Phylogenetic Position and Floral Function of (: ) Author(s): S. S. Renner, A. E. Schwarzbach and L. Lohmann Source: International Journal of Sciences, Vol. 158, No. 6, Supplement: Morphology and Evolution of Flowers (Nov., 1997), pp. S89-S98 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/2475169 Accessed: 24-09-2015 08:01 UTC

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This content downloaded from 128.252.67.66 on Thu, 24 Sep 2015 08:01:58 UTC All use subject to JSTOR Terms and Conditions Int. J. Plant Sci. 158(6 Suppl.):S89-S98. 1997. C 1997 by The Universityof Chicago. All rightsreserved. 1058-5893/97/5806S-0007$03.00

PHYLOGENETICPOSITION AND FLORAL FUNCTION OF SIPARUNA(SIPARUNACEAE: LAURALES)

S. S. RENNER,' A. E. SCHWARZBACH, AND L. LOHMANN Departmentof Biology, Universityof Missouri-St.Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121-4499, U.S.A.

Nucleotide sequences for two chloroplastgenome regions, the rbcL gene and the trnL-trnFspacer region, were obtainedfor 22 genera and 30 representingall major lineages of Laurales, witha special samplingeffort being made in the phylogeneticallyproblematic lato. Magnoliaceae, Winteraceae,Austrobaileyaceae, and Saururaceae were used as outgroups.A morphologicalcharacter matrix for the same taxa was compiled and includes new floral-anatomicaldata for Siparunaceae, a lineage traditionallyplaced in Monimiaceae. Phylogeneticanalyses of the molecular and morphologicaldata based on maximum parsimonyreveal that Siparuna and its sister taxon, the monotypicWest Africangenus ,are not closely relatedto the remainingMonimiaceae, supportingthe view thatthe Monimiaceae in the wide sense are polyphyletic.Based on morphologyand chromosomenumbers, Siparuna formsa clade with Atherospermataceaeand Gomortegaceae, while based on rcbL sequences, it is in a clade with Hernandiaceae, ,and Gomortegaceae. The trnL-trnFsequences provide no resolutionfor basal nodes in Laurales but agree with the rbcL and morphologicalanalyses in stronglysupporting a placementof Siparun- aceae away fromMonimiaceae s.str.Based on the phylogenetichypotheses, we analyze some of the reportedfloral- morphologicaltrends noted in Monimiaceae and Laurales, such as miniaturizationof ovules, increasinglycomplete enclosure of reproductiveorgans, and aquisitionof functionalsyncarpy. Both Siparuna and Glossocalyx have polycar- pellate gynoecia embedded in massive receptacles covered by a membraneand uniovulate carpels with unitegmic ovules. The membrane,or floralroof, has a small, central pore for the styles or anthersto emerge at anthesis.It is more developed and thickerin female flowersthan in male ones. Consequently,the stylesin particularare forcedinto close physical contact.Flowers are pollinatedby gall midges thatoviposit into themthrough the pore in the floralroof, wherebythey contact stamens or styles.Anatomical studies of flowersrepresenting eight species show thatstyles fuse postgenitallyat the heightwhere theyemerge throughthe pore, resultingin a joint transmissiontrack for pollen tubes thatoriginally landed on differentstigmas. Lateral growthof pollen tubes,which resultsin switchingbetween carpels, was observed in an experimentallypollinated species thathad received large pollen loads.

Introduction Endress (1979, 1980b, 1982; Endress and Lorence 1983) is fromcompletely free carpels, withoutany in- Comparativestudies of floralevolution in Monimi- tercellularcommunication between theirinner spaces, aceae have emphasized morphological trends that to "functionally syncarpous" gynoecia. Functional seem to characterizebasal angiospermlineages (En- syncarpycan be achieved in differentways, withmor- dress 1980a, 1980b, 1986, 1990, and 1994, pp. 230- phologicallyfree carpels sharingeither a joint pollen- 232). One such trenddiscerned by Endress (see esp. receiving region formed by massive secretions or a Endress 1990) is towardminiaturization of the ovules, pollen-exchange zone at their bases as in Illicium, resultingin unitegmicand/oi tenuinucellar conditions. where tubes can enter adjacent carpels via theirun- While most basal angiospermshave bitegmic ovules fused margins (Williams et al. 1993). Ecologically, with abundantendo- or perisperm,minute ovules oc- these mechanismscould be increasingreproductive ef- cur in both Laurales and Piperales: Calycanthaceae, ficiency.This may be particularlyimportant in groups Lauraceae, and Hernandiaceae have endospermless in which flowershave numerous carpels but solitary seeds; Peperomia has ovules with a single integument ovules: if insect-depositedpollen loads can be distrib- (Tucker 1980; Tucker et al. 1993). Within Laurales, only Siparuna was known untilrecently to have a sin- uted to more than one carpel, this must increase the gle integument(Heilborn 1931; Endress 1972; S. Ren- numberof ovules that can be fertilized.In Laurales, ner,personal observation),but a screeningof potential functionalsyncarpy via a common pool of mucilage relativesof Siparuna revealed the presence of uniteg- is known fromthe monimiaceous genera Faika, He- mic ovules in the monotypicWest Africangenus Glos- dycarya,, Tambourissa,and Wilkiea (En- socalyx, thus providinga potentialsynapomorphy for dress, 1979, 1980b, 1982, and 1994, p. 232). Below a clade consistingof these two genera. Siparuna com- we reporta new type of functionalsyncarpy by post- prises ca. 72 species of ,straggling shrubs, and genital fusion of stylesin Siparuna. , occurringfrom tropical Mexico throughoutthe A thirdtrend noticed by Endress in the Monimi- West Indies and northernSouth America to Bolivia aceae is towardan increasinglycomplete enclosureof and Paraguay (Renner,ongoing revision). The flowers the reproductiveorgans in massive cup-like recepta- are strictlyunisexual and measure a few millimeters cles thatraise the floralperiphery around or above the in diameter(figs. 1, 2). gynoecium.While fleshycupules were presentin now A second floral evolutionarytrend emphasized by extincthigher seed (K. Nixon, personal com- munication),within angiospermsthey characterizea 'Authorfor correspondence and reprints. groupof familiesfirst united under the name Laurineae Manuscript received May 1997; revised manuscriptreceived July by Hallier (1905). The Laurineae (or Laurales) include 1997. the Calycanthaceae (threegenera; includingIdiosper-

S89

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_~~~ _,

Figs.l, 2 Female flowersof Siparuna. Fig. l, S. thecaphora.The floralroof in this species is glabrous and consists of an outerbulge and an inner,narrower collar just visible to the rightof the stylarcomplex. (Real heightof flowerca. 1.6 mm) Fig. 2, S. muricata. The floral roof consists of a wide outer area (not shown) and an innermostcollar thattightly surrounds the styles. Pollen grains visible on stigmatic papillae.

mum), Gomortegaceae (monotypic), Hemandiaceae also examines the hypothesisthat Monimiaceae in the (five genera; including Gyrocarpus), Lauraceae (50 wide sense are polyphyleticas suggestedby R. Brown genera), and Monimiaceae s.l. (i.e., Atherospermata- (1814), Schodde (1969, 1970), Endress (1972), and A. ceae with seven genera, Siparunaceae with two or C. Smith (1972). Our understandingof (floral) evolu- three genera, and Monimiaceae with ca. 18). These tionary trends in Monimiaceae, Siparunaceae, and taxa share several charactersbesides the cup-like re- Atherospermataceaestands to be improvedby knowl- ceptacles, includinginaperturate pollen (except Caly- edge of their closest relatives in Laurales. However, canthaceae and Atherospermataceae)usually withspi- trendsalso need to be relatedto the functionof flowers nulose exines, unilacunartwo-trace nodes (also present in pollinationor . To do this we report in some potentialoutgroups and perhapsplesiomorph- new resultsof floral-anatomicalstudies on Glossocalyx ic), decussate leaves (perhaps plesiomorphicand lost and Siparuna and observationson pollen tube growth in Lauraceae and Hernandiaceae), and carpels with a in Siparuna and relate themto the pollinationof these single ovule (except Calycanthaceae,which have two plants by ovipositinggall midges. ovules of which only one formsa matureembryo sac The molecular data presentedare part of ongoing [Nicely 1965], and Gomortegaceae,which have a 2- work on the phylogeneticsystematics of Laurales. or 3-merous syncarpous gynoecium). Four of seven lauralean familieshave stamensdehiscing by apically- Materialand methods hinged valves and with large, paired nectarglands at Nucleotide sequences of rbcL and/or the trnLUAA3'- the filamentbases. Both charactersseem to have arisen trnFGAA5' intergenicspacer regionof thechloroplast genome early in the evolutionof the orderand to have become were obtainedfrom 30 species (table 1, whichalso lists coupled or uncoupled several times. Thus, the Sipa- voucherinformation for each taxon),representing 22 genera runaceae have valvate antherdehiscence but no glands, and all majorlauralean lineages identified by previousmor- while three genera of Monimiaceae s.str. (Hortonia, phologicaland molecularstudies (Qiu et al. 1993,personal Peumus, and Monimia with togetherfive or six spe- communication;J. A. Doyle, personalcommunication; K. have or also lateral de- Ueda, personal communication).Thirteen rbcL sequences cies) longicidal (in Monimia) were obtainedfrom GenBank (table 1); two rbcL and 19 hiscence and glands on the filamentbases. trnL-trnFsequences were produced for this study; and an This article places the three floral-morphological rbcL sequence of (Ueda et al. 1997) was con- trends,miniaturization of ovules, increasinglycom- tributedby K. Ueda (personal communication). As out- plete enclosure of reproductiveorgans, and aquisition groups we used Magnolia macrophylla and M. hypoleuca of functionalsyncarpy, in a phylogeneticcontext. It (Magnoliaceae), Drimys winteri(Winteraceae), Austrobail-

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Table1

SOURCES OF rbcL AND trnL-trnFSEQUENCES USED IN THIS STUDY GenBank accession numbers Taxon Voucher or citation rbcL trnL-trnF Atherospermataceae: aromatica (FM. Bail.) L.S. Smith ...... Ablettet al. 1997 L77211 .. sempervirens(R. & P.) Tul...... EdinburghBot. Gard. 19931681 ... AF012402 Calycanthaceae: Calycanthusoccidentalis Hook. & Arn...... Missouri Bot. Gard. 897423 AF012396 Calycanthusfloridus L...... Chase et al. 1993 L14291 ... Chimonanthuspraecox (L.) Link ...... Qiu et al. 1993 L12639 ... Idiospermumaustraliense (Diels) S.T Blake ...... Qiu et al. 1993 L12651 ... Gomortegaceae: Gomortegakeule (Molina) I.M. Johnson...... Ueda et al. 1997 D89561 ... Gomortegakeule (Molina) I.M. Johnson...... Rodriquez 3070 (CONC) ... AF012404 Hernandiaceae: Gyrocarpusamericanus Jacq...... Qiu et al. 1993, DNA aliquot L12647 AF012398 Hernandia albiflora (C.T White) Kubitzki ...... Ablettet al. 1997 L77210 Hernandia ovigera L ...... Qiu et al. 1993, DNA aliquot L12650 AF012397 Lauraceae: Cinnamomumcamphora (L.) T Nees & Eberm...... Qiu et al. 1993 L12641 ... Litsea japonica (Thun.) Juss...... PG. Martinand J. Dowd, unpubl. U06843 ... Nectandra turbacensis(Kunth) Nees ...... Taylor 11746 (MO) ... AF012400 Ocotea leucoxylon(Sw.) Lanessan ...... Taylor 11733 (MO) ... AF012399 Persea americana Mill...... Golenberg et al. 1990 X54347 ... Persea americana Mill...... Missouri Bot. Gard. 897543 ... AF012401 Monimiaceae: Hedycarya arborea J.R. & G. Forst...... Qiu et al. 1993, DNA aliquot L12648 AF012412 Hennecartia omphalandraPoisson ...... Pena s.n. (MO) AF022950 ... Kibara coriacea (Bl.) Tul...... Coode 7879 (K), DNA aliquot ... AF012413 Peumus boldus Molina ...... EdinburghBot. Gard. 19870707 ... AF012403 Tambourissaficus (Tul.) A. DC ...... National Trop. Bot. Gard. 940043 ... AF012410 Tambourissa tau Lorence ...... National Trop. Bot. Gard. 940044 ... AF012411 Siparunaceae: Glossocalyx longicuspisBenth ...... Sothers 2109-74 (INPA) ... AF012407 Siparuna brasiliensis(Spreng.) A. DC ...... Stahl 2254 (QCA) ... AF012406 Siparuna depressa Jangoux ...... Madrinadnet al. 1504 (COL) AF012409 Siparuna lepidota (H.B.K.) A. DC ...... Pignal 309 (P) AF013246 AF012409 Siparuna sessiliflora(H.B.K.) A. DC ...... Bos 4659 (MO) ... AF012405 Magnoliaceae: Magnolia hypoleuca Siebold & Zucc ...... Qiu et al. 1993 L12655 ... Magnolia hypoleuca Siebold & Zucc ...... Missouri Bot. Gard. 732556 ... AF012395 Winteraceae: Drimyswinteri J.R. & G. Forster ...... Albertet al. 1992 L01905 Austrobaileyaceae: Austrobaileyascandens C.T White ...... Qiu et al. 1993 L12632 Saururaceae: Saururus cernuusL ...... Chase et al. 1993 L14294

eya scandens (Austrobaileyaceae), and Saururus cernuus Sequences were aligned visually (the rbcL sequences had (Saururaceae), a choice reflectingthe currentuncertainty no gaps, the trnL-trnFsequences, very few gaps). The mo- about relationshipsin the Magnoliidae. lecular data were analyzed with PAUP 3.1.1 (Swofford Total DNA was extractedfrom fresh or silica gel-dried 1993), using Multiple Parsimony (MULPARS) and the leaves, using the CTAB method (Doyle and Doyle 1987). branch-and-boundsearch option. Number of potentiallyin- Following DNA purificationwith QIAGEN Genomic-tip formativecharacters, number- and length of most-parsimo- columns (G-20; QIAGEN 1995), targetloci were amplified nious trees, consistency index (uninformativecharacters by PCR with a Hybaid Thermal Cycler. A 5' primerthat excluded), and retentionindex were obtained fromPAUP anneals to the first16 base pairs of the rbcL gene (IF) and The robustnessof treeswas evaluated by bootstrapping(Fel- a 3' primer(1460R ) thatanneals to a flankingregion down- senstein 1985), using 100 replicates.The presentarticle fo- streamfrom the 3' end was used to amplifythe entirechlo- cuses on theposition of Siparuna and its immediaterelatives roplast-encodedrbcL gene, while the e and f primers(Ta- in Laurales, and thereforeonly a small numberof represen- berlet et al. 1991) were used for amplificationof the tativesof otherlauralean lineages were included in the anal- intergenicspacer. Single-strandedDNA productswere pu- yses as place holders once the monophylyof these lineages rified with the QlAquick PCR Purificationkit (QIAGEN was clear (cf. table 1). This is the case for - 1997) and automaticallysequenced. taceae (Schodde 1969; Renner et al. 1997, and ongoing

This content downloaded from 128.252.67.66 on Thu, 24 Sep 2015 08:01:58 UTC All use subject to JSTOR Terms and Conditions S92 INTERNATIONAL JOURNAL OF PLANT SCIENCES work), Lauraceae (Rohwer 1993; H. van der Werff,personal 9. Epigyny: 0 = absent, 1 = present. communication;ongoing work in our lab), and Calycantha- 10. Chromosome base number: 0 = 19, 1 = 11-12, 2 = 21- ceae (includingIdiospermum; Qiu et al. 1993). The mono- 22, 3 = 39 (Peumus), 4 = 44 (Monimia), 5 = 96 (Hen- phyly of Hernandiaceae (including Gyrocarpus) needs fur- necartia). Hernandiaceae and Winteraceae,which have thertesting (see also Kubitzki 1993c); currently,sequences variable chromosome numbers, were coded as "?." Data are available for threespecies representingtwo of five gen- fromMorawetz (1986). era, Hernandia and Gyrocarpus,and these do not always 11. Ovules: 0 = several ventral, 1 = one apical, 2 = one group together. basal, 3 = two ventral(autapomorphic for Calycantha- For the morphological cladistic analysis, data were de- ceae). The syncarpousGomortegaceae were scored in- rived from S. S. Renner's observations of herbariumand applicable for this characterbecause of unclear homol- living materialas well as fromthe literature,as notedbelow ogies. in the discussion of individualcharacters. Particularly useful 12. Number of integuments:0 = two, 1 = one. Data for were the familysummaries found in Kubitzki et al. (1993) Gomortega fromP K. Endress and A. Igersheim(per- and the charactermatrix compiled by Donoghue and Doyle sonal communication). (1989) fortheir phylogenetic analysis of basal angiosperms. 13. Fruit type: 0 = drupe (endozoochorous, buoyant, or Donoghue and Doyle (1989) found that Monimaceae s.l., winged, that is, dispersed in differentways), 1 = Gomortegaceae, Hernandiaceae, and Lauraceae (termed achene, 2 = capsule (autapomorphicfor Magnoliaceae), "core Laurales" and abbreviated "MON" in their trees) 3 = enclosed druplets(inside a fleshyreceptacle that were united by stamen filamentswith basal nectaries and usually tears open at maturity),4 = berry. inaperturatepollen. In a preliminaryanalysis, not published 14. Endosperm: 0 = present, 1 = absent. in Donoghue and Doyle (1989), they had broken up the 15. Nodes: 0 = tri- or multilacunar,1 = unilacunar.Data Monimiaceae into Atherospermataceae,Siparunaceae, Mon- fromMoney et al. (1950). imiaceae s.str.,and Hortonia. The resultingtree, but not the Parsimony analyses of morphological data were per- data matrix,was published in Doyle et al. (1994) as figure formedwith PAUP 3.1.1 using Multiple Parsimony(MUL- 8b, and an unpublishedelectronic version of the matrixwas PARS), Accelerated Transformation,and the branch-and- kindlysent to us by JimDoyle. It contains 28 charactersof bound option. which 10 appear in our matrix,albeit sometimes with dif- Field observationson floralfunction and experimentson ferentcodings. To achieve greaterresolution within Laura- pollen tube growthwere made by D. Schulz-Burck(as part les, we added five charactersto yield a total of 15 (appen- of his MSc project,Schulz-Burck 1997) in the Ducke Forest dix); all were unorderedand polarized using Magnoliaceae, Reserve near Manaus, Brazil (59?58'W, 2?53'S). Controlled Winteraceae,and Austrobaileyaceaeas outgroups. pollinationswere performedon Siparuna cristata (Poeppig 1. Vegetativephyllotaxy: 0 = alternate,1 = decussate, 2 & Endl.) A. DC. by rubbingentire fresh male flowersonto = spiral-alternate. receptivestigmatic areas. Receptiveness of stigmaswas as- 2. Floral cup, cupular receptacle,or cupule: 0 = absent, 1 sessed by the fresh,glossy green appearance of stigmatic = present. papillae; postantheticpapillae appear brown.Treated flowers 3. Innermosttepals: 0 = free,1 = connate.Mollinedia was were collected after15 h, togetherwith other flowers in dif- scored as inapplicable for this characterbecause its pis- ferentstages of development.In addition,flowers from four tillateflowers have a calyptrawhile the staminateflowers other species (S. decipiens [Tul.] A. DC., S. depressa Jan- have free tepals. goux, S. guianensis Aublet, and S. poeppigii [Tul.] A. DC.) 4. Fixed stamennumber: 0 = absent, 1 = present. were collected from tagged trees already vouchered and 5. Basal filamentglands: 0 = absent, 1 = present. identifiedby SSR as partof an ongoing floristicproject cur- 6. Antherdehiscence: 0 =- longicidal, 1 = valvate with 2 rentlybeing carried out at the InstitutoNacional de Pes- pollen sacs, 2 = valvate with fourpollen sacs. The last quisas da Amaz8nia and the Royal Botanic Gardens Kew. is an autapomorphyof Lauraceae, which ancestrallyare Voucher specimens (collected by projectstaff) are deposited thoughtto have had fourpollen sacs per anther.We opt- in the herbariumof the InstitutoNacional de Pesquisas da ed for this coding to reflectthe possibilitythat valvate Amaz8nia. All flowerswere preserved in FAA (formalin- antherdehiscence in Lauraceae is not directlyhomolo- acetic acid-alcohol) and later stored in 70% alcohol to be gous to thatin the otherlauralean groups. dissected and/ortrimmed and sectioned to reveal stages in 7. Apertures:0 = monosulcate, 1 = meridionosulcateor floraldevelopment. For comparison,spirit-preserved flowers dicolpate (autapomorphicfor Atherospermataceae), 2 = of S. aspera (Ruiz & Pavon) A. DC., S. muricata (Ruiz & disulculate(autapomorphic for Calycanthaceae), 3 = in- Pavon) A. DC., and S. thecaphora (Poeppig & Endl.) A. aperturate,4 = porate (autapomorphicfor Winteraceae). DC. fromEcuador were also sectioned.For sectioning,flow- Data for Atherospermataceaeand Monimiaceae from ers were embedded in Historesin (Leica); sections were Sampson (1993, 1996, in press), Foreman and Sampson stained with Toluidine blue. (1987), and Sampson and Foreman (1990); data forLau- Species concepts follow a monographof Siparuna (Ren- raceae, Hernandiaceae,Gomortegaceae, and Calycantha- ner and Hausner,in press; Renner,in prep.). ceae fromHesse and Kubitzki (1983), van der Merwe et al. (1990), and Kubitzki (1993a, 1993b, 1993c). Resultsand discussion 8. Carpels: 0 = several free, 1 = one, 2 = syncarpous. The last is an autapomorphyof Gomortegakeule, which has PHYLOGENETICRELATIONSHIPS OF THE syncarpousovaries of 2-3 carpels (Leinfellner1968); the MONIMIACEOUSGROUPS characteris included here because of our interestin its possible origin. Tambourissa and Hennecartia were The rbcL maximum parsimonyanalysis found six scored inapplicable forthis characterbecause the former equally parsimonioustrees (L = 403 steps; CI [Con- has numerouscarpels embedded in the receptacle tissue sistencyIndex, informativecharacters only] = .722; while the latterhas 1 (-2) carpels. RI [RetentionIndex] = .576), the strictconsensus of

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29 | Calycanthus 28 10loo IChimonanthus Calycanthaceae 99 Idiospermum Doryphora | Atherospermataceae H. ovigera 20 18 | 27 19 | loo0 IH. albiflora Hemandiaceae <50 | 59 5 1 Gyrocarpus Siparuna | Siparunaceae 21 , Hedycarya Monimiaceae Hennecartia 24 <50 22 Persea 23 | 64 | Litsea Lauraceae 100 Cinnamomum I Winteraceae 25 | Drimys...... 26 S S t Magnolia...... IMagnoliaceae Austrobaileya|Austrobaileyaceae Saururus | Saururaceae Fig.3 Strictconsensus of the six shortesttrees obtained fromthe rbcL analysis (L = 403 steps; CI .722; RI = .576). The numberof character-statetransitions supporting each node is given above the horizontallines, percentage bootstrap replicability below the lines. Inclusion of an rbcL sequence of the monotypicChilean familyGomortegaceae in the analysisplaces Siparuna as sisterto Hernandia and Gyrocarpus, while Gomortegabecomes sisterto Doryphora (Ueda et al. 1997; K. Ueda, personal communication). which is shown in figure3. Siparuna formsa trichot- mortega in the data set. The rbcL data thus indicate omy withAtherospermataceae and Hernandiaceae.In- thatthe Monimiaceae in the wide sense are polyphy- clusion of an unpublishedrbcL sequence of the mono- letic: theirrepresentatives Siparuna, Doryphora,Hen- typic Chilean family Gomortegaceae in the analysis necartia, and Hedycarya come out in three different resolves the trichotomyand places Siparuna as sister places in the Laurales. to Hemandiaceae, while Gomortega is sister to Ath- Parsimonyanalysis of the trnL-trnFsequences re- erospermataceae(K. Ueda, personal communication, sultedin 16 equally parsimonioustrees (L = 191 steps; July 1997). The Monimiaceae s.str. (Hedycarya and CI = .838; RI = .875), the 50% majorityrule consen- Hennecartia) are sisterto the Lauraceae, a relationship sus of which is shown in figure 4. In the strict thatis not affectedby the presence or absence of Go- consensus, the Hernandiaceae-Lauraceae-Monimi-

CalycanthusICalycanthaceae 20 Hernandia Ir 100 Gyrocarpus Hemandiaceae Ocotea 22 21 r 22 1 55 Nectandra Lauraceae 25 99 l Persea 56 Peumus 23 . Tambourissa 24 92 T. ficus Monimiaceae 93 Hedycarya Kibara Laurelia Atherospennataceae Gomortega Gomortegaceae 29 Glossocalyx 28 26 | S. lepidota 100 2 86 S. brasiliensisSiparunaceae S. sessiliflora 100 S. depressa Magnolia | Magnoliaceae Fig.4 Phylogenetichypothesis for Laurales based on the majorityrule consensus of 16 equally parsimonioustrees obtained from the trnL- tmnFanalysis (L = 191 steps; CI = .838; RI = .875). The numberof character-statetransitions supporting each node is given above the horizontallines, percentagebootstrap replicability below the lines. In the strictconsensus, the Hernandiaceae-Lauraceae-Monimiaceaeclade collapses.

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7.2 11.3 13.1 Calycanthaceae ic, his view of the Atherospermataceaeas close to the Hemandiaceae Gomortegaceaeis supportedby parsimonyanalyses of 10.1 14.11 1 Lauraceae rbcL data (Ueda et al. 1997). 4.1 5.1 8. .2 Glossocalyx OF .1 1021 I Siparuna MINIATURIZATION OVULES .13. 1.1133GomortegaceaeI1 6.1 10.2 11.2 . . Endress (1990) identifieda trendtoward miniaturi- 5.1 7.1 13.1Atherospermnataceae Hedycarya zation of ovules in Laurales. Based on the phyloge- l ll ~~~~~~~~Tambourissa I 1113.3 netic hypotheses (figs. 3-5), it apparentlyoccurred 2.1 115.1110.3 Peumus with differentmorphological manifestations in several 115.15.11l 102Monimia Kibara unrelatedclades: once witha loss of endosperm(char. Hennecartia 14.1 in fig. 5) in the Calycanthaceae,Hernandiaceae, Wilkiea and Lauraceae; a second time witha loss of one of the Mollinedia two integuments(char. 12.1) in Siparuna and Glos- 1I Hortonia socalyx. 5.1 ~--~~-Magnoliaceae Differentspecies of Siparuna have between three .2 Winteraceae Austrobaileyaceae and 35 carpels, or potentialseeds, and the tightpack- 10.2 ing of these numerouscarpels in the floralcups may Fig.5 Strictconsensus of the 38 shortesttrees obtained from the have selected fordiminutive carpels and ovules. (Male morphologicalanalysis (L = 38 steps; CI = .789; RI = .778). Num- flowershave 2-72 stamens immersedin a fleshyre- bers referto charactersas discussed in the textand are followedby ceptacle of the same general shape as that of female characterstates as listed in appendix; equivocal states not shown. See textfor discussion. flowers.There are no consistentpatterns in termsof size differencesor numbers of reproductiveorgans among male and femaleflowers.) Siparuna ovule mor- aceae clade collapses. Exclusion of the calycantha- phology has been studiedin detail by Heilborn (1931, ceous sequence resulted in an almost completelyre- S. eggersii), Endress (1972, 1980b; S. thecaphora as solved single most parsimonioustree (L = 168; CI = S. nicaraguensis), and Schulz-Burck (1997; esp. S. .863; RI = .903), indicatingthat Calycanthaceae and thecaphora,S. cristata,S. guianensis). All investigated outgroups need to be sampled more broadly. In all species have ovules witha single integument.Sections trees, Siparuna and Glossocalyx form a clade sup- of liquid-preservedflowers of Glossocalyx longicuspis portedby a bootstrapvalue of 100% and the highest Benth.,the closest relativeof Siparuna based on flow- numberof nucleotide changes (22) found on the . er morphology(below) and trnL-trnFspacer sequenc- As in the rbcL data, thereis no supportfor a mono- es (fig. 4), showed that Glossocalyx, too, has ovules phyleticMonimiaceae. with a single integument(contra Philipson 1987, Parsimony analysis of the morphological matrix 1993). This provides a synapomorphyfor these two yielded 38 equally parsimonioustrees (L = 38 steps; genera because all otherlauralean groups have ovules CI = 0.789; RI = 0.778), the strictconsensus of which withtwo integuments(P. K. Endress and A. Igersheim, is shown in figure5. The only synapomorphywe could personal communication).Together with Atherosper- findfor Laurales is the presence of a well-developed mataceae, Siparuna and Glossocalyx are among the cup-like receptacle (character[char.] 2.1 in fig. 5). A few angiospermsthat have plicate carpels with mar- doublingof the chromosomenumber from n= 11 (char. ginal closure and basal insertionof the ovules. 10.1) to n=22 (10.2) appears to distinguishtwo major Glossocalyx consists of a single species of strag- clades withinthe ,and staminalglands (fig. 5.1) gling shrubsand is quite common along forestmargins appear to have arisen several times. The sistergroup in Cameroon (D. Thomas and R. Condit, personal relationshipbetween Siparuna and Glossocalyx is sup- communication).It differsfrom Siparuna in having ported by char. 3.1 (innermosttepals connate and stronglyasymmetric leaf pairs and perigons,but shares forminga floralroof) and 12.1 (one integument).In withthat at least threeuniquely derived features: addition,they share disporangiateanthers in whichthe disporangiateanthers in which the two thecae open by two thecae open not by two, but by a single or incom- a single or incompletelyseparated flap; the possession pletely separated flap, a unique state in the Magnoli- of a floralroof (below); and ovules with a single in- idae (Endress and Hufford1989). tegument.Because of the firsttwo features,Glosso- The results of all three analyses (rbcL, trnL-trnF, calyx has long been interpretatedas being closely re- morphology)thus supportthe conclusion of Schodde lated to Siparuna (Bentham 1880, pl. 1301; contra (1969, 1970) who suggested that the Atherosperma- Philipson 1987, 1993), a hypothesissupported by the taceae, which he monographed,as well as the Sipa- data reportedhere. runaceae (Glossocalyx, Siparuna, and an enigmatic close relativeof Siparuna, Bracteanthuswith two spe- ENCLOSURE OF REPRODUCTIVE ORGANS AND FUNCTION cies in Brazil) should be recognizedat the familylevel OF FLOWERS IN POLLINATION because there was no evidence that either shared a An unusual featureof Siparuna flowersis a mem- unique common ancestor with the Monimiaceae or brane, called the floralroof or velum. This membrane each other.Although Schodde's approach was phenet- covers the sexual organs except fora small pore in the

This content downloaded from 128.252.67.66 on Thu, 24 Sep 2015 08:01:58 UTC All use subject to JSTOR Terms and Conditions RENNER ET AL.-PHYLOGENETIC POSITION AND FLORAL FUNCTION OF SIPARUNA S95 center. At anthesis, the styles or anthers emerge throughthis pore. In male flowers,the membraneis thin and sometimestears. In female flowers,it forms a thick collar that surroundsthe emergingstyle tips tightly,and it does not tear (figs. 1, 2). There are no diurnalmovements of floralparts. Based on his study of S. thecaphora (as S. nicaraguensis), Endress sug- gested thatthe floralroof evolved froman innerwhorl of tepals thathave become completelyfused: "the ve- lum is initiatedin a ring-likezone of nearlynonmer- istematictissue between the ... tepal primordiaand the highlymeristematic floral apex in the centreof the floralcup" and "its position between the tepals and the sporophyllsand its veryearly initiation ... suggest that it may have evolved froman inner whorl of te- pals" (Endress 1980b). Pollinationin Siparuna has been studiedin Ecuador (Feil and Renner 1991; Feil 1992) and in Manaus (Schulz-Burck 1997). Siparuna is pollinated at night by cecidomyiids (Asynapta, Clinodiplosis, and Dasi- neura, Oligotrophini, Pornicondylinae).These gall midges are ca. 3 mm long and capable of directed flight(although usually poor fliers;R. Gagn6, personal communication).They are nocturnaland find food, Fig.6 Siparuna thecaphora. Transversesection of flowerat the heightwhere the styles (in this case 14) pass throughthe pore in mates, and oviposition sites by scent. Receptive Si- the floralroof. Note the small-celledcollar formedby the floralroof paruna flowers,like the rest of the plant,are strongly aroundthe stylarcomplex and the stylarexudate (staineddark blue). lemon-scented.Female midges alighton flowers,insert Abundantyellow oil inclusions are typicalof Laurales. their abdomens into the pore in the floral roof, and then move it rhythmicallyfor ca. 1-2 min during which theydeposit an egg into the flower.Gall midges the presence of large nectary glands at the filament have long hairs on theirabdomens (Gagne 1989), and bases it is likely to be by small flies or bees. Phylo- pollen grainsbecome lodged betweenthese hairs when genetically,Siparunaceae may have evolved froman- the abdomen is insertedinto male flowers.Plant-feed- cestors that had stamens with nectar glands and re- ing midges distributetheir numerous eggs onto differ- warded their pollinators with liquid food. With an ent flowersand plants (Gagn6 1989). Sixty of the 72 evolutionaryswitch fromsmall bee or flypollination species of Siparuna are dioecious and can only set oviposition sites as a fruitif theyare visitedand pollinatedby insects,which to gall midge pollination and implies that pollen-covered midges visit both sexes reward,nectar glands may have become unnecessary regularly.Tropical midge species produce a new gen- (these large convex glands also seem unsuitedfor nec- eration every 10-20 d (Gagn6 1994), and flowersof tar-uptakeby gall midge mouthparts). differentspecies of Siparuna last 3-24 d (Feil 1992; Gall midge pollination,which afterall involves the Schulz-Burck 1997). Larvae may thereforecomplete presence of plant-feedinglarvae in flowers,may also developmentin flowerson the tree,or theymay hatch have providedthe selective pressurefor floral closure, fromflowers that have fallen to the ground.In popu- at least of the female flowers,to preventexcessive lations studiedin Ecuador (Feil and Renner 1991; Feil damage. When a midge visitsa femaleflower, she tries 1992), male flowersregularly contain at least two ce- to inserther ovipositorinto the pore of the floralroof, cidomyiid larvae (which can be identifiedby their but differentfrom the situationin staminateflowers, characteristicmorphology) while female flowersand the pore in pistillate ones is smaller and moreover mature fruitsalmost never do. Thus, either female closed by the densely packed styles(figs. 1, 2, 6). We flowersare less suitable as egg-layingsites or female have never found larvae or eggs inside stylartissue, flowerswith larvae abort. supportingthe idea thategg layinginto the stylarcom- Of the otherlauralean lineages,Atherospermataceae plex is rare. Apparently,the contact between pollen- are pollinated by flies and bees (Schodde 1969), Ca- carryingmidge abdomens and styles during (unsuc- lycanthaceaeby beetles (summaryin Kubitzki 1993a), cessful) ovipositionattempts is enough to ensure pol- Lauraceae by small bees, flies, and sometimesthrips lination.Over evolutionarytime, an increasingclosure (Kubitzki and Kurz 1984; Norton 1984; D. Roubik, of flowersto protectthem against egg-layingmidges personal communication),and Monimiaceae s.str.by would have leftless and less space forglandular struc- flies and small beetles (Lorence 1985). Pollinationin tures on the stamens,but it is difficultto disentangle Hernandiaceae and Gomortega keule remainsunstud- the sequence of these ecological and morphological ied, but based on the size and shape of the flowersand changes.

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FUNCTIONAL SYNCARPY aceae (Kubitzki 1993b; contra Schodde 1969, 1970), but in termsof wood anatomyit is closest to Athero- The third floral-morphologicaltrend identifiedby spermataceae (H. G. Richter,personal communica- Endress (1979, 1980b, 1982) in lower angiosperms tion). Its chromosome number of n=21 (Goldblatt concernsthe aquisition of functionalsyncarpy in apo- 1976) fitswell withthose of both Atherospermataceae, carpous gynoecia. Two formsof this have evolved in n=22, and Siparunaceae, n=22, while Hemandiaceae the Laurales, all of themin lineages with strictlyuni- are strikinglyvariable in chromosomenumber (Mor- sexual flowers.In the Monimiaceae s.str.,styles and/or awetz 1986). the upper rim of the floral cup may secrete large amountsof mucilage (Faika, Hedycarya,Hennecartia, Conclusions Tambourissa, Wilkiea). Pollen loads germinatein this mucilage and may be distributedonto differentcarpels Reconstructionof phylogeneticrelationships within (each with one ovule). In Siparuna and Glossocalyx, Laurales is still in its initial phase. This investigation by contrast,functional syncarpy is achieved by fusion has shown how the topological position of Siparuna of the styles, startingjust below the point at which near Glossocalyx,the Hemandiaceae, Gomortegaceae, they emerge throughthe pore in the floralroof (figs. and Atherospermataceae,and away from the Moni- 1, 2, 6). The tightpacking of the stylesapparently sets miaceae s.str.,affects the interpretationof the evolu- the stage for theirpostgenital fusion and thus the de- tion of floral-morphologicaltrends in thisgenus. How- velopmentof a joint pollen transmissiontrack. In the ever, floralmorphological trends, such as the loss of eight species of which flowers were sectioned (see nectaryglands in the androeciumof Siparuna and the "Material and Methods" for species names), stylar evolution of its closed flowersand stylarcomplexes, complexes of various lengths(0.3 mm long in thevery need to be placed in an ecological as well as phylo- small flowersof S. depressa, ca. 1 mm long in S. poep- genetic context.Thus, the peculiar pollinationof Si- pigii) and complexitywere observed,with the identity paruna by ovipositinggall midges is what set the stage of individualstyles more or less lost in the centerpor- for loss of nectar and divergencebetween male and tion of the stylar complexes. In S. cristata, Schulz- female flowersin the extentto which they are sealed Burck (1997) was able to reconstructthe path individ- off and protected.Postgenital stylar fusion may have ual pollen tubes had taken in the stylarcomplex in arisen as a means to completelyclose the centralpore, consecutive cross sections from the stigmaticareas the only opening in the floralroof and latermay have down to where tubes enteredthe carpel and then mi- assumed a role in interstylarexchange of pollen tubes cropyle. Lateral growthof pollen tubes in the middle between basally free carpels. portionof stylarcomplex, and thus switchingbetween Acknowledgments "styles," was observed in a flowerthat had been ex- perimentallypollinated and thus had received (unusu- We thankJim Doyle fordiscussion of lauraleanphy- ally?) large pollen loads. Nothingis known about the logeny, Hans Georg Richterfor dittoof wood anato- size of pollen loads normallydeposited on stigmasby my, Bruce Sampson for access to at-the-timeunpub- midges. Based on field and herbariumobservations, lished palynological data, Rick Condit and Thomas seed set in Siparuna seems regular,with young fruiting Duncan for Glossocalyx flowersfrom Cameroon, and flowers containing only slightlyfewer fruitletsthan Mike Hopkins and Cynthia Sothers for helping S. S. theyhave carpels. Renner's student,D. Schulz-Burck,with his studyof Based on rbcL data (fig.3), Siparunaceae are closest Siparuna pollinationin the Ducke forestreserve near to Hernandiaceae, Gomortegaceae, and Atherosper- Manaus. Bruce Sampson, Peter Endress, and Gerlinde mataceae, while morphologicallythey are closest to Hausner kindly commented on the manuscript.The the Atherospermataceaeand Gomortegaceae (fig. 5); National Tropical Botanical Garden, Lawai, Kauai, the trnL-trnFdata provide no resolutionat this level Hawaii, the Royal Botanic Garden Edinburgh,and the (fig. 4). Gomortega keule is the only species in the Missouri Botanical Garden provided leaf material as Laurales with a syncarpous and inferiorgynoecium. did Carlos Baeza, Bertil St'ahl,Marc Pignal, and San- Gynoecia in Hernandiaceae are inferiorbut not syn- tiago MadriiaTn.Total DNA extractsof Gyrocarpus, carpous, while Siparunaceae and Atherospermataceae Hernandia, and Hedycarya were generouslyprovided have perigynousflowers and apocarpous gynoecia.Be- by Yin-Long Qiu, an extract of Kibara came from cause of its pollen exine structureGomortega has tra- Mark Chase's lab, and Kanehiko Ueda completedthe ditionallybeen placed near Lauraceae and Hernandi- rbcL data set with a sequence of Gomortega.

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Appendix

DATA SET USED IN MORPHOLOGICAL CLADISTIC ANALYSIS OF LAURALES

1 6 11 Austrobaileyaceae 1 0 0 0 0 0 0 0 0 1 0 0 4 0 1 Magnoliaceae 2 0 0 0 0 0 0 0 0 0 0 0 2 0 0 Winteraceae 2 0 0 0 0 0 4 0 0 ? 0 0 4 0 0 Calycanthaceae 1 1 0 0 0 0 2 0 0 1 3 0 1 1 1 Hedycarya 1 1 0 0 0 0 3 0 0 0 1 0 0 0 1 Tambourissa 1 1 0 0 0 0 3 ? 0 0 1 0 3 0 1 Peumus 1 1 0 0 1 0 3 0 0 3 1 0 0 0 1 Monimia 1 1 0 0 1 0 3 0 0 4 1 0 3 0 1 Kibara 1 1 0 0 0 0 3 0 0 1 1 0 0 0 1 Hennecartia 1 1 0 0 0 0 3 ? 0 5 1 0 3 0 1 Wilkiea 1 1 0 0 0 0 3 0 0 0 1 0 0 0 1 Mollinedia 1 1 ? 0 0 0 3 0 0 0 1 0 0 0 1 Hortonia 1 1 0 0 1 0 3 0 0 0 1 0 0 0 1 Glossocalyx 1 1 1 0 0 1 3 0 0 ? 2 1 3 0 1 Siparuna 1 1 1 0 0 1 3 0 0 2 2 1 3 0 1 Gomortegaceae 1 1 0 0 1 1 3 2 1 2 ? 0 0 0 1 Atherospermataceae 1 1 0 0 1 1 1 0 0 2 2 0 1 0 1 Hernandiaceae 0 1 0 1 1 1 3 1 1 ? 1 0 0 1 1 Lauraceae (0/1) 1 0 1 1 2 3 1 0 1 1 0 0 1 1

Note. Inapplicable data and missing data are indicated as "?" and polymorphisms are enclosed in brackets.

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