthe total of 10,113 past 70 yr,new cases of dioecyhave been reported,and angiospermgenera then recognized, 972 (9.6%)comprised manyothers mentioned by Yampolskyand Yampolsky dioeciousand/or polygamodioecious species. However, have turnedout to be in error.In anotherpaper, the same theirlist includesat least 90 generasince mergedwith data set willbe used to studythe distribution of dioecy othergenera; some, such as Streblus,are listed eight times in theframework of recently published angiosperm phy- underdifferent names. There are also 43 unpublished logenies(Renner, unpublished data). names(nomina nuda),
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