Reversal in Ovary Position from Inferior to Superior in the : Evidence from Floral Ontogeny Author(s): Michael G. Simpson Reviewed work(s): Source: International Journal of Sciences, Vol. 159, No. 3 (May, 1998), pp. 466-479 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/2475232 . Accessed: 26/07/2012 14:32

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http://www.jstor.org Int. J. Plant Sci. 159(3):466-479. 1998. C 1998 by The Universityof Chicago. All rightsreserved. 1058-5893/98/5903-0005$03.00

REVERSALIN OVARYPOSITION FROM INFERIOR TO SUPERIORIN THEHAEMODORACEAE: EVIDENCEFROM FLORAL ONTOGENY

Michael G. Simpson' Departmentof Biology, San Diego State University,San Diego, California92182-4614, U.S.A.

Floral anatomy and development were studied in Wachendorfiathyrsiflora and Lachnanthes caroliniana of the monocot family Haemodoraceae in order to evaluate the hypothesisthat a superior-ovaryposition arose from an ancestral inferior-ovariedcondition. In Wachendorfiathree conduplicate carpel primordiadevelop at the floralapex, followed by postgenitalfusion forming a superiorovary. The lower receptaculartissue at thecentral floral axis elongates at about the same extentas the peripheralreceptacular tissue. In the extended receptacularregion, two lateral com- missures develop by differentialtissue growth,followed by differentiationof inner epithelial cells to form septal nectaries. The receptacularcommissures and nectaries are continuous with carpellary commissuresof the superior ovary. Junctionof the median outertepal vein and dorsal carpellaryvein occurs well below the septal nectariesat the base of the receptacle. In Lachnanthes threesmall, conduplicatecarpel primordiadevelop at the floralapex. Growth of the lower receptaculartissue at the centralfloral axis is relativelyretarded, such thatthe peripheraltissues elongate differentially,surrounding the now laterallypositioned carpels. Subsequent postgenitalfusion results in an inferior- ovary position, relative to perianthinsertion. Incomplete postgenitalfusion of intercarpellaryspaces results in the formationof septal commissures.These commissureslater matureinto septal nectaries,which extend to the apex of the inferiorovary. Junctionof the median outer vein and dorsal carpellaryvein occurs just beneath the ovary locules. It is proposed thatthe floralreceptacular region of Wachendorfiaand of othersuperior-ovaried Haemodoraceae is homologous withan ancestralinferior ovary withregard to position,development, and vasculature.A superiorovary in the Haemodoraceae arose by the co-option of an ancestralinferior ovary into an elongated receptacle,along with extension of the intercarpellarycommissures to the peripheryof the receptaculartissue, and modificationof those peripheralcommissures to nectaries. The adaptive significanceof this evolutionaryevent is unclear but apparently relatedto a shiftin pollinationmechanism. Introduction phology, anatomy,palynology, and karyology,Simp- son (1990) proposed that the common ancestor of The position of the ovary-whether superior,infe- extantHaemodoraceae possessed an inferiorovary and rior,or intermediate-has long been consideredan im- that a change in ovary position, fromsuperior to in- portant,phylogenetically informative character in sys- ferior,was a unique evolutionaryevent shared by all tematicstudies. Within the angiospermsas a whole, an familymembers. However, this study also concluded inferiorovary has been assumed by many botaniststo that a second change in ovary position,from inferior be a derived and irreversiblefeature (Bessey 1915; to superior,occurred for a single clade of the Hae- Sporne 1975; Cronquist 1981). Although an inferior- modoraceae, constitutingan apomorphy(portrayed in ovary position has evolved numeroustimes in various the analysis as an evolutionaryreversal) for all five taxonomic groups,its adaptive significanceis not cer- superior-ovariedgenera of the family(Simpson 1990). tain. It may have arisen in some groups because of The latter findingwas problematicin that, as men- selective pressureby floralherbivores or pollinatorsor tioned above, a reversal in ovary position,from infe- in responseto an adaptive advantagecaused by greater rior back to superior,generally has been viewed as protectionof or increased energy allocation to very unlikely;in addition,no obvious adaptive signif- developing ovules (Grant 1950; Stebbins 1974). icance was recognized for such a reversalin the Hae- Ovary position is uniformwithin virtuallyall an- modoraceae (Simpson 1990). giosperm plant families. One exception is the mono- A more recent studyof floralanatomy in the Hae- cotyledon family Haemodoraceae. The Haemodora- modoraceae (Simpson 1993) demonstratedthe occur- ceae are a monophyletic group consisting of 13 rence of three major types of septal nectaries,based currentlyrecognized genera and ca. 100 species on theirnumber per flowerand theirposition relative (Simpson 1990; Anderbergand Eldenas 1991; see also to otherfloral parts. One of these septal nectarytypes, MacFarlane et al. 1987), with distributionsspanning termed "infralocular,"is characterizedby having two Australia, South Africa, South and Central America, septal nectarieslocated almost entirelywithin the re- and eastern North America. Of the 13 genera in the ceptaculartissue, well beneaththe locules of the ovary family,five (Barberetta,Schiekia, Pyrrorhiza,Wach- but withinthe verticalplane of the ovary septa (Simp- endorfia,and Xiphidium) have a superiorovary; the son 1993). Interestingly,the infralocularseptal nectary othereight genera have an inferiorto half-inferiorova- type is found exclusively in four of the five genera ry. Based on a cladistic analysis using data frommor- with a superior ovary: Barberetta, Schiekia, Pyrror- hiza, and Wachendorfia.The other superior-ovaried I E-mail [email protected] , Xiphidium,lacks any trace of nectariesin both Manuscriptreceived July 1997; revisedmanuscript received Decem- of its species. (As reviewed in Simpson [1993], Smets ber 1997. and Cresens [1988] proposed that the name "gyno-

466 SIMPSON-REVERSAL IN OVARY POSITION 467

pleural" nectary replace that of "septal" nectaryin scope images were photographedand subsequentlyscanned. orderto indicatepossible homologybetween nectaries Voucher informationis as follows: Wachendorfiathyrsiflora that occur on outer carpellarysurfaces and those oc- L.-R. Ornduff7691 (UC); Lachnanthescaroliniana (Lam.) curringinternally. I chose to retainthe term "septal" Dandy [L. caroliana (Lam.) Dandy]-M. G. Simpson nectaryin the 1993 and the presentarticle because of 14VI80A (DUKE); Dilatris pilansii Barker-P V. D. Meri- we 30X81-2 (STEU); Haemodorumspicatum R. Br.-M. G. its more widespread use in comparative literature.I Simpson 16IX81C (DUKE); Philydrumlanuginosum Gaert- recognize the fact that some "septal" nectariesin the ner-E. E Constable; U. Hamann 959 (NSW); Pontederia Haemodoraceae do not, in fact, occupy the septal cordata L.-M. G. Simpson 28IX81A (DUKE). regions; however,these nectariesare always vertically In orderto bettervisualize the spatial distributionof major aligned along the septal planes of the ovary and are floral components,sequential cross-sections of flowers or hypothesizedto be positionallyhomologous to septal flower buds were examined along two radii: one along a nectariesthat are actuallypositioned within ovary sep- midlocularregion and the otheralong an adjacent (in Wach- ta.) endorfia)or opposite (in Lachnanthes) midseptalregion. At This raises two importantquestions. First,what is intervalsof 1-10 sections, measurementswere recorded on the evolutionarysignificance of the derivedseptal nec- a data sheet fromthe centerof the flowerto various floral components,including veins and the boundaries of the loc- tary anatomyin the above four superior-ovariedgen- ule, septal nectary,ovary surface,, and . These era? And, second, is the evolutionof thatderived anat- were graphicallyimaged using the computersoftware Free- omy correlated with the occurrence of a putatively hand by Macromedia (Macintosh version 5.5). Using this derived superior-ovaryposition in these taxa? Two of software,rulers were set up on X and Y axes corresponding the four genera with infralocular septal nectaries, to micrometermeasurements. For each floral component Wachendorfiaand Schiekia, are unique in having peri- (e.g., dorsal vein) interconnectingpoints were placed using anth "apertures" (Ornduffand Dulberger 1978; see the curved line function,each point correspondingto the Simpson 1990, 1993), which consist of two lateral, vertical distance from an arbitrarypedicel base and to the cup-shaped cavities at the receptacularregion of the horizontaldistance fromthe flowercenter. Some lines were flowerinto which nectaris secreted,which is exposed closed and the areas shaded to representvarious floralcom- ponents. The final graphics representswhat is, in effect,a to the outside (fig. 2). The perianthapertures are de- longitudinalsection of the flower. limitedby decurrenttepal marginsthat form surround- For scanning electron microscopy (SEM) observations, ing flaps of tissue thatappear as an opening,hence the buds were dissected to reveal criticalorgans, dehydratedto term"aperture." A narrowchannel leads distallyfrom 100% ethanol,and thengradually infiltrated to 100% Freon the aperturesto an opening at the frontof the flower, 113 or methylal, (dimethoxymethane).The material was allowing nectar to be siphoned by an insect (fig. 1). placed in a metal capsule and critical-pointdried witha Tou- The two septal nectariesrun adjacent to the simis critical-pointdryer using pressurizedcarbon dioxide aperturesand extend distally only to the base of the as the transitionfluid. The materialwas transferredonto a ovary locules, at the level of perianthdetachment (see stub covered with double-stick tape, sputter-coatedwith in and Simpson 1993). From a previous study (Simpson gold/palladium a Hummer-4 sputteringapparatus, photographedon a Hitachi S500 scanning electron micro- 1993) I concluded that (1) two infralocularnectaries scope (20 kV). Images were captured digitally.All photo- evolved in the common ancestorof all five of the su- graphic figureswere preparedusing the Freehand software. perior-ovariedgenera, concomitantlywith the evolu- tion of perianthapertures and arisingvia the evolution Results of zygomorphyand basal displacement of nectaries Wachendorfia Carpel and Septal into the receptaculartissue; (2) perianthapertures were thyrsifiora Nectary Development lost in the genera Pyrrorhizaand Barberetta; and (3) septal nectaries were probably independentlylost in The flowers of Wachendorfia thyrsifiora are zygo- the genus Xiphidium,perhaps in response to a shiftin morphic, with three outer and three inner imbricate, pollinationmechanism. glabrous to abaxially hispidulous tepals (fig. 1). The The purpose of this article is to reportanatomical flowers have an extended "receptacular region," de- and developmentalfindings that help supportthe hy- fined as the tissue between the ovary base and the pothesisthat ovary positionin the Haemodoraceae un- short, stalklike pedicel. The outer posterior tepal is derwentan evolutionaryreversal, from inferior to su- fused basally both to the inner posterior tepals and to perior,and to review the possible adaptive significance the upper margins of the outer anterior tepals (fig. 3), of thattransformation. forming lateral pouchlike perianth "apertures" (after Ornduff and Dulberger 1978) at their junction in the Materialand Methods receptacular region (fig. 2). The perianth apertures function as repositories for secreted nectar. From the Maturebuds or recentlyopened flowers were preserved in thefield in FAA (formalin-aceticacid-alcohol), embed- front face of the flower, two openings leading to the ded in Paraplast,and cross-sectionedserially at thicknesses perianth apertures occur (fig. 1); these apparently serve rangingfrom 8 to 15 ,umdepending on thedevelopmental as conduits for the proboscis of an insect during pol- stage.Sections were stainedwith safranin, fast-green, and lination (Omduff and Dulberger 1978; Helme and Lin- hematoxylinaccording to standardprocedures (Johansen der 1992). There are three, free and distinct, incurved 1940; Sass 1958; Berlynand Miksche1976). Lightmicro- stamens positioned opposite the inner tepals (figs. 1, 468 INTERNATIONAL JOURNAL OF PLANT SCIENCES

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Figs. 1-12 WachendorfiathyrsiflZora floral development.Figs. 1-2, Light micrographsof mature flower.Fig. 1, Front view, showing posteriorouter tepal ( pot), two posteriorinner tepals ( pit), anteriorouter tepals (act), anteriorinner tepal (ait), two posteriorstamens ( psta), anteriorstamen (asta), and oppositelycurved style(sty). Also note two perianthaperture openings (pac). Fig. 2, Side view, showingperianth aperture(pa) of receptacularregion, style (sty), anteriorstamen (asta), and two posteriorstamens (psta). Fig. 3, Floral diagram,oriented relative to horizontalflower, posterior above. Abbreviationsas above. Figs. 4-12, Scanning electronmicrographs of various developmental stages. Fig. 4, Early stage, showing primordiaof anteriorouter tepals (act), anteriorinner tepal (ait), anteriorstamen (asta), posterior SIMPSON-REVERSAL IN OVARY POSITION 469

3). The two posteriorstamens exhibit little lateral cur- nectaryis contiguouswith the septal nectarycommis- vature; however,the anteriorstamen is stronglybent sure, which extendsto the exteriorperiphery (fig. 15). to one side (fig. 1), eitherto the leftor right,depending The septal nectariesand adjacent commissuresin the on the individual plant. The ovary is superior,ovoid, receptacularregion (fig. 14) extend withoutinterrup- three-lobed,densely pubescent,with three locules and tion to the base of the superiorportion of the ovary carpels. There is one ovule per locule, arising from and are confluentwith septal commissuresof theovary turgid,longitudinally oriented placentae. The style is that developed between the posteriorcarpel and the incurved and stronglybent to the side opposite the two, adjacent anteriorcarpels (figs. 16; 39B, C). Sim- anterior , i.e., exhibiting strong enantiostyly ilarly,protruding flanges of tissue thatborder the sep- (figs. 1, 2). tal commissure in the receptacularregion (arrows at At an early developmentalstage, the four series of fig. 15) are contiguous with the flanges of the two floralprimordia initiate: outer tepals, innertepals, sta- adjacent carpels that flankeach commissureand nec- mens, and two anteriorcarpels (fig. 4). The two an- tarythere (arrows at fig. 16). teriorcarpel primordiaappear to develop priorto the As the flower matures,the margins of the single posteriorcarpel primordium(fig. 4). At a later stage, outer posteriortepal overlap distallythose of the ad- the posteriorcarpel forms(fig. 5) and becomes com- jacent outeranterior tepals (fig. 9). In the receptacular parable in size to the anteriorcarpels (fig. 6), but dif- region, these overlappingtepals differentiateto form ferentialdevelopment of anteriorand posteriorcarpels the "perianthaperture," which becomes borderedby resultsin a slightbilateral symmetry of the gynoecium the decurrentoutgrowth of outer posteriorand outer (fig. 7); this bilateral symmetryis evident in that the anteriortepals (figs. 10, 11, 18). The receptacularre- locule of the posteriorcarpel is largerand is medially gion undergoes considerable axial growthduring de- aligned with the center point of the three carpels, velopment, resulting in significantextension of the whereas the locules of the anteriorcarpels are smaller septal nectaries (fig. 39A-C). At maturitythe septal and orientedslightly askew to the centerpoint (fig.7). nectariesbecome convolutedin outlinewith an evident Carpel primordiadifferentiate into a typical folded, gap between the epitheliallayers (figs. 17, 18). At this conduplicateform (figs. 6, 7) with subsequent appar- stage, the densely stained epithelialcells are palisade- entlypostgenital fusion of adjacent carpels to forma shaped and are surroundedby two to three layers of three-lobedovary, style, and (fig. 8). This post- slightlyless densely stained cells (fig. 17). In the re- genital fusion transformsthe intercarpellaryspaces ceptacular region, the slitlike comnmissuresextend (fig. 7) into ovary septal conumissures(fig. 8). fromthe two septal nectarycavities to the exterior(fig. Prior to carpellaryfusion, accelerated cell divisions 17). These two septal nectarycommissures open fully occur in the lower, receptacularregion of the flower, fromthe septal nectaryto the outside only at the ex- resultingin verticalridges or flanksof tissue that are tremebase of the perianthaperture (figs. 11, 12). The continuouswith the marginsof the distal, free tepals; septal nectarycommissures are confluentwith the sep- these ridges thus appear as "decurrent"extensions of tal commissuresthat traversethe entirelength of the the tepal margins.This acceleratedgrowth also results superiorovary and style (fig. 19). The locules of the in an internalcleft of the receptaculartissue (arrow at ovary remain confluentwith a canal that extends the fig. 13) between each decurrentridge of the posterior lengthof the style (fig. 39C). innertepal and the adjacent anteriorouter tepal. With continued differentialgrowth, the upper margin of Wachendorfiathyrsiflora Floral Venation each decurrentanterior outer tepal overlaps the lower Early in development,each median (posterior)outer marginof the adjacent decurrentposterior inner tepal tepal vein and the dorsal carpellary vein are joined at the base of the receptacle (figs. 9, 14); the recep- togetherin the basal region of the flower(fig. 39A). tacular cleftbetween themdifferentiates into a periph- At a later stage, the junction between median outer eral septal commissureand an inner "septal" nectary tepal and dorsal carpellaryveins becomes positioned thatis verticallyaligned withthe two anteriorsepta of at the very base of the receptacle, below the septal the ovary (figs. 14, 15). The immatureseptal nectary nectaries,as the resultof intercalary(zonal) expansion consists of a single layer of densely staining,cuboidal of the receptacularaxis (fig. 39B, C). Column veins, epithelial cells that line the cleft (fig. 15). The septal which extend to the placentae and ovules, develop at

stamens (psta), and two anteriorcarpels (ac). Fig. 5, Slightlylater stage, showing formationof posteriorcarpel (pc) as well as anterior carpels (ac) and enlarged stamens. Other abbreviationsas above. Fig. 6, Later stage, showing initiationof conduplicatecarpels, including enlarged posteriorcarpel (pc). Fig. 7, Later stage, showing slightbilaterally symmetric arrangement of posteriorcarpel (pc) and anterior carpels (ac). Note formationof locules (lo) and intercarpellaryspace (ics). Fig. 8, Early ovary development,showing postgenitalfusion of conduplicate carpels, immaturestyle (sty), and septal commissures(sco) of ovary. Fig. 9, Flower bud, side view of receptacularregion, showing overlap of posteriorinner tepal (pit) by anteriorouter tepal (aot) and the latterby posteriorouter tepal (pot). Note position of futureperianth aperture (pa). Fig. 10, Later stage, showingclose-up of incipientperianth aperture region, with surrounding, dense trichomes. Fig. 11, Mature stage, perianthaperture, side view, showing ridges of decurrentposterior outer tepal (pot) and anteriorouter tepal (aot). Note opening of septal nectary(sno). Fig. 12, Close-up of septal nectaryopening. 470 INTERNATIONAL JOURNAL OF PLANT SCIENCES

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Figs.13-19 Wachendorfiathyrsiflora floral development, light micrographs of flowercross-sections. Postenior (upper) side of flowerat top in all figures.Fig. 13, Very early stage, receptacularregion, showing initiationof posteriorinner tepal (pit) and anteriorouter tepal (act). Note cleft between them (arrow), which becomes futureseptal commissureand nectary.Fig. 14, Intermediatestage, receptacularregion, showing overlap of lower marginof posteriorinner tepal (pit) by the uppermargin of anteriorouter tepal (act) and developmentof immature septal nectarycommissure/septal commissure (snco/sco) between them. Fig. 15, Close-up, showing margin of posteriorinner tepal (pit), septal nectarycommissure (snco), and immatureseptal nectary(sn). Note flangesof tissue (arrows) adjacent to septal commissure.Fig. 16, SIMPSON-REVERSAL IN OVARY POSITION 471 a later stage and are joined to the dorsal carpellary erated in the elliptic-shapedwalls of the carpel pri- vein above the outertepal-dorsal vein junction but still mordia themselves as well as in the surroundingpe- below the septal nectaries(fig. 39B, C). Veins of the ripheral tissues of the receptacular region. The inner tepals and stamens are joined below the septal surroundingperipheral receptacular tissue grows up- nectaries(fig. 39B, C). ward and around the locules and intercarpellaryspac- es. This, combined with postgenitalfusion of the car- Lachnanthes caroliniana Carpel and pel walls at the floralcenter (see below), resultsin the Septal Nectary Development ovary being embedded withinand surroundedby re- The flowers of Lachnanthes caroliniana are acti- ceptaculartissue (fig. 40A-D). nomorphic with a biseriate, imbricate,abaxially pu- The locules initiallydevelop as constricted,tangen- bescentperianth consisting of threesmall, narrow,out- tially orientedslits, associated with the growthof in- er tepals, and threelarge, relativelywide, innertepals truded,densely stainingplacental primordia(fig. 34). (figs. 20-22). There are three distinctand essentially In the center of the ovary, the intercarpellaryspace free stamens, one opposite each of the inner tepals develops as three,confluent, radiating slits (figs. 34; (figs. 21, 22). The ovary is inferior,ovoid to globose, 40A) that extend distally as septal commissures.The and externallypubescent to tomentose,with three loc- region of this intercarpellaryspace at the centerof the ules and carpels. There are five to seven ovules per flowerbecomes filledwith tissue by postgenitalfusion locule, arisingfrom a turgid,peltate placenta. The style of adjacent tissues. However,the outer,peripheral por- is stronglybent to one side opposite one of the outer tion of the slits persists and differentiatesinto septal tepals, but thereis no correspondingasymmetric cur- nectaries at about the same time as ovule formation vatureof stamens(fig. 21). (figs. 35; 40B). Each septal nectaryinitially consists Outer and innertepal primordiainitiate at an early of two, abuttinguniseriate plates of epithelialcells (fig. developmentalstage (fig. 23). Slightlylater in devel- 36). With furtherdevelopment, the epithelialcells ex- opment,stamen primordiadevelop opposite the inner pand and become cytoplasmicallydense, and the septal tepals,with no initialevidence of carpel formation(fig. nectarycavity enlarges considerably(figs. 37, 38). 24). Earliest carpel developmentis evident with the Furtheraccelerated upward growthof the apical re- subsequent formationof pouch-shaped primordia at gion of thethree postgenitally fused carpels results in the the flowerapex (fig. 25). Carpel primordiadevelop by formationof the styleand stigma(figs. 28, 29). As the the accelerated growth of cells along three elliptic- styleand stigmagrow (fig. 30), the septal nectariesre- shaped rings, which forms the carpel walls, and no main continuouswith septal nectary openings at the top detectable growthin the center of each of the three of the ovary (fig. 31), the openingsbeing remnantsof rings,which formsthe cavities of the locules. Growth the originalintercarpellary space. These porelikeopen- is also minimalbetween adjacent carpels as well as at ings functionas the site of nectarsecretion. The septal the centraljunction of the threecarpels (arrow at figs. nectarycavities are continuouswith the originalinter- 25-27). The region between the walls of adjacent car- carpellaryslits (figs.27, 28) thatoccur up the lengthof pels, the intercarpellaryspace, laterbecomes the septal the styleas septal commissures(figs. 29, 30; 40C, D), region (figs. 26, 32). similarto those seen in the ovary and style of Wach- At a laterstage, acceleratedgrowth at the peripheral endorfia. region of each of the threeelliptical carpel walls oc- Epidermalcells of the stigmaticregion form papillate curs, causing the carpels to arch inward (fig. 27) and outgrowthsduring development (figs. 29, 30). The loc- ultimatelycome into close contact(fig. 28), assuming ules of theinferior carpels remain confluent with a stylar a typical conduplicate form.Where the two margins canal thattraverses the length of thestyle (figs. 37; 40C). of individualcarpels come into close contact,a carpel commissureis evident (figs. 32, 33). Lachnanthes caroliniana Floral Venation The ovary becomes inferiorin position by a com- During development,each median outer tepal vein bination of differentialgrowth and congenitalfusion. and the dorsal carpellaryvein are joined at the apex Growthis retardedat threegeneral locations: (1) at the of the receptacularregion, at or below the level of the centraljunction of the threecarpel primordia(arrows extreme base of the locule (fig. 40B-D). Column at figs. 25, 26, 32); (2) in the center of each of the veins, which extendto theplacental regions, are joined three carpel rings, the locular cavities (figs. 25, 26); to the vein thatdistally extends to the outertepal and and (3) between the walls of adjacent carpel walls, the dorsal veins (fig.40D). In the same regionof the flow- intercarpellaryspaces (figs. 26, 32). Growthis accel- er, a vein leading to the base of the septal nectary

Intermediatestage, ovary base, showing apical region of septal nectaries(sn) and contiguous septal nectarycommissures (snco), the latter extendinginto septal regions between anteriorcarpels (ac) and the posteriorcarpel (above). Note tissue flanges(arrows) adjacent to septal commissures,contiguous with those below in figure15. Other abbreviationsas above. Fig. 17, Mature stage, close-up of convoluted septal necary (sn) and contiguous,peripheral septal nectarycommissures (snco). Fig. 18, Mature stage, receptacularregion cross-section, showing septal nectaries (sn), septal nectarycommissures (snco), and cavity of perianthaperture (pa). Fig. 19, Mature stage, close-up of septal commissure(sco) of ovary, which is contiguouswith the lower septal nectarycommissures. 472 INTERNATIONAL JOURNAL OF PLANT SCIENCES 22 ~~ot

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Figs.20-31 Lachnanthes caroliniana floraldevelopment. Figs. 20-2 1, Light micrographsof matureflower. Fig. 20, Side view, showing inferiorovary (ova), outer tepals (ot), innertepals (it), stamens(sta), and curved style (sty). Fig. 21, Top view, showing curved style (sty) and three stamens (sta), the latteropposite the inner tepals (it). Fig. 22, Floral diagram. Abbreviationsas above. Figs. 23-31, Scanning electronmicrographs. Fig. 23, Early stage, showing primordiaof outertepals (ot) and innertepals (it). Fig. 24, Slightlylater stage, showing formationof stamens (sta) opposite innertepals (it). Fig. 25, Later stage, showing more maturestamen (sta) and initiationof three,pouch- shaped carpel primordia(c) with locules (lo). Arrow indicatescentral junction point of carpels. Fig. 26, Later stage, showing threecarpels (c), intercarpellaryspace (ics), and carpel commissures(cc). Arrow as above. Fig. 27, Later stage, with enlarged carpels, having carpel commissures(cc). Arrowas above. Fig. 28, Later stage, showing early,postgenital fusion of carpels and intercarpellaryspace (ics). Fig. 29, Early style development,showing septal commissures(sco) of style and papillate cells of incipientstigma (sti). Fig. 30, More maturestyle, showing region of septal commissure(sco). Fig. 31, Close-up at base of style,showing slitlikeseptal nectaryopening (sno). SIMPSON-REVERSAL IN OVARY POSITION 473

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Figs.32-38 Lachnanthes caroliniana floraldevelopment, light micrographsof flowercross-sections. Fig. 32, Very early stage, showing young carpels, with incipientintercarpellary spaces (ics) and carpel commissures(cc). Arrow indicatescentral junction of carpels. Fig. 33, Later stage, showing carpels (c), carpel commissures(cc), and intercarpellaryspaces (ics). Fig. 34, Later stage, inferiorovary cross-section, showing threelocules (lo), placentae (pl), and intercarpellaryspace (ics). Fig. 35, Later stage, inferiorovary cross-section,showing locules (lo), ovules (ovu), and immatureseptal nectaries(sn). Fig. 36, Close-up of immatureseptal nectary(sn). Fig. 37, Mature stage, inferior ovary cross-section,showing septal nectaries(sn), ovule (ovu), and stylarcanal (styca) contiguouswith locule (lo). Fig. 38, Close-up mature septal nectary. 474 INTERNATIONAL JOURNAL OF PLANT SCIENCES

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pot Dl~~~~~~~~~~~~~~~~~~~~~~o

105cc Wachendorfiathyrsiflora~~~~~~~~~ Lacnath ~~~~~~\dcroinan

Fig.39 Wachendorfiathyrsiflora. Diagrams of flowerlongitudinal Fig.40 Lachnanthescaroliniana. Diagrams of flowerlongitudinal sections,below, with correspondingtransverse sections, above or to sections. Longitudinaland cross-sectionalviews as in figure39. A, right.In longitudinalviews, section throughcarpel centeris at left Young stage, illustratingunfused carpel (c) withcarpel commissure and throughseptum or septal region centeris at right,the direction (cc) and adjacent intercarpellaryspace (ics). Arrowindicates central correspondingto labeled dashed line in transversesection. Trans- junction point of carpels. B, Slightlylater stage, showing develop- verse views are at a florallevel correspondingto labeled dashed line mentof placenta (pl) and vasculature,including outer tepal (ot) and in longitudinalsectional view. A, Young stage, illustratingunfused dorsal (do) veins. Arrowas above. C, Middle stage, showinginferior posteriorcarpel (pc) and adjacent intercarpellaryspace (ics). B, ovary position.Note contiguousseptal nectary(sn) and septal com- Middle stage, showing postgenitalfusion of carpels. Note contigu- missure (sco) of ovary. D, Mature flower,showing septal nectary ous septal nectary(sn) and septal commissure (sco) of ovary. C, opening (sno) at top of inferiorovary and septal nectaryat same Mature flower,showing septal nectaryopening (sno) withinperianth approximatelevel to thatof ovule and upper locule. Locule (lo) is aperturecavity. Note contiguouslocule (lo) and stylarcanal (styca). contiguouswith stylar canal (styca). Note junction (*) of outertepal Also note junction (*) of posteriorouter tepal (pot) vein and dorsal (ot) vein and dorsal vein (do) at base of ovary. Abbreviationsand vein (do) at extremebase of receptacularregion. Abbreviationsand symbols: * = junction of centralvein of posteriorouter tepal and symbols: * = junction of central vein of posteriorouter tepal and dorsal carpellaryvein; c = carpel; cc = carpel commissure;col = dorsal carpellaryvein; ait = anteriorinner tepal; col column vein; column vein(s); do = dorsal vein; ics = intercarpellaryspace; it = do = dorsal vein; ics = intercarpellaryspace; lo locule; ovu = innertepal; lo = locule; ot outer tepal; ovu = ovule; pl = pla- ovule; pc = posteriorcarpel; pl = placenta; pot posteriorouter centa; se septal veins; sn septal nectary;sco = septal commis- tepal; sco = septal commissure;sn = septal nectary;snco = septal sure; sno septal nectaryopening; sta = stamen; styca = stylar nectarycommissure; sno = septal nectaryopening; sta = stamen; canal. styca = stylarcanal. connects to the vein thatleads to the inner tepal and to the centralregion of the locule (fig. 41A). Column stamen vein (fig. 40D). The septal nectariesare posi- veins are joined to thiscommon outer tepal-dorsal vein tioned at the level of ovule attachment(fig. 40C, D). at the base of the inferiorovary and extend to the Septal nectaries are continuous with septal nectary single ovule and into the apical region of the column commissures that extend into the peripheryof the tissue (fig. 41A). Veins of the innertepals and stamens styles (fig. 40C, D). are joined near the base of the ovary (fig. 41A). Septal veins arise fromthis common innertepal-stamen vein Dilatris pilansii Floral Venation slightlyproximal to the junction of the latterand ex- In matureflowers, each median outertepal vein and tend a shortdistance into the base of the ovary (fig. dorsal carpellaryvein are joined togetherslightly distal 41A). The threeseptal nectariesare vestigial,occurring SIMPSON-REVERSAL IN OVARY POSITION 475

ot styca stait found in all zygomorphicHaemodoraceae (fig. 41C). ot stycasta it snco In matureflowers, the median anteriorouter tepal vein Ido and dorsal carpellaryvein are joined togetherjust be- low the locule of the superiorovary (fig. 41C). The stamen vein and dorsal carpellary vein are joined -~~~-.%. ~ ~ ~ ~ ~ ~ ~ Th~~ ovu ...... thisjunction (fig. 41C). No septal veins * . ~~~~~~~~~~~colslightly above are evident. Septal nectariesare absent,as theyare in aot sta I pait aot Intapi all membersof this family(fig. 41C). 5r Pontederia cordata (Pontederiaceae) Floral Venation A.A Dilatrisplansii. Haemodorumseictum Flowers of this species are horizontaland zygomor- phic, with six stamens.The median outer tepal is an- aot sta styca it aot stycaat teriorin position,opposite thatfound in all zygomor- I I I It t Ise ta i t phic Haemodoraceae and similar to that in the 4 PI PI Philydraceae(fig. 41D). In matureflowers, the median anteriorouter tepal vein and dorsal carpellaryvein are dou joined togetherslightly below the locule of the supe- rior ovary (fig. 41D). The median posteriorstamen carpl cete is left and .hog setu orspaeio ... etri vein and median posteriorinner tepal vein are joined snO slightlyabove the ovary base (fig. 41D). No septal veins are evident. Septal nectaries are present at the base of the locule; a septal nectary commissureex- tends only a shortdistance to the extremeovary base, at the point of the septal nectaryopening (fig. 41D).

venen(o0eo n osl basedof ovr. ,Potdeicr Discussion atovryfig.rihtAhilatrum 41DiAg Abrvain 0 splanugnNotem sifeo is rDue9 ua0 soteeptalnctaryd)atape The major goal of this study was to evaluate the carpelacenterissatpleftiandcthroughasptum Forseptal regaioncnt developmentaland anatomical evidence regardingthe donl atteetem vr pe,na hesyebs hypothesisthat ovary position in the Haemodoraceae of inferiorovary Also notejunction (*) of outertepal (ot) vein and has undergonea shiftfrom inferior to superiorin one dorsal vein (do) at middle of ovary B spicatum. Note septal nectary(sn) level withlocules of inferiorovary. Note junction clade of the family.Previous cladistic analyses of the (*) of outertepal (ot) vein and dorsal vein (do) below base of ovary. Haemodoraceae (Simpson 1990, 1993) providethe ev- C, Philydrum lanuginosum. Note absence of septal nectaries and idence thata superiorovary, as foundin Wachendorfia junction (*) of fused anteriorouter tepal (act) with stamen (sta) and fourother genera, was derivedfrom a preexisting, veins and dorsal vein (do) below base of ovary. D, Pontederia cor- data. Note septal nectariesat base of ovary. Note junction (*) of inferior-ovariedcondition (see fig.43). This hypothesis anteriorouter tepal (act) vein and dorsal vein (do) below base of restson the totalityof morphological,anatomical, em- ovary. Abbreviationsas in figs. 39, 40. bryological,chemical, and karyologicalcharacters and the assumptionsof charactercoding and polarityas- signmentin parsimonyanalyses. In the cited cladistic only at the extreme ovary apex, near the style base analyses, all outgroups(Pontederiaceae and Philydra- (fig. 4 1A). ceae; see Simpson 1990, 1993) have a superiorovary, and the common ancestor(ingroup node) of the Hae- Haemodorum Floral Venation spicatum modoraceae has an inferiorovary, an apomorphyfor In matureflowers, each median outertepal vein and the family as a whole. Molecular data (Duvall et al. dorsal carpellaryvein are joined togetherwell below 1993; Clark et al. 1994) provide evidence thatyet an- the locule in the apical regionof thepedicel (fig.41B). otherfamily, the , is a close relativeto Column veins arise from a lower level (fig. 41B). the Haemodoraceae. All membersof this familyalso Veins of the innertepals and stamens are joined near have a superiorovary, supportingthe notion thatthis the base of the inferiorovary (fig. 41B). No septal featureis ancestralrelative to the Haemodoraceae, i.e., veins are evident.The threeseptal nectariesare large, presentat the outgroupnode. occurringonly in the apical region of the ovary; a The derivationof a superiorovary withinthe Hae- commissureopens to allow nectarsecretion at thebase modoraceae would technicallybe termeda "reversal." of the style (fig. 41B). This is true only if (as would normallybe done) the ovary position of the superior-ovariedtaxa is original- Philydrumlanuginosum (Philydraceae) ly coded as homologous to thatof the outgrouptaxa. Floral Venation However, it should be emphasized thatthe secondary Flowers of this species are horizontaland zygomor- evolution of a superiorovary in the Haemodoraceae, phic, with a single anteriormedian stamen and the though termed a reversal, is a unique evolutionary threeposterior tepals fused into one structure.The me- event in itself. This is only the second corroborated dian outer tepal is anteriorin position, opposite that example of a reversalin ovary position,the firstbeing 476 INTERNATIONAL JOURNAL OF PLANT SCIENCES

septalnectary commissure septal 7 / (develops internally) nectary

carpel primordia Aepal(outer)

~~~~ ~~~~~~Vlocule/ A B D Lachnanthescaroliniana inferiorovary development

septal commissure

septalnectary commissure septal L (develops externally) nectary carpel I ..... primordia (outer) > / ; - X - .KI../ locule tepal(outer) ......

F G - lr H -7 Wachendorfiathyrsiflora superior ovary development Fig.42 Summary diagram of ovary development,illustrating two adjacent carpels and interveningseptal region. A-D, Lachnanthes caroliniana. A, Initiationof carpel primordiawith retardedgrowth of centralreceptacular tissue and accelerated growthof peripheraltissue (arrows). B, Growthof laterallypositioned, conduplicate carpels. C, Furthergrowth of carpels and expansion of locules (dark outline) with developmentof internalseptal nectarycommissures. D, Relativelymature stage, showingfusion of carpels and differentiationof interlocular septal nectaries.E-H, Wachendorfiathyrsiflora. E, Initiationof carpel primordiawith relativelyaccelerated growthof centralreceptacular tissue. F, Growthof apically positioned,conduplicate carpels. G, Furthergrowth of carpels and locules (dark outline) withexternal extension of septal nectarycommissure. H, Relativelymature stage, showing fusionof carpels and differentiationof infralocularseptal nectaries.* = junction of posteriorouter tepal vein and dorsal carpellaryvein. that reportedby Eyde and Tseng (1969) for Tetra- is embedded withinand surroundedby peripheraltis- plasandra of the Araliaceae, a studynot corroborated sue, well beneaththe point of insertionof the perianth by a strictcladistic analysis. If we accept that the (figs. 40A-D; 42C, D). Thus, inferior-ovarydevelop- above hypothesisof ovary positionreversal is correct, ment in Lachnanthes appears to be rathersimple dif- the observations of floral developmentand anatomy ferentialgrowth resultingin lateral displacement of describedhere may be consideredas to how thattrans- typicalfoliar-like carpels followed by theircongenital formationtook place. fusion.No "recurrent"(invaginated) vascular bundles The ovary of Lachnanthes becomes inferiorin po- occur, as are presentin some inferior-ovarieddicots. sitionby a combinationof differentialgrowth and con- (See Douglas 1944 and Sattler1974 forinterpretations genital fusion. Afterthe three carpel primordiahave on ovary position and carpel development.) initiated,growth becomes retardedin threegeneral lo- The ovary of Wachendorfiaalso develops by a com- cations: (1) at the centraljunction of the threecarpel bination of differentialgrowth and congenital fusion primordia(fig. 32); (2) at the center of each of the similarto thatof Lachnanthes.In fact,carpel initiation threecarpel rings,the locular cavities (fig. 25); and (3) and developmentare quite similarin thetwo taxa (figs. between the walls of adjacent carpel walls, the inter- 6-8). The differenceis thatin Wachendorfiathe cen- carpellary spaces (figs. 26, 32). Growth is relatively tral axis of the receptacle grows and extends upward accelerated in the elliptic-shapedwalls of the carpel to about the same degree as the peripheraltissues of primordia (figs. 25-28; 40A, B). However, as illus- the receptacle (figs. 39A; 42E). The carpels become trateddiagrammatically in fig.42, growthis relatively orientedin a more apical position (fig. 42F). Subse- retardedin the centralaxis of the receptacle(fig. 42A). quent congenitalfusion results in the locules being el- This, combined with extension growth of the sur- evated relative to perianthinsertion, forming a supe- roundingperipheral tissue, reorientsthe carpels to a rior-ovaryposition (fig. 42G, H). The ovary and style more lateral position (fig. 42B). This growthis fol- of Wachendorfia develop similarly to the style of lowed by postgenitalfusion of the carpel walls at the Lachnanthes. floralcenter, with the resultthat the now inferiorovary In interpretingthe details of the transformationfrom SIMPSON-REVERSAL IN OVARY POSITION 477 inferior-to superior-ovaryposition, the concepts of those of Lachnanthes and the genus Haemodorum, structuraland positional homology are used; features both of which have "interlocular"septal nectaries,oc- that are structurallyor positionally similar in two or cupying the septal regions between the locules in an more taxa may representan ancestralcondition com- inferiorovary (Simpson 1993). Thus, I hypothesize mon to those taxa. In addition, as Carlquist (1969) thatthe receptacularregion in at least fourof the five emphasized, it is vital to consider the functionalsig- superior-ovariedgenera of the Haemodoraceae is pos- nificanceof floralanatomy, particularly with regard to itionallyhomologous (homotopous) with the inferior- pollination mechanism and fruit or dispersal. ovary region in othermembers of the family.This po- Thus, an overridingquestion in this studyis assessing sitionalsimilarity in septal nectarydevelopment, there- what possible functionthe change from inferior-to fore,supports the homology between an ancestralin- superior-ovaryposition had in termsof overall lifehis- ferior ovary and a derived "inferior" receptacular tory and what the possible selective pressurefor that region. With regardto investigatedoutgroup taxa, all change mighthave been. of which have superior ovaries, septal nectaries are One line of evidence for ovary position reversal absent in P. lanuginosum(fig. 41C), as theyare in all concernsthe vasculatureof the flower.In the superior- membersof the familyPhilydraceae. Septal nectaries ovaried Wachendorfia,the median outer tepal vein are also absent in all members of the family Com- joins withthe common dorsal-columnvein well below melinaceae, the recentlyproposed close relativeto the the locule base, at the base of the receptacularregion Haemodoraceae. The septal nectariesof P. cordata are (fig. 42H). In the inferior-ovariedLachnanthes, the located at the base of a superiorovary, above the point junction of outer tepal and dorsal vein occurs at or of insertionof the perianthand not beneath in the re- above the locule base (fig.42D). The venationpatterns ceptacularregion (fig. 41D); this is true for all mem- of Dilatris and Haemodorum,two otherinferior-ovar- bers of the Pontederiaceae that have septal nectaries ied taxa somewhat closely related to Lachnanthes,is (M. G. Simpson, unpublishedobservation; see Burton somewhat variable. In Dilatris the outer tepal-dorsal and Simpson 1996). vein junctionoccurs in the midregionof thelocule (fig. A final line of evidence corroboratingovary posi- 41A). In Haemodorum, the outer tepal-dorsal vein tion in the Haemodoraceae, relatedto the above, con- junction occurs just beneath the locule (fig. 41B). In cerns the developmentof the septal nectaries.Septal any case, if floralvasculature in these taxa is position- nectarieshave been interpretedpreviously as being de- ally homologous, these results indicate that the junc- rived by the incomplete closure of adjacent carpels tion of dorsal and outer tepal veins in the superior- (Schmid 1985), and thisappears to be corroboratedfor ovaried Wachendorfiais positionallyhomologous with investigatedHaemodoraceae. Septal nectariesin all in- the middle to basal regionof an ancestralinferior ova- vestigatedinferior-ovaried taxa of the familydevelop ry. The floral venation of two investigatedoutgroup within intercarpellaryspaces, the slitlike suturesbe- family species, Pontederia cordata (Pontederiaceae) tween carpels (e.g., figs.34-38; 42B-D). Thus, septal and Philydrumlanuginosum (Philydraceae) is similar nectarydevelopment in these taxa is integrallyrelated to that of Haemodorum spicatum in that the dorsal to carpel development.In addition,septal nectariesin carpellaryvein and outertepal vein are joined just be- inferior-ovariedtaxa are continuouswith the intercar- neath the locule, but of a superior(not inferior)ovary. pellarycommissures that extend upward to the base of Thus, all outgrouptaxa are differentin floral vascu- the style(figs. 40C, D; 41A, B; 42D). Septal nectaries lature fromthe superior-ovariedWachendorfia of the in the superior-ovariedWachendorfia differ from those Haemodoraceae, indicatinga de novo originof the ex- of the inferior-ovariedtaxa by developingin continuity tended receptaculartissue of the latter. withthe outside of the receptacularregion of the flow- A second line of evidence thatcorroborates reversal er (figs. 14, 15; 42F-H), ratherthan on the inside of in ovary position in the Haemodoraceae concernsthe the inferiorovary. However, nectaries of Wachendorfia positionalhomology of the septal nectaries.Recall that are similar to those of inferior-ovariedtaxa in being Wachendorfiais one of four superior-ovariedgenera completely continuous with intercarpellarycommis- unique with two septal nectariesthat are infralocular sures thatextend into the ovary and style(figs. 16, 19; in position,i.e., located beneaththe locules, in an elon- 39B, C; 42F-H). The receptaculartissues flankingthe gate receptacular region. (The fifthsuperior-ovaried septal nectariesin Wachendorfia(fig. 15) are contin- genus, Xiphidium,lacks nectaries altogetherand can- uous with flankingtissues of the carpels at the ovary not be evaluated in thisregard.) A comparisonof com- base (fig. 16). This continuityappears to have arisen parable developmental stages of Wachendorfia(figs. via an evolutionarychange resultingin relativelyac- 39; 42E-H) and Lachnanthes (figs. 40; 42A-D) celeratedvertical growth of the centralreceptacular tis- demonstratesthat, relative to the insertionof the peri- sue immediatelybeneath the carpels and extensionof anth,the positional relationshipof septal nectariesin the intercarpellaryspaces, which formseptal commis- the receptacularregion of Wachendorfiais virtually sures,down the lengthof the outerreceptacle, forming identical with thatof septal nectarieswithin the infe- the septal nectarycommissures and septal nectaries.I rior ovary of Lachnanthes. With referenceto the in- hypothesize that this continuityis the result of ho- sertionpoint of the perianth,the septal nectariesin all mology betweenthe externallydeveloping infralocular foursuperior-ovaried genera are similarin positionto septal nectaries and the adjacent carpels, furtherevi- 478 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Septal nectary# 2 2 0 2 2 3 3 3 3(0) Septal nectarytype INFR INFR ABS INFR INFR INTE INTE INTE ABS,INTE,orSUPR Perianthaperture + - - + Ovaryposition SU SU SU SU SU IN IN IN IN

u Tribe B a: I uU I I co >

3 - loss of perianthapertures \// v/; , (but not septal nectaries) 2 t// f -

2 - extensionof two intercarpellary 1 + / i spaces intoexternal commissures \ and septal nectaries,these , associatedwith perianth apertures \g/ /

1 - transformationfrom inferior to\ / superiorovary by accelerated\/ growthof centralreceptacular tissue/

Fig.43 Cladogram of Haemodoraceae, fromSimpson (1990, 1993). Abbreviationsas follows: Septal nectarytype (fromSimpson 1993): INFR = infralocular;ABS = absent; SUPR = supralocular;INTE = interlocular.Perianth aperture: "+" = present; "-" =absent. Ovary position: SU = superior;IN = inferior. dence that the receptacular region of the superior- for this evolutionarynovelty was probably a special- ovaried taxa is homologous to the ovary region of the ized pollination mechanism associated with the peri- inferior-ovariedtaxa. I suggest that the same devel- anth apertures,structures that collect and containnec- opmentalgenes may be involved in the two processes. tar at the outer base of the flower. The perianth In the outgrouptaxa withseptal nectaries(i.e., mem- aperturesmay function,in part,to directionallyorient bers of the Pontederiaceae), septal nectary develop- an insect (via the perianthaperture openings) formore ment has not been studied. However, these outgroup efficientpollination (Ornduffand Dulberger 1978). taxa lack any evidence of septal commissuresextend- The reductionin septal nectarynumber, from 3 to 2, ing into the receptaculartissue (fig. 41D), supporting is correlatedwith the occurrenceof only two perianth the hypothesisthat septal nectaries evolved indepen- apertures,which itselfmay be relatedto the evolution dentlyfrom those of the superior-ovariedHaemodor- of zygomorphyand a horizontalorientation in the su- aceae. perior-ovariedHaemodoraceae (otherthan Xiphidium; In conclusion,the scenariohypothesized here forthe Simpson 1993). Two other superior-ovariedmembers Haemodoraceae is thatan ancestralinferior ovary was of the Haemodoraceae, Barberetta and Pyrrorhiza, evolutionarilytransformed into a superior ovary by lack perianthapertures but do have two, infralocular relativelyaccelerated, extension growth of the central septal nectaries (Simpson 1993). Although not the receptaculartissue, resulting in apically positionedcar- most parsimoniousexplanation, it seems most proba- pels, such that the peripheralreceptacular tissue no ble thatBarberetta and Pyrrorhizaeach independently longer overarched and surroundedthe laterallyposi- lost perianthapertures after their ancestral acquisition tioned carpel primordia.In addition,the retardationof (Simpson 1993; fig. 43). The evolution of the genus growthbetween carpels, in the intercarpellaryspace, Xiphidiumwithin the complex of superior-ovariedtaxa extendedto the externaltissue of the receptacle.Nec- of the Haemodoraceae stillremains a mystery(fig. 43). tary formation,which ancestrallyoccurred between One possibilityis thatXiphidium lost septal nectaries adjacent carpel walls, was displaced to the outer re- altogether(correlated with a shiftin pollinationmech- ceptacle, well beneaththe pointof insertionof thenow anism; see Simpson 1990, 1993) aftera transformation superior ovary. A final evolutionary transformation to a superiorovary with nectariesin the externalre- was the loss of the anteriornectary altogether, perhaps ceptacular tissue, either before or afterreduction in correlatedwith the horizontalorientation of superior- nectarynumber to two (fig. 43). ovaried taxa in the Haemodoraceae (Simpson 1993). Althoughthe evolution of a superiorovary and of Acknowledgments infralocularseptal nectariesare portrayedas two sep- I thank Kim Marsden for help in the histological arate evolutionaryevents in figure43, it is likely that preparationof floral tissue, Scott McMillan for in- they are correlated and occurred concomitantly.As volvementin initial observations,and Gwen Simpson discussed by Simpson (1993), the selective pressure for useful commentson the manuscript. SIMPSON-REVERSAL IN OVARY POSITION 479

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