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Phylogeny and Historical Biogeography of Lauraceae

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Phylogeny and Historical Biogeography of Lauraceae PHYLOGENY Andre'S. Chanderbali,2'3Henk van der AND HISTORICAL Werff,3 and Susanne S. Renner3 BIOGEOGRAPHY OF LAURACEAE: EVIDENCE FROM THE CHLOROPLAST AND NUCLEAR GENOMES1 ABSTRACT Phylogenetic relationships among 122 species of Lauraceae representing 44 of the 55 currentlyrecognized genera are inferredfrom sequence variation in the chloroplast and nuclear genomes. The trnL-trnF,trnT-trnL, psbA-trnH, and rpll6 regions of cpDNA, and the 5' end of 26S rDNA resolved major lineages, while the ITS/5.8S region of rDNA resolved a large terminal lade. The phylogenetic estimate is used to assess morphology-based views of relationships and, with a temporal dimension added, to reconstructthe biogeographic historyof the family.Results suggest Lauraceae radiated when trans-Tethyeanmigration was relatively easy, and 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 representationprimarily derived 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 throughouttropical to subtropicallatitudes. Given their antiquity, widespread distribution, They are among the more speciose basal angio- and ecological prominence, Lauraceae provide a spermfamilies and have a fossilrecord that reaches model system for investigating angiosperm bioge- back to the Mid-Cretaceous(Drinnan et al., 1990; ography. Moreover, the three tribes recognized by Eklund & Kvacek, 1998). Currenttaxonomic di- van der Werffand Richter (1996) suggest thatmajor versityis centeredin tropicalAmerica and Aus- divisions in the familydraw along geographic lines. tralasia,and althoughpoorly represented in conti- Laureae include three genera with North Ameri- nentalAfrica, Lauraceae flourishin Madagascar.In can-Asian disjunctions (Litsea, Lindera, Sassafras), the Americantropics they list among the most Mediterranean Laurus, and Asian endemics (e.g., I The authorsthank anonymous reviewers for insightful comments; K. Ueda foreight unpublished trnL-trnF sequenc- es; J. Rohwerfor six unpublishedITS sequences; M. Zanis forfive at the timeunpublished ITS/5.8S/26S sequences; Y-L. Qiu forproviding three DNA aliquots;the HarvardHerbaria for providing leaf materialof Eusideroxylon; Andrea Schwarzbachfor guidance in moleculartechniques; and innumerablecolleagues who helped to collect materialof Lauraceae forthis study.This studywas undertakenas partof ASC's doctoraldissertation research at the University of Missouri-St.Louis, and was supportedby grantsfrom the MallinckrodtFoundation administered by theInternational Centerfor Tropical Ecology, University of Missouri-St. Louis, and fromthe Smithsonian Institution's Biological Diversity ofthe Guianas Program to ASC; NationalGeographic Society grants 4631-91, 5635-96,and 6571-99 to HW; and grants fromthe Universityof Missourisystem and Universityof Missouri-St.Louis to SSR. This articleis Number45 in the SmithsonianInstitution's Biological Diversity of the Guianas Publicationseries. 2Department of Biology,University of Missouri-St.Louis,8001 NaturalBridge Road, St. Louis, Missouri63121- 4499, U.S.A. 3Missouri BotanicalGarden, P.O. Box 299, St. Louis, Missouri63166, U.S.A. ANN. MISSOURI BOT. GARD. 88: 104-134. 2001. This content downloaded on Thu, 21 Feb 2013 09:43:34 AM All use subject to JSTOR Terms and Conditions Volume 88, Number1 Chanderbaliet al. 105 2001 Phylogenyand Biogeographyof Lauraceae Actinodaphneand Neolitsea). Cryptocaryeaein- lowedthat Persea was an "old Laurasiangenus" but clude pantropicalBeilschmiedia and Cryptocarya, suggestedthat subgenus Eriodaphne, like all other and other predominantlySouthern Hemispheric membersof the family,arrived in South America generawith narrower ranges (e.g., Endiandra and via Africa.Alternatively, Taylor (1988) suggested Potameia).Perseeae are centeredin theNeotropics that the fossil flowerAndroglandula tennessensis withthree widespread genera. Cinnamomum is dis- Taylor,from the Eocene of NorthAmerica, is com- junct between the American and Asian parable to Cinnamomum,Ocotea, and Nectandra, (sub)tropics;Persea (includingMachilus) ranges indicatinga boreotropicalhistory for this groupof throughoutthe Neotropics(into the southeastern genera,with subsequent migration to SouthAmer- U.S.), theCanary Islands, and Asia; and Ocoteahas ica. Raven and Axelrod(1974) and Taylor(1988) about300 neotropicalspecies, one in Macaronesia, allowed thatalthough differing in the directionof a fewin Africa,and about30 morein Madagascar. migration,the high level of species diversityand Apartfrom a fewAsian genera(e.g., Dehaasia and genericendemism require a Late Cretaceous-Early Phoebe) consideredclosely related to Persea, all Tertiaryarrival in SouthAmerica. In contrast,Roh- othergenera of Perseeae are endemicto the Neo- wer and Kubitzki(1993) preferreda morerecent tropics(e.g., Aiouea, Aniba, Endlicheria,Licaria, arrivalof this group,possibly as late as the Plio- Nectandra,Pleurothyrium, and Rhodostemonoda- cene closureof the PanamanianIsthmus, followed phne). The distributionsof Laureae and Cryptocar- by rapid radiationin SouthAmerica. yeae are consistentwith Laurasian and Gondwanan These alternativeviews are here assessed by histories,respectively, but thatof Perseeae is am- addinga temporaldimension to a phylogenetices- biguous in this regard.The trans-Atlanticdistri- timatefor Lauraceae reconstructedwith molecular butionof Ocoteasuggests West Gondwanan history, charactersretrieved from both chloroplast and nu- but the tropicalamphi-Pacific distributions of Cin- clear genomes. namomumand Persea suggestLaurasian affinities. Whetheror not these ambiguitiesare artifactsof MATERIALS AND METHODS tribaland/or generic circumscription is unclear. The systematicsof Lauraceae is unsettled.Lau- TAXON AND MOLECULAR SAMPLING reae are recognizedin most priorclassifications, A total of 131 species, 122 representing44 of but othertribal concepts are not widelyaccepted. the 55 currentlyrecognized genera of Lauraceae, Van der Werffand Richter's(1996) Cryptocaryeae and 9 representing3 outgroupfamilies (Gomorte- and Perseeae are revised concepts supportedby gaceae, Hernandiaceae,and Monimiaceae)were in- Richter's(1981) studyof wood and bark anatomy. cluded in this study.Seventy-seven in-group spe- Some aspects of Cryptocaryeaegain supportfrom cies wereincluded in a broad-scalestudy based on embryology(Heo et al., 1998), but charactersfor sequence variationin the trnL-trnFand psbA-trnH furthersubdivision of the family were not found. A intergenicspacers of cpDNA. Guided by the find- cladisticanalysis of molecular data (Rohwer,2000) ings of this molecularand taxonsampling a two- also providedsupport for Cryptocaryeae and united tieredapproach was adoptedto obtainbetter rep- Perseeae and Laureae in a well-supportedbut un- resentationand phylogeneticresolution at the resolved lade. This Perseeae-Laureae lade ac- genericlevel. Thus a subset of the species repre- commodatesmost of the family, and its distribution sentingbasal lineages in Lauraceae was also se- implies a disjunctionbetween the Americanand quenced forthe trnT-trnL spacer, and therpll6 in- Asian tropicswith a minorAfrican presence. Such tronof cpDNA, as well as the 5' end of26S rDNA, distributionscan be creditedto extinctionof Gond- while 94 species representingPerseeae, Laureae, wanan lineages in Africa(e.g., Raven & Axelrod, and theirsister group were sampled forthe ITS/ 1974), butLaurasian ancestry followed by radiation 5.8S regionof nrDNA.Table 1 providesGenBank in tropicalAsia and Americawas favoredby Roh- informationfor all accessions. wer(2000). TropicalAsia is acknowledgedas a har- bor for Laurasian relicts (e.g., Wolfe,1975), but DNA EXTRACTION, PCR AMPLIFICATION, AND Rohwer'shypothesis that the approximately800 SEQUENCING neotropicalspecies of Perseeae are derivedfrom Laurasianimmigrants contrasts with the Gondwan- Total DNA was obtainedfrom silica-gel-dried, an origincredited to mostmajor neotropical plant herbarium,or freshleaves usingDneasy (QIAGEN) groups(e.g., Raven & Axelrod,1974; Gentry,1982; extractionkits. PCR amplificationof
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