sign in sign up
<<
Home , Actinodaphne, Aiouea, Aniba, Apollonias, Apollonias barbujana, Aspidostemon

PHYLOGENY Andre'S. Chanderbali,2'3Henk van der AND HISTORICAL Werff,3 and Susanne S. Renner3 BIOGEOGRAPHY OF : EVIDENCE FROM THE CHLOROPLAST AND NUCLEAR GENOMES1

ABSTRACT

Phylogenetic relationships among 122 of Lauraceae representing 44 of the 55 currentlyrecognized genera are inferredfrom sequence variation in the chloroplast and nuclear genomes. The trnL-trnF,trnT-trnL, psbA-trnH, and rpll6 regions of cpDNA, and the 5' end of 26S rDNA resolved major lineages, while the ITS/5.8S region of rDNA resolved a large terminal lade. The phylogenetic estimate is used to assess morphology-based views of relationships and, with a temporal dimension added, to reconstructthe biogeographic historyof the family.Results suggest Lauraceae radiated when trans-Tethyeanmigration was relatively easy, and lineages are established on either Gondwanan or Laurasian terrains by the Late . Most genera with Gondwanan place in Cryptocaryeae, but a small group of South American genera, the -Mezilauruls lade, represent a separate Gondwanan lineage. and may be the only extant representatives of the ancient Lauraceae docu- mented in Mid- to Late Cretaceous Laurasian strata. Remaining genera place in a terminal Perseeae-Laureae lade that radiated in Early Eocene Laurasia. Therein, non-cupulate genera associate as the group, and cupuliferous genera sort to Laureae of most classifications or Cinnamomeae sensu Kostermans. Laureae are Laurasian relicts in . The Persea group and group (of Cinnamomeae) show tropical amphi-Pacific disjunctions here credited to disruption of boreotropical ranges by Eocene- climatic cooling. The complex accommodates re- maining Cinnamomeae and shows a trans-Atlantic disjunction possibly derived from a Madrean-Tethyan ancestral distribution.These findings support Laurasian ancestry for most extant Lauraceae, with their considerable neotropical representationprimarily derived fromEarly radiation of the Ocotea complex upon reaching . Key words: biogeography,boreotropical, chloroplast DNA, , Lauraceae, Laurasia, Madrean-Tethyan,mo- lecular clock, phylogeny,ribosomal DNA.

Lauraceae forma large familyof woodyplants prominent components of lowland and are (except the herbaceous parasite ),with frequentlydominant elements in montane vegeta- about50 generaand 2500 to 3000 species distrib- tion (Gentry,1988). uted throughouttropical to subtropicallatitudes. Given their antiquity, widespread distribution, They are among the more speciose basal angio- and ecological prominence, Lauraceae provide a spermfamilies and have a fossilrecord that reaches model system for investigating angiosperm bioge- back to the Mid-Cretaceous(Drinnan et al., 1990; ography. Moreover, the three tribes recognized by Eklund & Kvacek, 1998). Currenttaxonomic di- van der Werffand Richter (1996) suggest thatmajor versityis centeredin tropicalAmerica and Aus- divisions in the familydraw along geographic lines. tralasia,and althoughpoorly represented in conti- Laureae include three genera with North Ameri- nentalAfrica, Lauraceae flourishin .In can-Asian disjunctions (, , ), the Americantropics they list among the most Mediterranean , and Asian endemics (e.g.,

I The authorsthank anonymous reviewers for insightful comments; K. Ueda foreight unpublished trnL-trnF sequenc- es; J. Rohwerfor six unpublishedITS sequences; M. Zanis forfive at the timeunpublished ITS/5.8S/26S sequences; Y-L. Qiu forproviding three DNA aliquots;the HarvardHerbaria for providing materialof ; Andrea Schwarzbachfor guidance in moleculartechniques; and innumerablecolleagues who helped to collect materialof Lauraceae forthis study.This studywas undertakenas partof ASC's doctoraldissertation research at the University of Missouri-St.Louis, and was supportedby grantsfrom the MallinckrodtFoundation administered by theInternational Centerfor Tropical Ecology, University of Missouri-St. Louis, and fromthe Smithsonian Institution's Biological Diversity ofthe Guianas Program to ASC; NationalGeographic Society grants 4631-91, 5635-96,and 6571-99 to HW; and grants fromthe Universityof Missourisystem and Universityof Missouri-St.Louis to SSR. This articleis Number45 in the SmithsonianInstitution's Biological Diversity of the Guianas Publicationseries. 2Department of Biology,University of Missouri-St.Louis,8001 NaturalBridge Road, St. Louis, Missouri63121- 4499, U.S.A. 3Missouri BotanicalGarden, P.O. Box 299, St. Louis, Missouri63166, U.S.A. ANN. MISSOURI BOT. GARD. 88: 104-134. 2001.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbaliet al. 105 2001 Phylogenyand Biogeographyof Lauraceae

Actinodaphneand ). Cryptocaryeaein- lowedthat Persea was an "old Laurasiangenus" but clude pantropicalBeilschmiedia and , suggestedthat subgenus Eriodaphne, like all other and other predominantlySouthern Hemispheric membersof the family,arrived in South America generawith narrower ranges (e.g., and via Africa.Alternatively, Taylor (1988) suggested ).Perseeae are centeredin theNeotropics that the flowerAndroglandula tennessensis withthree widespread genera. Cinnamomum is dis- Taylor,from the Eocene of NorthAmerica, is com- junct between the American and Asian parable to Cinnamomum,Ocotea, and , (sub)tropics;Persea (includingMachilus) ranges indicatinga boreotropicalhistory for this groupof throughoutthe Neotropics(into the southeastern genera,with subsequent migration to SouthAmer- U.S.), theCanary Islands, and Asia; and Ocoteahas ica. Raven and Axelrod(1974) and Taylor(1988) about300 neotropicalspecies, one in , allowed thatalthough differing in the directionof a fewin Africa,and about30 morein Madagascar. migration,the high level of species diversityand Apartfrom a fewAsian genera(e.g., Dehaasia and genericendemism require a Late Cretaceous-Early ) consideredclosely related to Persea, all Tertiaryarrival in SouthAmerica. In contrast,Roh- othergenera of Perseeae are endemicto the Neo- wer and Kubitzki(1993) preferreda morerecent tropics(e.g., , , ,, arrivalof this group,possibly as late as the Plio- Nectandra,, and Rhodostemonoda- cene closureof the PanamanianIsthmus, followed phne). The distributionsof Laureae and Cryptocar- by rapid radiationin SouthAmerica. yeae are consistentwith Laurasian and Gondwanan These alternativeviews are here assessed by histories,respectively, but thatof Perseeae is am- addinga temporaldimension to a phylogenetices- biguous in this regard.The trans-Atlanticdistri- timatefor Lauraceae reconstructedwith molecular butionof Ocoteasuggests West Gondwanan history, charactersretrieved from both chloroplast and nu- but the tropicalamphi-Pacific distributions of Cin- clear genomes. namomumand Persea suggestLaurasian affinities. Whetheror not these ambiguitiesare artifactsof MATERIALS AND METHODS tribaland/or generic circumscription is unclear. The systematicsof Lauraceae is unsettled.Lau- TAXON AND MOLECULAR SAMPLING reae are recognizedin most priorclassifications, A total of 131 species, 122 representing44 of but othertribal concepts are not widelyaccepted. the 55 currentlyrecognized genera of Lauraceae, Van der Werffand Richter's(1996) Cryptocaryeae and 9 representing3 outgroupfamilies (Gomorte- and Perseeae are revised concepts supportedby gaceae, ,and )were in- Richter's(1981) studyof and bark anatomy. cluded in this study.Seventy-seven in-group spe- Some aspects of Cryptocaryeaegain supportfrom cies wereincluded in a broad-scalestudy based on embryology(Heo et al., 1998), but charactersfor sequence variationin the trnL-trnFand psbA-trnH furthersubdivision of the family were not found. A intergenicspacers of cpDNA. Guided by the find- cladisticanalysis of molecular data (Rohwer,2000) ings of this molecularand taxonsampling a two- also providedsupport for Cryptocaryeae and united tieredapproach was adoptedto obtainbetter rep- Perseeae and Laureae in a well-supportedbut un- resentationand phylogeneticresolution at the resolved lade. This Perseeae-Laureae lade ac- genericlevel. Thus a subset of the species repre- commodatesmost of the family, and its distribution sentingbasal lineages in Lauraceae was also se- implies a disjunctionbetween the Americanand quenced forthe trnT-trnL spacer, and therpll6 in- Asian tropicswith a minorAfrican presence. Such tronof cpDNA, as well as the 5' end of26S rDNA, distributionscan be creditedto extinctionof Gond- while 94 species representingPerseeae, Laureae, wanan lineages in Africa(e.g., Raven & Axelrod, and theirsister group were sampled forthe ITS/ 1974), butLaurasian ancestry followed by radiation 5.8S regionof nrDNA.Table 1 providesGenBank in tropicalAsia and Americawas favoredby Roh- informationfor all accessions. wer(2000). TropicalAsia is acknowledgedas a har- bor for Laurasian relicts (e.g., Wolfe,1975), but DNA EXTRACTION, PCR AMPLIFICATION, AND Rohwer'shypothesis that the approximately800 SEQUENCING neotropicalspecies of Perseeae are derivedfrom Laurasianimmigrants contrasts with the Gondwan- Total DNA was obtainedfrom silica-gel-dried, an origincredited to mostmajor neotropical herbarium,or freshleaves usingDneasy (QIAGEN) groups(e.g., Raven & Axelrod,1974; Gentry,1982; extractionkits. PCR amplificationof chloroplast referencesin Goldblatt,1993; Burnham& Graham, loci was conductedusing standardprotocols (e.g., 1999). Further,Raven and Axelrod(1974: 563) al- White et al., 1990). For nuclear markers,10%

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Table 1. Sources of plantmaterial. 'Previously submitted to Genbank.Contributed by: 2J. Rohwer,Univ. Hamburg; 3K. Ueda, Univ.Osaka.; and 4M. Zanis, WashingtonState Univ.

Genbankaccession numbers Taxon Provenance Voucher trnL-trnF psbA-trnH trnT-trnL rpll6 26S ITS/5.8S Lauraceae Actinodaphnesesquipedalis Malaysia,Kuala Lumpur Saw Leng Guan s.n. (KEP) AF268695 AF268787 - AF268239 - AF272247 Meisn. Adenodaphneuniflora (Guill.) New Caledonia,Province van der Werif15895 (MO) - - AF272248 Kosterm. du Sud Aiouea costaricensis(Mez) Kos- Costa Rica, Heredia Grayum8241 (HBG) (J. - - - - - AF2722492 term. Rohwersequence) Aiouea dubia (HBK) Mez ,Loja Madsen 75433 (AAU) (J. AF2722502 Rohwersequence) Aiouea guianensisAubl. Guyana,Demerara, Timer- Taylor12085 (MO) AF268696 AF268780 - - - AF272251 hi Alseodaphnesemecarpifolia Sri Lanka, CentralProv, Malcomber2753 (MO) AF268697 AF268799 - - - AF272252 Nees Kandy Anaueriabrasiliensis Kosterm. ,Loreto, Iquitos Vdsquez25228 (MO) AF268698 AF268800 AF268840 AF268247 - AF272253 Aniba cinnamomiforaC. K. Al- ,Trujillo, Bo- Cuello955 (MO) AF268700 AF268770 AF268823 - - AF272254 len con6 o . Anibaexcelsa Kosterm. Guyana,Demerara, Mabu- Chanderbali226 (MO) - - - - - AF272255 | * ra Hill Anibahypoglauca Sandwith Guyana,Essequibo, Iwok- Chanderbali165 (MO) AF268699 AF268771 AF268822 - - - ramaReserve Anibapanurensis (Meisn.) Mez Guyana,Essequibo, Iwok- Chanderbali248 (MO) AF272256 ramaReserve O Apolloniasbarbulana (Cav.) CanaryIslands, Bramwell628 (MO) - - - - - AF272257 a Bornm. Aspidostemonsp. Madagascar,Toliara van der Werff12737 (MO) AF268701 AF268819 AF268843 AF268251 Beilschmiediabrenesii C. K. Al- Costa Rica, Puntarenas Yasuda 1310 (MO) AF268702 AF268809 AF262004' len Beilschmiediamadagascariensis Madagascar, Toliara Lowry5015 (MO) AF268810 Kosterm. Beilschmiediaovalis (Blake) C. Costa Rica, San Jose Yasuda 1301 (MO) AF268703 AF268811 AF270472 K. Allen Beilschmiediasary Kosterm. Madagascar,Toamasina van der Werif12800 (MO) - AF268812

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Table 1. Continued. | . C I Genbankaccession numbers Taxon Provenance Voucher trnL-trnF psbA-trnH trnT-trnL rpll6 26S ITS/5.8S

Beilschmiediatilaranensis Nish- Costa Rica, Guanacaste Yasuda 1313 (MO) AF1290141 AF1290451 AF1290151 AF1272651 - - c ida Beilschmiediavelutina (Kos- Madagascar,Antsiranana Georges361 (MO) AF268704 AF268813 -- term.)Kosterm. Caryodaphnopsisbilocellata van Vietnam,Ninh Binh van der Werif14195 (MO) AF230321 AF2619951 AF2336031 AF2327431 AF262005' der Werff Caryodaphnopsistomentosa van Peru,Loreto, Iquitos Vdsquez25239 (MO) AF268705 AF268807 AF268842 AF268248 der Werff CassythafiliformisL. Guyana,Rupununi, Kar- Chanderbali205 (MO) AF2320341 AF2619961 AF2336051 AF2327441 AF262006' anambo Cassythapubescens R. Br. ,Victoria, Gee- Foreman1913 (MEL) AF2320331 AF2336041 AF262007' long Chlorocardiumrodiei (R. H. Guyana,Demerara, Mabu- Chanderbali246 (MO) AF268706 AF268802 AF268245 AF272258 Schomb.)Rohwer, H. G. ra Hill Richt.& van der Werff Chlorocardiumvenenosum (Kos- Peru,Loreto, Iquitos Vdsquez25236 (MO) AF268707 AF268801 AF268840 - - AF272259 C term.& Pinkley.)Rohwer, H. G. Richt.& van der Werff Cinnamomumcamphora (L.) MissouriBG Chanderbali322 (MO) AF1290203 AF1290481 AF1290211 AF1290191 - AF272260 Presl. Cinnamomumchavarrinum Costa Rica Gomez-Lauritos.n. (J. - - - - - AF2722612 | CD (Hammel)Kosterm. Rohwersequence) Q > Cinnamomumcinnamomifolium Ecuador Thomsen8942 (AAU) (J. - - - - - AF2722622 (HBK) Kosterm. Rohwersequence) Cinnamomumjaponicum Sie- Japan,Honshu, Kyoto Yasuda 1351 (MO) AF2687083 AF268782 - - - AF272263 bold Cinnamomumoleifolium (Mez) ,Minas Gerais Lorea-Hernandez5582 AF272264 Kosterm. (MO) o Cinnamomumquadrangulum Brazil,Minas Gerais Lorea-Hernandez5585 - AF268781 - - - AF272265 (Meisn.)Kosterm. (MO) Cinnamomumsp. Vietnam,Lao Cai van der Werff14396 (MO) - AF268783 - - AF270473 AF272266 Cinnamomumverum Presl. ,Kumbhave, Dapoli Godbole45108 (MO) AF268709 AF268784 - - - AF272267 Cryptocaryachinensis (Hance) Asia K. Ueda sequence AF26871O31D - - - - - Hemsl. -4

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Table 1. Continued.0

Genbankaccession numbers Taxon Provenance Voucher trnL-trnF psbA-trnH trnT-trnL rpll6 26S ITSI5.8S

Cryptocaryarhodosperma Hy- Australia,Queensland Gray7556 (QRS) AF268711 AF268817 --AF270474 - land

Cryptocaryascierophylla Hyland BrisbaneCity Botanic Schwarzbachs~n. (voucher AF268712 AF268818 ---- Garden destroyed) Cryptocaryathouvenotii Madagascar,Toliara van der Werif12723 (MO) AF232035' AF261997' AF233606' AF232745' AF262008' (Danguy)Kosterm. Dehaasia incrassata(Jack) Kos- ,Palawan, Tay- Soelarto7693 (MO) -----AF272268 term. tay Dicypelliumcaryophyllaceum Brazil,Para Pires16756 (HBG) -----AF272269 (Mart.)Nees Dicypelliummanausense W. Brazil,Amazonas, Manaus Assun~yio749 (INPA) AF268713 AF268775 AF268830 --AF272270 Rodr. Endiandramicroneura C. White Australia,Queensland Schulmans~n. (QRS) AF268714 AF268814 --AF270475 - Endlicheriachalisea Chander- Guyana,Essequibo, Iwok- Chanderbali252 (MO) AF268715 AF268756 AF268829 --AF272271 bali ramaReserve Endlicheriacitriodora van der Peru,Loreto, Iquitos Vasquez25231 (MO) AF268716 AF268757 ---AF272272 Werif Endlicheriapunctulata (Mez) C. FrenchGuiana, Tumac de Granville1448 (MO) -----AF272273 K. Allen Humac Endlicheriareflectens (Nees) Guyana,Essequibo, Rupu- Chanderbali208 (MO) AF268717 AF268758 AF268828 --AF272274 ~ C Mez nuni

Gen. & sp. nov.aff. Peru,Loreto, Iquitos Vdsquez25230 (MO) AF268719 AF268803 AF268838 -AF270483 - Eusideroxylonzwageri Te- Borneo,Kalimantan Laman 1275 (HUH) AF268718 AF268820 -AF268252 --0 ijsmann& Binnendijka Hypodaphniszenkeri (Engl.) Gabon,Ogooue-Ivindo, McPherson16184 (MO) AF232036' AF261998' AF233607' AF232746' AF262009' _C Stapf Lop&6Okanda Iteadaphnesp. Vietnam,Lao Cai van der Werif14360 (MO) AF268720 AF268786 AF268834 AF268241 -AF272275 Kubitzkiamezii (Kosterm.) van Guyana,Essequibo, Iwok- Chanderbali249 (MO) AF268721 AF268772 --AF270476 AF272276 der Werff rama Laurusnobilis L. MissouriBG Chanderbali327 (MO) AF268722 AF268785 AF268835 --AF272278 Licaria cannella (Meisn.)Kos- Guyana,Demerara, Mabu- Chanderbali234 (MO) AF268723 AF268773 ---AF272280 term. ra Hill Licaria guianensisAubl. Brazil,Amazonas, Manaus Vicentini1238 (MO) -----AF272281

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Table 1. Continued.

Genbankaccession numbers CD Taxon Provenance Voucher trnL-trnF psbA-trnH trnT-trnL rpll6 26S ITS/5.8S

Licaria martiniana(Mez) Kos- Guyana,Essequibo, Iwok- Chanderbali264 (MO) - - - - - AF272279 c term. ramaReserve 3 Licaria triandra(Sw.) Kosterm. FairchildTropical Garden, Qiu 90019 (NCU) AF268724 AF268774 - - AF272282 Fl., U.S.A. Linderabenzoin (L.) Blume MissouriBG Chanderbali324 (MO) AF2687253 AF268788 AF268833 AF272283 Linderaerythrocarpa Makino Japan,Honshu, Kyoto Yasuda 1353 (MO) AF2687263- AF272284 Linderaumbellata Thunb. Japan,Honshu, Kyoto Yasuda 1354 (MO) AF2687273 AF268789 - AF272285 Litseacoreana Leveille Japan,Honshu, Kyoto Yasuda 1356 (MO) AF2687283 AF268791 AF262010' AF272286 cf.Litsea elongata (Nees) ,Yunnan, Kunming Hyland14912 (MO) - AF272277 Benth.& Hook. f. (Distribut- BG ed to MO as Phoebeforrestii W. W. Sm.) Litseaglaucescens HBK Mexico,Guerrero, Chichi- Lorea-l:ernandez5496 AF1290351 AF1290631 AF1290361 AF127266 - hualco (MO) Mezilaurustriunca van der Peru,Amazonas, Iquitos Vdsquez25227 (MO) AF268729 AF268804 AF268837 AF268246 AF272287 Werff Mocinnodaphnecinnamomoidea Mexico, Guerrero, El Mol- Lorea-Hernandez5536 AF272288 - - Lorea-Hern. ste (MO) o m Nectandraarnazonum Nees Guyana,Essequibo, Iwok- Chanderbali217 (MO) - - - - - AF272289 ramaReserve Nectandracoriacea (Sw.) Gri- U.S.A. Florida,Monroe Prinzie125 (MO) - - - - - AF272290 seb. County Nectandracuspidata Nees & Guyana,Essequibo, Ka- Chanderbali279 (MO) - - AF272291 o Mart. marang CD Nectandramembranacea (Sw.) Brazil,Sao Paulo, Serra Lorea-Hernandez5596 AF268730 AF268767 AF268825 AF268244 - - Griseb. do Mar (MO) Nectandrapsammophila Nees Brazil,Sao Paulo, Serra Lorea-Hernandez5595 - - - - - AF272292 & C. Mart. do Mar (MO) o Nectandrapurpurea (Ruiz & Peru,Cajamarca, San Ig- Camposet al. 3165 (MO) - AF272293 Pav.) Mez nacio C Nectandrasalicifolia (HBK) Costa Rica Gomez-Lauritosn. (J - - - - - AF2722942 Nees Rohwersequence) C Nectandraturbacensis (HBK) PuertoRico, Rio Grande, Taylor11746 (MO) AF0124001 AF268768 AF268826 AF272295 CD Nees El Verde co

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Table 1. Continued.

Genbankaccession numbers Taxon Provenance Voucher trnL-trnF psbA-trnH trnT-trnL rpll6 26S ITS/5.8S Neocinnamomummekongense China,Yunnan Li Heng 8547 (MO) AF268731 AF268806 AF268841 AF268249 AF270477 (Hand.-Mazz)Kosterm. Neolitseasericea (Blume) Koidz. Japan,Honshu, Kyoto Yasuda 1355 (MO) AF2687323 AF268792 - AF268243 AF270478 AF272296 Ocoteabotrantha Rohwer U. C. Riverside Scora 99-1 (UCR) AF268733 AF268776 - - AF272297 Ocoteabullata (Burchell)E. SouthAfrica, Natal, Sky- Abbot6208 (MO) AF268734 AF267778 - - - AF272298 Mey. line Arboretum Ocoteaceanothifolia (Nees) Mez Guyana,Demerara, Mabu- Chanderbali244 (MO) - - - - AF272299 ra Hill Ocoteafoetens(Aiton) Baill. ,Porto Moniz Maas 8642 (MO) AF268735 - - - AF272300 Ocoteagrayi van der Werff Madagascar,Toliara van der Werff12732 (MO) AF268736 AF2327471 AF270479 AF272301 Ocoteaguianensis Aubl. Guyana,Demerara, Mabu- Chanderbali232 (MO) AF268737 AF268762 - AF272302 ra Hill Ocoteahelicterifolia (Meisn.) Mexico,Oaxaca, Miahu- Torres11911 (MO) - - - AF272303 Hemsl. atlan Ocoteaheydeana (Mez & Donn. Honduras,Yoro, Pico Pijol Evans 1760 (MO) - - - - - AF272304 D Sm.) Bernardi Ocoteaikonyokpe van der WerffCameroon, SW Prov., Thomas10456 (MO) - - - - - AF272305 RumpiHills | n Ocoteainsularis (Meisn.) Mez Costa Rica, Puntarenas, Rojas 3682 (MO) - - - - - AF272306 Coco Is Ocotealeucoxylon (Sw.) Laness. PuertoRico, San Jose Taylor11733 (MO) AF123991 AF268763 - - Ocoteamalcomberi van der Madagascar,Toliara van der Werff12756 (MO) AF268779 - AF272307 Werff O Ocoteanigra Benoist Guyana,Essequibo, Iwok- Chanderbali162 (MO) - - - - - AF272308 ramaReserve Ocoteaodorifera (Vell.) Rohwer Brazil,Minas Gerais, Lorea-Hernandez5578 AF268738 AF268762 - - AF272309 Parque Ecol. CEMIG (MO) Ocoteapaucifiora (Nees) Mez Guyana,Demerara, Mabu- Chanderbali219 (MO) - AF268764 - - AF272310 ra Hill Ocoteapercoriacea (Mez) Kos- Brazil,Goias, Fazenda Lorea-Hernandez5584 AF268739 - AF272311 term. Galheiro (MO) Ocoteapulchella Mart. Brazil,Minas Gerais,Fa- Lorea-Hernandez5575 AF268740 - - AF262312 zenda Caiera (MO)

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Table 1. Continued.

Genbankaccession numbers CD Taxon Provenance Voucher trnL-trnF psbA-trnH trnT-trnL rpll6 26S ITS/5.8S

Ocoteaquixos (Lam.) Kosterm. Ecuador,Napo, JatunSa- Neill 9487 (MO) AF2320371 AF261999' AF2336081 - AF2620111 AF272313 c cha 2 Ocotearhynchophylla (Meisn.) Guyana,Demerara, Mabu- Chanderbali220 (MO) - AF268766 - - - AF272314 |D Mez ra Hill Ocoteaschomburgkiana (Nees) Guyana,Essequibo, Iwok- Chanderbali286 (MO) - - - AF272315 Mez ramaReserve Ocoteaspixiana (Nees) Mez Brazil,Minas Gerais, Lorea-Hernandez5574 - - AF272316 Parque Ecol. Tripui (MO) Ocoteatomentella Sandwith Guyana,Essequibo, Ka- Chanderbali284 (MO) AF268741 AF268765 - - AF272317 marang Ocoteatristis (Nees & Mart.) Brazil,Minas Gerais, Lorea-Hernandez5577 AF268742 - -_ AF272318 Mez Parque Ecol. CEMIG (MO) Ocoteaveraguensis (Meisn.) Nicaragua,Chontales Stevens24177 (MO) - - - AF272319 Mez bracteataRohwer, H. G. Brazil,Amazonas, Iquitos Vicentini1288 (MO) AF268743 - - AF272320 Richt.& van der Werff Parasassafrasconfertiflora China,Yunnan, Lishui Co. Li Heng 10030 (MO) - AF268790 - AF268238 AF270480 AF272321 (Meisn.)Long Persea americanaMill. MissouriBG Chanderbali323 (MO) AF268744 AF268794 - - - AF272322 (Ruiz & Pav.) Peru,Amazonas van der Werff14744 (MO) - AF268795 - - - AF272323 2 . Mez a D (Ruiz & Pav.) Chile Greissl640-99 (MJG) - AF268796 - AF272324 w P Nees ex Kopp Persea meridensisKopp Venezuela,Trujillo, Bo- Cuello943 (MO) AF268745 AF267797 AF268836 - - AF272325 C con6 Persea sp. Vietnam,Vinh Phuc van der Werff14071 (MO) - - - - - AF272326 Persea thunbergiiSiebold & MissouriBG Chanderbali328 (MO) AF268746 AF268798 - AF272327 Zucc. o Phoebeformosana (Hayata) Bonn BG Rohwer156 (MJG) - - - - - AF2723282 Hayata (J.Rohwer sequence) c Pleurothyriumcinereum van der Peru,San Martin,Riojas van der Werff15325 (MO) AF268747 AF268769 - - - AF272329 Werff C Pleurothyriuminsigne van der Ecuador,Napo, JatunSa- Neill 9033 (MO) - - AF272330 CD Werff cha

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Table 1. Continued.

Genbankaccession numbers Taxon Provenance Voucher trnL-trnF psbA-trnH trnT-trnL rpll6 26S ITS/5.8S

Potameiamicrantha van der Madagascar,Toamasina van der Werif12777 (MO) AF268749 AF268815 - - AF270481 - Werff Potameiamicrophylla Kosterm. Madagascar,Fianarantsoa van der Werif12655 (MO) AF268750 AF268816 - AF268250 - - Potoxylonmelagangai (Syming- Brunei, Tutong, Kampong Hyland14969 (MO) AF268748 AF268821 ton)Kosterm. Lamumin Guyana,Essequibo, Iwok- Chanderbali265 (MO) AF268751 AF268759 - - AF272331 crenaticupulaMadrifian ramaReserve Rhodostemonodaphnepraeclara Guyana,Essequibo, Iwok- Chanderbali256 (MO) AF268752 AF268760 AF268827 - - AF272332 (Sandwith)Madrinian ramaReserve Rhodostemonodaphnerecurva Brazil,Amazonas, Manaus Vicentini653 (MO) - - - - - AF272333 van der Werff Rhodostemonodaphnescandens Guyana,Essequibo, Iwok- Chanderbali271 (MO) - - - - - AF272334 Madrinian ramaReserve Sassafrasalbidum (Nutt.) Nees MissouriBG Chanderbali325 (MO) AF268753 AF268793 AF268832 AF268242 AF2641404 AF272335 Sassafrastzumu (Hemsl.) Hemsl China,Hunan, Xining Co. Luo Lin-bo1242 (MO) - - - - AF272336 Sextoniapubescens van der Peru,Loreto, Iquitos Vdsquez25229 (MO) AF2320381 AF2620001 AF2336091 AF2327481 AF2620121 AF268808 Werff Sextoniarubra (Mez) van der Brazil,Amazonas, Manaus Nascimento574 (MO) AF268754 AF268805 - - AF270482 - | . Werff WZ Umbellulariacalifornica (Hook. MissouriBG Chanderbali326 (MO) AF268755 AF268777 - AF272337 p CD & Am.) Nutt. Urbanodendronbahiense Brazil,Rio de Janeiro Martinelli10019 (MO) - AF272338 (Meisn.)Rohwer Urbanodendronverrucosum Brazil,Minas Gerais,Faz. Braga s.n. (BHCB) 19385 - - - - - AF272339 a (Nees) Mez Maced6nea (MO) Gomortegaceae

Gomorteganitida Ruiz and Pav. Chile Rodriguez3070 (CONC) AF0124041 AF1290531 - AF1272601 AF262014' Hernandiaceae

Gyrocarpusamericanus Jacq. Sri Lanka, ColomboBG Chase 317 (NCU) AF0123981 AF1290541 AF1290251 AF1272611 AF262001 - Hernandiamoerenhoutiana Australia,Brisbane, Mt. notavailable AF0521981 AF1290551 AF1290261 AF130310O Guillem. CoothaBG

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbaliet al. 113 2001 Phylogenyand Biogeographyof Lauraceae

DMSO was added and the PCR protocoldescribed by Kuzoffet al. (1998) was followed.The trnL-trnF and trnT-trnLregions were amplified using primers designedby Taberletet al. (1991). The trnL-trnF spacersequences begin near the 5' end ofthe spac- e er and include 138 bp of the 5' end of the tRNA- Co _ Phe (trnF)gene. The spacer betweentRNA-Leu (trnL)and tRNA-Thr(trnT) aligns readily with oth- er lauraleantrnT-trnL sequences produced by Ren- ner (1999), but is difficultto align withthe few available trnT-trnLsequences in GenBank, the mostsimilar of which are trnT-trnLsequences from =k z z z z z Dioscorea (48% similarity).The psbA-trnHspacer ? ? Z F-0 ? and rpll6 intronwere amplifiedusing primersof Sang et al. (1997) and Asmussen(1999), respec- r d c t coCS C) c tively.The psbA-trnHsequences obtainedfor Laur- aceae includethe entirespacer regionand overlap 'e ; ocec c: coc c by about40 base pairswith the 3' end ofthe psbA = A N N N~~'IN 0 N 't gene and 5' end of the trnH gene of Helianthus annuusL. depositedin Genbank(X60428). The 5' regionthat includes the first two expansion domains

=- Cfo O o:1 of26S rDNA was amplifiedusing a forwardprimer (D. Nickrent,pers. comm.)that anneals at ca. 70 nucleotidepositions downstream from the 5' end of the gene and the 641 R reverseprimer of Kuzoff et al. (1998). To increaseefficiency of PCR ampli-

Cd ficationof ITS, the fewlauraceous sequences ob- tainedusing angiosperm-specific ITS A and ITS B k C) :C C)~~~~~~~~~~~~C primers(Blattner, 1999) wereused to designa for- CS C) SC ;~ ~ ee - ward primer (5'-ACCACCACCGGCAACCA-3') thatanneals at about 10 bp downstreamof the 3' end of 18S. This primer(hereafter LAUR 1) ap- pears to be specificto a large terminalclade in Lauraceae that includes the tribesPerseeae and Laureae and theirsister group. In mostcases it was possible to amplifythe entire ITS region using LAUR 1 and ITS B, butfor some poor-quality tem- platesit was necessaryto amplifythe region in sec- tions(ITS1 & ITS2) by combiningthe appropriate universalprimers of White et al. (1990) withLAUR 1 and ITS B. The ITS/5.8S sequences produced includeall but the firstca. 10 bp of ITS 1 and the 0C> g entireITS 2 and 5.8S regions.Rarely, only ITS 1 or ITS 2 was obtained. PCR productswere purifiedfollowing the pro- 20 iE tocol provided by QlAquick gel extractionkits (QIAGEN) and sequencedusing the dye terminator cycle sequencing protocol(Applied Biosystems). Sequence reactionswere analyzedon ABI 373 or ABI 377 automatedsequencers (University of Mis- souri-ColumbiaDNA Core SequencingFacility and Universityof Missouri-St.Louis D. E. Lee and FamilySequencing Facility). Except forthe psbA- trnHregion, which could onlybe sequenced from the 5' end, both strandsof DNA were read and

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 114 Annals of the Missouri Botanical Garden

consensussequences generatedusing Sequencher were calculatedfor the ITS data set using log de- vers. 3.1 (Gene Codes Corp., 1998). Sequences terminant(LogDet) and maximumlikelihood esti- were manuallyaligned using the sequence editing mates of genetic distances. Maximumlikelihood facilitiesof Seqpup VERSION 0.6 (D. Gilbert,In- distances were calculated using the Hasegawa- diana University,Bloomington, 1996). Sequence Kishino-Yano(1985) modelwith rate heterogeneity alignmentwas relativelystraightforward in Laura- amongsites (HKY-F). ceae. However,the first290 bp of the trnT-trnL spacer were removedfrom analysis because of MOLECULAR CLOCK ANALYSES alignmentdifficulties among basal Lauraceae and In orderto add a temporaldimension to thephy- outgroupfamilies. Alignment difficulties with the logenetic estimate,divergence times for major outgroupwere also encounteredin the 3' half of brancheswere estimated. Due to thecomputational the psbA-trnHspacer. However,unlike trnT-trnL demandsof maximumlikelihood calculations and sequences,psbA-trnH provided several informative because it was not necessaryto obtaindivergence characterswithin Lauraceae and insteadof remov- timesfor all nodes,likelihood scores were obtained ing it entirely,outgroup sequences weretruncated fromparsimony-based topologies that were reduced afteralignment became ambiguous(ca. position to exemplarsof majorclades. ITS/5.8S sequences 300). were used forterminal, and the cpDNA and 26S sequences forbasal lineages. PHYLOGENETIC ANALYSES Likelihood scores were calculated under the Hasegawa-Kishino-Yano(1985) model with rate Initialanalyses of the individualdata sets were heterogeneityamong sites, and values obtained conducted as heuristicsearches for most parsimo- withand withouta clock constraintcompared for nious with 10 randomtaxon additionsand significanceusing a x2 test[X2 2(log LClCk - log TBR branchswapping PAUP* using version4.0b4 Ltook); d.f. = numberof taxa -2]. For each in- (Swofford,1998). Both the MULPARS and COL- ternalnode, HKY-F distances(branch lengths) to LAPSE optionswere in effect,but the STEEPEST the tip were computedby PAUP* withthe clock DESCENT option was not employed.Characters constraintenforced. These values representthe were assumed to be unordered(i.e., Fitch parsi- numberof substitutionsper site accumulatedalong mony),equally weighted,and gaps weretreated as each daughterlineage, and were eitherdivided by missingdata. Parsimonyuninformative characters timeto determinesubstitution rates, or dividedby were excluded. Bootstrapanalyses (Felsenstein, estimatedrates to obtaindivergence times. Overlap 1985) with500 replicationswere performedwith in taxonsample betweenterminal and basal topol- the above heuristicsearch settings but withMAX- ogies alloweduse of divergencetimes estimated in TREES set to 100. Since these initial searches one to calibratesubstitution rates and calculatedi- showedno stronglysupported conflict, i.e., alter- vergencetimes in the other.Standard deviations of native > clades supportedby 70% bootstrapvalues divergencetimes were estimatedas follows.First, (Hillis & Bull, 1993), and P-valuesfrom partition- standarddeviations of HKY-r distanceswere cal- homogeneitytests ranged from 1.0 to 0.6 (strongly culatedusing a formuladerived from the relation- indicatingcongruence), three matrices were com- ship S = Np, whereS is the numberof nucleotide piled forfurther analyses. MatrixI combined86 substitutions,N is the totalnumber of nucleotide that species were sequenced forthe trnL-trnFand positionsin a sequence, and p is the proportionof psbA-trnHregions. Matrix II combinedtrnL-trnF, nucleotides substituted (HKY-r distancefrom node psbA-trnH,trnT-trnL, rp116, and 26S sequencesfor to branchtips). Since the standarddeviation of S 42 taxa representingmajor lineages identifiedby is the square root of Np(l - p), or SD(S) = of I to analyses matrix furtherinvestigate basal re- sqrt(Np[l - p]), the standarddeviation of p is lationships.Matrix III included94 ITS sequences SD(S) dividedby N, or SD(p) = sqrt(p[l - p]/N). fromrepresentatives of a large terminallade that This value is calculatedfor each divergenceof in- was poorlyresolved by sequence variationin matrix terestand dividedby substitutionrate to obtainthe I. The onlymutation in matrixI thatprovided ge- standarddeviation of divergencetimes. neric-levelinformation in thisterminal lade, a 16- bp repeatin trnL-trnF,was includedin matrixIII. RESULTS Analysesof all threematrices were conductedas above withlength mutations (insertions and dele- PHYLOGENETIC ANALYSES tions) introducedas binary charactersof equal Sequence variationin chloroplastmarkers and weight.In addition,minimum evolution topologies partial26S sequences was almostlimited to basal

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume88, Number1 Chanderbaliet al. 115 2001 Phylogenyand Biogeographyof Lauraceae

Table 2. Characteristicsand comparisonsof phylogeneticinformation provided by matricesanalyzed in thisstudy. MatrixI combinestrnL-trnF and psbA-trnHcpDNA sequences, MatrixII combinestrnL-trnF, trnT-trnL, psbA-trnH, and rpll6 of cpDNA with26S rDNA sequences; MatrixIII is based on ITS rDNA sequences.

Parsimony-informative Numberof representativesof: substitutionsamong: Perseeae & Perseeae & Matrices Alignedlength Lauraceae Laureae Lauraceae Laureae trnL-trnF 510 76 48 103 7 psbA-trnH 616 75 48 135 35 trnT-trnL 530 33 19 105 12 rpll6 1049 24 10 103 9 26S 592 22 8 77 11 MatrixI 1126 77 48 238 42 MatrixII 3297 42 4 470 n/a MatrixIII 780 94 90 n/a 199 branchesin Lauraceae withvery little and oftenno lade is essentiallyunresolved but thereis some variationamong members of tribesPerseeae and supportfor a lade includingrepresentatives of Laureae (sensu van der Werff& Richter,1996). Persea and ,a large genericcomplex The trnL-trnFmatrix included 510 aligned posi- centeredaround Ocotea, and strongsupport for a tions and yielded 103 informativesubstitutions lade includingall Asian membersof Cinnamo- withinLauraceae, but onlyseven ofthese were in- mum.Furthermore, a lade unitingmost neotropi- formativeamong Perseeae and Laureae. Similarly, cal genera(Aniba, Endlicheria, Kubitzkia, Licaria, of 616 aligned positionsin thepsbA-trnH matrix, Nectandra,Pleurothyrium, and Rhodostemonoda- 135 substitutionswere parsimony informative with- phne) withneotropical (but not paleotropical)spe- in Lauraceae and 35 amongPerseeae and Laureae. cies of Ocotea and CalifornianUmbellularia is re- This trendwas also foundin otherchloroplast loci covered in all trees but does not receive strong and partial26S sequences. Only ITS showedsub- support.All membersof this lade, except0. leu- stantial variationwithin Perseeae and Laureae. coxylon(Sw.) Laness., have the 16-bp repeatmen- Characteristicsof individualgenetic markers and tionedabove. Caryodaphnopsis,Cassytha, and Neo- combineddata sets are summarizedin Table 2. cinnamomumconstitute a lade in all treesbut this CombinedtrnL-trnF and psbA-trnHmatrix (ma- associationdoes not receivemore than 50% boot- trixI) included 1126 aligned positionsof which strapsupport, and neitherdoes its positionas the 277 were informative.Four indels fromtrnL-trnF sistergroup of the second major infrafamilial group. were added as binarycharacters. Three of these MatrixII included3304 characters,of which 684 supporteda lade comprisedof , were parsimony-informativesubstitutions and 7 Cryptocarya,Endiandra, and Potameia, and the were binary-codedlength mutations.Parsimony fourthis a 16-base pair repeat foundin several analysisconverged on a singleisland of 2646 equal neotropicalgenera of Perseeae and Umbellulariaof lengthtrees (L = 2171, CI = 0.71, RI = 0.72), Laureae. Parsimonyanalyses of matrix I surpassed the majorityrule consensusof whichis shownin memorylimitations in the firstaddition replicate, Figure 2. The topologyis mostlycongruent with and 29,000 equally parsimonioustopologies were thatprovided by matrixI, differingmainly in that retainedafter 24 hoursof branchswapping (L = Hypodaphnisoccupies a fairlywell supportedpo- 796, CI = 0.74, RI = 0.89). The strictconsensus sition (foundin 81% of the bootstrapreplicates) topology(Fig. 1) showstwo well-supported clades sisterto the rest of the family.The placementof in Lauraceae. One of these includes membersof Caryodaphnopsis,Cassytha, and Neocinnamomum Cryptocaryeae(sensu van der Werff& Richter, in the second main lade receives very strong 1996), withHypodaphnis tenuously placed as its (98%) bootstrapsupport, and relationshipswithin sistergroup. The second major lade is unequally the Chlorocardium-Mezilauruslade are altered dividedinto a small lade of SouthAmerican gen- slightly. era (hereafterChlorocardium-Mezilaurus clade) MatrixIII, based mainlyon ITS sequences, in- and a large terminallade comprisedof represen- cluded 259 parsimony-informativesubstitutions tatives of Laureae and Perseeae (sensu van der and 19 lengthmutations that could be unambigu- Werff& Richter,1996). This Perseeae-Laureae ouslycoded. Parsimonyanalysis found a singleis-

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 116 Annals of the MissouriBotanical Garden

77 Endlicheriachalisea 53 Rhodostemonodaphnecrenaticupula Rhodostemonodaphnepraeclara Matrix I Endlicherla citrioddra 58 Endlicheriareflectens trnL-trnFTrnL-trnF 58 Ocotea auianensis puldhella psbA-trnH cpDNA Ocotea tristis Ocoteatomentella Ocotea complex l 97 Aniba cinnamomiflora Anibahypoglauca 54 Kubitzkiamezii Licaria cannella Licaria triandra Paraia bracteata Nectandramembranacea Nectandraturbacensis Pleurothyriumcinereum Ocotea botrantha Umbellulariacalifornica Perseeae OcoteabullataLare Ocotea grayi Laureae Aiouea guianensis clade Cinnamomumquadrangulum Cinnamomumcamphora 92 Cinnamomumrjaponicum Asian 100 Cinnamomumpv.rum Cinnamomum Iteadaphne sp. Actinodaphnesequipedalis Litsea coreana Linderaumbellata Laureae Linderaerythrocarpa * 100 Persea thunbergii 57 Persea amenicana Persea lingue Persea group 74 Persea meridensis Persea caerulea Alseodaphne semecarpifolia Anauena brasiliensis _ 99 Chlorocardiumvenenosum 66 Chlorocardiumrodiei Chlorocardium 10 01Gen. & sp.nov., aff. Mezilaurus Mezilaurus Sextoniapubescens clade rubra Neocinnamomummekongense Neocinnamomum Cassytha 100 Caryodaphnopsisbilocellata Caryodaphnopsistomentosa Caryodaphnopsis 78 Beifschmiedijbrenesii 91 Bellschmiediaovalis Bellschmiediatilaranensis Beilschmiediasary 93 Endiandramicroneura 90 Potameiamicrantha Cryptocaryeae Potameiamicrophylla 77 _97 Beilschmiediamadagascariensis sensu Bellschmiediavelutina vander Werff 62 ~~~~~~~~~~87 90 Cryptocaryascierophylla and Richter 98 Cryptocaryathouvenotil Cryptocaryarhodosperma 53 1 Aspidostemonsp. 100 Eusideroxylonzwageri Potoxylonmelagangai 100 I Hypodaphniszenkeri _ rocarpusamencanus nemandiamoerenhoutiana Sparattantheliumwonotoboense Illigeraluzonensis 95 . Hortoniafloribunda 70 * I 100. Monimiaovalis Outgroups 70 U- Palmeriascandens O Peumusboldus Gomorteganitida

Figure 1. Strict consensus of 29,000 trees retained fromparsimony analysis of matrix I (trnL-trnFand psbA-trnH cpDNA sequences). Numbers above branches indicate bootstrap support. The vertical bar throughthe branch supporting the terminal clade indicates a 16-bp repeat in the trnL-trnFintergenic spacer that unites taxa therein.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbaliet al. 117 2001 Phylogenyand Biogeographyof Lauraceae

76 76 Ocotea MA IOcotea complex a) grayi Matrix___MatrIx 76 Laurusnobilis ME I Laureae a, a -o trnL-trnF 100 { Persea thunbergiiAS I " C psbA-trnH Persea americanaCA |Persea group 0- trnT-trnL 100 Anaueriabrasiliensis SA rp116 cpDNA 100 ~~~~~100 rpll 6 cpDNA 100 88 100 Chlorocardiumrodiei SA E 26S rDNA 100 Chlorocardiumvenenosum SA opposite 96 1 Gen. & sp. nov.,aff. Mezilaurus SA 3 c 7; 60 100 93 Mezilaurustriunca SA Leaves O 100 100 tSextoniapubescensSA terminally clustered (. 95 Sextoniarubra SA

980 100 Caryodaphnopsisbiocellata AS E 100 Caryodaphnopsistomentosa SA I CZ Cn- 100 Cassythafilformis SA | Parasitic m 0

100 1 CassythapubescensAU | U) Neocinnamomummekongense AS I Evergreen o Aspidostemonsp. MA I Deep cupules

72 Beilschmiediabrenesfi CA 810 56Beilschmiedia saryMA 81 ~~~~~~56 100 Beilschmiediavelutina MA 98 54 Bellschmiediamadagascariensis MA 64 100 Endiandramicroneura AU Non-cupulate

90 U) 100 Beilschmiediaovalis CA CZ

58 Beilschmiediatilaranensis CA

100 100 Potameiamicrantha MA 0 100 100 98 Potameiamicrophylla MA C

68 Cryptocaryachinensis AS 0 100 Cryptocaryathouvenotii MA 89 Cryptocaryasclerophylla AU Deepcupules

100 Cryptocaryarhodosperma AU 59 100 I Eusideroxylonzwageri BO 100 Potoxylonmelagangai BO

Hypodaphnis zenkeri AF | inferior |

100 Gyrocarpusamericanus 100 100 Sparattantheliumwonotoboense 100 ~~~~~~~~~~~~~~~~~Hernandiaceae Hernandiamoerenhoutiana 1-00 100 Illigeraluzonensis Q

Hortoniafloribunda 0 100 100 Monimia 1 ovalis Monimiaceae =3 100 Palmeriascandens | 97 ! Peumus boldus Gomorteganitida I Gomortegaceae

Figure 2. Annotated 50% majority rule resulting fromparsimony analysis of matrix II (trnL-trnF,psbA-trnH, trnT-trnL,rpll6, and 26S sequences). Majority rule percentages are indicated above, and bootstrap values > 50% below, branches. Main clades and significantmorphological characters are indicated. Geographic regions represented by each species of Lauraceae are given: AF = Africa, AS = Asia, AU = Australia, BO = Borneo, CA = Central America, MA = Madagascar, ME = Mediterranean, and SA = South America.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 118 Annals of the MissouriBotanical Garden

Endlicheriachalisea Endlicheriareflectens FPhodostem.crenaticupula Endlicheriacitriodora 100 FShodostem.recurva FPhodostem.praeclara 74 Fhodostem. scandens 62 Ocotea guianensis Ocotea s.str., Matrix III 60 82 Ocotea ixnga Endlicheria, and TC1 93 { Ocotea percoriacea Rhodostemonodaphne ITS Ocotea tristis Ocotea pulchella 55 99 Ocotea ceanothifolia 84 Ocotea schomburgkiana Ocotea tomentella 100 Endlicheriapunctulata Ocotea pauciflora Nectandracuspidata 98 Nectandrapsammophila Nectandra s.str. 75 74 amazonum 75 74 ~~~~~NectandraNectandraturbacensis a) 100 Pleurothyriumcinereum _ Pleurothyriuminsigne | Pleurothyrium 0 Ocotea helicterifolia _100 100 ~~~~Ocoteaheydeana OcteEcotea O Ocotea botrantha helicterifoliaspecies gp. Umbellulariacalifornica i 99 Nectandracoriacea tU Nectandrapurpurea Nectandra Nectandrasalicifolia coriacea species gp. Ocotea odorifera 56 . Ocotea rhynchophylla O _ 96 Aniba cinnamomiflora 6 Aniba excelsa Anibapanurensis 100 | Aiouea costaricensis Ocotea insularis U) Dicypelliumcaryophyllaceum CL 78 Kubitzkiamezi Licaria group a 78_ 96 Dicypelliummanausense and allies 98 _ Ocotea veraguensis a Ocotea quixos O Paraia bracteata E 91_ Urbanodendronbahiense Cb Urbanodendronverrucosum Licariamartiniana Licariaguianensis . Licariacannella Licariatriandra Ocoteafoetens OldWorld ,99 Ocoteabullata Ocotea r Ocotea grayi Ocotea Ocotea malcomberi 82 *-~----- Aioueadubia 11 99.- Aiouea guianensis 75 I _68 Cinnamomumoleifolium Cinnamomumquadrangulum 1 68 -Cinnamomum chavarrinum 52 Mocinnodaph.cinnamomoidea Cinnamomum group Cinnamom.cinnamomifolium 88 Ocotea ikonyokpe Cinnamomum 64 I11oo.- japonicum I _ 90 _Cinnamomumsp. Cinnamomumverum Cinnamomumcamphora 93 1 75 Sassafras tzumu I Sassafras albidum Sassafras Laurusnobilis Linderaerythrocarpa 82 Linderabenzoin (ID 76 Linderaumbellata CZ Neolitsea sericea Core I D Actinodaphnesesquipedalis Parasassafras confertifolia Laureae = 57 | Adenodaphneuniflora CZ 77 cf. Litsea elongata Litsea coreana Iteadaphnesp. 81 Phoebe formosana Phoebe, Alseodaphne Alseodaphne semecarpifolaIa Dehaasia incrassata ' Dehaasia 1 Perseasp. | r~e 1 t Pes thunbergii | Persea subg. P~~~~~ersea 89 A i E | 8 | 8 yolloniasbarbujana group Ioerseanamericana I Persea subg. Persea g II Persea caerulea Persea mingue Persea subg. Eriodaphne I * ~~~~~~~~~~~~~~~~~~~PerseaMezilaurusmeridensisItunca Sextoniapubescens ChlorocardiumChocadu - 100.~ Chlorocardiumvenenosum Mezilaurus 1 ! Chlorocardiumrodiei I Anaueriabrasiliensis cade Figure 3. Adams consensus of 567 equally parsimonious trees obtained fromunconstrained analysis of matrix III (ITS sequences). Numbers above branches indicate bootstrap support, and vertical bars to the rightcircumscribe main clades. Cinnamom.= Cinnamomum,Mocinnodaph. = ,and Rhodostem.= Rhodostemonodaphne. land of 567 equal lengthtrees (L = 1050, CI = ofthe topological instability exists among members 0.44, RI = 0.75). The Adams consensustopology of Cinnamomum.Sassafras was placed between (Fig. 3) indicatesthat Perseeae sensuvan derWerff Laureae and a paraphyleticCinnamomum in all and Richter(1996) are paraphyletic,and thatmost trees. This reconstructiondoes not receive strong

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbali et al. 119 2001 Phylogenyand Biogeographyof Lauraceae

Endlicheriachalisea Endlicheriareflectens Rhodostemonodaphnecrenaticupula FRhodostemonodaphnepraeclara 100 Endlicheriacitriodora FRhodostemonodaphnerecurva Matrix III 74 FRhodostemonodaphnescandens Ocotea guianensis Ocotea nigra ITS 99 Ocotea spixiana 93 Ocotea percoriacea Primarily cotea tristis South America 85 100 Ocotea ceanothifolia Ocotea schomburgkiana Ocoteatomentella 10 Endlicheriapunctulata 93 *Ocotea pauciflora Nectandracuspidata Nectandraamazonum 98 Nectandrapsammophila 75 . Nectandraturbacensis 100 Pleurothvriumcinereum Pleurothyriuminsigne 10 00 Ocotea helicterifolia Ocotea heydeana .Madrean Ocotea botrantha CentralAmerica _ _Umbellularia caftornica UmbelluNectandra coriacea NotAmrcNorthAmerica Nectandrapurpurea CentralAmerica Nectandrasalicifohia 64 Ocotea odorifera 56 Ocotea rhynchophylla 92 Aniba cinnamomiflora Aniba excelsa Anibapanurensis Aiouea costaricensis Ocotea insularis Dicypelliumcaryophyllaceum Kubitzkiamezii 78 Dicypelliummanausense Primaril 98 89 Ocotea veraguensis Y Ocotea quixos South America 88 Paraia bracteata 8 Urbanodendronbahiense Urbanodendronverrucosum Licaria martiniana 53 Licariaguianensis 100 Licariacannella Licaria triandra 86 I Macaronesia 10 Ocoteabata Tethyan Ocotea malcomberi j Madagascar 82 Aiouea dubia 1 99 . Aiouea guianensis 75 68 Cinnamomumoleifolium 1 Cinnamomumquadrangulum Neotropics I68 Cinnamomumchavarrinum Mocinnodaphnecinnamomoidea 93 t1 Cinnamomumcinnamomifolium Boreo- Africa 7 ocote9 innamomumjaponicum, tropical 152 m Cinnamomumsp. Cinnamomumverum Asia I ~~~~Cinnamomumcamphora I 81 Sassafras tzumu I Asia Sassafrasalbidum INorth America Laurus nobilis Litsea coreana Mediterranean cf. Litsea elongata Adenodaphne uniflora Asia 82 'tea nesp. ~~~~~~~Boreo- Linderaerythrocarpa N tropical Parasassafras confertiolia | 1 4 _~~~~~~~7Neolitsea sericea .I I III Actinodaphnesesquipedalis Asia I Li~~~~~~~ndera umbellata I I _~~~~~~8 Phoebe formosana I Alseodaphne semecarpifolia I Asi I Deh~~~~~~~~aasia incrassata Asia Apolloniasbarbujana I 100 89 Persea sp.I | | 89 1 Persea| thunbergii Asia Boreo- I I _ ~~~~~Perseaamericana 92 Persea lnguea Neotropics tropical Persea meridensis 100 Mezilaurustriunca E Sextonia pubescens 100 venenosum . 1 100100 4Chlorocardium ~~~~~~~Chlorocardiumrodiei South America Gondwananod aa Anaueria brasiliensis 5 changes Figure4. One of 126 equally parsimonioustrees obtained with monophyly of the Cinnamomumgroup (Cinnamo- mum,Aiouea p.p., Mocinnodaphne,and Ocotea p.p.) and Laureae enforced(thick vertical bars) as topologicalcon- straints.Bootstrap support values are indicatedabove unconstrainedbranches. Annotated bars to theright indicate the distributionand inferredancestry of clades.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 120 Annals of the Missouri Botanical Garden

bootstrapsupport, and constrainingmonophyly of a ported generic-level phylogenyfor Lauraceae. Data lade comprisedof Cinnamomumand its allies fromchloroplast markers and partial 26S sequenc- (Aiouea p.p., Mocinnodaphne, Ocotea p.p.) required es resolve main clades, while ITS provides novel only one extrastep while constrainingmonophyly resolution among members of Perseeae and Lau- of Laureae to includeSassafras added threeextra reae (sensu van der Werff& Richter, 1996). To pro- stepsto parsimony-basedtrees. One of 126 equally vide a basis for subsequent biogeographic consid- parsimonious trees (L = 1054, CI = 0.44, RI = erations, phylogenetic relationships among 0.75) calculated withboth topologicalconstraints Lauraceae are firstdiscussed. enforcedis shownin Figure4. Bothminimum-evo- lution analyses recoveredtopologies that showed PHYLOGENETIC RELATIONSHIPS thesame mainclades foundby parsimony analyses. AlthoughCinnamomum was again notmonophylet- Several previously recognized taxonomic groups, ic, minimumevolution placed Sassafras sisterto albeit in differentschemes, compare favorablywith remainingLaureae, albeit togetherwith Cinnamo- clades supported by our molecular data. Among mumcamphora (L.) Presl.Differences between par- these, Cryptocaryeae as circumscribed by van der simony and minimumevolution reconstructions Werff and Richter (1996), Laureae of most classi- suggestthat some instability in parsimony-basedto- fications (e.g., Kostermans, 1957; van der Werff& pologiescan be attributedto charactersshared be- Richter, 1996; Rohwer, 1993a), and Cinnamomeae tween Sassafras and C. camphora. With C. cam- in the sense of Kostermans (1957) are the largest. phora removedthe numberof treesresulting from In addition, a generic grouping centered around unconstrainedparsimony analyses is greatlyre- Persea, informallyrecognized by Rohwer (1993a), duced (to 36, L = 1022 CI = 0.44, RI = 0.76), herein receives considerable support. A fifthmajor but Sassafrasis still placed betweenLaureae and generic grouping, the Chlorocardium-Mezilaurus paraphyletic Cinnamomum. lade, is comprised of taxa whose taxonomic posi- tions have previously been uncertain. Outside of MOLECULAR CLOCK ANALYSES these main clades the position of a few small genera is unsettled. A likelihoodratio test on the ITS data set re- duced to 25 representativesof main lineages in Hypodaphnis and Cryptocaryeae. Monotypic Hy- higherLauraceae (Fig. 5a) indicatedthat substi- podaphnis, consisting of H. zenkeri (Engl.) Stapf tutionwas approximatelyclock-like. Log likeli- fromCentral Africa, is the only member of Laura- hood scores with(-2844.00) and withouta clock ceae with an inferiorovary, and the two analyses constraint(-2827.85) were not significantlydif- that investigated basal relationships in Lauraceae ferent(X2 = 32.30, d.f. = 23, P > 0.05). Of mo- suggested differentpositions (compare Figs. 1 and lecular markersused to resolve basal relation- 2). The trnL-trnFand psbA-trnH data sets analyzed ships, only rpll6 did not reject the molecular in matrix I weakly support a sister group relation- clock [X2 = 2(2590.76 - 2582.73) = 16.06; d.f. ship between Hypodaphnis and Cryptocaryeae(Fig. = 10, P > 0.05], providedNeocinnamomum and 1). Association with Cryptocaryeaeis supported by Cassytha were removedfrom analysis (Fig. 5b). irregular thyrsoidinflorescences (van der Werff& Results of two calibrationssimulating alternative Richter, 1996) and morphological similarity with biogeographicscenarios are summarizedin Table Eusideroxylon and Potoxylon, two monotypic In- 3, and those of our preferredcalibration are de- donesian genera that consistentlyplace basally in picted in Figure5. Cryptocaryeae (Figs. 1, 2). Like Hypodaphnis, they have with fourcollaterally arranged locelli, DISCUSSION but their ovaries are only semi-inferior.However, The two-tieredtaxon and molecularsampling the larger molecular sample (matrix II) places Hy- adoptedin thisstudy provides a generallywell sup- podaphnis sister to remaining Lauraceae with mod-

Figure5. Phylogramsshowing clock enforcedHKY-F distanceson reducedparsimony-based topologies depicting terminal(5a) and basal (5b) clades in Lauraceae. Divergencetimes in Figure5a are based on ITS and thosein Figure 5b on rpll6 sequences.The timescale beloweach phylogramreflects a calibrationin whichequivalent nodes (indicated by *) in Figure5a and Figure5b are fixedat 90 millionyears. Node labels (a-f, x, z, and A-G) correspondto those listed in Table 3. The geographicdistributions of terminaltaxa are given:AF = Africa,AS = Asia, BO = Borneo, CA = CentralAmerica, CI = CanaryIslands, MA = Madagascar,MC = Macaronesia,NA = NorthAmerica, and SA = SouthAmerica.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 5a 5b rpl6Ocotea6 Endlicheriachalisea SA grayiMA Rhodostemonodaphnescandens SA Cinnamomum Ocotea guianensis SA camphora AS Ocotea tristisSA Ocotea tomentellaSA Chlorocardium SA f l Nectandral [ amazonum SA rodiei Pleurothyriuminsigne SA brAnaueria e Ocotea helicterifoliaCA brasiliensisSA ITS! Ocotea heydeana CA Sextonia Ocotea foetensMC E pubescens SA d Ocotea bullataAF Mezilaurus Ocotea grayiMA triuncaSA

Cinnamomumoleifolium SA Caryodaphnopsis SA C Cinnamomumquadrangulum bilocellataAS C | Cinnamomumjaponicum AS B Cinnamomumverum AS Caryodaphnopsis tomentosaSA -. Sassafras tzumuAS x Cpo y b _ SasrSassafras albidumNA CryptocaryathouvenotiiMA Linderabenzoin NA D Linderaumbellata AS A Bellschmiedia P - Apoalonias barbujana Cl C tilaranensisCA a z Persea thunbergiiAS Eusideroxylon Persea caerulea SA zwageri BO Persea lingueSA Hypodaphnis Sextonia pubescens SA zenkeriAF 0.01 substitutions/site 0.01 substitutions/site

a b f A B C D,G F | p

0 2 .Time (Mya) I74 Time (Mya) go 45 20 174 158 120 90 44

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 122 Annals of the Missouri Botanical Garden

Table 3. Clock enforcedHKY-F, distancesaccumu- carya, Endiandra, Eusideroxylon,Potameia, and lated afterdivergence events among terminal (Table 3a) Potoxylonis considerablein both analyses inves- and basal (Table 3b) lineagesin Lauraceae,and estimates tigatingbasal relationshipsin Lauraceae (Figs. 1, of divergencetimes simulating two biogeographic scenar- 2). Anatomicalfeatures stress isolation of Aspido- ios. HKY-F, distancesin Table 3a are obtainedfrom ITS stemon,Eusideroxylon, and Potoxylonmore than and thosein Table 3b fromrpl6 sequences. Calibration 1 simulatesWest Gondwanan vicariance for the trans-At- theiraffinities (Richter, 1981), but close relation- lantic disjunctionin the Ocotea complex;calibration 2 ship withCryptocarya has been suggestedin recent simulatesGondwanan origin for the Chlorocardium-Me- morphology-basedsystems (e.g., Rohwer,1993a; zilaurus lade. Node labels are equivalentto thosein Fig- van der Werff& Richter,1996). WithCryptocarya ure 5, and ages fixedfor calibration purposes are under- they share a deeply urceolatefloral hypanthium lined. * = Equivalentnodes. that develops into deep cupules enclosing the except fora small terminalorifice. Unlike HKY-F Calibration1 Calibration2 the previousgenera, in Beilschmiediaand Endian- distancefrom time(Mya) time(Mya) Node node to tip + SD + SD ? SD dra the hypanthiumis shallowand a cupule never develops,while the fruitsof Potameia are either a. Terminallineages in Lauraceae. freeor seated in a small discoid structure.Koster- a* 0.09740 ? 0.0106 354 ? 30 90 mans (1957), stressingthe degreeof cupule devel- b 0.05715 ? 0.0083 171 ? 21 44 ? 7 opment in his scheme for Lauraceae, placed c 0.04309 ? 0.0073 156 ? 20 40 ? 7 Beilschmiedia,Endiandra, and Potameiawith Per- d 0.03793 ? 0.0068 138 ? 19 35 ? 6 sea (also non-cupulate,but of the distalPerseeae- e 0.02476 ? 0.0055 90 23 ? 5 f 0.02175 ? 0.0052 79 ? 14 20 ? 5 Laureae clade). Close relationshipwith Cryptocarya x 0.01437 ? 0.0042 52 ? 12 13 ? 4 has since gainedsupport from wood and barkanat- z 0.03499 ? 0.0066 127 + 18 32 ? 6 omy(Richter, 1981), inflorescencemorphology (van der Werff& Richter,1996), embryology(Heo et al., b. Basal lineagesin Lauraceae. 1998), and moleculardata (Rohwer,2000; herein). A 0.03886 ? 0.0059 682 ? 105 174 ? 32 The topologyin Cryptocaryeaereveals a trend B 0.03513 ? 0.0056 620 ? 100 158 ? 31 C 0.02683 ? 0.0050 473 ? 88 120 ? 27 towardincreased ovaryexsertion, in both D 0.02038 ? 0.0044 360 ? 77 91 ? 20 and .Eusideroxylon and Potoxylon,with semi- E 0.03162 ? 0.0054 558 ? 95 142 ? 24 inferiorovaries, lie sisterto generawith superior F 0.00977 ? 0.0058 172 ? 54 44 ? 14 ovaries. branches next (Fig. 2), and G* 0.02006 ? 0.0043 354 90 Cryptocaryalies sisterto thenon-cupulate clade of Beilschmiedia,Endiandra, and Potameia (Figs. 1, 2). Endiandraand Potameia have a reducednum- ber of floralparts relativeto Beilschmiedia,but erately high support (Fig. 2). This peripheral po- whetherthey nest withinthe latter(Figs. 1, 2) is sition for Hypodaphnis is also indicated by matK notwell resolved. sequences, albeit with < 50% bootstrap support Othergenera that have been allied to members (Rohwer, 2000), but difficultto support with mor- of Cryptocaryeaebut not hereinare eithermono- phology. Any outgroup comparison is stymied by typicor oligotypic.Their generic status is also con- the unsettled sister family relationship of Laura- troversial(e.g., Rohwer, 1993a). Dahlgrenodendron, ceae. Hernandiaceae, with inferiorovaries, are fa- withonly D. natalensis(J. H. Ross) J.J. M. van der vored over Monimiaceae with 100% bootstrapsup- Merwe & A. E. van Wyk,has distinctivepollen port by morphology(Doyle & Endress, 2000), but ornamentation(van der Merweet al., 1988) but is molecular data have been ambiguous (Renner, otherwisenot differentfrom Cryptocarya (Rohwer, 1999; Renner & Chanderbali, 2000; Qiu et al., 1993a). Triadodaphne,with three species, is ten- 1999). A Hernandiaceae-Lauraceae lade receives tativelydistinguished from Endiandra by its un- modest support here (Figs. 1, 2), and when Hypo- equal perianthwhorls and deeper hypanthium daphnis lies sister to remaining Lauraceae (Fig. 2), (Kostermans,1993). In Hexapora,comprised of H. inferior ovaries are a potential synapomorphyfor curtisiiHook. f.,the outer six stamensare extrorse, the two families. However, given the non-inferior and the thirdand fourthwhorls staminodial, but state of all other Lauraceae, independent gain, re- otherwisethe is similarto Beilschmiedia. quired also by the topology in Figure 1, is equally Brassiodendron,with only B. fragransC. K. Allen, parsimonious. also has onlysix fertilestamens, and accordingto Cryptocaryeaesensu stricto. Support for the lade Kostermans(1957) and Hyland (1989) should be comprisedof Aspidostemon, Beilschmiedia, Crypto- includedin Endiandra.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbali et al. 123 2001 Phylogenyand Biogeographyof Lauraceae

Cassytha, Caryodaphnopsis,and Neocinnamo- that can mislead phylogeneticestimates (Felsen- mum. These three genera are among the most stein,1978; Lyons-Weiler& Hoelzer,1997). enigmaticof the family.In our analyses of matrix Caryodaphnopsisand Neocinnamomumare mor- I, they constitutea statisticallyuncorroborated phologicallysimilar, sharing triplinerved venation lade (with< 50% bootstrapsupport) that lies sis- and four-locularanthers with the locelli arranged ter to the rest of the family,also withoutsupport in a shallow arc (sometimestwo-locular in Cary- (Fig. 1). This alliance is disbandedby additional odaphnopsis,in a horizontalrow in Neocinnamo- molecularcharacters provided by matrixII, but mumdelavayi (Lecomte) H. Liu). In contrast,Car- theirposition in thispart of the tree receives strong yodaphnopsishas opposite leaves, a perianthof support(Fig. 2). Some elementsof Cassytha'spo- stronglyunequal ,and lacks a cupule,while sition may be due to long brancheffects in our Neocinnamomumhas alternate(spiral) leaves, sub- analyses. equal tepals,and a shallowcupule withpersistent The herbaceousparasitic twiner, Cassytha, is the tepals. Close relationshipbetween Neocinnamo- sole exceptionto the arborescencetypical of Laur- mumand Cinnamomum(Kostermans, 1974a), and aceae, and it has usuallybeen placed in a separate betweenCaryodaphnopsis and Persea (Kostermans, subfamily(e.g., Kostermans,1957; van der Werff 1974b; Rohwer,1993a), can be ruled out,but the & Richter,1996). Subfamilialposition is supported relationshipsof these two genera are not clearly by ab initio cellular endospermCassytha shares indicated by our data. They either constitutea withHernandiaceae, Monimiaceae, and otherLaur- lade, albeit with Cassytha(Fig. 1), or Caryoda- ales (Heo & Tobe, 1995; Heo et al., 1998). Such phnopsislies betweena Neocinnamomum-Cassytha endospermformation is also reportedfrom - lade and the restof thefamily (Fig. 2). WithCas- lularia (Bambacioni-Mezzetti,1941), but nuclear sythaexcluded, either Caryodaphnopsis or Neocin- endospermis found in all other Lauraceae that namomumlies sisterto therest of the family (clad- ograms not shown). Neocinnamomumwas not have been examined,including Hypodaphnis (Heo included in Rohwer'smatK study,and Caryoda- et al., 1998). In Rohwer'smatK study Cassytha was phnopsiswas placed as it is in Figure2. Anatomical placed betweenHypodaphnis and the rest of the affinitiesof Neocinnamomum and Caryodaphnopsis family,but without strong statistical support. Here, withChlorocardium and Cryptocaryeae,respective- close relationshipwith Neocinnamomum receives ly (Richter,1981), are consistentwith their rela- veryhigh statistical support from matrix II (Fig. 2), tivelybasal positionin the family. but morphologicalsynapomorphies for these two generaare not known.Instead, Cassytha and Neo- Chlorocardium-Mezilauruslade. The lade com- cinnamomumhave the longestbranches in the to- prised of Anaueria, Chlorocardium,Mezilaurus, pology,differing from each otherby over279 mu- Sextonia,and a novel taxon(Gen. & sp. nov.)re- tations(uncorrected "p" distances,uninformative ceives 99% and 96% bootstrapsupport from matrix charactersincluded), while the branch uniting them I and II, respectively(Fig. 1). It is one ofthe more is supportedby comparativelyfew (66) mutations. intriguingclades in the family.Close relationship WithNeocinnamomum removed from the analysis, betweenAnaueria and Mezilaurushas been sug- Cassythaand Caryodaphnopsisconstitute a lade gested(Richter, 1981; Rohwer,1993a), butthe pos- (cladogramnot shown).In both genera the outer sibilitythat all thesetaxa constitutea lade oftheir whorlof tepals is stronglyreduced, but this con- own has neverbeen consideredon morphological ditionappears elsewherein Lauraceae (e.g., Per- grounds.So far,characters uniting them have only sea), and othercharacters to supporta Cassytha- been providedby moleculardata. A lade com- Caryodaphnopsislade are unknown.However, prisedof Chlorocardiumand Mezilaurus(plus Wil- with both Neocinnamomumand Caryodaphnopsis liamodendron,a small genusof 3 species differing removed,Cassytha still lies sisterto the restof the fromMezilaurus primarily in the numberof locelli; family.If long branchescannot attract in theirmu- not herein)received moderate support from matK tual absence (Sidall & Whiting,1999), thisfinding sequences, but Rohwer(2000) questioneda close would implythat Cassythais correctlyplaced in relationshipciting anatomical and floraldifferenc- this general part of the phylogeny.Alternatively, es. Here, Chlorocardiumand Mezilaurusplace in long branchedtaxa, such as Cassytha,experience separate subclades that can be characterizedby multiplesubstitutions that erode genealogicalsig- phyllotaxy. nal, randomizecharacter states with respect to true The subclade ofGen. & sp. nov.,Mezilaurus, and relatives,and lead to chance convergenceon the Sextonia accommodatestaxa withobovate, coria- molecularstates of distantlineages, all qualities ceous leaves borne in terminalclusters (Fig. 2).

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 124 Annals of the Missouri Botanical Garden

Unlikemost other Lauraceae withterminally clus- relationshiphas never been formallyrecognized. teredleaves, in thesetaxa the clustersare notsep- OnlyKostermans (1957) placed thesetwo tribes in arated by seasonal growthspurts. Instead, growth close proximityin his graphicalscheme for Laur- is continuous,and apparentlyquite slow,resulting aceae, conceivablyto expresshis observationthat in a continuousspiral of leaf scars. This growth fleshyhemispherical cupules are typicalof, and re- patternis rare but not unique to this lade; such strictedto, generatherein. Elsewhere in Lauraceae leafclusters are at least also knownin Alseodaphne, hemispherical,but rather woody, cupules also occur of the Persea group(below). In the othersubclade, in Chlorocardiumand Sextonia,both included in Anaueriaand Chlorocardiumshare opposite leaves Cinnamomeaeby Kostermans(as Ocotea), but of (Fig. 2). This subclade receivesconsiderable mo- the Chlorocardium-Mezilauruslade herein. lecularsupport, but both genera find morphological Persea group. This lade (Fig. 3), includingAl- allies withinthe othersubclade. Anaueriais ana- seodaphne,Apollonias, Dehaasia, Persea,and Phoe- tomicallymore similar to Mezilaurus (Richter, be, accommodatesall non-cupulategenera of van 1981), withwhich it also sharesglandless . der Werffand Richter's(1996) Perseeae. It is Roh- Chlorocardiumis unique withits xylemof coronat- wer's(1993a) Persea group,without Caryodaphnop- ed vessel elements(Kostermans et al., 1969), and sis. Nothaphoebewas notinvestigated herein but is its largerotate flowers with an increasednumber of morphologicallyclose to Alseodaphne. stamens(to 20) are unmatchedin the lade. How- Generic delimitationin the Persea group has ever,its papillose,tongue-shaped stamens, all with been controversial,and all generawith four-locular a pair of small basal glands,are much like those anthers.have at some pointbeen placed in synon- foundin the second and thirdstaminal whorls of ymyunder Persea (e.g., Bentham,1880; Koster- Sextonia. mans,1957). Apolloniasand Dehaasia have always All South Americangenera that do not clearly been segregatedon the basis of theirtwo-locular assign to genericgroups based on wood and bark anthers,but the genericimportance of this char- anatomyor inflorescencestructure (van der Werff acterand its use to delimitApollonias from Phoebe & Richter,1996) place in a Chlorocardium-Mezi- and Dehaasia fromAlseodaphne is questionable laurus lade. MonotypicCosta Rican Povedada- (Rohwer et al., 1991; Rohwer,1993a; van der phne (not examinedhere) was consideredclose to Werff,in press). Othergeneric characters, includ- Mezilaurusby Rohwer(1993a), but his matK data ing relativetepal sizes, whethertepals persistin (Rohwer,2000) suggesteda place withgenera here fruit,and if so, mannerof persistence,have also placed in Cinnamomeae(below) whereit is mor- been questioned(van der Werff,1989; Rohweret phologicallyclose to the Ocoteacomplex. No other al., 1991). Our presentsampling does not ade- membersof the Chlorocardium-Mezilauruslade quatelyaddress these issues. Only Persea is rep- are suspectedon morphologicalgrounds. resentedby morethan one species. Asian Persea MonophyleticGroups in the Perseeae-Laureae (subg. Machilus) places withpaleotropical Alseo- lade. The large terminallade thataccounts for ,Apollonias, Dehaasia, and Phoebe, while mostof the moderngeneric and species diversity AmericanPersea (subg.Eriodaphne and subg.Per- of Lauraceae includes Laureae of mostclassifica- sea) constitutesa separate lade (Fig. 3), but the tionsystems and van derWerff and Richter's(1996) implicationthat Persea is notmonophyletic has lit- Perseeae. The presentresolution does not support tle support.Detailed morphologicaland molecular the dichotomyimplied by these tribal concepts studies are needed to resolverelationships within (Fig. 3). Instead,five genera of Perseeae (Persea thislarge groupof ca. 400 species, mostof which group)lie sisterto a lade comprisedof Laureae are foundin tropicalAsia. and remainingPerseeae. The genericcomposition Laureae. Close relationshipamong , of the lattergroup compares favorably with Koster- Adenodaphne,Laurus, Lindera, Litsea, Neolitsea, mans' (1957) Cinnamomeae(Fig. 3). Possible res- Parasassafras,and Sassafrashas been recognized olutionof a Perseeae-Laureae lade into a small in almostall classificationsof Lauraceae. All are Persea groupand a large Laureae-Cinnamomeae dioecious and mosthave umbellateinflorescences lade was indicatedby matK sequences (Rohwer, subtendedby involucralbracts. In this study,par- 2000), but topologywas unstableand lacked sta- simonyanalyses place Sassafrasbetween well-sup- tisticalsupport. Support is strongerhere withthe portedcore Laureae and remaininggenera (Fig. 3). Persea groupand Laureae-Cinnamomeaelade re- However,membership in Laureae was foundby ceiving89% and 93% bootstrapsupport, respec- minimumevolution analyses, and parsimony-based tively(Figs. 3, 4). A close Laureae-Cinnamomeae treesin whichSassafras lies sisterto core Laureae

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbaliet al. 125 2001 Phylogenyand Biogeographyof Lauraceae

(Fig. 4) are just threesteps longer.Introrsely po- tropicalgenera in Cinnamonium.Monotypic Mocin- sitionedlocelli in all staminalwhorls support a nodaphnewas describedto recognizea reduction place forSassafras in Laureae. Elsewherein Laur- in numberof staminalwhorls (Lorea-Hemandez, aceae introrselypositioned locelli are restrictedto 1995), and Aiouea p.p. [A. dubia (HBK) Mez and the outer two staminalwhorls. Another potential A. guianensisAubl. herein]differs mainly in locelli synapomorphyis the dioecious breedingsystem number,both characters of traditionalgeneric val- shownby Sassafras and core Laureae. In Laura- ue. The findingthat Ocotea ikonyokpevan der ceae, dioecyis otherwiseonly found in basallypo- Werff,a recently described species fromCameroon, sitionedHypodaphnis (Fig. 1) and a distalclade of is placed with Cinnamomumis surprising.How- Ocotea s. str.,Endlicheria, and Rhodostemonoda- ever, a leaf fragmentfrom the holotypesheet phne (Fig. 3). and ,not (Thomas10456, MO) was extracted,amplified, and herein,should also place in Laureae on the basis sequenced onlywith other species of Ocotea. Fur- of dioecyand introrselocelli. thermore,ITS1 and ITS2 regionsof 0. ikonyokpe Umbellulariais usually placed in Laureae be- were amplifiedand sequenced separately.Neither cause of its umbellateinvolucrate section is identicalwith accessions of Cinnamo- (e.g.,van derWerff & Richter,1996), butits flowers mum,and bothsupport a place withCinnamomum. are bisexual and locelli of the innermoststaminal In Africa,0. ikonyokpeshares (sub)opposite leaves whorlare extrorse,not introrse.A 16-bp repeatin withEast African0. michelsoniiRobyns & Wilczek trnL-trnF(Fig. 1) and ITS sequences (Figs. 3, 4) and 0. usambarensisEngl. (not herein).All other distanceUmbellularia from Laureae and place it in AfricanOcotea have spirallyarranged leaves (van the Ocotea complex(below). der Werff,1996). Interestingly,0. ikonyokpeasso- Genericdelimitation in Laureae is unsettled.Lit- ciates withAsian Cinnamomum(mostly opposite- sea alone accommodatesca. 400 of the approxi- leaved) insteadof mostlyalternate-leaved neotrop- mately700 species, and most genericlimits are ical Cinnamomum(Figs. 3, 4). The staminodes, probablyartificial (Rohwer, 1993a; Li & Christo- relativelysmaller than seen in Cinnamomum,and phel,2000). As withthe Persea group,detailed sys- withoutsagittate apices (althoughglandular as in tematicstudies are needed to resolvenatural line- Cinnamomum),refer this species to Oco- ages in Laureae. tea, but leaf arrangementis perhapsan overlooked characterhere. Cinnamomeae. All remaininggenera were pre- Neithermolecular nor morphological synapomor- viously placed in Cinnamomeae(sensu Koster- phies readilyappear forthe Cinnamomumgroup mans, 1957), albeit togetherwith Sassafras, Acti- (Cinnamomum, Aiouea p.p., Mocinnodaphne, and nodaphne,and Neocinnamomum.With these three Ocotea p.p.), but enforcingmonophyly adds only genera excluded, Cinnamomeaeis van der Werff one step to parsimony-basedtrees (Fig. 4). Still, and Richter's(1996) Perseeae withoutthe Persea New and Old World remainseparate sub- group.Cinnamomeae are thusa sizeable subsetof species clades in the constrained This New World- the Perseeae-Laureaeclade (Fig. 3), accommodat- clade. in ing all ofits majorneotropical genera (e.g., Aiouea, Old Worlddichotomy is also evident wood and Aniba, Endlicheria,Licaria, Nectandra,Pleuroth- barkanatomy (Richter, 1981), and can be deduced yrium,and Rhodostemonodaphne)as well as wide- fromtraditional placement of neotropicalCinna- spread Cinnamomumand Ocotea. momum in Phoebe (of the Persea group above) until Cinnamomeae share hemispherical cupules transferredby Kostermans(1961). Withover 350 (rarelypoorly developed) with Laureae and retain species distributedfrom (sub)tropical Asia to the the thyrsoidnon-involucrate inflorescences of the Neotropics,one Africanmember; and a fewrepre- Persea group.Thus, uniquelyderived features are sentativesin Australiaand thePacific Islands (pri- not obvious. Bootstrapsupport for Cinnamomeae marilyFiji), the Cinnamomumgroup is speciose reaches only 52% in unconstrainedparsimony and widespread. analyses (Fig. 3), but raised to 86% by enforcing Ocotea complex. The remaininggenera of Cinna- monophylyof a genericalliance centeredaround momeae forma stronglysupported clade within Cinnamomum(Fig. 4). which membersof Ocotea are widely dispersed Cinnamomumgroup. The delimitationof Cinna- (Figs. 3, 4). Findingthat Umbellularia places here, momumis based on its nine stamenswith four- and not in the Laureae, clarifiesconflicting indi- locular anthersand a fourthandroecial whorl of cations fromfloral morphology and well-developedstaminodes provided with sagittate structure(discussed underLaureae, above). Apart glandularapices. The presentdata nest two neo- froma fewOld Worldspecies of Ocotea,the com-

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 126 Annals of the MissouriBotanical Garden

plex is restrictedto the New Worldand accounts bitzki,1993). A relativelybasal positionin theOco- for most of the generic and species diversityof tea complexis suggestedby ITS sequences (Figs. Lauraceae in the Neotropics. 3, 4). Clades resolvedwithin the Ocotea complexcan Ocotea helicterifoliaspecies group. The clade be circumscribedin geographic,and sometimes (Figs. 3, 4) comprisedof Ocoteabotrantha Rohwer, morphological,terms. Basal branchesin the com- 0. helicterifolia(Meisn.) Hemsl.,and 0. heydeana plex are occupiedby Old Worldspecies of Ocotea, (Mez & Donn. Sm.) Bernardirepresents a diverse NorthAmerican Umbellularia, and primarilyCen- butcohesive assemblage of species in Ocotea.Core tral Americanspecies groups in Nectandraand membersare characterizedby hirsuteleaves and Ocotea. Two derivedclades are centeredin South twigs,bisexual flowerswith partially papillose te- America.In the more speciose, Nectandras. str. pals, glabrousor weaklypapillose anthers with four and Pleurothyriumlie sisterto a dioecious lade pollen sacs arrangedin two superimposedpairs, comprisedof Endlicheria,Ocotea s. str.,and Rho- and well-developedstaminodes (van der Werff, dostemonodaphne.In the second and less speciose 1999). Close relationshipwith non-hirsute species South America-centeredlade, Aniba, an assort- withthis generalfloral structure, i.e., the Ocotea mentof Ocotea species, and mostlymono- to oli- heydeanaspecies group,and withthe Ocotea sin- gotypicgenera associate with Licaria. uata species group,which differs by moreheavily Old WorldOcotea. Outside of the Neotropics, papillose tepals and anthers(here representedby Ocoteais representedby 0. foetens(Aiton) Baill. in 0. botranthaRohwer) was anticipatedby Rohwer Macaronesia,7 species in mainlandAfrica, and (1991). Withthe Nectandra coriacea species group, about 30 species in Madagascar. In this study, and Umbellularia,the Ocotea helicterifoliaspecies South African0. bullata (Burch.) E. Mey. and 2 groupshares well-developed staminodes with glan- species fromMadagascar, 0. grayi van der Werff dular apices, while theirpapillose anthersand te- and 0. malcomberivan der Werff,constitute a pals suggestan affinitywith Nectandra s. str.and stronglysupported lade. Ocoteafoetens is almost Pleurothyrium.Their place in the presentphylog- indistinguishablefrom 0. bullata,but surprisingly enyis consistentwith this intermediate morphology. its place withOld WorldOcotea receives < 50% The groupis distributedthroughout Central Amer- bootstrapsupport (Figs. 3, 4). Morphologicalchar- ica and numbersaround 30 species. acters distancingOld World Ocotea fromNew Ocotea s. str.,Endlicheria, and Rhodostemonoda- Worldrelatives do not readilyappear. In the pre- phne. A clade comprisedof all dioecious Ocotea sent reconstructionOld WorldOcotea lie sisterto sampled for this studyand the only neotropical the New Worldcomponent of the Ocotea complex. generawith this breeding system, Endlicheria and Nectandracoriacea speciesgroup, Nectandra s. str., Rhodostemonodaphne,is found in all ITS-based and Pleurothyrium.Representatives of the Nec- trees.It receiveslow bootstrapsupport as a whole tandra coriacea species group,N. coriacea (Sw.) (55%), but much better(93%) supportwithin the Griseb.,N. salicifolia(HBK) Nees, and N. purpurea group above the branch separatingEndlicheria (Ruiz & Pav.) Mez, place distantfrom a lade in punctulata(Mez) C. K. Allen and Ocoteapauciflora whicha broadmorphological representation of Nec- (Nees) Mez fromthe rest (Fig. 3). As seen in Figure tandras. str.pairs withPleurothyrium (Figs. 3, 4). 4, E. punctulataand 0. paucifloraappear to diverge Close relationshipbetween Nectandra s. str.and early,shortening the branchsupporting the entire Pleurothyriumwas also indicated by matK se- clade, but thiseffect could also be obtainedby re- quences (Rohwer,2000). The two share relatively versals to ancestral molecular states along the large rotateflowers with heavilypapillose tepals branchuniting these two species. and stamens,and relativelypoorly developed stam- Taxa placed here include the type species of inodes. Nectandras. str. and Pleurothyriumare Ocotea,0. guianensisAubl., and representseveral centeredin South Americawith ca. 100 and 40 species groupsrecognizable among dioecious Oco- species, respectively.The Central America-cen- tea (e.g., Rohwer,1986). Since representativesof tered Nectandra coriacea species group (ca. 20 Endlicheriaand Rhodostemonodaphnealso sample spp.) was perceived as accommodatingthe most a wide range of morphologicalvariation within primitiveelements of Nectandra, retaining Ocotea- these moderatelysized but heterogeneousgenera, like non-scalariformvenation, and all approximately300 dioeciousspecies ofthe Oco- non-papillosity,distinct filaments, and a well-de- tea complexshould place here. In this clade ge- velopedfourth androecial whorl of staminodeswith nericlimits based on locelli arrangementand num- glandularapices (Rohwer,1993b; Rohwer& Ku- ber are not supported.The Ocotea species forma

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbaliet al. 127 2001 Phylogenyand Biogeographyof Lauraceae

paraphyleticassemblage withinwhich Rhodoste- Ocotea insularis(Meisn.) Mez and Aiouea costari- monodaphneand Endlicheriaare nested (Figs. 3, censis(Mez) Kosterm.are unitedwith 100% boot- 4). Rhodostemonodaphnehas four-locularanthers strapsupport (Figs. 3, 4). The twodiffer only in the like Ocotea,but the locelli are arrangedin a shal- numberof locules per anther,again illustratingthe low arc or horizontalrow rather than superimposed weaknessof this characterin genericdelimitation pairs,at least in the outerstamens. Endlicheria is (van der Werff,1984). Curiously,as notedby van two-locular,but withE. punctulatapaired with 0. der Werff(1988) and Rohweret al. (1991), like A. pauciflora,and otherspecies placed withRhodos- costaricensis,other Aiouea species withcloser ties temonodaphne(Figs. 3, 4), it is at least di-phyletic. to Ocoteaare CentralAmerican (e.g., A. lundelliana C. K. Allen, not herein),while South American Licaria group. The branch unitingDicypellium, Aiouea associatewith Cinnamomum (e.g., A. dubia Kubitzkia,Licaria, Paraia, ,and two and A. guianensis,Fig. 3). species of Ocotea receives93% bootstrapsupport (Fig. 3) and seems to be a naturalalliance. Ga- BIOGEOGRAPHY mantheraand (neither here- in) associate withthe Licaria groupon morpholog- Genera and clades in Lauraceae sort into two ical grounds.All these generahave cupules with main geographicgroups (Figs. 2, 4). Hypodaphnis, double-rimmed(or more)margins. Given these un- the Cryptocaryeae,Cassytha, and the Chlorocar- usual cupules, a genericalliance centeredaround dium-Mezilauruslade as seen in Figure1 are pre- Licaria has been informallyrecognized in recent dominantlyor entirelysouthern hemispheric, while morphologicalsystems (Kostermans, 1957; Rohwer, Caryodaphnopsis,Neocinnamomum, the Persea 1993a). Ocotea quixos(Lam.) Kosterm.and 0. ver- group,the Cinnamomumgroup, and Laureae are aguensis (Meisn.) Mez representthe Ocotea den- either Asian or have amphi-Pacificdistributions drodaphnespecies group,a groupof 8 species re- (Figs. 2, 4). The distributionsof these two main markablein Ocotea fortheir ligulate stamens and groupsare consistentwith Gondwanan and Laura- double-rimmedcupules. A place in the Licaria sian histories,respectively, but thegeographic dis- groupis thus not surprising.Their distancefrom tributionof the Ocoteacomplex is notas easilycat- the restof Ocotea has been acknowledgedby sub- egorized.This diverse lade is mostlyneotropical generic(e.g., Mez, 1889; Rohwer,1986) and even witha Macaronesia-Afro-Malagasyelement added genericstatus; e.g., Sassafridium(Meissner, 1864). by approximately40 Old Worldspecies of Ocotea. Hutchinson(1964) even placed 0. veraguensis(as Whetherancestors of the Ocoteacomplex migrated Sassafridium)in a monotypictribe because he in- into SouthAmerica via Africa(Raven & Axelrod, terpretedthe locelli in the thirdstaminal whorl to 1974) or via NorthAmerica (Rohwer, 1986; Taylor, be introrse,a conditiononly known in Laureae. In 1988; Rohwer& Kubitzki,1993; Rohwer,2000) is factthe locelli are latrorse-introrse,as also found notevident from the topologyalone. in Dicypelliumand Urbanodendron,both of theLi- Paleogeographicreconstructions of West Gond- caria group.Elsewhere in Ocotea,double-rimmed wana breakupestimate that direct land connections cupules are foundin a fewdioecious species, e.g., betweenAfrica and SouthAmerica were lost by the 0. cujumaryMart. and 0. floribunda(Sw.) Mez. It Upper Mid-Cretaceous,ca. 90 Mya (Sclateret al., is unlikelythat these species will assign to theLi- 1977; Scotese et al., 1988; Parrish,1993). There- caria groupsince theirmorphologically close rela- fore,if the trans-Atlanticdisjunction in the Ocotea tives, 0. guianensis Aubl. and 0. percoriacea complex can be attributedto West Gondwanan (Meisn.)Kosterm., respectively, are firmlyseated in breakup,it would have to be at least 90 Mya old. the dioeciousclade discussedabove. This biogeographicscenario was simulatedon the Remainingtaxa place near the Licaria group parsimony-basedITS topologyby fixingthe New withoutstrong support (Fig. 3). Ocotea rhyncho- World-OldWorld divergence (node e in Fig. 5a and phylla(Meisn.) Mez and 0. odorifera(Vell.) Rohwer Table 3a) at 90 My and usingthe resultingrate of representspecies groupsthat Rohwer (1986) con- molecularevolution to estimatedivergence times sideredintermediate between the 0. dendrodaphne for othernodes. This calibrationyields a rate of species group (including0. quixos and 0. vera- 0.000275 substitutionsper site per millionyears, a guensisherein) and the restof Ocotea.Their posi- rate that halves the lowestever reportedfor ITS tionnear theLicaria groupis consistentwith Roh- (Suh et al., 1993), and whichplaces thedivergence wer'sinterpretation. Aniba, too, has been associated ofthe Chlorocardium-Mezilauruslade (Fig. 3; and withLicaria (e.g., Kubitzki,1982), but has simple- representedby Sextoniapubescens van der Werffin rimmedor rarelyweakly double-rimmed cupules. Fig. 5a) fromthe Perseeae-Laureae lade (includes

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 128 Annals of the MissouriBotanical Garden

the Ocoteacomplex) at 354 Mya (node a in Fig. 5a BASAL LINEAGES and Table 3a). This Devonianage precedesearliest undisputedangiosperm . Furthermore, if the Raven and Axelrod(1974) situatedthe cradle of equivalentnode in the basal topology(node G in the angiospermsin WestGondwana, and its prox- Fig. 5b and Table 3b) is fixedat 354 Mya and imityto Laurasiawas pivotalto theMid-Cretaceous divergencetimes for earlier lineages calculated, the presenceof angiospermpollen in the SouthLaur- radiationof the familyis placed in the Pre-Cam- asia Province(sensu Brenner,1976). Any expla- nationof the biogeographichistory of Lauraceae brian,ca. 682 Mya. Therefore,the neotropical-Af- also requiresearly migratory routes between Laur- rican disjunctionshown by the Ocotea complexis asia and West Gondwana.Southern hemispheric likelyto be much youngerthan West Gondwanan Hypodaphnis,Cryptocaryeae, Cassytha, and the breakup,and some amountof dispersalmust have Chlorocardium-Mezilauruslade indicate Gond- been involved. wanan history,but Caryodaphnopsisand Neocin- How did theOcotea complex, and othermembers namomumappear to be Laurasian. of the family,reach the New World?In bothmor- Caryodaphnopsisis disjunct between tropical phologicaland molecularattributes the Chlorocar- Americaand tropicalAsia, whileNeocinnamomum dium-Mezilauruslade occupies a basal and iso- is knownonly from tropical Asia. They represent lated positionin Lauraceae. It is also the only the onlyearly lineages in Lauraceae thatare pre- lineage of basal Lauraceae restrictedto South sent in Asia but are not also knownto occur in America(reaching its northernlimit in Costa Rica). Africa,Madagascar, and Australia,in contrastto These qualitiesargue for early isolation of the Chlo- widespreadgenera in Cryptocaryeaeand Cassytha. rocardium-Mezilauruslade in SouthAmerica, pre- The fossilrecord suggests that both Caryodaphnop- sumablyinitiated by WestGondwana breakup. To sis and Neocinnamomumhave an ancientLaurasian assess this biogeographicscenario on otherdiver- history.The fossilwood taxon Caryodaphnopsoxylon gencetimes, substitution rates in theITS and rpll6 richteriGottwald (1992) places the unique xylem data sets were re-calibratedusing an Upper Mid- anatomyof Caryodaphnopsisin Late Eocene Ger- Cretaceous(90 Mya) separationof SouthAmerica many.The fossilflower Neusenia tetrasporangiata fromAfrica to date the divergenceof the Chioro- Eklundfrom Late CretaceousNorth America com- cardium-Mezilauruslade fromits sister group pares favorablywith Neocinnamomum, and flowers (node a in Fig. 5a and Table 3a, node G in Fig. 5b and fruitsfrom the same localitycan be compared and Table 3b). Withthis second calibration,radi- to Caryodaphnopsis(e.g., Eklund,2000). Although ationof Lauraceae was estimatedat 174 ? 32 Mya the affinitiesof the latterfossils cannot be unam- (node A in Fig. 5b and Table 3b), and radiationof biguouslyassigned, the impliedantiquity of Cary- theterminal Perseeae-Laureae lade was placed in odaphnopsisand Neocinnamomumis consistent the Eocene, 44 + 7 Mya (node b in Fig. 5a and withtheir relatively basal positionsin Lauraceae. Table 3a). This estimatefor Eocene radiationof the Most likely,these moderngenera are descendants lattergroup is supportedby the fossilrecord. The ofthe Cretaceous Laurasian flora of Lauraceae doc- hemisphericalcupules of the London Clay Flora umentedby the fossilgenera Mauldinia (Drinnan (Reid & Chandler,1933) are restrictedto Laureae et al., 1990; Herendeenet al., 1994, 1999; Eklund and Cinnamomeaeof the Perseeae-Laureae lade. & Kvacek, 1998) and Perseanthus(Herendeen et Well-preservedflowers with the general floral struc- al., 1994). tureof generain the Persea groupand Cinnamo- The timingof events that resulted in themodern meae, but not othermembers of Lauraceae, have distributionof Caryodaphnopsiscan furthereluci- been described fromEocene deposits in North date its biogeographichistory. A relictualpresence America(Taylor, 1988) and Late Eocene Balticam- in SouthAmerica would imply a continuouspaleo- ber (Conwentz,1886). Thus,our second calibration, distributionfrom South America to Eurasia. How- thatwhich credits South American isolation of the ever,such continentalconfiguration also provides Chlorocardium-Mezilaurusclade to WestGondwan- directconnections between South America and oth- an breakup,estimates a realisticage forradiation er Gondwananterrains (reviewed in Hallam,1994), of the familyand complementsfossil evidence of and preferentialextinction in these Southernland- radiationof the Perseeae-Laureae groupin Early masses would be necessaryto explainthe modem TertiaryLaurasia. This congruenceprovides confi- disjunction.Alternatively, the rpll6 data set esti- dence thatage estimatesbased on our second cal- matesa relativelyrecent separation (44 ? 14 Mya) ibrationare good approximationsof actual diver- ofSouth American C. tomentosavan derWerff from gence times. Asian C. bilocellatavan der Werff(node F in Fig.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbaliet al. 129 2001 Phylogenyand Biogeographyof Lauraceae

5b and Table 3b). This would rule out a relictual cannot be discounted.All otherSouthern Hemi- presencein SouthAmerica and is consistentwith sphericgenera have narrowerranges. theview that disjunct distributions between tropical Hypodaphnismay be relictualin CentralAfrica Asia and tropicalAmerica are derivedfrom ances- since its ancestorsapparently diverged from the tralboreotropical ranges disrupted by Late Eocene rest of the familywhen directmigration between climaticcooling (e.g., Wolfe,1975; Tiffney,1985a, Gondwanaand Laurasia was possible (node A in b; Zhengyi,1983). Moreover,this calibrationim- Fig. 5b and Table 3a). Eusideroxylonranges from plies thatisolation of Caryodaphnopsis from the rest Borneo to Sumatra,and Potoxylonis endemicto ofthe family can be stagedin theEarly Cretaceous Borneo. With their placement in predominantly about 140 Mya (node E in Fig. 5b and Table 3b). SouthernHemispheric Cryptocaryeae, it is possible Increasingseparation of Laurasia fromGondwana, to regardthem as Gondwananrelicts as well. How- a salientfeature of Early Cretaceouspaleogeogra- ever,their separation from the rest of the tribeis phy (reviewedin Hallam, 1994), would have dis- dated at about 120 Mya (node C, Fig. 5b), an age ruptedtrans-Tethyan ancestral ranges and precip- thatpermits early migrationinto Laurasia, as en- itatedthe nextbiogeographic phase in Lauraceae, visioned for Caryodaphnopsisabove. Further, i.e., radiationon increasinglydistant Laurasian and Triantheraeusideroxylon Conwentz, an amber-em- Gondwananlandmasses. bedded flowerfrom the Eocene-Oligocenebound- Accordingly,in the NorthernHemisphere, the ary of the Baltic area (Conwentz,1886) compares Mid-Cretaceousfossil taxa, and thedirect ancestors remarkablywell with Eusideroxylon and adds to the of Caryodaphnopsisand Neocinnamomum,would possibilityof a Gondwanan-Laurasiandichotomy in have spreadthroughout southern Laurasia until de- Cryptocaryeae.Upper Cretaceous appearance of creasingtemperatures and theopening of the north theboreotropical Aquilapollenites in Borneo(Wolfe, Atlanticconstricted their descendants to tropical 1975; and referencestherein), and the composite of the Indo-Malayanregion (Bur- Asia and America.To the south,truly pantropical geologicalnature rettet al., 1991; Michaux,1991; and references generaand clades wouldhave attainedtheir wide- therein),are also consistentwith Laurasian history spread distribution,with seafloor spreading in the forEusideroxylon and Potoxylon. South Atlanticand Indian Oceans leading to in- All othermembers of Cryptocaryeaeand their creased regionalendemicity. These continentalre- allies are restrictedto, or best representedin, aus- configurationsappear to be reflectedin the distri- tral partsof the Old World,i.e., East Gondwanan butionof SouthernHemispheric genera. and derivedterrains. At theother end ofthe former Of pantropicalgenera, Beilschmiedia and Cryp- southerncontinent, the Chlorocardium-Mezilaurus tocaryaare the mostwidespread. The geneticdis- lade is restrictedto SouthAmerica. Thus, among tance-based age estimationsindicate that these these SouthernHemispheric genera and clades, generadiverged from their most recent common an- morebasal groupsare eitherwidespread or relic- ? cestorabout 90 20 Mya (node D in Fig. 5b and tual, and more derived groups are restrictedto Table 3b). Variancearound these age estimations Easternor WesternGondwanan fragments, consis- arguesfor direct migration throughout Gondwana, tentwith the progressive dismantling of Gondwana. and a widespreadpre-drift distribution for both Beilschmiediaand Cryptocarya.The presence of THE PERSEEAE-LAUREAE CLADE bothgenera in continentalAsia maybe due to the raftingof the Indian subcontinentand otherGond- ROUTES TO LAURASIA wanan fragmentsto the Asian plate. Later accre- The Perseeae-Laureae lade divergedfrom its tionsof Gondwananfragments with the Asian plate sistergroup, the Chlorocardium-Mezilauruslade, and Miocene island hoppingacross the Indo-Ma- since the Upper Mid-Cretaceous,but until fossil layanregion may also have been involved.The pan- membersappeared in Eocene Laurasia its biogeo- tropicaldistribution of Cassythais mostlydue to graphichistory is a mystery.Three alternative sce- one widespreadspecies, C. filiformisL.; all other nariosare conceivable.In a vicariantvein, consider approximately20 species are restrictedto the Old a West Gondwanancommon ancestor for the Per- Worldand show high regionalendemism in Aus- seeae-Laureae lade and its sistergroup, with tec- tralia(Weber, 1981). Althoughthe SouthernHemi- tonicactivity isolating direct ancestors of the Chlo- sphericdistribution centered in the Old Worldfa- rocardium-Mezilauruslade on South America vors a predominantlyEast Gondwananhistory for while strandingthose of the Perseeae-Laureae Cassytha,the possibilityof a Laurasianhistory fol- lade on Africa.Ancestors of the Perseeae-Laureae lowed by radiationinto its associatedxeric lade then migrateto Laurasia via NorthAfrica.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 130 Annals of the MissouriBotanical Garden

Alternatively,the northernroute of the Perseeae- gestthat its Asian and Americanmembers diverged Laureae lade could have includeda SouthAmer- around the Eocene-Oligocene boundary,ca. 32 ican phase with subsequent migrationto North Mya (node z in Fig. 5a and Table 3a). America and Eurasia. Precursorsof the Greater The distributionand representationof the Cin- Antilles spanned the PanamanianIsthmus as an namomumgroup in the Neotropicsand Asia is al- island chain in the Mid-Cretaceous(Pindell et al., mostidentical to thatof the Persea group.Whether 1988) providinga stepping-stonemigratory route New and Old Worldclades in the Cinnamomum out of SouthAmerica. Yet a thirdpossibility is that groupconstitute a monophyleticgroup is not yet the commonancestor of the Perseeae-Laureaeand clear. From age estimatesobtained by enforcing Chlorocardium-Mezilaurusclades was Laurasian monophyly(Fig. 5a), the assumedcommon ances- and sharedthe former northern continent with Car- tral gene pool divided aroundthe Eocene-Oligo- yodaphnopsisand Neocinnamomum.This scenario cene boundary,a divergencetime coincident with would requirethat the Chlorocardium-Mezilaurusthat calculated forthe Persea group.These simi- lade migratedinto South Americavia the Mid- laritiesin thetropical amphi-Pacific disjunctions in Cretaceousstepping-stone route provided by proto- the Cinnamomumand Persea groupssuggest com- GreaterAntilles. Evidence of an earlyfaunal and monality.Disruption of boreotropical ranges by cli- floristicexchange across this regionhas accumu- matic cooling around the Eocene-Oligocene lated (e.g., Cadle, 1985; Estes & Baez, 1985; Gra- boundary(Wolfe, 1975; Tiffney,1985a, b; Zhengyi, ham, 1995; Burnham& Graham,1999), but the 1983) wouldbe consistentwith the present age es- taxa involvedare usually distributedthroughout timates.Already tenuous biotic links across the northernCentral America and South America, NorthAtlantic and/or Pacific were severedat this while the Chlorocardium-Mezilauruslade only time,and dividedCinnamomum and Persea groups reaches Costa Rica to the north. receded to warmerpaleolatitudes in Asia and the Withoutan unambiguousCretaceous fossil re- Americas. cord forthe Perseeae-Laureae lade, we favorthe Like the Cinnamomum and Persea groups, Lau- firstor Africanscenario. North Africa is todaypart reae are mostdiverse in Asia witha smallerrange of the largestdesert system in the world,but was and representationin the New World.Lindera, Lit- covered by tropicalforest well into the Miocene sea, and Sassafrasreach the Americas, but of these (Axelrod& Raven, 1978). Duringthe Tertiary,Af- onlyLitsea rangessouth of temperateNorth Amer- rica movedprogressively northward, and migration ica, to Costa Rica. The unsettledgeneric delimi- to Eurasia across the narrowingTethys would have tationof Litsea and Lindera cautions against as- become increasinglyfeasible. The SouthAmerican sessmentof their disjunctions from morphology, but scenarioinvokes a circuitousroute to Eurasia and monophylyof Sassafras is well supportedhere fails to explainwhy no membersof the Perseeae- (Figs. 3, 4), providingan opportunityto assess the Laureae lade remainrelictual in SouthAmerica. classic NorthAmerica-Eastern Asia disjunction An earlyLaurasian history would have to account firstbrought into scientificfocus by Asa Gray forthe absence of the Chlorocardium-Mezilaurus(Boufford & Spongberg,1983). In Sassafras,diver- lade in Asia. gence of Asian S. tzumu (Hemsl.) Hemsl. from NorthAmerican S. albidum(Nutt.) Nees was esti- ROUTES TO THE NEW WORLD I: PERSEA GROUP, matedat about12 Mya(node x in Fig. 5a and Table CINNAMOMUMGROUP, AND LAUREAE 3a). This northerntemperate disjunction is much youngerthan the ? 30 Mya old tropicalamphi- The Persea groupis mostdiverse in Asia, with Pacific disjunctionsshown by Cinnamomumand onlyca. 80 of its approximately400 species found Persea groups.While climaticcooling in the Eo- in the New World.These occurmainly in montane cene and Oligocene (Wolfe,1975; Hallam, 1994) forestsin Centraland South America and range restrictedtropical taxa to lowerpaleolatitudes, for fromMexico to Chile,reaching the Atlantic coastal temperatetaxa intercontinentalconnections across forestsin southeasternBrazil. In theOld World,two northernlatitudes would have been possible until taxa are presentin the CanaryIslands. Apollonias much later in the Tertiary.The estimateddiver- barbujana(Cav.) Bornm.is placed in an unresolved gence timeseparating Asian fromNorth American Asian lade withAlseodaphne, Dehaasia, Persea Sassafrascoincides well withopening of the Bering subg. Machilus,and Phoebe (Figs. 3, 4). The other Strait,and supportsWolfe and Leopold's (1967) CanaryIsland endemic, (L.) Spreng., view that Mid-Mioceneloss of the Bering land was not sampled here. Pendingbetter resolution bridgeis the mostlikely cause of north-temperate withinthe Persea group,current age estimatessug- disjunctionsbetween and Asia.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbaliet al. 131 2001 Phylogenyand Biogeographyof Lauraceae

ROUTES TO THE NEW WORLD II: THE OCOTEA proximately20 Mya (nodef in Fig.5a and Table 3a) COMPLEX arguesfor arrival of the Ocotea complexin South Americaprior to Pliocene closureof the Panaman- The Ocotea complexaccommodates most of the ian isthmus.As the timingof the separationcoin- taxonomicdiversity of neotropicalLauraceae. In cides withincreased uplift of the northernAndes the Old Worldthe complexis weaklyrepresented in theearly Miocene, it is conceivablethat Andean in Macaronesia, Africa, and Madagascar. Any orogenydivided the ancestralrange. Further, since trans-Atlanticdisjunction produced by WestGond- lowlandgenera of the Ocotea complexplace in ei- wanan vicariancewas discounted(above) and in- ther South- or Central America-centeredclades stead the disjunctiondates to around the Oligo- (Fig. 4), Andean orogenyappears to maintainge- cene-Mioceneboundary, ca. 23 ? 5 Mya (node e nericendemism while allowing lower montane Cin- in Fig. 5a and Table 3a). The estimatedEocene- namomumand Persea groupsto rangewidely. Ex- Oligoceneage (node d in Fig. 5a and Table 3a) of ceptionally,South America-centeredclades range the Ocotea compleximplies an originconcurrent throughoutCentral America with widespread spe- withthe southwardmovement of megathermalfor- cies, e.g., N. cuspidata Nees of Nectandra s. str. ests (Wolfe,1975; Hallam, 1994), and its derived (Fig. 4), and vice versa, e.g., N. purpureaof the positionrelative to the previousclades indicates Nectandracoriacea species group(Fig. 4). Although boreotropicalancestry. Unlike previousLaurasian thesemay be secondaryrange expansions of indig- taxa,the Ocotea complexis absentin Asia. While enous Southand CentralAmerican taxa (e.g., Roh- Persea and Cinnamomumgroups appear as lower wer& Kubitzki,1993), theyindicate the underlying montanetaxa in theNeotropics, the Ocotea complex complexityof biogeographicpatterns. is especiallydiverse in thelowlands of South Amer- The biogeographichistory of Lauraceae outlined ica. Giventhese differencesin distributionand a hereshares much with that proposed by Doyle and relativelyrecent trans-Atlantic disjunction, their Le Thomas(1997) forAnnonaceae. As in thatdi- biogeographichistory may be quite differentfrom versemagnoliid family, three main phases are rec- thatof the otherboreotropical lineages. In thisre- ognizable.Early radiationof bothfamilies appar- gard xeric tolerancesshown by AfricanOcotea, entlyoccurred when migration between Gondwana CalifornianUmbellularia, and theCentral America- and Laurasia was possible. Next, diversification centeredNectandra coriacea group may be signifi- throughoutthe Cretaceous produced lauraceous cant.These taxa place basallyin the complex,and Cryptocaryeae,perhaps Cassytha, and the Chloro- theirsclerophyllous , unusual forLauraceae, cardium-Mezilaurus lade on Gondwana, with Car- adds to taxa thatlink the Madrean-Tethyanscler- yodaphnopsisand its allies on Laurasia. In Annon- ophyllousflora discussed by Axelrod(1975). This aceae, Anaxagoreaappears to be thecounterpart of broad-leavedflora ranged along the Tethyancoast Caryodaphnopsis.In bothfamilies, renewed contact fromNorth America to southeasternEurasia and betweenGondwanan and Laurasian fragmentsin NorthAfrica, and existed relativelycontinuously the EarlyTertiary resulted in a secondradiation on since the Late Eocene, onlydisrupted by increased Laurasianterrains. In Lauraceae,this boreotropical climaticcooling and dryingat the end of the Oli- phase producedthe Perseeae-Laureae lade, but gocene (Axelrod,1975). The 23 + 5 Mya estimate unlike Annonaceae,its descendantsdid not only ofthe trans-Atlantic disjunction in theOcotea com- recede to the Asian tropicswith climatic cooling. plex is consistentwith that expected for taxa with Three of the four major lineages of Lauraceae ancestral Madrean-Tethyanranges (e.g., Fritsch, evolved duringthis period,migrated to the Neo- 1996). Great disparityin species diversityon the tropics,and one of these,the Ocotea complex,un- twosides of the Atlanticmay be attributedto dis- derwenta majorradiation in the New World.This proportionateopportunities for speciation and dif- latterradiation has fewparallels in neotropicalphy- ferentiation.In the Neogene, continentalAfrica togeography.There are indicationsthat some line- moves progressivelynorthward into a drier and ages in the Leguminosae(Lavin & Luckow,1993) coolerclimate (Hallam, 1994), whiletectonic uplift and Melastomataceae(Renner & Meyer,in press) in the Panamanianisthmus (Pindell et al., 1988) are derived from boreotropicalancestors, and providesthe Madreanflora of southeasternNorth Krutzsch (1989) listed possible examples from Americawith opportunities for stepping-stone dis- Bombacaceae,Olacaceae, and Symplocaceae.The persal intoSouth America. emergingprospect of a largercontingent of Laura- Separationof the Central America-centered Oco- sian elementsin the lowlandNeotropics than pre- tea helicterifoliaspecies group fromits speciose viouslyrecognized can be assessed whenphyloge- South America-centeredsister group (Fig. 4) ap- nies of moretropical taxa become available.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 132 Annals of the Missouri Botanical Garden

OUTLOOK: TOWARD A PHYLOGENETIC cumscribedto accommodatejust thePersea group, ARRANGEMENT OF LAURACEAE and Umbellulariaremoved from Laureae to Cin- namomeae.The latteralso includes all remaining The utilityof morphologicalclassification that genera of van der Werffand Richter'sPerseeae. expresses evolutionaryhistory and relationships Several smaller,although morphologically distinc- withsupport from molecular data is obvious.For tive,taxa are notclearly placed, particularlyin the Lauraceae, appropriatecharacters to be employed case of Cassytha,to a lesser extentfor Caryoda- in such a scheme are elusive. Amongtraditional phnopsisand Neocinnamomum,and perhaps Hy- morphologicalcharacters, the numberof locules podaphnis.At a lowertaxonomic level, increased per antherattains generic and even supra-generic samplingis necessaryfor a thoroughreconsidera- importancein early schemes (Nees, 1836; Meis- tionof currentgeneric concepts among Lauraceae. sner,1864; Bentham,1880; Pax, 1889; Mez, 1889; In this study,only the Ocotea complexhas been Kostermans,1957). Severalexamples of the weak- representativelysampled; seemingly natural groups ness of thischaracter have been identifiedand are of genera and parts of largergenera have been confirmedby the presentmolecular data. Other identifiedwithin this complex. Similarly, increased charactersdo notfare much better. The use ofum- samplingin othermain clades identifiedhere will bellate involucrateinflorescences to circumscribe improveour understandingof relationshipsamong Laureae is a salient featureof mostclassification Lauraceae. schemes (e.g., Rohwer,1993a; van der Werff& but this clearlyevolved Richter,1996), syndrome LiteratureCited independentlyin Umbellularia.Similarly, dioecy appears threetimes on the phylogenyherein, in Asmussen,C. 1999. Towarda chloroplastDNA phylog- eny of the tribeGeonomeae (Palmae). Mem. New York Hypodaphnis,in Laureae, and again in the Ocotea Bot. Gard.83: 121-129. complex. Further,Kostermans' (1957) system Axelrod,D. 1975. Evolutionand biogeographyof Mad- stressesdegree of cupule development,but both rean-Tethyansclerophyll vegetation. Ann. Missouri Bot. extremesare foundin Cryptocaryeae,and the non- Gard.62: 280-334. and Tertiary cupulatecondition of Beilschmiedia and Endiandra & P. Raven. 1978. Late Cretaceous vegetationhistory of Africa.Pp. 77-130 in M. Werger thereinreappears in the distantlyrelated Persea (editor),Biogeography and Ecologyof SouthernAfrica. group.Equally problematical,morphological syna- Junk,The Hague. pomorphiesare notreadily noted for several clades Bambacioni-Mezzetti,V. 1941. Ricerche morfologiche thatreceive strongmolecular support. In the case sulle Lauracee,embriologia della Umbellulariacalifor- nica Nutt.e del Laurus canariensisWebb. Ann. Bot. of Cassythaand Neocinnamomumlong branchat- (Rome) 22: 99-119. tractioncan be held responsible,but on closerex- Benthain,G. 1880. Laurinae.Pp. 146-165. in G. Ben- aminationgenera of the Chlorocardium-Mezilaurus tham & J. Hooker (editors),Genera Plantarum3. L. lade can be allied by a mosaic of characters. Reeve, London. Blattner,F. 1999. Directamplification of the entireITS Althoughmajor clades identifiedby molecular regionfrom poorly preserved plant materialusing re- charactersdo notyield easily to morphologicalin- combinantPCR. Biotechniques29: 1180-1186. terpretation,a consensus over major generic group- Boufford,D. & J. Spongberg.1983. EasternAsian-east- ingsin Lauraceae appearsto be withinreach. Cryp- ern NorthAmerican phytogeographical relationships- A fromthe time of Linnaeus to the twentieth as circumscribed van der Werffand history tocaryeae by century.Ann. MissouriBot. Gard. 70: 423-439. Richter(1996), butprobably without Hypodaphnis, Brenner,G. 1976. MiddleCretaceous floral provinces and are nowsupported by anatomy(Richter, 1981), em- earlymigrations of angiosperms. Pp. 23-47 in C. Beck bryology(Heo et al., 1998), and moleculardata (editor),Origins and Early Evolutionof Angiosperms. (Rohwer,2000; herein). Considerablemolecular ColumbiaUniv. Press, New York. Burnham,R. & A. Graham. 1999. The historyof neo- supportexists for the Chlorocardium-Mezilaurus tropicalvegetation: New developmentsand status.Ann. lade, a group that is unique fromboth biogeo- MissouriBot. Gard.86: 546-589. graphic and morphologicalperspectives. Further Burrett,C., N. Duhig,R. & R. Varne. 1991. Asian consensus concerns a large lade comprisedof and south-westernPacific continental terranes derived fromGondwana, and theirbiogeographic significance. mostremaining genera in Lauraceae thathas been Austral.Syst. Bot. 4: 13-24. foundby this and previousmolecular data (Rohwer, Cadle, J. 1985. The neotropicalColubrid snake fauna 2000) and supportedby anatomy(Richter, 1981). (Serpentes:Colubridae): Lineage componentsand bio- This groupincludes all generaplaced in thetribes geography.Syst. Zool. 34: 1-20. Conwentz,H. 1886. Die Florades Bernsteins,Vol. 2. Die Perseeae and Laureae byvan derWerff and Richter Angiospermsdes Bernsteins.Willhelm Engelmann, (1996), butits subdivisionwarrants re-examination. Danzig. Towardthis, Perseeae could be morenarrowly cir- Doyle, J. & A. Le Thomas. 1997. Phylogenyand geo-

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbaliet al. 133 2001 Phylogenyand Biogeographyof Lauraceae

graphichistory of Annonaceae.Geogr. Phys. Quatern. Kobylinska.1999. A preliminaryconspectus of the Al- 51: 353-361. Ion floraof the late Cretaceous(Late Santonian)of Cen- & P. Endress. 2000. Morphologicalphylogenetic tralGeorgia, U.S.A. Ann. MissouriBot. Gard.86: 407- analysisof basal angiosperms:Comparison and combi- 471. nationwith molecular data. Int.J. PI. Sci. 161(Suppl.): Hillis,D. & J. Bull. 1993. An empiricaltest of bootstrap- S121-S153. ping as a methodfor assessing confidence in phyloge- Drinnan,A., P. Crane, E. Friis & K. Pedersen. 1990. neticanalysis. Syst. Bot. 42: 182-192. Lauraceousflowers form the PotomacGroup (Mid-Cre- Hutchinson,J. 1964. The Genera of FloweringPlants taceous)of Eastern North America. Bot. Gaz. 151: 370- (Dicotyledonae),Vol. 1. ClarendonPress, London. 384. Hyland,B. 1989. A revisionof Lauraceae in Australia Eklund,H. 2000. Lauraceousflowers from the Late Cre- (excludingCassytha). Austral. Syst. Bot. 2: 135-267. taceousof North Carolina, U.S.A. Bot.J. Linn. Soc. 132: Kostermnans,A. 1957. Lauraceae. Reinwardtia4: 193- 397-428. 256. & J. Kvacek. 1998. Lauraceous inflorescences . 1961. The New Worldspecies of Cinnamomum. and flowersfrom the Cenomanianof Bohemia(Czech Trew(Lauraceae). Reinwardtia6: 17-24. Republic, CentralEurope). Int. J. PI. Sci. 159: 668- . 1974a. A monographof the genus Neocinna- 686. momumLiou Ho. Reinwardtia9: 85-96. Estes, R. & A. Baez. 1985. Herpetofaunasof Northand . 1974b. A monographof CaryodaphnopsisA. SouthAmerica during the Late Cretaceousand Ceno- Shaw. Reinwardtia9: 123-137. zoic: Evidencefor interchange? Pp. 139-197 in F. Steh- . 1993. Noteson TriadodaphneKosterm. (Laura- li & S. Webb (editors),The GreatAmerican Biotic In- ceae). Rheedea 3: 129-131. terchange.Plenum Press, New York. , H. Pinkley& W. Stern. 1969. A newAmazonian Felsenstein,J. 1978. Cases in whichparsimony or com- arrowpoison: Ocotea venenosa.Bot. Mus. Leafl. 22: patibilitymethods will be positivelymisleading. Syst. 241-252. Zool. 27: 401-410. Krutzsch,W. 1989. Paleogeographyand historicalphy- . 1985. Confidencelimits on phylogenies:An ap- togeography(paleochorology) in the Neophyticum.P1. proachusing the bootstrap.Evolution 39: 783-791. Syst.Evol. 162: 5-61. Fritsch,P. 1996. Isozymeanalysis of intercontinental dis- Kubitzki,K. 1982. Lauraceae:Aniba. Fl. Neotrop.Mon- junctswithin (): Implications for the ogr.31: 1-84. Madrean-Tethyanhypothesis. Amer. J. Bot. 83: 342- Kuzoff,R., J. Sweere,D. Soltis,P. Soltis & E. Zimmer. 355. 1998. The phylogeneticpotential of entire26S rDNA Gentry,A. 1982. Neotropicalfloristic diversity: Phyto- sequences in .Molec. Biol. Evol. 15: 251-263. geographicalconnections between Central and South Lavin,M. & M. Luckow. 1993. Originsand relationships America,Pleistocene climate fluctuations, or an acci- of tropicalNorth America in the contextof the boreo- dentof the Andeanorogeny? Ann. MissouriBot. Gard. tropicshypothesis. Amer. J. Bot. 80: 1-14. 69: 557-593. Li, J. & D. Christophel.2000. Systematicrelationships . 1988. Changesin plantcommunity diversity and withinthe Litsea complex (Lauraceae): A cladisticanal- floristiccomposition on environmentaland geographical ysison thebasis ofmorphological and leafcuticle data. gradients.Ann. MissouriBot. Gard. 75: 1-34. Austral.Syst. Bot. 13: 1-13. Goldblatt,P. (Editor). 1993. BiologicalRelationships Be- Lorea-Hernandez,F. 1995. Mocinnodaphne:Un genero tweenAfrica and SouthAmerica. Yale Univ.Press, New nuevo de la familiaLauraceae en la florade Mexico. Haven. Acta Bot. Mex. 32: 25-32. Gottwald,H. 1992. Hdlzeraus marinenSanden des ob- Lyons-Weiler,J. & G. Hoelzer. 1997. Escapingthe Fel- eren EozAnvon Helmstedt(Niedersachsen). Palaeonto- sensteinZone by detectinglong branchesin phyloge- graphica,Abt. B. Paliophytol.225: 27-103. neticdata. Molec. Phylogenet.Evol. 8: 375-384. Graham,A. 1995. Developmentof affinitiesbetween Meissner,C. 1864. Lauraceae. Pp. 1-260 in A. de Can- Mexican/CentralAmerican and northernSouth Ameri- dolle (editor),Prodromus Systematis Naturalis Regni can lowlandand lowermontane vegetation during the Vegetablis.XV. SumptibusVictoris Masson et Fillil, Tertiary.Pp. 11-22 in S. Churchill,H. Balslev,E. For- Paris. ero & J. Luteyn(editors), Biodiversity and Conservation Merwe,J. van der,A. van Wyk& P. Kok. 1988. Dahl- of NeotropicalMontane Forests. The New YorkBotan- grenodendron,a remarkablenew genus of Lauraceae ical Garden,New York. fromNatal and Pondoland.S. Afr.J. Bot. 54: 80-88. Hallam,A. 1994. An Outlineof PhanerozoicBiogeogra- Mez, C. 1889. LauraceaeAmericanae. Jahrb. Konigl. Bot. phy.Oxford Univ. Press, New York. Gart.Berlin 5: 1-556. Hasegawa,M., H. Kishino& T. Yano. 1985. Datingthe Michaux,B. 1991. Distributionalpatterns and tectonic human-apesplitting by a molecularclock. J. Molec. developmentin :Wallace reinterpreted.Aus- Evol. 22: 160-174. tral.Syst. Bot. 4: 25-36. Heo, K. & H. Tobe. 1995. Embryologyand relationships Nees, C. 1836. SystemaLaurinarum. Sumtibus Veitii et of Gyrocarpusand Hernandia(Hernandiaceae). J. PI. Sociorum.Berlin. Res. 108: 327-341. Parrish,J. 1993. The paleogeographyof the opening , H. van der Werff& H. Tobe. 1998. Embryology SouthAtlantic. Pp. 8-27 in W. George& R. Lavocat and relationshipsof Lauraceae ().Bot. J. Linn. (editors),The Africa-SouthAmerica Connection. Clar- Soc. 126: 295-322. endonPress, Oxford. Herendeen,P., W. Crepet& K. Nixon. 1994. Fossil flow- Pax, F. 1889. Lauraceae. Pp. 106-126 in A. Engler& ers and pollenof Lauraceaefrom the Upper Cretaceous K. Prantl(editors), Die nattirlichenPflanzenfamilien. of New Jersey.PI. Syst.Evol. 189: 29-40. Vol. III. Engelmann,Leipzig. , S. Magallon-Puebla,R. Lupia, R. Crane & J. Pindell,J., S. Cande, W. Pitman,D. Rowley,J. Dewey,J.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions 134 Annals of the Missouri Botanical Garden

LaBrecque & W. Haxby. 1988. A plate-kinematic ular evolutionand phylogeneticimplications of internal frameworkfor models of Caribbeanevolution. Techno- transcribedspacer sequences of ribosomalDNA in physics155: 121-138. Winteraceae.Amer. J. Bot. 80: 1042-1055. Qiu, Y-L., J. Lee, F. Bernasconi-Quadroni,D. Soltis,P. Swofford,D. 1998. PAUP*: PhylogeneticAnalysis Using Soltis,M. Zanis, E. Zimmer,Z. Chen,V. Savolainen& Parsimony(and OtherMethods). Version 4.0b4. Illinois M. Chase. 1999. The earliestangiosperms: Evidence NaturalHistory Survey, Champaign, Illinois. frommitochondrial, plastid, and nucleargenomes. Na- Taberlet,P., L. Gielly,G. Pautou& J. Bouvet. 1991. Uni- ture402: 404-407. versalprimers for amplification of three non-coding re- Raven,P. & D. Axelrod.1974. Angiospermbiogeography gions of chloroplastDNA. P1. Molec. Biol. 17: 1105- and past continentalmovements. Ann. MissouriBot. 1109. Gard.61: 539-673. Taylor,D. 1988. Eocene floralevidence of Lauraceae: Reid, E. & M. Chandler.1933. The Flora ofthe London Corroborationof the North American megafossil record. Clay. BritishMuseum (Natural History), London. Amer.J. Bot. 75: 948-957. Renner,S. 1999. Circumscriptionand phylogenyof the Tiffney,B. 1985a. Perspectiveson the originof the flo- Laurales: Evidence frommolecular and morphological risticsimilarity between eastern Asia and easternNorth data. Amer.J. Bot. 89: 1301-1315. America.J. ArnoldArbor. 66: 243-273. & A. Chanderbali.2000. What is the relation- . 1985b. The Eocene NorthAtlantic land bridge: ship among Hernandiaceae,Lauraceae, and Monimi- Its importancein Tertiaryand modernphytogeography aceae, and whyis thisquestion so difficultto answer? of the NorthernHemisphere. J. ArnoldArbor. 66: 3- Int. J. P1. Sci. 161(Suppl.):S109-S119. 94. & K. Meyer.Melastomeae come fullcircle: Bio- Weber,J. 1981. A taxonomicrevision of Cassytha(Laur- geographicreconstruction and moleculardating. Evo- aceae) in Australia.J. Adelaide Bot. Gard.3: 187-262. lution(in press). Werff,H. van der. 1984. Noteson neotropicalLauraceae. Richter,H. 1981. Anatomiedes sekundarenXylems und Ann. MissouriBot. Gard. 71: 1180-1183. der Rinde der Lauraceae. Sonderb.Naturwiss. Vereins . 1988. Eightnew species and one new combi- Hamburg5: 1-148. nation of neotropicalLauraceae. Ann. MissouriBot. Rohwer,J. 1986. Prodromuseiner Monographie der Gat- Gard. 75: 402-419. tung Ocotea Aubl. (Lauraceae). Mitt.Inst. Allg. Bot. 1989. A newspecies ofPersea (Lauraceae)from Hamburg20: 3-278. Surinam,with a discussionof its positionwithin the . 1991. Borderlinecases betweenOcotea, Nectan- genus.Ann. MissouriBot. Gard. 76: 939-941. dra and Phoebe (Lauraceae): The marginalspecies of . 1991. A key to the generaof Lauraceae in the the Ocotea helicterifolia-group,including the 0. hey- New World.Ann. MissouriBot. Gard. 78: 377-387. deana-group.Bot. Jahrb.Syst. 112: 365-397. . 1996. Ocoteaikonyokpe, a new species ofOcotea . 1993a. Lauraceae. Pp. 426-437 in K. Kubitzki, fromCameroon. Novon 6: 460-462. J. Rohwer& V. Bittrich(editors), The Families and . 1997. Sextonia,a new genusof Lauraceae from Generaof FloweringPlants. Springer-Verlag, Berlin. SouthAmerica. Novon 7: 436-439. . 1993b. Nectandra.Fl. Neotrop.Monogr. 60: 1- . 1999. New taxa and combinationsin theOcotea 332. helicterifolia(Lauraceae) species group.Novon 9: 571- . 2000. Towardsa phylogeneticclassification of 583. the Lauraceae: Evidence frommatK sequences. Syst. . An annotatedkey to the generaof Lauraceae in Bot. 25: 60-71. the Flora Malesiana region.Blumea (in press). & K. Kubitzki. 1993. Ecological differentiation & H. G. Richter.1996. Towardan improvedclas- in Nectandra(Lauraceae) and its historicalimplica- sificationof Lauraceae. Ann. MissouriBot. Gard. 83: tions.Bot. Acta 106: 88-99. 409-418. , H. Richter& H. van der Werff.1991. Twonew White,T., T Birns,S. Lee & J. Taylor. 1990. Amplifi- generaof NeotropicalLauraceae and criticalremarks cationand directsequencing of fungalribosomal RNA on the genericdelimitation. Ann. MissouriBot. Gard. genes forphylogenetics. Pp. 315-332 in M. Innis,D. 78: 388-400. Gelfand,J. Sninsky& T White(editors), PCR Proto- Sang, T., D. Crawford& T. Stuessy. 1997. Chloroplast cols: A Guide to Methodsand Applications.Academic DNA phylogeny,reticulate evolution, and biogeography Press,San Diego. ofPaeonia (Paeoniaceae).Amer. J. Bot. 84: 1120-1136. Wolfe,J. 1975. Some aspects of plant geographyof the Sclater,J., S. Hellinger& C. Tapscott.1977. The paleo- NorthernHemisphere during the late Cretaceousand bathymetryof the AtlanticOcean fromthe Jurassicto Tertiary.Ann. MissouriBot. Gard.62: 264-279. the present.J. Geol. 85: 509-952. & E. Leopold. 1967. Neogeneand EarlyQuater- Scotese, C., L. Gahagan & R. Larsen. 1988. Plate tec- nary vegetationof northwesternNorth America and tonic reconstructionsof the Cretaceousand Cenozoic northeasternAsia. Pp. 193-206 in D. Hopkins(editor), ocean basins. Technophysics155: 27-48. The BeringLandbridge. Stanford Univ. Press, Stanford. Siddall, M. & M. Whiting.1999. Long-branchabstrac- Zhengyi,W. 1983. On the significanceof Pacificinter- tions.Cladistics 15: 9-24. continentaldiscontinuity. Ann. MissouriBot. Gard.70: Suh, Y., L. Thein,H. Reeve & E. Zimmer.1993. Molec- 577-590.

This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions