Molecular Ecology (2003) 12 , 1451–1460 doi: 10.1046/j.1365-294X.2003.01810.x© 2003 Blackwell Publishing Ltd Blackwell Publishing Ltd. Chloroplast DNA phylogeography reveals colonization history of a Neotropical tree, Cedrela odorata L., in Mesoamerica S. CAVERS, * C. NAVARRO † and A. J. LOWE * * Centre for Ecology and Hydrology-Edinburgh, Bush Estate, Penicuik, Midlothian EH26 0QB, UK, † Centro Agrónomico Tropical de Investigación y Enseñanza, Cartago, Turrialba 7170, Costa Rica AbstractSpanish Cedar ( Cedrela odorata L.) is a globally important timber species which has beenseverely exploited in Mesoamerica for over 200 years. Using polymerase chain reaction–restriction fragment length polymorphisms, its chloroplast (cp) DNA phylogeography wasstudied in Mesoamerica with samples from 29 populations in six countries. Five haplotypeswere characterized, phylogenetically grouped into three lineages (Northern, Central andSouthern). Spatial analysis of ordered genetic distance confirmed deviation from a patternof isolation by distance. The geographically proximate Northern and Central cpDNAlineages were genetically the most differentiated, with the Southern lineage appearingbetween them on a minimum spanning tree. However, populations possessing Southernlineage haplotypes occupy distinct moist habitats, in contrast to populations possessingNorthern and Central lineage haplotypes which occupy drier and more seasonal habitats.Given the known colonization of the proto-Mesoamerican peninsula by South Americanflora and fauna prior to the formation of the Isthmus of Panama, it seems most likely thatthe observed population structure in C. odorata results from repeated colonization ofMesoamerica from South American source populations. Such a model would imply anancient, pre-Isthmian colonization of a dry-adapted type (possessing the Northern lineageor a prototype thereof), with a secondary colonization via the land bridge. Following this,a more recent (possibly post-Pleistocene) expansion of moist-adapted types possessing theSouthern lineage from the south fits the known vegetation history of the region. Keywords : Cedrela odorata , differentiation, dispersal, Meliaceae, Spanish Cedar, universal cpDNAmarkers Received 19 December 2002; revision received 13 January 2003; accepted 13 January 2003 Introduction Phylogeography examines the correspondence betweengenetic relationships and geographical distribution (Avise et al . 1987). Population genetic structure is as much aproduct of history as of present-day migration patternsand isolation of populations, hence a synthesis of gene-alogical data with independent information, includinggeology, palynology and archaeology (Avise et al . 1987;Bermingham & Moritz 1998) may disentangle the histor-ical component of population structure from that which isthe result of contemporary gene flow processes.In plants, the recent development of universal primersets targeting noncoding regions of the chloroplast(cp) genome (Taberlet et al . 1991; Demesure et al . 1995;Dumolin-Lapegue et al . 1997b; Hamilton 1999) has revealedsubstantial amounts of intraspecific variation (Newton et al .1999a), and cpDNA data have now been successfully usedfor several phylogeographic studies of plants (Petit et al .1993; Petit et al . 1997; Caron et al . 2000; Dutech et al . 2000;Raspe et al . 2000). As a result of its usual maternal inherit-ance in angiosperms, cpDNA is transmitted only throughseeds, and therefore has less potential for gene flow thannuclear genes, which can also move by pollen dispersal.Consequently, genetic variation in the chloroplast genomeis often more highly geographically structured than thatin the nuclear genome. Furthermore, as the rate of cpDNA Correspondence: S. Cavers. Fax: 0131 4453943; E-mail: [email protected] S. CAVERS, C. NAVARRO and A. J. LOWE © 2003 Blackwell Publishing Ltd, Molecular Ecology , 12, 1451–1460 sequence evolution is slow (Wolfe et al . 1987), observedpatterns reflect the outcome of processes over long time-scales (Ennos et al . 1999) so cpDNA is ideal for studyinghistorical patterns of gene flow, in particular migrationand colonization.Several recent studies have taken advantage of thesecharacteristics to investigate vegetation changes, in par-ticular those related to glacial cycles. In Europe ( Alnus glu-tinosa , King & Ferris 1998; Quercus sp., Dumolin-Lapegue et al . 1997a), North America ( Dryas integrifolia , Tremblay& Schoen 1999; Liriodendron tulipifera , Sewell et al . 1996)and the tropics ( Vouacapoua americana , Dutech et al . 2000; Dicorynia guianensis , Caron et al . 2000), cpDNA has beensuccessfully used to detect spatiotemporal patterns offragmentation and dispersal resulting from climatic vari-ations during the Pleistocene epoch.The region of interest in this study is tropical Mesoamericabetween southern Mexico and northern Colombia, encom-passing Guatemala, Honduras, Nicaragua, Costa Ricaand Panama. Present day Mesoamerica is a region richin diversity: there are still more than a quarter of a millionsquare kilometres of primary vegetation, around 24 000plant species (of which some 5000 are endemic) and nearly3000 vertebrate species (of which over 1000 are endemic,Myers et al . 2000).The distribution and composition of the Mesoamericanflora and fauna have been strongly influenced by geo-logical and climatic events (Burnham & Graham 1999).Prior to the formation of the Isthmus of Panama, there wasconsiderable interchange of flora between the separateland masses of North and South America (Raven & Axelrod1974), possibly via an island chain. At this time, populationswould have been isolated in the proto-Mesoamericanpeninsula, by the sea to the south and by the more tem-perate climate to the north (Savage 1982). Following theformation of the Panamanian land link [between 5and 3 million years ago (Ma), Coney 1982] the GreatAmerican Interchange resulted in numerous invasionsof Mesoamerica by South American angiosperm flora(Burnham & Graham 1999). Later, the climatic fluctu-ations of the Pleistocene (1.6–0.01 Ma) had a substantialinfluence on the Mesoamerican flora (Prance 1982a,b;Toledo 1982). Major fragmentation of the extensive tro-pical forest took place (Toledo 1982; Leyden 1984; Islebe &Hooghiemstra 1997; Williams et al . 1998; Hewitt 2000),with many species restricted to refuge populations in theregion of present day Guatemala and northwest Colombiaduring glacial
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