Missouri Botanical Garden Press

Phylogeny and Historical Biogeography of Lauraceae: Evidence from the Chloroplast and
Nuclear Genomes
Author(s): Andre S. Chanderbali, Henk van der Werff and Susanne S. Renner
Source: Annals of the Missouri Botanical Garden, Vol. 88, No. 1 (Winter, 2001), pp. 104-134
Published by: Missouri Botanical Garden Press
Stable URL: http://www.jstor.org/stable/2666133 .
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PHYLOGENY Andre'S. Chanderbali,2'3Henk van der
AND HISTORICAL 3 and Susanne S. Renner3
Werff,
BIOGEOGRAPHY OF
LAURACEAE: EVIDENCE
FROM THE CHLOROPLAST
AND NUCLEAR GENOMES1
ABSTRACT
Phylogenetic relationships among 122 species of Lauraceae representing44 of the 55 currentlyrecognized genera
are inferredfromsequence 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-Tethyeanmigrationwas relatively easy, and basal lineages are established on either Gondwanan
or Laurasian terrains by the Late Cretaceous. Most genera with Gondwanan histories place in Cryptocaryeae, but a
small group of South American genera, the Chlorocardium-Mezilauruls lade, represent a separate Gondwanan lineage.
Caryodaphnopsis and Neocinnamomum may be the only extant representatives of the ancient Lauraceae flora 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 Persea group, and cupuliferous
genera sort to Laureae of most classifications or Cinnamomeae sensu Kostermans. Laureae are Laurasian relicts in Asia.
The Persea group and Cinnamomum group (of Cinnamomeae) show tropical amphi-Pacific disjunctions here credited
to disruption of boreotropical ranges by Eocene-Oligocene climatic cooling. The Ocotea 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
representationprimarilyderived fromEarly Miocene radiation of the Ocotea complex upon reaching South America.
Key words: biogeography,boreotropical, chloroplast DNA, Gondwana, Lauraceae, Laurasia, Madrean-Tethyan,mo-
lecular clock, phylogeny,ribosomal DNA.
Lauraceae forma large familyof woodyplants prominent components of lowland forests and are
(except the herbaceous parasite Cassytha),with frequentlydominant elements in montane vegeta-
about50 generaand 2500 to 3000 species distrib- tion (Gentry,1988).
uted throughout tropicalto subtropicallatitudes. Given their antiquity, widespread distribution,
They are among the more speciose basal angio- and ecological prominence, Lauraceae provide a
spermfamiliesand have a fossilrecordthatreaches model system for investigatingangiosperm bioge-
back to the Mid-Cretaceous(Drinnanet al., 1990; ography. Moreover, the three tribes recognized by
Eklund & Kvacek, 1998). Currenttaxonomicdi- van der Werffand Richter (1996) suggest thatmajor
versityis centeredin tropicalAmericaand Aus- divisions in the familydraw along geographic lines.
tralasia,and althoughpoorlyrepresented in conti- Laureae include three genera with North Ameri-
nentalAfrica,Lauraceaeflourish in Madagascar.In can-Asian disjunctions (Litsea, Lindera, Sassafras),
the Americantropicsthey list among the most Mediterranean Laurus, and Asian endemics (e.g.,
I The authorsthankanonymous forinsightful

reviewers comments;K. Ueda foreightunpublishedtrnL-trnF sequenc-
es; J. Rohwerforsix unpublishedITS sequences; M. Zanis forfiveat the timeunpublishedITS/5.8S/26Ssequences;
Y-L. Qiu forproviding threeDNA aliquots;the HarvardHerbariaforproviding leafmaterialofEusideroxylon; Andrea
Schwarzbachforguidance in moleculartechniques;and innumerablecolleagues who helped to collect materialof
Lauraceae forthisstudy.This studywas undertaken as partof ASC's doctoraldissertationresearchat the University
ofMissouri-St. Louis,and was supportedbygrantsfromtheMallinckrodt Foundationadministered bytheInternational
CenterforTropicalEcology,University ofMissouri-St.
Louis,and fromtheSmithsonian Institution's
BiologicalDiversity
oftheGuianasProgramto ASC; NationalGeographicSocietygrants4631-91,5635-96,and 6571-99 to HW; and grants
fromthe University of Missourisystemand Universityof Missouri-St.Louis to SSR. This articleis Number45 in the
Smithsonian BiologicalDiversityofthe GuianasPublicationseries.
Institution's
2Department of Biology,University 8001 NaturalBridgeRoad, St. Louis, Missouri63121-
of Missouri-St.Louis,
4499, U.S.A.
3Missouri BotanicalGarden,P.O. Box 299, St. Louis, Missouri63166, U.S.A.
ANN. MISSOURI BOT. GARD. 88: 104-134. 2001.

Volume 88, Number1 Chanderbaliet al. 105
2001 Phylogenyand Biogeographyof Lauraceae
Actinodaphneand Neolitsea). Cryptocaryeaein- lowedthatPerseawas an "old Laurasiangenus"but

clude pantropicalBeilschmiediaand Cryptocarya, suggestedthatsubgenusEriodaphne,like all other
and other predominantly SouthernHemispheric membersof the family,arrivedin SouthAmerica
generawithnarrower ranges(e.g., Endiandra and via Africa.Alternatively, Taylor(1988) suggested
Potameia).Perseeae are centeredin theNeotropics that the fossil flowerAndroglandulatennessensis
withthreewidespreadgenera.Cinnamomum is dis- Taylor,fromthe Eocene ofNorthAmerica,is com-
junct between the American and Asian parable to Cinnamomum, Ocotea,and Nectandra,
(sub)tropics;Persea (includingMachilus) ranges indicatinga boreotropical historyforthisgroupof
throughout the Neotropics(into the southeastern genera,withsubsequentmigration to SouthAmer-
U.S.), theCanaryIslands,and Asia; and Ocoteahas ica. Raven and Axelrod(1974) and Taylor(1988)
about300 neotropicalspecies,one in Macaronesia, allowed thatalthoughdiffering in the directionof
a fewin Africa,and about30 morein Madagascar. migration, the highlevel of species diversityand
Apartfroma fewAsian genera(e.g.,Dehaasia and genericendemismrequirea Late Cretaceous-Early
Phoebe) consideredclosely relatedto Persea, all Tertiary arrivalin SouthAmerica.In contrast, Roh-
othergeneraof Perseeae are endemicto the Neo- wer and Kubitzki(1993) preferred a morerecent
tropics(e.g., Aiouea, Aniba, Endlicheria,Licaria, arrivalof this group,possiblyas late as the Plio-
Nectandra,Pleurothyrium, and Rhodostemonoda- cene closureof the PanamanianIsthmus,followed
phne).The distributions ofLaureae and Cryptocar- by rapidradiationin SouthAmerica.
yeae are consistent withLaurasianand Gondwanan These alternativeviews are here assessed by
histories,respectively, but thatof Perseeae is am- addinga temporaldimensionto a phylogenetic es-
biguous in this regard.The trans-Atlantic distri- timateforLauraceae reconstructed withmolecular
butionof OcoteasuggestsWestGondwananhistory, charactersretrievedfrombothchloroplastand nu-
but the tropicalamphi-Pacific distributionsofCin- clear genomes.
namomumand Persea suggestLaurasianaffinities.
Whetheror not these ambiguitiesare artifactsof MATERIALS AND METHODS
tribaland/orgenericcircumscription is unclear.
The systematics of Lauraceae is unsettled.Lau- TAXON AND MOLECULAR SAMPLING
reae are recognizedin mostpriorclassifications, A totalof 131 species, 122 representing 44 of
but othertribalconceptsare notwidelyaccepted. the 55 currently recognizedgeneraof Lauraceae,
Van der Werff and Richter's(1996) Cryptocaryeae and 9 representing 3 outgroupfamilies(Gomorte-
and Perseeae are revised concepts supportedby gaceae, Hernandiaceae,and Monimiaceae)werein-
Richter's(1981) studyof wood and bark anatomy. cluded in this study.Seventy-seven in-groupspe-
Some aspects of Cryptocaryeae gain supportfrom cies wereincludedin a broad-scalestudybased on
embryology (Heo et al., 1998), but charactersfor sequence variationin thetrnL-trnF andpsbA-trnH
further subdivisionofthefamilywerenotfound.A intergenicspacers of cpDNA. Guided by the find-
cladisticanalysisofmoleculardata (Rohwer,2000) ings of this molecularand taxonsamplinga two-
also providedsupportforCryptocaryeae and united tieredapproachwas adoptedto obtainbetterrep-
Perseeae and Laureae in a well-supported but un- resentationand phylogeneticresolutionat the
resolved lade. This Perseeae-Laureae lade ac- genericlevel. Thus a subsetof the species repre-
commodates mostofthefamily, and itsdistribution sentingbasal lineages in Lauraceae was also se-
implies a disjunctionbetweenthe Americanand quenced forthetrnT-trnL spacer,and therpll6 in-
Asian tropicswitha minorAfricanpresence.Such tronofcpDNA, as well as the5' end of26S rDNA,
distributions can be creditedto extinction ofGond- while 94 species representing Perseeae, Laureae,
wanan lineages in Africa(e.g., Raven & Axelrod, and theirsistergroupwere sampled forthe ITS/
1974), butLaurasianancestry followedbyradiation 5.8S regionof nrDNA.Table 1 providesGenBank
in tropicalAsia and Americawas favoredby Roh- information forall accessions.
wer(2000). TropicalAsia is acknowledged as a har-
bor forLaurasian relicts(e.g., Wolfe,1975), but DNA EXTRACTION, PCR AMPLIFICATION, AND
Rohwer'shypothesisthat the approximately 800 SEQUENCING
neotropicalspecies of Perseeae are derivedfrom
Laurasianimmigrants contrastswiththeGondwan- Total DNA was obtainedfromsilica-gel-dried,
an origincreditedto mostmajorneotropicalplant herbarium, orfreshleaves usingDneasy(QIAGEN)
groups(e.g.,Raven& Axelrod,1974; Gentry, 1982; extractionkits. PCR amplification of chloroplast
references in 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%

Table 1. Sources of plantmaterial.'Previouslysubmitted
to Genbank.Contributed
by: 2J. Rohwer,Univ.Hamburg;3K. Ueda
Univ.
Genbanka
Taxon Provenance Voucher trnL-trnF psbA-trnH trnT-tr
Lauraceae
Actinodaphne sesquipedalis Malaysia,Kuala Lumpur Saw Leng Guan s.n. (KEP) AF268695 AF268787 -
Meisn.
Adenodaphne uniflora(Guill.) New Caledonia,Province van der Werif
15895 (MO) -
Kosterm. du Sud
Aiouea costaricensis
(Mez) Kos- Costa Rica, Heredia Grayum8241 (HBG) (J. - - -
term. Rohwersequence)
Aiouea dubia (HBK) Mez Ecuador,Loja Madsen 75433 (AAU) (J.
Rohwersequence)
AioueaguianensisAubl. Guyana,Demerara,Timer- Taylor12085 (MO) AF268696 AF268780 -
hi
Alseodaphnesemecarpifolia Sri Lanka,CentralProv, Malcomber 2753 (MO) AF268697 AF268799 -
Nees Kandy
AnaueriabrasiliensisKosterm. Peru,Loreto,Iquitos Vdsquez25228 (MO) AF268698 AF268800 AF268840
Anibacinnamomifora C. K. Al- Venezuela,Trujillo,Bo- Cuello955 (MO) AF268700 AF268770 AF268823
len con6
AnibaexcelsaKosterm. Guyana,Demerara,Mabu- Chanderbali226 (MO) - - -
ra Hill
AnibahypoglaucaSandwith Guyana,Essequibo,Iwok- Chanderbali165 (MO) AF268699 AF268771 AF268822
ramaReserve
Anibapanurensis(Meisn.)Mez Guyana,Essequibo,Iwok- Chanderbali248 (MO)
ramaReserve
Apolloniasbarbulana(Cav.) CanaryIslands,Tenerife Bramwell628 (MO) - - -
Bornm.
Aspidostemonsp. Madagascar,Toliara van der Werff
12737 (MO) AF268701 AF268819 AF268843
BeilschmiediabrenesiiC. K. Al- Costa Rica, Puntarenas Yasuda1310 (MO) AF268702 AF268809
len
BeilschmiediamadagascariensisMadagascar,Toliara Lowry5015 (MO) AF268810
Kosterm.
Beilschmiediaovalis(Blake) C. Costa Rica, San Jose Yasuda 1301 (MO) AF268703 AF268811
K. Allen
BeilschmiediasaryKosterm. Madagascar,Toamasina van der Werif 12800 (MO) - AF268812

Table 1. Continued.
Genbanka
tilaranensis
Beilschmiedia Nish- Costa Rica, Guanacaste Yasuda1313 (MO) AF1290141 AF1290451 AF129015
ida
velutina(Kos-
Beilschmiedia Madagascar,Antsiranana Georges361 (MO) AF268704 AF268813 --
term.)Kosterm.
Caryodaphnopsisbilocellatavan Vietnam,NinhBinh van der Werif
14195 (MO) AF230321 AF2619951 AF233603
der Werff
Caryodaphnopsistomentosa van Peru,Loreto,Iquitos Vdsquez25239 (MO) AF268705 AF268807 AF268842
der Werff
L.
Cassythafiliformis Guyana,Rupununi,Kar- Chanderbali205 (MO) AF2320341 AF2619961 AF233605
anambo
CassythapubescensR. Br. Australia,Victoria,Gee- Foreman1913 (MEL) AF2320331 AF233604
long
Chlorocardium rodiei(R. H. Guyana,Demerara,Mabu- Chanderbali246 (MO) AF268706 AF268802
Schomb.)Rohwer,H. G. ra Hill
Richt.& van der Werff
Chlorocardium venenosum (Kos- Peru,Loreto,Iquitos Vdsquez25236 (MO) AF268707 AF268801 AF268840
term.& Pinkley.)Rohwer,H.
G. Richt.& van der Werff
Cinnamomum camphora(L.) MissouriBG Chanderbali322 (MO) AF1290203 AF1290481 AF129021
Presl.
Cinnamomum chavarrinum Costa Rica s.n. (J.
Gomez-Laurito - - -
(Hammel)Kosterm. Rohwersequence)
Cinnamomum cinnamomifolium Ecuador Thomsen8942 (AAU) (J. - - -
(HBK) Kosterm. Rohwersequence)
Cinnamomum japonicumSie- Japan,Honshu,Kyoto Yasuda1351 (MO) AF2687083 AF268782 -
bold
Cinnamomum oleifolium (Mez) Brazil,Minas Gerais Lorea-Hernandez5582
Kosterm. (MO)
Cinnamomum quadrangulum Brazil,Minas Gerais Lorea-Hernandez5585 - AF268781 -
(Meisn.)Kosterm. (MO)
Cinnamomum sp. Vietnam,Lao Cai van der Werff
14396 (MO) - AF268783 -
Cinnamomum verumPresl. India,Kumbhave,Dapoli Godbole45108 (MO) AF268709 AF268784 -
Cryptocaryachinensis(Hance) Asia K. Ueda sequence AF26871O3
1D - -
Hemsl.

Table 1. Continued.0
Genbanka
Cryptocaryarhodosperma Hy- Australia,Queensland Gray7556 (QRS) AF268711 AF268817 --AF27047
land
CryptocaryascierophyllaHyland BrisbaneCityBotanic Schwarzbach s~n.(voucher AF268712 AF268818 ----
Garden destroyed)
Cryptocaryathouvenotii Madagascar,Toliara van der Werif12723 (MO) AF232035' AF261997' AF23360
(Danguy)Kosterm.
Dehaasia incrassata(Jack)Kos- Philippines,Palawan,Tay- Soelarto7693 (MO) -----AF272268
term. tay
Dicypelliumcaryophyllaceum Brazil,Para Pires16756 (HBG) -----AF272269
(Mart.)Nees
DicypelliummanausenseW. Brazil,Amazonas,Manaus Assun~yio 749 (INPA) AF268713 AF268775 AF26883
Rodr.
Endiandramicroneura C. White Australia,Queensland Schulmans~n.(QRS) AF268714 AF268814 --AF27047
EndlicheriachaliseaChander- Guyana,Essequibo,Iwok- Chanderbali252 (MO) AF268715 AF268756 AF26882
bali ramaReserve
Endlicheriacitriodoravan der Peru,Loreto,Iquitos Vasquez25231 (MO) AF268716 AF268757 ---AF27227
Werif
Endlicheriapunctulata(Mez) C. FrenchGuiana,Tumac de Granville1448 (MO) -----AF272273
K. Allen Humac
Endlicheriareflectens
(Nees) Guyana,Essequibo,Rupu- Chanderbali208 (MO) AF268717 AF268758 AF26882
Mez nuni
Gen. & sp. nov.aff.Mezilaurus Peru,Loreto,Iquitos Vdsquez25230 (MO) AF268719 AF268803 AF26883
EusideroxylonzwageriTe- Borneo,Kalimantan Laman 1275 (HUH) AF268718 AF268820 -AF268252
ijsmann& Binnendijka
Hypodaphnis zenkeri(Engl.) Gabon,Ogooue-Ivindo, McPherson16184 (MO) AF232036' AF261998' AF23360
Stapf Lop&6Okanda
Iteadaphnesp. Vietnam,Lao Cai van der Werif
14360 (MO) AF268720 AF268786 AF26883
Kubitzkiamezii(Kosterm.)van Guyana,Essequibo,Iwok- Chanderbali249 (MO) AF268721 AF268772 --AF27047
der Werff rama
LaurusnobilisL. MissouriBG Chanderbali327 (MO) AF268722 AF268785 AF26883
Licaria cannella(Meisn.)Kos- Guyana,Demerara,Mabu- Chanderbali234 (MO) AF268723 AF268773 ---AF27228
term. ra Hill
LicariaguianensisAubl. Brazil,Amazonas,Manaus Vicentini
1238 (MO) -----AF272281

Table 1. Continued.
Genbanka
Licaria martiniana(Mez) Kos- Guyana,Essequibo,Iwok- Chanderbali264 (MO) - - -
term. ramaReserve
Licaria triandra(Sw.) Kosterm. FairchildTropicalGarden, Qiu 90019 (NCU) AF268724 AF268774 -
Fl., U.S.A.
Linderabenzoin(L.) Blume MissouriBG Chanderbali324 (MO) AF2687253 AF268788 AF268833
Linderaerythrocarpa Makino Japan,Honshu,Kyoto Yasuda 1353 (MO) AF2687263-
LinderaumbellataThunb. Japan,Honshu,Kyoto Yasuda 1354 (MO) AF2687273 AF268789 -
LitseacoreanaLeveille Japan,Honshu,Kyoto Yasuda 1356 (MO) AF2687283 AF268791
cf.Litseaelongata(Nees) China,Yunnan,Kunming Hyland14912 (MO)
Benth.& Hook. f. (Distribut- BG
ed to MO as Phoebeforrestii
W. W. Sm.)
LitseaglaucescensHBK Mexico,Guerrero, Chichi- Lorea-l:ernandez
5496 AF1290351 AF1290631 AF129036
hualco (MO)
Mezilaurustriuncavan der Peru,Amazonas,Iquitos Vdsquez25227 (MO) AF268729 AF268804 AF268837
Werff
Mocinnodaphne cinnamomoideaMexico,Guerrero, El Mol- Lorea-Hernandez5536
Lorea-Hern. ste (MO)
Nectandraarnazonum Nees Guyana,Essequibo,Iwok- Chanderbali217 (MO) - - -
ramaReserve
Nectandracoriacea(Sw.) Gri- U.S.A. Florida,Monroe Prinzie125 (MO) - - -
seb. County
NectandracuspidataNees & Guyana,Essequibo,Ka- Chanderbali279 (MO) - -
Mart. marang
Nectandramembranacea (Sw.) Brazil,Sao Paulo, Serra Lorea-Hernandez 5596 AF268730 AF268767 AF268825
Griseb. do Mar (MO)
NectandrapsammophilaNees Brazil,Sao Paulo, Serra Lorea-Hernandez 5595 - - -
& C. Mart. do Mar (MO)
Nectandrapurpurea(Ruiz & Peru,Cajamarca,San Ig- Camposet al. 3165 (MO)
Pav.) Mez nacio
Nectandrasalicifolia(HBK) Costa Rica Gomez-Lauritosn. (J - - -
Nees Rohwersequence)
Nectandraturbacensis (HBK) PuertoRico, Rio Grande, Taylor11746 (MO) AF0124001 AF268768 AF268826
Nees El Verde

Table 1. Continued.
Genbanka
Neocinnamomum mekongense China,Yunnan Li Heng 8547 (MO) AF268731 AF268806 AF26884
(Hand.-Mazz)Kosterm.
Neolitseasericea(Blume)Koidz. Japan,Honshu,Kyoto Yasuda1355 (MO) AF2687323 AF268792 -
Ocoteabotrantha Rohwer U. C. Riverside Scora 99-1 (UCR) AF268733 AF268776 -
Ocoteabullata(Burchell)E. SouthAfrica,Natal,Sky- Abbot6208 (MO) AF268734 AF267778 -
Mey. line Arboretum
Ocoteaceanothifolia (Nees) Mez Guyana,Demerara,Mabu- Chanderbali244 (MO) - - -
ra Hill
Ocoteafoetens(Aiton)Baill. Madeira,PortoMoniz Maas 8642 (MO) AF268735 - -
Ocoteagrayivan der Werff Madagascar,Toliara van der Werff12732 (MO) AF268736
OcoteaguianensisAubl. Guyana,Demerara,Mabu- Chanderbali232 (MO) AF268737 AF268762 -
ra Hill
Ocoteahelicterifolia(Meisn.) Mexico,Oaxaca, Miahu- Torres11911 (MO) - -
Hemsl. atlan
Ocoteaheydeana(Mez & Donn. Honduras,Yoro,Pico Pijol Evans 1760 (MO) - - -
Sm.) Bernardi
Ocoteaikonyokpe van der WerffCameroon,SW Prov., Thomas10456 (MO) - - -
RumpiHills
Ocoteainsularis(Meisn.)Mez Costa Rica, Puntarenas, Rojas 3682 (MO) - - -
Coco Is
Ocotealeucoxylon (Sw.) Laness. PuertoRico, San Jose Taylor11733 (MO) AF123991 AF268763
Ocoteamalcomberi van der Madagascar,Toliara van der Werff12756 (MO) AF268779
Werff
OcoteanigraBenoist Guyana,Essequibo,Iwok- Chanderbali162 (MO) - - -
ramaReserve
Ocoteaodorifera (Vell.)Rohwer Brazil,Minas Gerais, Lorea-Hernandez 5578 AF268738 AF268762
Parque Ecol. CEMIG (MO)
Ocoteapaucifiora(Nees) Mez Guyana,Demerara,Mabu- Chanderbali219 (MO) - AF268764
ra Hill
Ocoteapercoriacea(Mez) Kos- Brazil,Goias, Fazenda Lorea-Hernandez 5584 AF268739 -
term. Galheiro (MO)

OcoteapulchellaMart. Brazil,Minas Gerais,Fa- Lorea-Hernandez 5575 AF268740
zenda Caiera (MO)

Table 1. Continued.
Genbanka
Ocoteaquixos(Lam.) Kosterm. Ecuador,Napo,JatunSa- Neill 9487 (MO) AF2320371 AF261999' AF23360
cha
Ocotearhynchophylla (Meisn.) Guyana,Demerara,Mabu- Chanderbali220 (MO) - AF268766 -
Mez ra Hill
Ocoteaschomburgkiana (Nees) Guyana,Essequibo,Iwok- Chanderbali286 (MO) - -
Mez ramaReserve
Ocoteaspixiana(Nees) Mez Brazil,Minas Gerais, Lorea-Hernandez5574 -
Parque Ecol. Tripui (MO)
Ocoteatomentella Sandwith Guyana,Essequibo,Ka- Chanderbali284 (MO) AF268741 AF268765
marang
Ocoteatristis
(Nees & Mart.) Brazil,Minas Gerais, Lorea-Hernandez5577 AF268742 -
Mez Parque Ecol. CEMIG (MO)
Ocoteaveraguensis (Meisn.) Nicaragua,Chontales Stevens24177 (MO) -
Mez
Paraia bracteataRohwer,H. G. Brazil,Amazonas,Iquitos Vicentini
1288 (MO) AF268743 - -
Richt.& van der Werff
Parasassafrasconfertiflora China,Yunnan,LishuiCo. Li Heng 10030 (MO) - AF268790 -
(Meisn.)Long
PerseaamericanaMill. MissouriBG Chanderbali323 (MO) AF268744 AF268794 -
Perseacaerulea(Ruiz & Pav.) Peru,Amazonas van der Werff
14744 (MO) - AF268795 -
Mez
Persealingue(Ruiz & Pav.) Chile Greissl640-99 (MJG) - AF268796
Nees ex Kopp
Perseameridensis
Kopp Venezuela,Trujillo,Bo- Cuello943 (MO) AF268745 AF267797 AF26883
con6
Persea sp. Vietnam,VinhPhuc van der Werff
14071 (MO) - - -
Siebold&
Perseathunbergii MissouriBG Chanderbali328 (MO) AF268746 AF268798
Zucc.
Phoebeformosana(Hayata) BonnBG Rohwer156 (MJG) - - -
Hayata (J.Rohwersequence)
cinereum
Pleurothyrium van der Peru,San Martin,Riojas van der Werff
15325 (MO) AF268747 AF268769 -
Werff
insignevan der Ecuador,Napo,JatunSa-
Pleurothyrium Neill 9033 (MO) - -
Werff cha

Table 1. Continued.
Genbanka
Potameiamicrantha van der Madagascar,Toamasina van der Werif 12777 (MO) AF268749 AF268815 -
Werff
Potameiamicrophylla Kosterm. Madagascar,Fianarantsoa van der Werif 12655 (MO) AF268750 AF268816 -
Potoxylon melagangai(Syming-Brunei,Tutong,Kampong Hyland14969 (MO) AF268748 AF268821
ton)Kosterm. Lamumin
Rhodostemonodaphne Guyana,Essequibo,Iwok- Chanderbali265 (MO) AF268751 AF268759
crenaticupula Madrifian ramaReserve
Rhodostemonodaphne praeclara Guyana,Essequibo,Iwok- Chanderbali256 (MO) AF268752 AF268760 AF26882
(Sandwith)Madrinian ramaReserve
Rhodostemonodaphne recurva Brazil,Amazonas,Manaus Vicentini 653 (MO) - - -
van der Werff
Rhodostemonodaphne scandens Guyana,Essequibo,Iwok- Chanderbali271 (MO) - - -
Madrinian ramaReserve
Sassafrasalbidum(Nutt.)Nees MissouriBG Chanderbali325 (MO) AF268753 AF268793 AF268832
Sassafrastzumu(Hemsl.)Hemsl China,Hunan,XiningCo. Luo Lin-bo1242 (MO) - - -
Sextoniapubescensvan der Peru,Loreto,Iquitos Vdsquez25229 (MO) AF2320381 AF2620001 AF233609
Werff
Sextoniarubra(Mez) van der Brazil,Amazonas,Manaus Nascimento 574 (MO) AF268754 AF268805 -
Werff
Umbellularia californica(Hook. MissouriBG Chanderbali326 (MO) AF268755 AF268777 -
& Am.) Nutt.
Urbanodendron bahiense Brazil,Rio de Janeiro Martinelli10019 (MO) -
(Meisn.)Rohwer
Urbanodendron verrucosum Brazil,Minas Gerais,Faz. Braga s.n. (BHCB) 19385 - - -
(Nees) Mez Maced6nea (MO)
Gomortegaceae
nitidaRuiz and Pav. Chile
Gomortega Rodriguez3070 (CONC) AF0124041 AF1290531 -
Hernandiaceae
americanusJacq.
Gyrocarpus Sri Lanka,ColomboBG Chase 317 (NCU) AF0123981 AF1290541 AF129025
Hernandiamoerenhoutiana Australia,Brisbane,Mt. notavailable AF0521981 AF1290551 AF129026
Guillem. CoothaBG

DMSO was added and the PCR protocoldescribed

by Kuzoffet al. (1998) was followed.The trnL-trnF
and trnT-trnL regionswereamplified usingprimers
designedby Taberletet al. (1991). The trnL-trnF
spacersequencesbeginnearthe5' end ofthespac-
e er and include 138 bp ofthe 5' end ofthe tRNA-
Co _
Phe (trnF)gene. The spacer betweentRNA-Leu
(trnL)and tRNA-Thr(trnT)alignsreadilywithoth-
er lauraleantrnT-trnL sequencesproducedbyRen-
ner (1999), but is difficult to align withthe few
available trnT-trnL sequences in GenBank, the
=k z z z
mostsimilarofwhichare trnT-trnL sequencesfrom
z z
Dioscorea (48% similarity). The psbA-trnHspacer
Z ? ?
and rpll6 intronwere amplifiedusing primersof
F-0 ?
d
Sang et al. (1997) and Asmussen(1999), respec-
r
c t co
CS C) c tively.The psbA-trnH sequencesobtainedforLaur-
aceae includethe entirespacerregionand overlap
'e ; ocec c: coc c by about40 base pairswiththe3' end ofthepsbA
= AN N N~~'I
N
gene and 5' end of the trnHgene of Helianthus
0 N 't
annuusL. depositedin Genbank(X60428). The 5'

regionthatincludesthefirst twoexpansiondomains
=- Cfo O o:1
of26S rDNA was amplifiedusinga forward primer
(D. Nickrent,pers. comm.)thatanneals at ca. 70
nucleotidepositionsdownstream fromthe5' end of
the gene and the 641 R reverseprimerof Kuzoff
et al. (1998). To increaseefficiency ofPCR ampli-
Cd ficationof ITS, the fewlauraceoussequences ob-
tainedusingangiosperm-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 downstream of 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 theirsistergroup.In mostcases itwas
possible to amplifythe entireITS regionusing
LAUR 1 and ITS B, butforsomepoor-quality tem-
platesitwas necessaryto amplify theregionin sec-
tions(ITS1 & ITS2) by combiningthe appropriate
universalprimersofWhiteet al. (1990) withLAUR
1 and ITS B. The ITS/5.8S sequences produced
includeall butthefirstca. 10 bp ofITS 1 and the
0C> g entireITS 2 and 5.8S regions.Rarely,onlyITS 1
or ITS 2 was obtained.
PCR productswere purifiedfollowingthe pro-
20 iE
tocol providedby QlAquick gel extractionkits
(QIAGEN) and sequencedusingthedyeterminator
cycle sequencing protocol(Applied Biosystems).
Sequence reactionswere analyzedon ABI 373 or
ABI 377 automatedsequencers(University ofMis-
souri-Columbia DNA CoreSequencingFacilityand
Universityof Missouri-St.Louis D. E. Lee and
FamilySequencingFacility).ExceptforthepsbA-
trnHregion,whichcould onlybe sequenced from
the 5' end, both strandsof DNA were read and

114 Annals of the
Missouri Botanical Garden
consensussequences generatedusing Sequencher werecalculatedforthe ITS data set usinglog de-

vers. 3.1 (Gene Codes Corp., 1998). Sequences terminant (LogDet) and maximumlikelihoodesti-
weremanuallyalignedusingthe 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) modelwithrateheterogeneity
alignmentwas relativelystraightforward in Laura- amongsites (HKY-F).
ceae. However,the first290 bp of the trnT-trnL
spacer were removedfromanalysis because of MOLECULAR CLOCK ANALYSES
alignmentdifficulties amongbasal Lauraceae and In orderto add a temporaldimensionto thephy-
outgroupfamilies.Alignmentdifficulties withthe logenetic estimate,divergencetimes for major
outgroupwere also encounteredin the 3' half of brancheswereestimated.Due to thecomputational
the psbA-trnHspacer. However,unlike trnT-trnL demandsof maximumlikelihoodcalculationsand
sequences,psbA-trnH providedseveralinformative because it was notnecessaryto obtaindivergence
characterswithinLauraceae and insteadofremov- timesforall nodes,likelihoodscoreswereobtained
ing it entirely,outgroupsequences weretruncated fromparsimony-based topologiesthatwerereduced
afteralignmentbecame 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
Initialanalysesof the individualdata sets were heterogeneity among sites, and values obtained
conductedas heuristicsearchesformostparsimo- withand withouta clock
constraint comparedfor
nious trees with 10 randomtaxon additionsand significance usinga x2 test[X2 2(log LClCk - log
TBR branchswappingusingPAUP* version4.0b4 Ltook); d.f. = numberof taxa -2]. For each in-
(Swofford, 1998). Both the MULPARS and COL- ternalnode,HKY-F distances(branchlengths)to
LAPSE optionswerein effect,but the STEEPEST the tip were computedby PAUP* withthe clock
DESCENT optionwas not employed.Characters constraintenforced.These values representthe
were assumed to be unordered(i.e., Fitch parsi- numberofsubstitutions per siteaccumulatedalong
mony),equallyweighted,and gaps weretreatedas each daughterlineage,and wereeitherdividedby
missingdata. Parsimonyuninformative characters timeto determinesubstitution rates,or dividedby
were excluded. Bootstrapanalyses (Felsenstein, estimatedratesto obtaindivergencetimes.Overlap
1985) with500 replicationswere performed with in taxonsamplebetweenterminaland basal topol-
theabove heuristicsearchsettingsbutwithMAX- ogies alloweduse ofdivergencetimesestimatedin
TREES set to 100. Since these initial searches one to calibratesubstitution ratesand calculatedi-
showedno stronglysupportedconflict,i.e., alter- vergencetimesin theother.Standarddeviationsof
nativeclades supportedby> 70% bootstrap values divergencetimeswere estimatedas follows.First,
(Hillis & Bull, 1993), and P-valuesfrompartition- standarddeviationsof HKY-r distanceswerecal-
homogeneity testsrangedfrom1.0 to 0.6 (strongly culatedusinga formuladerivedfromthe relation-
indicatingcongruence),threematriceswere com- ship S = Np, whereS is the numberofnucleotide
piled forfurther analyses. MatrixI combined86 substitutions, N is the totalnumberof nucleotide
species thatweresequenced forthe trnL-trnF and positionsin a sequence,and p is theproportion of
psbA-trnHregions.MatrixII combinedtrnL-trnF,nucleotidessubstituted (HKY-r distancefromnode
psbA-trnH, trnT-trnL, rp116,and 26S sequencesfor to branchtips). Since the standarddeviationof S
42 taxa representing majorlineages identifiedby is the square root of Np(l - p), or SD(S) =
analysesofmatrixI to further basal re- sqrt(Np[l - p]), the standarddeviationof p is
investigate
lationships.MatrixIII included94 ITS sequences SD(S) dividedby N, or SD(p) =
sqrt(p[l - p]/N).
fromrepresentatives of a largeterminallade that This value is calculatedforeach divergenceofin-
was poorlyresolvedbysequencevariationin matrix terestand dividedby substitution rateto obtainthe
I. The onlymutationin matrixI thatprovidedge- standarddeviationof divergencetimes.
neric-levelinformation in thisterminallade, a 16-
bp repeatin trnL-trnF, was includedin matrixIII. RESULTS
Analysesof all threematriceswere conductedas
above withlengthmutations(insertionsand dele- PHYLOGENETIC ANALYSES
tions) introducedas binarycharactersof equal Sequence variationin chloroplastmarkersand
weight.In addition,minimumevolutiontopologies partial26S sequences was almostlimitedto basal

Volume88, Number1 Chanderbali
et al. 115
2001 Phylogeny
and Biogeography
ofLauraceae
Table 2. Characteristics
and comparisonsofphylogenetic informationprovidedby matricesanalyzedin thisstudy.
MatrixI combinestrnL-trnFand psbA-trnHcpDNA sequences, MatrixII combinestrnL-trnF, psbA-trnH,
trnT-trnL,
and rpll6 ofcpDNA with26S rDNA sequences; MatrixIII is based on ITS rDNA sequences.
Parsimony-informative
Numberofrepresentatives
of: substitutions
among:
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 withverylittleand oftenno lade is essentiallyunresolvedbut thereis some

variationamongmembersof tribesPerseeae and supportfor a lade includingrepresentatives of
Laureae (sensu van der Werff& Richter,1996). Persea and Alseodaphne,a large genericcomplex
The trnL-trnF matrixincluded 510 aligned posi- centeredaroundOcotea,and strongsupportfora
tions and yielded 103 informative substitutions lade includingall Asian membersof Cinnamo-
withinLauraceae,but onlyseven ofthesewerein- mum.Furthermore, a lade unitingmostneotropi-
formative amongPerseeae and Laureae. Similarly, cal genera(Aniba,Endlicheria,Kubitzkia,Licaria,
of 616 alignedpositionsin thepsbA-trnHmatrix, Nectandra,Pleurothyrium, and Rhodostemonoda-
135 substitutionswereparsimony informativewith- phne) withneotropical(but notpaleotropical)spe-
in Lauraceae and 35 amongPerseeae and Laureae. cies of Ocotea and CalifornianUmbellulariais re-
This trendwas also foundin otherchloroplastloci covered in all trees but does not receive strong
and partial26S sequences. OnlyITS showedsub- support.All membersofthis lade, except0. leu-
stantial variationwithinPerseeae and Laureae. coxylon(Sw.) Laness., have the 16-bp repeatmen-
Characteristics of individualgeneticmarkersand tionedabove. Caryodaphnopsis, Cassytha,and Neo-
combineddata sets are summarizedin Table 2. cinnamomum a lade in all treesbutthis
constitute
CombinedtrnL-trnF and psbA-trnHmatrix(ma- associationdoes notreceivemorethan50% boot-
trixI) included 1126 aligned positionsof which strapsupport,and neitherdoes its positionas the
277 were informative. Four indels fromtrnL-trnF sistergroupofthesecondmajorinfrafamilial group.
were added as binarycharacters.Three of these MatrixII included3304 characters, ofwhich684
supporteda lade comprisedof Beilschmiedia, were parsimony-informative substitutionsand 7
Cryptocarya, Endiandra, and Potameia, and the were binary-codedlength mutations.Parsimony
fourthis a 16-base pair repeat foundin several analysisconvergedon a singleislandof2646 equal
neotropicalgeneraofPerseeae and Umbellularia of lengthtrees(L = 2171, CI = 0.71, RI = 0.72),
Laureae. ParsimonyanalysesofmatrixI surpassed the majorityrule consensusof whichis shownin
memorylimitationsin the firstadditionreplicate, Figure 2. The topologyis mostlycongruentwith
and 29,000 equally parsimonioustopologieswere thatprovidedby matrixI, differing mainlyin that
retainedafter24 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) showstwowell-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), withHypodaphnistenuouslyplaced as its (98%) bootstrapsupport,and relationships within
sistergroup.The second major lade is unequally the Chlorocardium-Mezilaurus lade are altered
dividedintoa small lade ofSouthAmericangen- slightly.
era (hereafterChlorocardium-Mezilaurus clade) MatrixIII, based mainlyon ITS sequences,in-
and a large terminallade comprisedofrepresen- cluded 259 parsimony-informative substitutions
tativesof Laureae and Perseeae (sensu van der and 19 lengthmutationsthatcould be unambigu-
Werff& Richter,1996). This Perseeae-Laureae ouslycoded. Parsimonyanalysisfounda singleis-

116 Annals of the
MissouriBotanical Garden
77 Endlicheriachalisea
53 Rhodostemonodaphnecrenaticupula
Matrix I Rhodostemonodaphne
Endlicherla
praeclara
citrioddra
TrnL-trnF
trnL-trnF 58 Endlicheriareflectens
58 Ocotea auianensis
psbA-trnH cpDNA Ocotea puldhella

Ocotea tristis
Ocotea odorifera
Ocoteatomentella Ocotea complex

l 97 Aniba cinnamomiflora
Aniba
hypoglauca
54 Kubitzkiamezii
Licaria cannella
Licaria triandra
Ocotea quixos
Paraia bracteata
Nectandramembranacea
Nectandraturbacensis
Pleurothyrium cinereum
Ocotea botrantha
Umbellulariacalifornica Perseeae
Ocotea bullataLare
Ocotea grayi Laureae
Aiouea guianensis clade
Cinnamomumquadrangulum
Cinnamomumcamphora
92 Cinnamomumrjaponicum Asian
100 Cinnamomumpv.rum Cinnamomum
Laurus nobilis
Iteadaphne sp.
Actinodaphnesequipedalis
Litsea coreana
Linderaumbellata Laureae
Linderaerythrocarpa
100 * Litsea glaucescens
Neolitsea sericea
Sassafras albidum
Persea thunbergii
57 Persea amenicana
Persea lingue Persea group
74 Persea meridensis
Persea caerulea
Alseodaphne semecarpifolia
Anauena brasiliensis
_ 99 Chlorocardiumvenenosum
66 Chlorocardiumrodiei Chlorocardium
10 1Gen. & sp.nov.,aff.Mezilaurus
0 Mezilaurus
Sextoniapubescens clade
Sextonia rubra
Neocinnamomummekongense
Neocinnamomum
Cassytha pubescens Cassytha
100 Caryodaphnopsisbilocellata
Caryodaphnopsistomentosa Caryodaphnopsis
78 Beifschmiedijbrenesii
91 Bellschmiediaovalis
Bellschmiediatilaranensis
Beilschmiediasary
93 Endiandramicroneura
90 micrantha
Potameia Cryptocaryeae
Potameia
microphylla
77 _97 madagascariensis sensu
Beilschmiedia
Bellschmiedia
velutina vander Werff
62
90
~~~
~~~~~~~87 chinensis
Cryptocarya
scierophylla
Cryptocarya andRichter
98 Cryptocaryathouvenotil
Cryptocaryarhodosperma
53 1 Aspidostemon sp.
100 Eusideroxylonzwageri
Potoxylonmelagangai
100 I Hypodaphnis zenkeri
_ rocarpus amencanus
moerenhoutiana
nemandia
wonotoboense
Sparattanthelium
luzonensis
Illigera
95 . Hortoniafloribunda
7070 * I 100.U- Monimiaovalis Outgroups
Palmeriascandens O
Peumus boldus
Gomortega nitida
Figure 1. Strict consensus of 29,000 trees retained fromparsimony analysis of matrix I (trnL-trnFand psbA-trnH
cpDNA sequences). Numbers above branches indicate bootstrapsupport. The vertical bar throughthe branch supporting
the terminal clade indicates a 16-bp repeat in the trnL-trnFintergenic spacer that unites taxa therein.

76 76 Ocotea MA IOcotea complex a)

MatrIx
Matrix___ 76 grayi
Laurusnobilis ME I Laureae a, a -o
trnL-trnF 100 { Persea thunbergii
AS I " C
psbA-trnH Persea americanaCA |Persea group 0-
trnT-trnL 100 AnaueriabrasiliensisSA

rpll 6 cpDNA
rp116 cpDNA 100
100 ~~~~~100
88 100 Chlorocardium
rodieiSA Leaves E
26S rDNA 100 Chlorocardium
venenosum
SA opposite
96 1 Gen. & sp. nov.,aff.MezilaurusSA 3 c
7;
60 100 93 MezilaurustriuncaSA Leaves O
100 100 tSextoniapubescensSA terminally
clustered (.
95 SextoniarubraSA
980 100 CaryodaphnopsisbiocellataAS E

100 CaryodaphnopsistomentosaSA I Evergreen
CZ Cn-
100 SA
Cassythafilformis | Parasitic m 0
100 1 CassythapubescensAU | U)
Neocinnamomum
mekongenseAS I Evergreen o
Aspidostemonsp. MA I Deep cupules
72 BeilschmiediabrenesfiCA
810 56Beilschmiedia saryMA
81 ~~~~~~56
100 BeilschmiediavelutinaMA
98 54 BellschmiediamadagascariensisMA
64 100 EndiandramicroneuraAU Non-cupulate
90 U)
100 BeilschmiediaovalisCA CZ
58 BeilschmiediatilaranensisCA
100 100 Potameiamicrantha

MA 0
100 100 98 Potameiamicrophylla
MA C
68 chinensisAS
Cryptocarya 0
100 MA
thouvenotii
Cryptocarya
89 Cryptocarya AU
sclerophylla Deepcupules
100 Cryptocarya
rhodosperma
AU
59 100 I Eusideroxylon
zwageriBO
100 PotoxylonmelagangaiBO
Hypodaphnis zenkeri AF | Ovary inferior | Hypodaphnis
100 Gyrocarpusamericanus
100 wonotoboense
100
100 Sparattanthelium
~~~~~~~~~~~~~~~~~Hernandiaceae
Hernandiamoerenhoutiana
1-00
100 Illigeraluzonensis Q
Hortoniafloribunda 0
100 100 Monimiaovalis
1 Monimiaceae =3
100 Palmeriascandens |
97 ! Peumus boldus
Gomorteganitida I Gomortegaceae
Figure 2. Annotated 50% majorityrule tree 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.

118 Annals of the
Endlicheriachalisea
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
ITS
TC1 93 { Ocotea percoriacea Rhodostemonodaphne
Ocotea tristis
Ocotea pulchella
55
84
99 Ocotea ceanothifolia
Ocotea schomburgkiana
Ocotea tomentella
100 Endlicheriapunctulata
Ocotea pauciflora
Nectandracuspidata
Nectandrapsammophila Nectandra s.str.
75 74
98
amazonum
~~~~~Nectandra
75 74 Nectandraturbacensis a)
100 Pleurothyrium cinereum _
0
Pleurothyriuminsigne | Pleurothyrium
_100 Ocotea helicterifolia
100 ~~~~Ocotea
heydeana Ecotea
Octe O
Ocotea botrantha helicterifoliaspecies gp.
Umbellulariacalifornica i Umbellularia
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
91
Paraia bracteata E
_ Urbanodendron bahiense Cb
Urbanodendronverrucosum
Licariamartiniana
Licariaguianensis .
Licariacannella
Licariatriandra
r ,99 Ocoteafoetens
Ocoteabullata
Ocotea grayi
OldWorld
Ocotea
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
64
I11oo.- Cinnamomum 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
| r~e 1 t Pes
1 Persea sp.
thunbergii | Persea subg. Machilus
P~~~~~ersea
E | 89
8
| 8
Ayollonias
Ioerseanamericana
barbujana i Apollonias
I Persea subg. Persea
group
g
II Persea caerulea
Persea mingue Persea subg. Eriodaphne
I * Mezilaurus ~~~~~~~~~~~~~~~~~~~Persea
meridensisI
tunca
Sextonia Chlorocardium
Chocadu
pubescens
- 100.~ Chlorocardium venenosum 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.= Mocinnodaphne,
and Rhodostem.= Rhodostemonodaphne.
land of 567 equal lengthtrees (L = 1050, CI = existsamongmembers

ofthetopologicalinstability
0.44, RI = 0.75). The Adams consensustopology of Cinnamomum.Sassafras was placed between
(Fig. 3) indicatesthatPerseeae sensuvan derWerff Laureae and a paraphyleticCinnamomumin all
and Richter(1996) are paraphyletic, and thatmost trees.This reconstructiondoes not receive strong

Endlicheriachalisea
Rhodostemonodaphnecrenaticupula
FRhodostemonodaphne praeclara
100 Endlicheriacitriodora
FRhodostemonodaphne recurva
Matrix III 74 FRhodostemonodaphne
Ocotea guianensis
scandens
ITS 99 Ocotea nigra

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 Pleurothvrium cinereum
Pleurothyrium insigne
10 00 Ocotea helicterifolia
Ocotea heydeana .Madrean
CentralAmerica
Ocotea botrantha
Umbellularia
_ _ caftornica NotAmrc
NorthAmerica
UmbelluNectandra coriacea
Nectandrapurpurea CentralAmerica
Nectandra
salicifohia
64 Ocotea odorifera
56 Ocotea rhynchophylla
92 Aniba cinnamomiflora
Aniba excelsa
Anibapanurensis
Aiouea costaricensis
Ocotea insularis
Dicypelliumcaryophyllaceum
78 Kubitzkiamezii Primaril
Dicypelliummanausense
98 89 Ocotea veraguensis Y
Ocotea quixos South America
88 Paraia bracteata
8 Urbanodendronbahiense
Urbanodendronverrucosum
Licariamartiniana
53 Licariaguianensis
100 Licariacannella
Licariatriandra
86 Ocotea foetens I Macaronesia
10 Ocoteabata South Africa 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-
7 ocote9 ,
innamomumjaponicum Africa tropical
152 m Cinnamomum
sp.
Cinnamomumverum Asia
I ~~~~Cinnamomum
camphora 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 _~~~~~~~7 Neolitsea sericea
Asia
.I
I III Actinodaphnesesquipedalis
I Li~~~~~~~ndera umbellata
I I
I
_~~~~~~8 Phoebe formosana
Alseodaphne semecarpifolia I Asi
I Deh~~~~~~~~aasia incrassata Asia
Apolloniasbarbujana I Canary Islands
100 Persea sp.I
| |89 89 1 |
Persea thunbergii Asia Boreo-
I I _ ~~~~~Persea
americana
92 Persea lnguea Neotropics tropical
Persea meridensis
100 Mezilaurustriunca
E 100 Sextonia pubescens
. 1 100
100
100 venenosum
4Chlorocardium ~~~~~~~Chlorocardium
rodiei South America od aa
Gondwanan
Anaueriabrasiliensis
5 changes
Figure4. One of 126 equallyparsimonious treesobtainedwithmonophyly ofthe Cinnamomum group(Cinnamo-
mum,Aiouea p.p., Mocinnodaphne, and Ocotea p.p.) and Laureae enforced(thickverticalbars) as topologicalcon-
straints.Bootstrapsupportvalues are indicatedabove unconstrainedbranches.Annotatedbarsto therightindicatethe
distributionand inferred
ancestryofclades.

120 Annals of the
bootstrapsupport,and constraining
monophyly
ofa ported generic-level phylogenyforLauraceae. 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
onlyone extrastep while constraining monophyly resolution among members of Perseeae and Lau-
of Laureae to includeSassafrasadded threeextra reae (sensu van der Werff& Richter, 1996). To pro-
stepsto parsimony-based trees.One of126 equally vide a basis for subsequent biogeographic consid-
parsimonious trees (L = 1054, CI = 0.44, RI = erations, phylogenetic relationships among
0.75) calculated withbothtopologicalconstraints Lauraceae are firstdiscussed.
enforcedis shownin Figure4. Bothminimum-evo-
lution analyses recoveredtopologiesthat showed PHYLOGENETIC RELATIONSHIPS
thesame mainclades foundbyparsimony analyses.
AlthoughCinnamomum was again notmonophylet- Several previously recognized taxonomic groups,
ic, minimumevolutionplaced Sassafras sisterto albeit in differentschemes, compare favorablywith
remainingLaureae, albeit togetherwithCinnamo- clades supported by our molecular data. Among
mumcamphora(L.) Presl.Differences betweenpar- these, Cryptocaryeae as circumscribed by van der
simony and minimumevolutionreconstructionsWerffand Richter (1996), Laureae of most classi-
suggestthatsomeinstability to- fications (e.g., Kostermans, 1957; van der Werff&
in parsimony-based
pologiescan be to characterssharedbe- Richter, 1996; Rohwer, 1993a), and Cinnamomeae
attributed
tween Sassafras and C. camphora. With C. cam- in the sense of Kostermans (1957) are the largest.
phora removedthe numberof treesresultingfrom In addition, a generic grouping centered around
unconstrainedparsimonyanalyses 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 fewsmall genera
is unsettled.
A likelihoodratiotest on the ITS data set re-
duced to 25 representatives of main lineages in
Hypodaphnis and Cryptocaryeae. MonotypicHy-
higherLauraceae (Fig. 5a) indicatedthatsubsti-podaphnis, consisting of H. zenkeri (Engl.) Stapf
tutionwas approximately clock-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 significantly dif-
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-trnHdata sets analyzed
ships, only rpll6 did not reject the molecularin matrixI 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 removedfromanalysis (Fig. 5b). irregular thyrsoidinflorescences (van der Werff&
Results of twocalibrationssimulatingalternative
Richter, 1996) and morphological similaritywith
biogeographicscenariosare summarizedin Table Eusideroxylon and Potoxylon, two monotypic In-
3, and those of our preferredcalibrationare de-
donesian genera that consistentlyplace basally in
picted in Figure5. Cryptocaryeae(Figs. 1, 2). Like Hypodaphnis, they
have stamens withfourcollaterally arrangedlocelli,
DISCUSSION but their ovaries are only semi-inferior.However,
The two-tieredtaxon and molecularsampling the larger molecular sample (matrixII) places Hy-
adoptedin thisstudyprovidesa generally
wellsup- podaphnis sister to remaining Lauraceae with mod-
Figure5. Phylograms showingclock enforcedHKY-F distanceson reducedparsimony-based topologiesdepicting

terminal(5a) and basal (5b) clades in Lauraceae. Divergencetimesin Figure5a are based on ITS and thosein Figure
5b on rpll6 sequences.The timescale beloweach phylogram reflectsa calibrationin whichequivalentnodes(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 geographicdistributionsof terminaltaxa are given:AF = Africa,AS = Asia, BO = Borneo,
CA = CentralAmerica,CI = CanaryIslands,MA = Madagascar,MC = Macaronesia,NA = NorthAmerica,and SA
= SouthAmerica.

5a 5b r
Endlicheriachalisea SA
Rhodostemonodaphnescandens SA
Ocotea guianensis SA
Ocotea tristisSA
Ocotea tomentellaSA
f l l [
Nectandraamazonum SA
PleurothyriuminsigneSA
CA
Ocotea helicterifolia
e
Ocotea heydeana CA
ITS!
Ocotea foetensMC E
d Ocotea bullataAF
Ocotea grayiMA
CinnamomumoleifoliumSA
C CinnamomumquadrangulumSA
C | CinnamomumjaponicumAS B
CinnamomumverumAS
x Sassafras tzumuAS
b _ SasrSassafras albidumNA
Linderabenzoin NA
LinderaumbellataAS A
Apoalonias barbujana Cl C
a z Persea thunbergiiAS
Persea caerulea SA
Persea lingueSA
Sextonia pubescens SA
0.01 substitutions/site
a b f A B
0 2 .Time(Mya) I74
go 45 20 174 158 1

122 Annals of the
Table 3. Clock enforcedHKY-F, distancesaccumu- carya, Endiandra, Eusideroxylon, Potameia, and

lated afterdivergenceeventsamongterminal(Table 3a) Potoxylonis considerablein bothanalysesinves-
and basal (Table 3b) lineagesin Lauraceae,and estimates tigatingbasal relationshipsin Lauraceae (Figs. 1,
of divergencetimessimulating twobiogeographic scenar-
2). AnatomicalfeaturesstressisolationofAspido-
ios. HKY-F, distancesin Table 3a are obtainedfromITS
stemon,Eusideroxylon, and Potoxylonmore than
and thosein Table 3b fromrpl6 sequences. Calibration
1 simulatesWestGondwananvicarianceforthetrans-At- theiraffinities
(Richter,1981), but close relation-
lantic disjunctionin the Ocotea complex;calibration2 shipwithCryptocarya has been suggestedin recent
simulatesGondwananoriginforthe Chlorocardium-Me- morphology-based systems(e.g., Rohwer,1993a;
zilaurus lade. Node labels are equivalentto thosein Fig- van der Werff& Richter,1996). WithCryptocarya
ure 5, and ages fixedforcalibrationpurposesare under- they share a deeply urceolatefloralhypanthium
lined. * = Equivalentnodes. that develops into deep cupules enclosing the
drupe except fora small terminalorifice.Unlike
HKY-F Calibration1 Calibration2 thepreviousgenera,in Beilschmiediaand Endian-
distancefrom time(Mya) time(Mya)
Node node to tip + SD + SD ? SD dra the hypanthium is shallowand a cupule never
develops,while the fruitsof Potameia are either
a. Terminallineagesin Lauraceae. freeor seated in a small discoid structure. Koster-
a* 0.09740 ? 0.0106 354 ? 30 90 mans (1957), stressingthedegreeofcupule 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 PotameiawithPer-
d 0.03793 ? 0.0068 138 ? 19 35 ? 6
sea (also non-cupulate, but ofthe distalPerseeae-
e 0.02476 ? 0.0055 90 23 ? 5
f 0.02175 ? 0.0052 79 ? 14 20 ? 5 Laureae clade). Close relationship withCryptocarya
x 0.01437 ? 0.0042 52 ? 12 13 ? 4 has since gainedsupportfromwoodand barkanat-
z 0.03499 ? 0.0066 127 + 18 32 ? 6 omy(Richter,1981), inflorescence morphology (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 Cryptocaryeae reveals a trend
B 0.03513 ? 0.0056 620 ? 100 158 ? 31
C 0.02683 ? 0.0050 473 ? 88 120 ? 27 towardincreased ovaryexsertion,in both flower
D 0.02038 ? 0.0044 360 ? 77 91 ? 20 and fruit.Eusideroxylon and Potoxylon, withsemi-
E 0.03162 ? 0.0054 558 ? 95 142 ? 24 inferiorovaries,lie sisterto generawithsuperior
F 0.00977 ? 0.0058 172 ? 54 44 ? 14 ovaries.Aspidostemon branchesnext(Fig. 2), and
G* 0.02006 ? 0.0043 354 90 Cryptocarya lies sisterto thenon-cupulate clade of
Beilschmiedia,Endiandra,and Potameia (Figs. 1,
2). Endiandraand Potameiahave a reducednum-
ber of floralparts relativeto Beilschmiedia,but
erately high support (Fig. 2). This peripheral po-
whethertheynest withinthe latter(Figs. 1, 2) is
sition for Hypodaphnis is also indicated by matK
notwell resolved.
sequences, albeit with < 50% bootstrap support
Othergenerathathave been allied to members
(Rohwer, 2000), but difficultto support with mor-
of Cryptocaryeae but not hereinare eithermono-
phology. Any outgroup comparison is stymied by
typicor oligotypic. Theirgenericstatusis also con-
the unsettled sister family relationship of Laura-
troversial(e.g.,Rohwer,1993a). Dahlgrenodendron,
ceae. Hernandiaceae, with inferiorovaries, are fa-
withonlyD. 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 different fromCryptocarya (Rohwer,
1999; Renner & Chanderbali, 2000; Qiu et al.,
1993a). Triadodaphne, withthreespecies, is ten-
1999). A Hernandiaceae-Lauraceae lade receives
tativelydistinguishedfromEndiandra 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,comprisedofH.
inferiorovaries are a potential synapomorphyfor
curtisiiHook. f.,theoutersix stamensare extrorse,
the two families. However, given the non-inferior
and the thirdand fourthwhorlsstaminodial,but
state of all other Lauraceae, independent gain, re-
otherwisethe genus is similarto Beilschmiedia.
quired also by the topology in Figure 1, is equally
Brassiodendron, withonlyB. fragransC. K. Allen,
parsimonious.
also has onlysix fertilestamens,and accordingto
Cryptocaryeaesensu stricto. Support forthe lade Kostermans(1957) and Hyland (1989) should be
comprisedofAspidostemon,
Beilschmiedia,Crypto- includedin Endiandra.

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 analysesof matrix Caryodaphnopsis and Neocinnamomum are mor-
I, they constitutea statisticallyuncorroboratedphologicallysimilar,sharingtriplinerved venation
lade (with< 50% bootstrapsupport)thatlies sis- and four-locular antherswiththe locelli arranged
ter to the rest of the family,also withoutsupport in a shallowarc (sometimestwo-locularin Cary-
(Fig. 1). This alliance is disbandedby additional odaphnopsis,in a horizontalrow in Neocinnamo-
molecularcharactersprovidedby matrixII, but mumdelavayi(Lecomte)H. Liu). In contrast, Car-
theirpositionin thispartofthetreereceivesstrong yodaphnopsishas opposite leaves, a perianthof
support(Fig. 2). Some elementsof Cassytha'spo- strongly unequal tepals,and lacks a cupule,while
sitionmay be due to long brancheffectsin our Neocinnamomum has alternate(spiral)leaves,sub-
analyses. equal tepals,and a shallowcupule withpersistent
The herbaceousparasitictwiner, Cassytha,is the tepals. Close relationshipbetweenNeocinnamo-
sole exceptionto thearborescencetypicalofLaur- 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). Subfamilialpositionis supported relationshipsof these two genera are not clearly
by ab initio cellular endospermCassythashares indicated by our data. They eitherconstitutea
withHernandiaceae,Monimiaceae,and otherLaur- lade, albeit withCassytha(Fig. 1), or Caryoda-
ales (Heo & Tobe, 1995; Heo et al., 1998). Such phnopsislies betweena Neocinnamomum-Cassytha
endospermformation is also reportedfromUmbel- lade and therestofthefamily(Fig. 2). WithCas-
lularia (Bambacioni-Mezzetti, 1941), but nuclear sythaexcluded,eitherCaryodaphnopsis or Neocin-
endospermis found in all otherLauraceae that namomum lies sister to the rest of the family(clad-
ograms not shown). Neocinnamomumwas not
have been examined,includingHypodaphnis (Heo
included in Rohwer'smatK study,and Caryoda-
et al., 1998). In Rohwer'smatKstudyCassythawas
phnopsiswas placed as itis in Figure2. Anatomical
placed betweenHypodaphnisand the rest of the
affinities
ofNeocinnamomum and Caryodaphnopsis
family, butwithoutstrongstatisticalsupport.Here,
withChlorocardium and Cryptocaryeae, respective-
close relationshipwithNeocinnamomum receives
ly (Richter,1981), are consistentwiththeirrela-
veryhighstatisticalsupportfrommatrixII (Fig. 2),
tivelybasal positionin thefamily.
but morphologicalsynapomorphies forthese two
generaare notknown.Instead,Cassythaand Neo- Chlorocardium-Mezilaurus lade. The lade com-
cinnamomum have the longestbranchesin the to- prised of Anaueria, Chlorocardium, Mezilaurus,
pology,differing fromeach otherby over279 mu- Sextonia,and a novel taxon(Gen. & sp. nov.)re-
tations(uncorrected"p" distances,uninformativeceives 99% and 96% bootstrap supportfrommatrix
charactersincluded),whilethebranchunitingthem I and II, respectively (Fig. 1). It is one ofthemore
is supportedby comparatively few(66) mutations. intriguingclades in the family.Close relationship
WithNeocinnamomum removedfromthe analysis, betweenAnaueria and Mezilaurushas been sug-
Cassythaand Caryodaphnopsis constitutea lade gested(Richter,1981; Rohwer,1993a), butthepos-
(cladogramnot shown).In both genera the outer sibilitythatall thesetaxaconstitute a lade oftheir
whorlof tepals is strongly reduced,but this con- own has neverbeen consideredon morphological
ditionappears elsewherein Lauraceae (e.g., Per- grounds.So far,charactersunitingthemhave only
sea), and othercharactersto supporta Cassytha- been providedby moleculardata. A lade com-
Caryodaphnopsislade are unknown.However, prisedof Chlorocardium and Mezilaurus(plus Wil-
with both Neocinnamomum and Caryodaphnopsis liamodendron, a small genusof3 species differing
removed,Cassythastilllies sisterto therestofthe fromMezilaurusprimarily in thenumberoflocelli;
family.If longbranchescannotattractin theirmu- not herein)receivedmoderatesupportfrommatK
tual absence (Sidall & Whiting,1999), thisfinding sequences, but Rohwer(2000) questioneda close
would implythat Cassythais correctlyplaced in relationshipcitinganatomicaland floraldifferenc-
this generalpart of the phylogeny. Alternatively,es. Here, Chlorocardium and Mezilaurusplace in
long branchedtaxa, such as Cassytha,experience separate subclades that can be characterizedby
multiplesubstitutions thaterode genealogicalsig- phyllotaxy.
nal, randomizecharacterstateswithrespectto true The subcladeofGen. & sp. nov.,Mezilaurus,and
relatives,and lead to chance convergenceon the Sextoniaaccommodatestaxa withobovate,coria-
molecularstates of distantlineages,all qualities ceous leaves borne in terminalclusters(Fig. 2).

124 Annals of the
UnlikemostotherLauraceae withterminally clus- relationshiphas never been formallyrecognized.

teredleaves, in thesetaxa theclustersare notsep- OnlyKostermans (1957) placed thesetwotribesin
aratedby seasonal growthspurts.Instead,growth close proximity in his graphicalschemeforLaur-
is continuous,and apparentlyquite slow,resulting aceae, conceivablyto expresshis observation that
in a continuousspiral of leaf scars. This growth fleshyhemispherical cupulesare typicalof,and re-
patternis rare but not unique to this lade; such strictedto,generatherein.Elsewherein Lauraceae
leafclustersare at leastalso knowninAlseodaphne, hemispherical, butratherwoody,cupulesalso occur
ofthePersea group(below).In theothersubclade, in Chlorocardium and Sextonia,both included in
Anaueriaand Chlorocardium shareoppositeleaves Cinnamomeaeby Kostermans(as Ocotea), but of
(Fig. 2). This subclade receivesconsiderablemo- the Chlorocardium-Mezilaurus lade herein.
lecularsupport,butbothgenerafindmorphological
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-cupulategeneraof van
1981), withwhichit also sharesglandlessflowers.
der Werff and Richter's(1996) Perseeae. It is Roh-
Chlorocardium is uniquewithits xylemofcoronat-
wer's(1993a) Persea group,without Caryodaphnop-
ed vessel elements(Kostermanset al., 1969), and
sis. Nothaphoebe was notinvestigated hereinbutis
its largerotateflowers withan increasednumberof
morphologically close 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 generawithfour-locular
a pair of small basal glands,are muchlike those
anthers.have at some pointbeen placed in synon-
foundin the second and thirdstaminalwhorlsof
ymyunder Persea (e.g., Bentham,1880; Koster-
Sextonia.
mans,1957). Apolloniasand Dehaasia have always
All SouthAmericangenerathatdo not clearly
been segregatedon the basis of theirtwo-locular
assign to genericgroupsbased on wood and bark
anthers,but the genericimportanceof this char-
anatomyor inflorescence structure (van der Werff
acterand its use to delimitApolloniasfromPhoebe
& Richter,1996) place in a Chlorocardium-Mezi-
and Dehaasia fromAlseodaphneis questionable
laurus lade. MonotypicCosta Rican Povedada-
(Rohwer et al., 1991; Rohwer,1993a; van der
phne (notexaminedhere) was consideredclose to
Werff, in press). Othergenericcharacters,includ-
Mezilaurusby Rohwer(1993a), but his matK data
ing relativetepal sizes, whethertepals persistin
(Rohwer,2000) suggesteda place withgenerahere
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 presentsamplingdoes not ade-
membersof the Chlorocardium-Mezilaurus lade
quatelyaddress these issues. OnlyPersea is rep-
are suspectedon morphological grounds. resentedby morethanone species. Asian Persea
MonophyleticGroups in the Perseeae-Laureae (subg. Machilus) places withpaleotropicalAlseo-
lade. The largeterminallade thataccountsfor daphne,Apollonias,Dehaasia, and Phoebe,while
mostof the moderngenericand species diversity AmericanPersea (subg.Eriodaphneand subg.Per-
of Lauraceae includes Laureae of mostclassifica- sea) constitutesa separate lade (Fig. 3), but the
tionsystemsand van derWerff and Richter's(1996) implicationthatPersea is notmonophyletic has lit-
Perseeae. The presentresolutiondoes not support tle support.Detailed morphological and molecular
the dichotomyimplied by these tribal concepts studiesare needed to resolverelationships within
(Fig. 3). Instead,fivegenera of Perseeae (Persea thislarge group of ca. 400 species, mostof which
group)lie sisterto a lade comprisedof Laureae are found in tropicalAsia.
and remainingPerseeae. The genericcomposition Laureae. Close relationship amongActinodaphne,
ofthelattergroupcomparesfavorably withKoster- 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 classifications of Lauraceae. All are
Persea groupand a large Laureae-Cinnamomeae dioecious and mosthave umbellateinflorescences
lade was indicatedby matK sequences (Rohwer, subtendedby involucralbracts.In thisstudy,par-
2000), but topologywas unstableand lacked sta- simonyanalysesplace Sassafrasbetweenwell-sup-
tisticalsupport.Supportis stronger here withthe portedcore Laureae and remaining genera(Fig. 3).
Persea groupand Laureae-Cinnamomeaelade re- However,membershipin Laureae was foundby
ceiving89% and 93% bootstrapsupport,respec- minimum evolutionanalyses,and parsimony-based
tively(Figs. 3, 4). A close Laureae-Cinnamomeae treesin whichSassafraslies sisterto core Laureae

(Fig. 4) are just threesteps longer.Introrsely po- tropicalgenerain Cinnamonium. Monotypic Mocin-
sitionedlocelli in all staminalwhorlssupporta nodaphnewas describedto recognizea reduction
place forSassafrasin Laureae. Elsewherein Laur- in numberof staminalwhorls(Lorea-Hemandez,
aceae introrsely positionedlocelli are restricted to 1995), and Aiouea p.p. [A. dubia (HBK) Mez and
the outertwo staminalwhorls.Anotherpotential A. guianensisAubl. herein]differs mainlyin locelli
synapomorphy is the dioecious breedingsystem number,bothcharactersof traditional genericval-
shownby Sassafras and core Laureae. In Laura- ue. The findingthat Ocotea ikonyokpevan der
ceae, dioecyis otherwise onlyfoundin basallypo- Werff, a recentlydescribedspeciesfromCameroon,
sitionedHypodaphnis (Fig. 1) and a distalclade of is placed withCinnamomumis surprising.How-
Ocotea s. str.,Endlicheria,and Rhodostemonoda- ever, a leaf fragmentfromthe holotypesheet
phne (Fig. 3). Dodecadenia and Cinnadenia,not (Thomas10456, MO) was extracted, amplified, and
herein,shouldalso place in Laureae on the basis sequenced onlywithotherspecies of Ocotea.Fur-
of dioecyand introrse locelli. thermore, ITS1 and ITS2 regionsof 0. ikonyokpe
Umbellulariais usually placed in Laureae be- were amplifiedand sequenced separately.Neither
cause of its umbellateinvolucrateinflorescences section is identicalwithaccessions of Cinnamo-
(e.g.,vanderWerff & Richter,1996), butitsflowers mum,and bothsupporta place withCinnamomum.
are bisexual and locelli of the innermost staminal In Africa,0. ikonyokpe shares(sub)oppositeleaves
whorlare extrorse, notintrorse. A 16-bp repeatin withEast African0. michelsonii Robyns& Wilczek
trnL-trnF (Fig. 1) and ITS sequences (Figs. 3, 4) and 0. usambarensis Engl. (not herein).All other
distanceUmbellularia fromLaureae and place it in AfricanOcotea have spirallyarrangedleaves (van
the Ocoteacomplex(below). der Werff, 1996). Interestingly,0. ikonyokpe asso-
Genericdelimitation in Laureaeis unsettled.Lit- ciates withAsian Cinnamomum (mostlyopposite-
sea alone accommodatesca. 400 of the approxi- leaved) insteadofmostlyalternate-leaved neotrop-
mately700 species, and mostgenericlimitsare ical Cinnamomum(Figs. 3, 4). The staminodes,
probablyartificial(Rohwer,1993a; Li & Christo- relativelysmallerthanseen in Cinnamomum, and
phel,2000). As withthePerseagroup,detailedsys- withoutsagittateapices (althoughglandularas in
tematicstudiesare needed to resolvenaturalline- Cinnamomum), referthisCameroonspeciesto Oco-
ages in Laureae. tea, butleaf arrangement is perhapsan overlooked
characterhere.
Cinnamomeae. All remaininggenerawere pre-
Neithermolecularnormorphological synapomor-
viously placed in Cinnamomeae(sensu Koster-
phies readilyappear forthe Cinnamomum group
mans, 1957), albeit togetherwithSassafras,Acti-
(Cinnamomum, Aiouea p.p., Mocinnodaphne, and
nodaphne,and Neocinnamomum. Withthesethree
Ocotea p.p.), but enforcingmonophyly adds only
generaexcluded,Cinnamomeaeis van der Werff
one step to parsimony-based trees (Fig. 4). Still,
and Richter's(1996) Perseeae withoutthe Persea
New and Old Worldspecies remainseparatesub-
group.Cinnamomeaeare thusa sizeable subsetof
the Perseeae-Laureaeclade (Fig. 3), accommodat- clades in the constrainedclade. This New World-
ingall ofitsmajorneotropicalgenera(e.g.,Aiouea, Old World dichotomy is also evidentin wood and
Aniba, Endlicheria,Licaria, Nectandra,Pleuroth- bark anatomy (Richter,1981), and can be deduced
yrium,and Rhodostemonodaphne) as well as wide- from traditional placement of neotropicalCinna-
and Ocotea. momum in Phoebe (of the Persea group above) until
spreadCinnamomum
Cinnamomeae share hemispherical cupules transferred by Kostermans(1961). Withover 350
(rarelypoorlydeveloped)withLaureae and retain species distributed from(sub)tropicalAsia to the
the thyrsoidnon-involucrate inflorescences of the Neotropics, one African member;and a fewrepre-
Persea group.Thus, uniquelyderivedfeaturesare sentativesin Australiaand thePacificIslands (pri-
not obvious. Bootstrapsupportfor Cinnamomeae marilyFiji), the Cinnamomumgroupis speciose
reaches only 52% in unconstrainedparsimony and widespread.
analyses (Fig. 3), but raised to 86% by enforcing
Ocotea complex. The remaininggeneraofCinna-
monophyly of a genericalliance centeredaround
momeae forma stronglysupportedclade within
Cinnamomum (Fig. 4). which membersof Ocotea are widely dispersed
Cinnamomum group. The delimitation of Cinna- (Figs. 3, 4). FindingthatUmbellulariaplaces here,
momumis based on its nine stamenswithfour- and not in the Laureae, clarifiesconflicting indi-
locular anthersand a fourthandroecialwhorlof cations fromfloralmorphology and inflorescence
well-developedstaminodesprovidedwithsagittate structure (discussedunderLaureae, above). Apart
glandularapices. The presentdata nest two neo- froma fewOld Worldspecies of Ocotea,the com-

126 Annals of the
plex is restrictedto the New Worldand accounts bitzki,1993). A relatively

basal positionin theOco-
for most of the genericand species diversityof tea complexis suggestedby ITS sequences (Figs.
Lauraceae in the Neotropics. 3, 4).
Clades resolvedwithinthe Ocotea complexcan
Ocotea helicterifoliaspecies group. The clade
be circumscribedin geographic,and sometimes
(Figs. 3, 4) comprisedofOcoteabotrantha Rohwer,
morphological, terms.Basal branchesin the com-
0. helicterifolia(Meisn.) Hemsl.,and 0. heydeana
plex are occupiedby Old Worldspecies ofOcotea,
(Mez & Donn. Sm.) Bernardirepresentsa diverse
NorthAmericanUmbellularia,and primarily Cen-
butcohesiveassemblageofspecies in Ocotea.Core
tral Americanspecies groups in Nectandraand
membersare characterizedby hirsuteleaves and
Ocotea. Two derivedclades are centeredin South
twigs,bisexual flowerswithpartiallypapillose te-
America.In the morespeciose, Nectandras. str.
pals, glabrousorweaklypapilloseantherswithfour
and Pleurothyrium lie sisterto a dioecious lade
pollen sacs arrangedin two superimposedpairs,
comprisedofEndlicheria,Ocotea s. str.,and Rho-
and well-developedstaminodes(van der Werff,
dostemonodaphne. In the second and less speciose
1999). Close relationship withnon-hirsute species
South America-centeredlade, Aniba, an assort-
withthis generalfloralstructure, i.e., the Ocotea
mentof Ocotea species, and mostlymono-to oli-
heydeanaspecies group,and withthe Ocoteasin-
gotypicgeneraassociatewithLicaria.
uata species group,whichdiffers by moreheavily
Old WorldOcotea. Outside of the Neotropics, papillose tepals and anthers(here representedby
Ocoteais represented by 0. foetens(Aiton)Baill. in 0. botranthaRohwer)was anticipatedby Rohwer
Macaronesia,7 species in mainlandAfrica,and (1991). WiththeNectandracoriaceaspecies group,
about 30 species in Madagascar. In this study, and Umbellularia,the Ocoteahelicterifolia species
South African0. bullata (Burch.)E. Mey. and 2 groupshareswell-developedstaminodeswithglan-
species fromMadagascar,0. grayi van der Werff dular apices, whiletheirpapillose anthersand te-
and 0. malcomberivan der Werff,constitutea pals suggestan affinity withNectandras. str.and
strongly supportedlade. Ocoteafoetensis almost Pleurothyrium. Theirplace in the presentphylog-
indistinguishable from0. bullata,but surprisingly enyis consistent withthisintermediate morphology.
its place withOld WorldOcotea receives < 50% The groupis distributed throughout CentralAmer-
bootstrapsupport(Figs. 3, 4). Morphological char- ica and numbersaround30 species.
acters distancingOld World Ocotea fromNew
Ocotea s. str.,Endlicheria,and Rhodostemonoda-
Worldrelativesdo notreadilyappear. In the pre-
phne. A clade comprisedof all dioeciousOcotea
sent reconstruction Old WorldOcotea lie sisterto
sampled for this studyand the only neotropical
the New Worldcomponent ofthe Ocoteacomplex.
generawiththisbreedingsystem,Endlicheriaand
Nectandracoriaceaspeciesgroup,Nectandras. str., Rhodostemonodaphne, is found in all ITS-based
and Pleurothyrium.Representatives of the Nec- trees.It receiveslow bootstrapsupportas a whole
tandra coriacea species group,N. coriacea (Sw.) (55%), but muchbetter(93%) supportwithinthe
Griseb.,N. salicifolia(HBK) Nees, and N. purpurea group above the branch separatingEndlicheria
(Ruiz & Pav.) Mez, place distantfroma lade in punctulata(Mez) C. K. Allenand Ocoteapauciflora
whicha broadmorphological representationofNec- (Nees) Mez fromtherest(Fig. 3). As seen in Figure
tandras. str.pairswithPleurothyrium (Figs. 3, 4). 4, E. punctulataand 0. paucifloraappeartodiverge
Close relationshipbetweenNectandras. str.and early,shortening the branchsupporting the entire
Pleurothyrium was also indicated by matK se- clade, but thiseffectcould also be obtainedby re-
quences (Rohwer,2000). The twoshare relatively versals to ancestral molecular states along the
large rotateflowerswithheavilypapillose tepals branchunitingthesetwospecies.
and stamens,and relatively poorlydevelopedstam- Taxa placed here include the type species of
inodes. Nectandras. str. and Pleurothyrium are Ocotea,0. guianensisAubl.,and representseveral
centeredin South Americawithca. 100 and 40 species groupsrecognizableamongdioeciousOco-
species, respectively.The Central America-cen- tea (e.g., Rohwer,1986). Since representatives of
tered Nectandracoriacea species group (ca. 20 Endlicheriaand Rhodostemonodaphne also sample
spp.) was perceivedas accommodating the most a wide range of morphologicalvariationwithin
primitive elementsofNectandra,retainingOcotea- these moderately sized but heterogeneous genera,
like non-scalariform venation,tepal and stamen all approximately 300 dioeciousspecies oftheOco-
non-papillosity,distinctfilaments, and a well-de- tea complexshould place here. In this clade ge-
velopedfourth androecialwhorlofstaminodeswith nericlimitsbased on locelli arrangement and num-
glandularapices (Rohwer,1993b; Rohwer& Ku- ber are not supported.The Ocotea species forma

paraphyleticassemblage withinwhich Rhodoste- Ocotea insularis(Meisn.) Mez and Aiouea costari-

monodaphneand Endlicheriaare nested (Figs. 3, censis(Mez) Kosterm.are unitedwith100% boot-
4). Rhodostemonodaphne has four-locular strapsupport(Figs. 3, 4). The twodiffer
anthers onlyin the
like Ocotea,but the locelli are arrangedin a shal- numberoflocules per anther,again illustrating the
low arc or horizontal rowratherthansuperimposed weaknessof this characterin genericdelimitation
pairs,at least in the outerstamens.Endlicheriais (van der Werff, 1984). Curiously,as notedby van
two-locular,but withE. punctulatapairedwith0. der Werff (1988) and Rohweret al. (1991), like A.
pauciflora,and otherspecies placed withRhodos- costaricensis,otherAiouea species withcloser ties
temonodaphne to Ocoteaare CentralAmerican(e.g.,A. lundelliana
(Figs. 3, 4), it is at least di-phyletic.
C. K. Allen, not herein),while South American
Licaria group. The branch unitingDicypellium, Aiouea associatewithCinnamomum (e.g.,A. dubia
Kubitzkia, Licaria,Paraia, Urbanodendron, and two and A. guianensis,Fig. 3).
species of Ocotea receives93% bootstrapsupport
(Fig. 3) and seems to be a naturalalliance. Ga-
BIOGEOGRAPHY
mantheraand Phyllostemonodaphne (neitherhere-
in) associatewiththeLicaria groupon morpholog- Genera and clades in Lauraceae sortinto two
ical grounds.All these generahave cupules with main geographicgroups(Figs. 2, 4). Hypodaphnis,
double-rimmed (or more)margins.Giventheseun- the Cryptocaryeae, Cassytha,and the Chlorocar-
usual cupules, a genericalliance centeredaround dium-Mezilauruslade as seen in Figure1 are pre-
Licaria has been informally recognizedin recent dominantly or entirelysouthernhemispheric, while
morphological systems(Kostermans, 1957; Rohwer, Caryodaphnopsis,Neocinnamomum,the Persea
1993a). Ocoteaquixos(Lam.) Kosterm.and 0. ver- group,the Cinnamomumgroup,and Laureae are
aguensis (Meisn.) Mez representthe Ocotea den- eitherAsian or have amphi-Pacificdistributions
drodaphnespecies group,a groupof 8 species re- (Figs. 2, 4). The distributions of these two main
markablein Ocotea fortheirligulatestamensand groupsare consistentwithGondwananand Laura-
double-rimmed cupules. A place in the Licaria sian histories,respectively, butthegeographicdis-
groupis thus not surprising.Their distancefrom tribution oftheOcoteacomplexis 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-Malagasy elementadded
genericstatus;e.g., Sassafridium (Meissner,1864). by approximately 40 Old Worldspecies of Ocotea.
Hutchinson(1964) even placed 0. veraguensis(as Whetherancestorsofthe Ocoteacomplexmigrated
Sassafridium) in a monotypic tribebecause he in- intoSouthAmericavia Africa(Raven & Axelrod,
terpreted the locelli in the thirdstaminalwhorlto 1974) or via NorthAmerica(Rohwer,1986; Taylor,
be introrse,a conditiononlyknownin Laureae. In 1988; Rohwer& Kubitzki,1993; Rohwer,2000) is
factthe locelli are latrorse-introrse, as also found notevidentfromthetopologyalone.
in Dicypellium and Urbanodendron, bothoftheLi- Paleogeographicreconstructions of West Gond-
caria group.Elsewherein Ocotea,double-rimmed wana breakupestimatethatdirectland connections
cupules are foundin a fewdioeciousspecies,e.g., betweenAfricaand SouthAmericawerelostbythe
0. cujumaryMart.and 0. floribunda(Sw.) Mez. It Upper Mid-Cretaceous, ca. 90 Mya (Sclateret al.,
is unlikelythatthesespecies will assignto theLi- 1977; Scotese et al., 1988; Parrish,1993). There-
caria groupsince theirmorphologically close rela- fore,if thetrans-Atlantic disjunctionin theOcotea
tives, 0. guianensis Aubl. and 0. percoriacea complex can be attributedto West Gondwanan
(Meisn.)Kosterm., respectively,are firmly seatedin breakup,it wouldhave to be at least 90 Mya old.
the dioeciousclade discussedabove. This biogeographicscenariowas simulatedon the
Remainingtaxa place near the Licaria group parsimony-based ITS topologyby fixingthe New
withoutstrongsupport(Fig. 3). Ocotea rhyncho- World-OldWorlddivergence(nodee in Fig. 5a and
phylla(Meisn.)Mez and 0. odorifera (Vell.)Rohwer Table 3a) at 90 My and usingthe resultingrateof
representspecies groupsthatRohwer(1986) con- molecularevolutionto estimatedivergencetimes
sideredintermediate betweenthe0. dendrodaphne forothernodes. This calibrationyields a rate of
species group (including0. quixos and 0. vera- 0.000275 substitutions per siteper millionyears,a
guensisherein)and the restof Ocotea.Theirposi- rate thathalves the lowestever reportedforITS
tionnear theLicaria groupis consistent withRoh- (Suh et al., 1993), and whichplaces thedivergence
wer'sinterpretation. Aniba,too,has been associated oftheChlorocardium-Mezilaurus lade (Fig. 3; and
withLicaria (e.g., Kubitzki,1982), buthas simple- represented bySextoniapubescensvan derWerff in
rimmedor rarelyweaklydouble-rimmed cupules. Fig. 5a) fromthePerseeae-Laureae lade (includes

128 Annals of the
MissouriBotanicalGarden
theOcoteacomplex)at 354 Mya (node a in Fig. 5a BASAL LINEAGES

and Table 3a). This Devonianage precedesearliest
undisputedangiospermfossils.Furthermore, ifthe Raven and Axelrod(1974) situatedthecradleof
equivalentnode in the basal topology(node G in the angiospermsin WestGondwana,and its prox-
Fig. 5b and Table 3b) is fixed at 354 Mya and imity to Laurasiawas pivotalto theMid-Cretaceous
divergencetimesforearlierlineagescalculated,the presenceof angiospermpollen in the SouthLaur-
radiationof the familyis placed in the Pre-Cam- asia Province(sensu Brenner,1976). Any expla-
brian,ca. 682 Mya.Therefore, theneotropical-Af- nationof the biogeographichistoryof Lauraceae
also requiresearlymigratory routesbetweenLaur-
rican disjunctionshownby the Ocotea complexis
asia and West Gondwana.Southernhemispheric
likelyto be muchyoungerthanWestGondwanan
Hypodaphnis,Cryptocaryeae,Cassytha,and the
breakup,and some amountof dispersalmusthave
Chlorocardium-Mezilaurus lade indicate Gond-
been involved.
wanan history,but Caryodaphnopsis and Neocin-
How did theOcoteacomplex,and othermembers
namomumappear to be Laurasian.
of the family,reach the New World?In bothmor-
Caryodaphnopsis is disjunct between tropical
phologicaland molecularattributes the Chlorocar-
Americaand tropicalAsia, whileNeocinnamomum
dium-Mezilauruslade occupies a basal and iso-
is knownonlyfromtropicalAsia. They represent
lated positionin Lauraceae. It is also the only
the onlyearlylineages in Lauraceae thatare pre-
lineage of basal Lauraceae restrictedto South
sent in Asia but are not also knownto occur in
America(reachingitsnorthern limitin CostaRica). Africa,Madagascar,and Australia,in contrastto
These qualitiesargueforearlyisolationoftheChlo- widespreadgenerain Cryptocaryeae and Cassytha.
rocardium-Mezilaurus lade in SouthAmerica,pre- The fossilrecordsuggeststhatbothCaryodaphnop-
sumablyinitiatedby WestGondwanabreakup.To sis and Neocinnamomum havean ancientLaurasian
assess thisbiogeographicscenarioon otherdiver- history. The fossilwoodtaxonCaryodaphnopsoxylon
gencetimes,substitution ratesin theITS and rpll6 richteriGottwald(1992) places the unique xylem
data sets were re-calibratedusing an Upper Mid- anatomyof Caryodaphnopsis in Late Eocene Ger-
Cretaceous(90 Mya) separationof SouthAmerica many.The fossilflowerNeuseniatetrasporangiata
fromAfricato date the divergenceof the Chioro- EklundfromLate CretaceousNorthAmericacom-
cardium-Mezilauruslade fromits sister group pares favorably withNeocinnamomum, and flowers
(node a in Fig. 5a and Table 3a, node G in Fig. 5b and fruitsfromthe same localitycan be compared
and Table 3b). Withthissecond calibration,radi- to Caryodaphnopsis (e.g., Eklund,2000). Although
ationofLauraceaewas estimatedat 174 ? 32 Mya the affinities of the latterfossilscannotbe unam-
(node A in Fig. 5b and Table 3b), and radiationof biguouslyassigned,the impliedantiquityof Cary-
theterminalPerseeae-Laureae lade was placed in odaphnopsisand Neocinnamomumis consistent
the Eocene, 44 + 7 Mya (node b in Fig. 5a and withtheirrelativelybasal positionsin Lauraceae.
Table 3a). This estimateforEocene radiationofthe Mostlikely,these moderngeneraare descendants
lattergroupis supportedby the fossilrecord.The oftheCretaceousLaurasianfloraofLauraceaedoc-
hemisphericalcupules of the London Clay Flora umentedby the fossilgeneraMauldinia (Drinnan
(Reid & Chandler,1933) are restricted to Laureae et al., 1990; Herendeenet al., 1994, 1999; Eklund
and Cinnamomeaeof the Perseeae-Laureae lade. & Kvacek, 1998) and Perseanthus(Herendeenet
Well-preserved flowerswiththegeneralfloralstruc- al., 1994).
tureof generain the Persea groupand Cinnamo- The timingofeventsthatresultedin themodern
meae, but not othermembersof Lauraceae, have distribution of Caryodaphnopsis can furthereluci-
been described fromEocene deposits in North date its biogeographic history. A relictualpresence
America(Taylor,1988) and Late Eocene Balticam- in SouthAmericawouldimplya continuouspaleo-
ber(Conwentz, 1886). Thus,oursecondcalibration, distribution fromSouthAmericato Eurasia. How-
thatwhichcreditsSouthAmericanisolationofthe ever,such continentalconfiguration also provides
Chlorocardium-Mezilaurus clade toWestGondwan- directconnections betweenSouthAmericaand oth-
an breakup,estimatesa realisticage forradiation er Gondwananterrains(reviewedin Hallam,1994),
of the familyand complements fossilevidenceof and preferential extinction in theseSouthernland-
radiationof the Perseeae-Laureae groupin Early masses wouldbe necessaryto explainthe modem
TertiaryLaurasia. This congruenceprovidesconfi- disjunction.Alternatively, the rpll6 data set esti-
dence thatage estimatesbased on our second cal- matesa relatively recentseparation(44 ? 14 Mya)
ibrationare good approximations of actual diver- ofSouthAmericanC. tomentosa van derWerff from
gence times. Asian C. bilocellatavan der Werff (node F in Fig.

5b and Table 3b). This would rule out a relictual cannot be discounted.All otherSouthernHemi-
presencein SouthAmericaand is consistentwith sphericgenerahave narrower ranges.
theviewthatdisjunctdistributions betweentropical Hypodaphnismaybe relictualin CentralAfrica
Asia and tropicalAmericaare derivedfromances- since its ancestorsapparentlydivergedfromthe
tralboreotropical rangesdisruptedby 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). Eusideroxylon rangesfrom
plies thatisolationofCaryodaphnopsis fromtherest Borneoto Sumatra,and Potoxylonis endemicto
ofthefamilycan be stagedin theEarlyCretaceous Borneo. With their placementin predominantly
about 140 Mya (node E in Fig. 5b and Table 3b). SouthernHemisphericCryptocaryeae, it is possible
Increasingseparationof Laurasia fromGondwana, to regardthemas Gondwananrelictsas well. How-
a salientfeatureof Early Cretaceouspaleogeogra- ever,theirseparationfromthe restof the tribeis
phy (reviewedin Hallam, 1994), would have dis- dated at about 120 Mya (node C, Fig. 5b), an age
ruptedtrans-Tethyan ancestralrangesand precip- thatpermitsearlymigration into Laurasia, as en-
itatedthe nextbiogeographic phase in Lauraceae, visioned for Caryodaphnopsisabove. Further,
i.e., radiationon increasinglydistantLaurasianand Trianthera eusideroxylonConwentz,an amber-em-
Gondwananlandmasses. bedded flowerfromthe Eocene-Oligocenebound-
Accordingly, in the NorthernHemisphere,the ary of the Baltic area (Conwentz,1886) compares
Mid-Cretaceous fossiltaxa,and thedirectancestors remarkably wellwithEusideroxylon and adds tothe
of Caryodaphnopsis and Neocinnamomum, would possibility ofa Gondwanan-Laurasian dichotomy in
have spreadthroughout southern Laurasiauntilde- Cryptocaryeae. Upper Cretaceous appearance of
creasingtemperatures and theopeningofthenorth theboreotropical in Borneo(Wolfe,
Aquilapollenites
Atlanticconstrictedtheirdescendantsto tropical 1975; and referencestherein),and the composite
Asia and America.To the south,trulypantropical geologicalnatureoftheIndo-Malayanregion(Bur-
rettet al., 1991; Michaux,1991; and references
generaand clades wouldhave attainedtheirwide-
therein),are also consistentwithLaurasianhistory
spread distribution, withseafloorspreadingin the
forEusideroxylon and Potoxylon.
South Atlanticand Indian Oceans leading to in-
All othermembersof Cryptocaryeae and their
creased regionalendemicity. These continental re-
to,or best represented
allies are restricted in, aus-
configurations appear to be reflectedin the distri-
tralpartsof the Old World,i.e., East Gondwanan
butionofSouthernHemisphericgenera.
and derivedterrains.At theotherend oftheformer
Of pantropicalgenera,Beilschmiediaand Cryp-
southerncontinent, the Chlorocardium-Mezilaurus
tocaryaare the mostwidespread.The geneticdis-
lade is restrictedto SouthAmerica.Thus,among
tance-based age estimationsindicate that these these SouthernHemisphericgenera and clades,
generadivergedfromtheirmostrecentcommonan- morebasal groupsare eitherwidespreador relic-
cestorabout90 ? 20 Mya (node D in Fig. 5b and tual, and more derived groups are restrictedto
Table 3b). Variancearoundthese age estimations Easternor WesternGondwananfragments, consis-
arguesfordirectmigration throughout Gondwana, tentwiththeprogressive dismantling ofGondwana.
and a widespreadpre-drift distribution for both
Beilschmiediaand Cryptocarya. The presence of THE PERSEEAE-LAUREAE CLADE
bothgenerain continental Asia maybe due to the
rafting oftheIndiansubcontinent and otherGond- ROUTES TO LAURASIA
wanan fragments to the Asian plate. Later accre- The Perseeae-Laureae lade divergedfromits
tionsofGondwananfragments withtheAsian plate sistergroup,the Chlorocardium-Mezilaurus lade,
and Miocene island hoppingacross the Indo-Ma- since the Upper Mid-Cretaceous,but untilfossil
layanregionmayalso havebeen involved.The pan- membersappearedin Eocene Laurasia its biogeo-
tropicaldistribution of Cassythais mostlydue to graphichistoryis a mystery. Threealternative sce-
one widespreadspecies, C. filiformis L.; all other nariosare conceivable.In a vicariantvein,consider
approximately 20 species are restrictedto the Old a WestGondwanancommonancestorforthe Per-
Worldand show highregionalendemismin Aus- seeae-Laureae lade and its sistergroup,withtec-
tralia(Weber,1981). AlthoughtheSouthernHemi- tonicactivityisolatingdirectancestorsoftheChlo-
sphericdistribution centeredin the Old Worldfa- rocardium-Mezilauruslade on South America
vors a predominantly East Gondwananhistoryfor while strandingthose of the Perseeae-Laureae
Cassytha,thepossibilityofa Laurasianhistory fol- lade on Africa.AncestorsofthePerseeae-Laureae
lowedby radiationintoits associatedxerichabitat lade then migrateto Laurasia via NorthAfrica.

130 Annals of the
Alternatively, the northern routeof the Perseeae- gestthatitsAsian and Americanmembersdiverged

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 distribution and representation of the Cin-
Antillesspanned the PanamanianIsthmusas an namomumgroupin the Neotropicsand Asia is al-
island chain in the Mid-Cretaceous(Pindellet al., mostidenticalto thatofthePersea group.Whether
1988) providinga stepping-stone migratory route New and Old Worldclades in the Cinnamomum
outofSouthAmerica.Yet a thirdpossibilityis that groupconstitutea monophyletic groupis not yet
thecommonancestorofthePerseeae-Laureaeand clear. From age estimatesobtainedby enforcing
Chlorocardium-Mezilaurus clades was Laurasian monophyly (Fig. 5a), the assumedcommonances-
and sharedtheformer northern continentwithCar- tral gene pool divided aroundthe Eocene-Oligo-
yodaphnopsis and Neocinnamomum. This scenario cene boundary, a divergencetimecoincidentwith
would requirethatthe Chlorocardium-Mezilaurusthatcalculated forthe Persea group.These simi-
lade migratedinto South Americavia the Mid- laritiesin thetropicalamphi-Pacific disjunctions in
Cretaceousstepping-stone routeprovidedbyproto- the Cinnamomum and Persea groupssuggestcom-
GreaterAntilles.Evidence of an earlyfaunaland monality. Disruptionofboreotropical rangesby cli-
floristicexchangeacross 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 consistent withthepresentage es-
taxa involvedare usually distributedthroughout timates.Alreadytenuousbiotic links across the
northernCentral America and South America, NorthAtlanticand/orPacificwere severedat this
while the Chlorocardium-Mezilaurus lade only time,and dividedCinnamomum and Persea groups
reachesCosta Rica to the north. receded to warmerpaleolatitudesin Asia and the
Withoutan unambiguousCretaceousfossilre- Americas.
cordforthe Perseeae-Laureae lade, we favorthe Like the Cinnamomum and Persea groups, Lau-
firstor Africanscenario.NorthAfricais todaypart reae are mostdiversein Asia witha smallerrange
of the largestdesertsystemin the world,but was and representation in the New World.Lindera,Lit-
covered by tropicalforestwell into the Miocene sea, and SassafrasreachtheAmericas,butofthese
(Axelrod& Raven, 1978). Duringthe Tertiary, Af- onlyLitsearangessouthoftemperateNorthAmer-
rica movedprogressively northward, and migration ica, to Costa Rica. The unsettledgenericdelimi-
to Eurasia acrossthenarrowing Tethyswouldhave tationof Litsea and Lindera cautionsagainstas-
becomeincreasingly feasible.The SouthAmerican sessmentoftheirdisjunctions frommorphology, but
scenarioinvokesa circuitousrouteto Eurasia and monophylyof Sassafras is well supportedhere
fails to explainwhyno membersof the Perseeae- (Figs. 3, 4), providingan opportunity to assess the
Laureae lade remainrelictualin SouthAmerica. classic NorthAmerica-EasternAsia disjunction
An earlyLaurasianhistorywould have to account firstbroughtinto 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
NorthAmericanS. albidum(Nutt.)Nees was esti-
ROUTES TO THE NEW WORLD I: PERSEA GROUP, matedat about12 Mya(nodex in Fig. 5a and Table
CINNAMOMUMGROUP, AND LAUREAE 3a). This northern temperatedisjunctionis much
youngerthan the ? 30 Mya old tropicalamphi-
The Persea groupis mostdiversein Asia, with Pacific disjunctionsshownby Cinnamomumand
onlyca. 80 of its approximately 400 species found Persea groups.While climaticcoolingin the Eo-
in the New World.These occurmainlyin montane cene and Oligocene (Wolfe,1975; Hallam, 1994)
forestsin Centraland South Americaand range restricted tropicaltaxa to lowerpaleolatitudes, for
fromMexicoto Chile,reachingtheAtlanticcoastal temperatetaxa intercontinental connectionsacross
forestsin southeastern Brazil.In theOld World,two northern latitudeswould 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 timeseparatingAsian fromNorthAmerican
Asian lade withAlseodaphne,Dehaasia, Persea Sassafrascoincideswell withopeningoftheBering
subg.Machilus,and Phoebe(Figs. 3, 4). The other Strait,and supportsWolfeand Leopold's (1967)
CanaryIsland endemic,Persea indica (L.) Spreng., view that Mid-Mioceneloss of the Bering land
was not sampled here. Pendingbetterresolution bridgeis the mostlikelycause of north-temperate
withinthePersea group,currentage estimatessug- disjunctionsbetweenNorthAmericaand Asia.

ROUTES TO THE NEW WORLD II: THE OCOTEA proximately 20 Mya(nodef in Fig.5a and Table 3a)
COMPLEX arguesforarrivalof the Ocotea complexin South
Americapriorto PlioceneclosureofthePanaman-
The Ocotea complexaccommodatesmostof the ian isthmus.As the timingof the separationcoin-
taxonomicdiversityof neotropicalLauraceae. In cides withincreasedupliftof the northern Andes
the Old Worldthe complexis weaklyrepresented in theearlyMiocene,it is conceivablethatAndean
in Macaronesia, Africa, and Madagascar. Any orogenydividedtheancestralrange.Further, since
trans-Atlantic disjunctionproducedbyWestGond- lowlandgeneraof the Ocoteacomplexplace in ei-
wanan vicariancewas discounted(above) and in- ther South- or CentralAmerica-centered clades
stead the disjunctiondates to aroundthe Oligo- (Fig. 4), Andean orogenyappears to maintainge-
cene-Mioceneboundary, ca. 23 ? 5 Mya (node e nericendemismwhileallowinglowermontaneCin-
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-centered clades range
the Ocotea compleximplies an originconcurrent throughout CentralAmericawithwidespreadspe-
withthe southward movement of megathermal for- 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
positionrelativeto the previousclades indicates Nectandracoriaceaspecies group(Fig.4). Although
boreotropical ancestry.Unlike previousLaurasian thesemaybe secondaryrangeexpansionsofindig-
taxa,the Ocoteacomplexis absentin Asia. While enous Southand CentralAmericantaxa (e.g.,Roh-
Persea and Cinnamomum groupsappear as lower wer& Kubitzki,1993), theyindicatetheunderlying
montane taxain theNeotropics, theOcoteacomplex complexity ofbiogeographic patterns.
is especiallydiversein thelowlandsofSouthAmer- The biogeographic historyofLauraceae outlined
ica. Giventhese differences in distribution and a heresharesmuchwiththatproposedby Doyleand
relativelyrecenttrans-Atlantic disjunction,their Le Thomas(1997) forAnnonaceae.As in thatdi-
biogeographic historymaybe quite different from versemagnoliidfamily, threemainphases are rec-
thatofthe otherboreotropical lineages.In thisre- ognizable.Early radiationof bothfamiliesappar-
gard xeric tolerancesshown by AfricanOcotea, entlyoccurredwhenmigration betweenGondwana
Californian Umbellularia,and theCentralAmerica- and Laurasia was possible. Next, diversification
centeredNectandracoriaceagroupmaybe signifi- throughoutthe Cretaceous produced lauraceous
cant.These taxa place basallyin thecomplex,and Cryptocaryeae, perhapsCassytha,and the Chloro-
theirsclerophyllous habit,unusual forLauraceae, cardium-Mezilaurus lade on Gondwana, with Car-
adds to taxa thatlink the Madrean-Tethyan scler- yodaphnopsis and its allies on Laurasia. In Annon-
ophyllousfloradiscussedby Axelrod(1975). This aceae, Anaxagoreaappearsto be thecounterpart of
broad-leavedflorarangedalong the Tethyancoast Caryodaphnopsis. In bothfamilies,renewedcontact
fromNorthAmericato southeastern Eurasia and betweenGondwananand Laurasian fragments in
NorthAfrica,and existedrelativelycontinuously theEarlyTertiary resultedin a secondradiationon
since theLate Eocene, onlydisruptedbyincreased Laurasianterrains.In Lauraceae,thisboreotropical
climaticcoolingand dryingat the end of the Oli- phase producedthe Perseeae-Laureae lade, but
gocene (Axelrod,1975). The 23 + 5 Myaestimate unlike Annonaceae,its descendantsdid not only
ofthetrans-Atlantic disjunction in theOcoteacom- recede to the Asian tropicswithclimaticcooling.
plex is consistentwiththatexpectedfortaxa with Three of the four major lineages of Lauraceae
ancestralMadrean-Tethyan ranges (e.g., Fritsch, evolved duringthis period,migratedto the Neo-
1996). Greatdisparityin species diversity on the tropics,and one ofthese,the Ocotea complex,un-
twosides of the Atlanticmaybe attributed to dis- derwenta majorradiationin the New World.This
proportionate opportunities forspeciationand dif- latterradiationhas fewparallelsin neotropical phy-
ferentiation. In the Neogene, continentalAfrica togeography. There are indicationsthatsome line-
moves progressively northwardinto a drier and ages in the Leguminosae(Lavin & Luckow,1993)
coolerclimate(Hallam,1994), whiletectonicuplift and Melastomataceae(Renner& Meyer,in press)
in the Panamanianisthmus(Pindell et al., 1988) are derived fromboreotropicalancestors, and
providesthe Madreanfloraof southeastern North Krutzsch (1989) listed possible examples from
Americawithopportunities forstepping-stone dis- Bombacaceae,Olacaceae, and Symplocaceae.The
persal intoSouthAmerica. emergingprospectof a largercontingent ofLaura-
SeparationoftheCentralAmerica-centered Oco- sian elementsin the lowlandNeotropicsthanpre-
tea helicterifoliaspecies groupfromits speciose viouslyrecognizedcan be assessed whenphyloge-
South America-centered sistergroup(Fig. 4) ap- nies of moretropicaltaxa becomeavailable.

132 Annals of the
OUTLOOK: TOWARD A PHYLOGENETIC cumscribedto accommodate just thePersea group,

ARRANGEMENT OF LAURACEAE and UmbellulariaremovedfromLaureae to Cin-
namomeae.The latteralso includes all remaining
The utilityof morphologicalclassificationthat genera of van der Werffand Richter'sPerseeae.
expresses evolutionaryhistoryand relationships Several smaller,althoughmorphologically distinc-
withsupportfrommoleculardata is obvious.For tive,taxa are notclearlyplaced, particularly in the
Lauraceae, appropriatecharactersto be employed case of Cassytha,to a lesser extentforCaryoda-
in such a scheme are elusive. Amongtraditional phnopsisand Neocinnamomum, and perhapsHy-
morphologicalcharacters,the numberof locules podaphnis.At a lowertaxonomiclevel, increased
per antherattainsgenericand even supra-generic samplingis necessaryfora thorough reconsidera-
importancein early schemes (Nees, 1836; Meis- tionof currentgenericconceptsamongLauraceae.
sner,1864; Bentham,1880; Pax, 1889; Mez, 1889; In this study,only the Ocotea complexhas been
Kostermans, 1957). Severalexamplesoftheweak- representatively sampled;seemingly naturalgroups
ness ofthischaracterhave been identified and are of genera and parts of largergenera have been
confirmedby the presentmoleculardata. Other identified withinthiscomplex.Similarly, increased
charactersdo notfaremuchbetter.The use ofum- samplingin othermain clades identified herewill
bellate involucrateinflorescences to circumscribe improveour understanding of relationships among
Laureae is a salientfeatureof mostclassification Lauraceae.
schemes (e.g., Rohwer,1993a; van der Werff&
Richter,1996), but this syndromeclearlyevolved LiteratureCited
independently in Umbellularia.Similarly,dioecy
appears threetimes on the phylogenyherein,in Asmussen,C. 1999. Towarda chloroplastDNA phylog-
enyof 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 biogeography of Mad-
stressesdegree of cupule development,but both rean-Tethyan vegetation.
sclerophyll Ann.MissouriBot.
extremesare foundin Cryptocaryeae, and thenon- Gard.62: 280-334.
& P. Raven. 1978. Late Cretaceousand Tertiary
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thereinreappearsin the distantlyrelatedPersea (editor),Biogeography and Ecologyof SouthernAfrica.
group.Equally problematical, morphological syna- Junk,The Hague.
pomorphies are notreadilynotedforseveralclades Bambacioni-Mezzetti, V. 1941. Ricerche morfologiche
thatreceivestrongmolecularsupport.In the case sulle Lauracee,embriologia della Umbellularia califor-
nica Nutt.e del Laurus canariensisWebb. Ann. Bot.
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tractioncan be held responsible,but on closerex- Benthain,G. 1880. Laurinae.Pp. 146-165. in G. Ben-
aminationgeneraofthe Chlorocardium-Mezilaurus tham& J. Hooker (editors),Genera Plantarum3. L.
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terpretation,a consensusovermajorgenericgroup- Boufford, D. & J. Spongberg.1983. EasternAsian-east-
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A historyfromthe timeof Linnaeus to the twentieth
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consensus concerns a large lade comprisedof and south-western Pacificcontinentalterranesderived
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Phylogeny and Historical Biogeography of Lauraceae: Evidence from the Chloroplast and

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I The authorsthankanonymous forinsightful

ANN. MISSOURI BOT. GARD. 88: 104-134. 2001.

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Actinodaphneand Neolitsea). Cryptocaryeaein- lowedthatPerseawas an "old Laurasiangenus"but

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term. Galheiro (MO)

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DMSO was added and the PCR protocoldescribed

annuusL. depositedin Genbank(X60428). The 5'

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consensussequences generatedusing Sequencher werecalculatedforthe ITS data set usinglog de-

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branchesin Lauraceae withverylittleand oftenno lade is essentiallyunresolvedbut thereis some

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psbA-trnH cpDNA Ocotea puldhella

Ocoteatomentella Ocotea complex

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76 76 Ocotea MA IOcotea complex a)

psbA-trnH Persea americanaCA |Persea group 0-

trnT-trnL 100 AnaueriabrasiliensisSA

980 100 CaryodaphnopsisbiocellataAS E

100 100 Potameiamicrantha

Hypodaphnis zenkeri AF | Ovary inferior | Hypodaphnis

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land of 567 equal lengthtrees (L = 1050, CI = existsamongmembers

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ITS 99 Ocotea nigra

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Figure5. Phylograms showingclock enforcedHKY-F distanceson reducedparsimony-based topologiesdepicting

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Table 3. Clock enforcedHKY-F, distancesaccumu- carya, Endiandra, Eusideroxylon, Potameia, and

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Cassytha, Caryodaphnopsis,and Neocinnamo- that can mislead phylogeneticestimates(Felsen-

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UnlikemostotherLauraceae withterminally clus- relationshiphas never been formallyrecognized.

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plex is restrictedto the New Worldand accounts bitzki,1993). A relatively

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paraphyleticassemblage withinwhich Rhodoste- Ocotea insularis(Meisn.) Mez and Aiouea costari-

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theOcoteacomplex)at 354 Mya (node a in Fig. 5a BASAL LINEAGES

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Alternatively, the northern routeof the Perseeae- gestthatitsAsian and Americanmembersdiverged

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OUTLOOK: TOWARD A PHYLOGENETIC cumscribedto accommodate just thePersea group,

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