Chloroplast dna phylogeography reveals colonisation history of a Neotropical tree, Cedrela odorata L., in Mesoamerica. Cavers S1,3, Navarro C2 and Lowe aj1




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Chloroplast DNA phylogeography reveals colonisation history of a Neotropical tree, Cedrela odorata L., in Mesoamerica.
Cavers S1,3, Navarro C2 and Lowe AJ1.

1 Centre for Ecology and Hydrology-Edinburgh, Bush Estate, Penicuik, Midlothian EH26 0QB, Scotland, UK
2 Centro Agrónomico Tropical de Investigación y Enseñanza, Cartago, Turrialba 7170, Costa Rica
3 To whom correspondence should be addressed. Centre for Ecology and Hydrology, Edinburgh, Bush Estate, Penicuik, Midlothian EH26 0QB, Scotland, UK,
Tel. 0131 445 4343, Fax. 0131 445 3943, Email scav@ceh.ac.uk

Key words: Spanish Cedar, Meliaceae, universal cpDNA markers, dispersal, differentiation, Cedrela odorata.
Short running title: Phylogeography of Cedrela odorata
Date Submitted: 19/12/02

Date Accepted:

Abstract

Spanish Cedar, (Cedrela odorata L.) is a globally important timber species which has been severely exploited in Mesoamerica for over 200 years. Using PCR-RFLP, its chloroplast (cp) DNA phylogeography was studied in Central America with samples from 29 populations in six countries. Five haplotypes were characterised, phylogenetically grouped into three lineages (Northern, Central and Southern). Spatial analysis of ordered genetic distance confirmed deviation from a pattern of isolation by distance. The geographically proximate Northern and Central cpDNA lineages were genetically the most differentiated, with the Southern lineage between them on a minimum spanning tree. However populations possessing Southern lineage haplotypes occupy distinct moist habitat, in contrast to populations possessing Northern and Central lineage haplotypes which occupy drier and more seasonal habitat. Given the known colonisation of the proto-Mesoamerican peninsula by South American flora and fauna prior to the formation of the Isthmus of Panama, it seems most likely that the observed population structure in C. odorata results from repeated colonisation of Mesoamerica from South American source populations. Such a model would imply an ancient, pre-Isthmian colonisation of a dry-adapted type (possessing the Northern lineage or a prototype thereof), with a secondary colonisation via the land bridge. Following this, a more recent (possibly post-Pleistocene) expansion of moist-adapted types possessing the Southern lineage from the south fits the known vegetation history of the region.



Introduction.

Phylogeography examines the correspondence between genetic relationships and geographic distribution (Avise et al. 1987). Population genetic structure is as much a product of history as of present-day migration patterns and isolation of populations, hence a synthesis of genealogical data with independent information, including geology, palynology and archaeology (Avise et al. 1987; Bermingham & Moritz 1998) may disentangle the historical component of population structure from that due to contemporary gene flow processes.
In plants, the recent development of universal primer sets targeting non-coding regions of the chloroplast (cp) genome (Taberlet et al. 1991; Demesure et al. 1995; Dumolin-Lapegue et al. 1997b; Hamilton 1999) has revealed substantial amounts of intraspecific variation (Newton et al. 1999), and cpDNA data has now been successfully used for 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). Due to its usual maternal inheritance in Angiosperms, cpDNA is transmitted only through seeds, and therefore has less potential for gene flow than nuclear genes, which can also move by pollen dispersal. Consequently, genetic variation in the chloroplast genome is often more highly geographically structured than that in the nuclear genome. Furthermore, as the rate of cpDNA sequence evolution is slow (Wolfe et al. 1987), observed patterns reflect the outcome of processes over long timescales (Ennos et al. 1999) so cpDNA is ideal for studying historical patterns of gene flow, in particular migration and colonisation.
Several recent studies have taken advantage of these characteristics to investigate vegetation changes, in particular those related to glacial cycles. In Europe (Alnus glutinosa, 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 been successfully used to detect spatiotemporal patterns of fragmentation and dispersal resulting from climatic variations during the Pleistocene epoch.
The region of interest in this study is tropical Mesoamerica between southern Mexico and northern Colombia, encompassing Guatemala, Honduras, Nicaragua, Costa Rica and Panama. Present day Mesoamerica is a region rich in diversity: there are still more than a quarter of a million square kilometres of primary vegetation, around 24,000 plant species (of which some 5000 are endemic) and nearly 3000 vertebrate species (of which over 1000 are endemic, Myers et al. 2000).
The distribution and composition of the Mesoamerican flora and fauna has been strongly influenced by geological and climatic events (Burnham & Graham 1999). Prior to the formation of the Isthmus of Panama, there was considerable interchange of flora between the separate land masses of North and South America (Raven & Axelrod 1974), possibly via an island chain. At this time populations would have been isolated in the proto-Mesoamerican peninsula, by the sea to the south and by the more temperate climate to the north (Savage 1982). Following the formation of the Panamanian land link (between 5 and 3 Mya, Coney 1982) the Great American Interchange resulted in numerous invasions of Mesoamerica by South American Angiosperm flora (Burnham & Graham 1999). Later, the climatic fluctuations of the Pleistocene (1.6-0.01 Mya) had a substantial influence on the Mesoamerican flora (Prance 1982a,b; Toledo 1982). Major fragmentation of the extensive tropical forest took place (Toledo 1982; Leyden 1984; Islebe & Hooghiemstra 1997; Williams et al. 1998; Hewitt 2000), with many species restricted to refugial populations in the region of present day Guatemala and northwest Colombia during glacial maxima. In general, for many plant and animal species of Mesoamerica, distinct biogeographic patterns remain, reflecting the significant influence of dispersal and isolation, extinction and colonisation on the populations of this dynamic and diverse region (Savage 1982; Bermingham & Martin 1998; Burnham & Graham 1999).
Spanish Cedar (C. odorata) is a neotropical member of the hardwood family Meliaceae (Swietenioideae), well known for high quality and value timber. The species (and family) has a long history of human exploitation and is still a valuable commodity, used in furniture making and construction (Lamb 1968, Rodan et al. 1992, Valera 1997). C. odorata is naturally distributed from the Mexican Pacific coast at 26°N and the Mexican Atlantic coast at 24°N, throughout the Caribbean islands, the Yucatan and lowland Central and South America to northern Argentina at 28°S. The tree is deciduous and grows in both dry and moist lowland areas where soils are not flooded, up to around 1200 m altitude. It is a fast growing, light-demanding species (Lamb 1968; Chaplin 1980; Valera 1997) reaching 40 m in height and 120 cm diameter. As with other Meliaceae, the species is monoecious (flowers are unisexual, Pennington et al. 1981, and pollinated by small bees, wasps and moths, Bawa 1985; Navarro et al. 2002). Flowering occurs annually in 10-15 year old trees, and a good seed crop is produced every 1-2 years (ICRAF Agroforestree database http://www.icraf.cgiar.org/). Seed is wind dispersed.
The value of C. odorata has resulted in over-exploitation of the species in its natural habitat for two centuries. A number of studies have been carried out on the species within Costa Rica, focussing on its known intraspecific variation, manifest primarily as tolerance for both dry and moist habitat. Common garden experiments have indicated that this environmental ‘tolerance’ has a genetic basis and that ecotypic differentiation has occurred within the species. For example, apical dominance experiments (Newton et al. 1995), Hypsipylla grandella resistance trials (Newton et al. 1999) and morphological studies (Navarro et al. 2002) all identify two distinct groups within Costa Rica that are correlated with habitat. RAPD analysis of Costa Rican populations (Gillies et al. 1997) showed differentiation between these ecotypes for neutral loci. To date, there has been no large-scale molecular study of C. odorata and the extent of intraspecific variation in the Mesoamerican population is unknown. Given the threat posed to the species by unsustainable logging practices and habitat loss, and evidence indicating significant population structuring, there is a clear need to assess the current levels and distribution of diversity in the Mesoamerican population.
This study investigates the phylogeographic structure of the Mesoamerican population of C. odorata. Universal chloroplast markers are employed to identify patterns of population structure that reflect the seed dispersal history of the species, assuming maternal inheritance of the chloroplast. The results are interpreted in the light of the known geological and climatic history of the Mesoamerican Isthmus to infer colonisation dynamics of C. odorata.

Methods

Samples were collected from a total of 580 C. odorata individuals in 29 populations throughout Central America (Fig. 1 & Table 1). Populations were defined as groups of trees at least 100 m apart but within a coherent geographic area, such that they are in potential reproductive contact. Twenty trees were sampled per population. Four populations were sampled from each of Mexico, Guatemala, Honduras and Nicaragua. Three populations were sampled from Panama and ten from Costa Rica. Individuals were sampled by collecting either leaf tissue (dried on silica gel) or cambium tissue (immersed in 70:30, Ethanol:CTAB buffer containing 100 mM Tris-HCl pH 8.0, 20 mM EDTA, 1.4 M NaCl, 1% PVP-40T, 2% CTAB). Genomic DNA was extracted using a modified CTAB protocol (Gillies et al. 1997).


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