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Wolter, M. S. Timlin, Weather 53, 315 (1998).32. We thank the reviewers and A. Keyser for helpfulcomments. This work was supported by grants fromthe NASA Earth Science Enterprise and IntelligentData Understanding program to R.R.N., S.W.R., R.B.M.,and C.J.T. C.D.K. and S.C.P. received financial supportfrom NSF (ATM-01-20527), the U.S. Department ofEnergy (DE-FG03-95ER62075), and NASA (NAG5-11217).Supporting Online Materialwww.sciencemag.org/cgi/content/full/300/5625/1560/DC1Materials and MethodsFigs. S1 to S9Tables S1 and S2References24 January 2003; accepted 29 April 2003Glacial Refugia: Hotspots But NotMelting Pots of Genetic DiversityRe´my J. Petit,1* Itziar Aguinagalde,2Jacques-Louis de Beaulieu,3Christiane Bittkau,4† Simon Brewer,3‡ Rachid Cheddadi,3Richard Ennos,5Silvia Fineschi,6Delphine Grivet,1§Martin Lascoux,7Aparajita Mohanty,2㛳 Gerhard Mu¨ller-Starck,4Brigitte Demesure-Musch,8Anna Palme´,7Juan Pedro Martı´n ,2Sarah Rendell,5¶ Giovanni G. Vendramin9Glacial refuge areas are expected to harbor a large fraction of the intraspecificbiodiversity of the temperate biota. To test this hypothesis, we studied chloroplastDNA variation in 22 widespread European trees and shrubs sampled in the sameforests. Most species had genetically divergent populations in Mediterranean re-gions, especially those with low seed dispersal abilities. However, the geneticallymost diverse populations were not located in the south but at intermediate lat-itudes, a likely consequence of the admixture of divergent lineages colonizing thecontinent from separate refugia.During the long glacial episodes of the Qua-ternary, European forests were considerablymore restricted than in the present intergla-cial, because the Mediterranean Sea in thesouth and unsuitable environment in the northrestricted temperate tree and shrub taxa to theIberian, Italian, and Balkan peninsulas. Forinstance, at the time of the last glacial max-imum, 25,000 to 17,000 years ago, networksof fossil pollen data and macrofossil remainssuch as charcoals indicate that several treespecies were localized in small favorablespots within the Mediterranean region butalso at the southern edge of the cold and drysteppe-tundra area in eastern, central, andsouthwestern Europe (1–5). After climatewarming, some of these surviving popula-tions expanded, whereas others remainedtrapped and either became extinct or persistedby shifting altitude (2, 6). As a consequenceof prolonged isolation, extant tree popula-tions situated close to refugia should be high-ly divergent, especially if they were not thesource of the expansion. Another related pre-diction is that intraspecific diversity shoulddecline away from refugia, as a consequenceof successive founder events during postgla-cial colonization (7, 8). However, speciesattributes such as colonizing ability may alterthese predictions (9). Furthermore, the indi-vidualistic migration behavior of tree speciesduring interglacial periods (6, 9) and the pres-ence of more northern refugia (4, 5) may haveblurred this pattern. In Europe, range-widegenetic surveys of a few well-investigatedtree species have been performed (10–12),but it is difficult to generalize from thesestudies. To get a broader picture and to testthe previous predictions, we gathered datafrom several woody angiosperm taxa acrossEurope using standardized sampling and mo-lecular screening techniques. Such knowl-edge on the genetic consequences of the re-cent history of woody plant species may becritical for the conservation and sustainablemanagement of their genetic resources.Plastids are generally maternally inheritedin angiosperms and, therefore, moved byseeds only. Because colonization of new hab-itats occurs through seeds, chloroplast DNA(cpDNA) markers provide information onpast changes in species distribution that isunaffected by subsequent pollen movements(13). We have investigated patterns of cp-DNA diversity in 22 woody species. Thesewere sampled in the same 25 European for-ests selected on the basis of their high speciesrichness and limited human influence (tableS1). About 10 individuals per species weresampled from each forest, following a stan-dard procedure (14 ). Polymorphisms weredetected by polymerase chain reaction (PCR)techniques (14 ) in all 22 species [4 to 50haplotypes per species, mean 16.9 (Table 1)].The degree of subdivision of cpDNA diver-sity (GST) was estimated for each species (15,16). This measure partly reflects the dispersalability of the species considered, althoughlong-term range fragmentation should alsoplay a role. Low GSTvalues (indicative ofhigh levels of gene flow through seeds) werefound in Salix and in Populus (0.09 to 0.11),characterized both by light, wind-dispersedcottony seeds. The species characterized byanimal-ingested seeds also tended to havebelow-average values. In contrast, specieswith animal-cached seeds (i.e., nuts) exhibit-ed higher than average values ( Table 1).To compare forests with each other, wecalculated the mean number of haplotypes andwithin-population gene diversity by averagingacross species in each forest (table S2). We alsocalculated a measure that expresses the averagegenetic divergence of the forest from all re-maining populations (17) (table S2). The high-est values were observed in Corsica, Italy, andthe Balkans, including Croatia and Romania,whereas average or below-average values were1Institut National de la Recherche Agronomique, UMRBiodiversite´, Ge´nes et Ecosyste´mes,
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