REPORTS 19 R S Defries M C Hanson J R G Townshend R Sholberg Int J Remote Sens 19 3141 1998 20 S D Prince S N Goward J Biogeogr 22 815 1995 21 M A White P E Thornton S W Running R R Nemani Earth Interactions 4 1 2000 22 L Zhou et al J Geophys Res Atmos 106 20069 2001 23 M E James S N V Kalluri Int J Remote Sens 15 3347 1994 24 C D Keeling et al S I O Reference Series No 00 21 Scripps Institution of Oceanography University of California San Diego 2001 25 D J Barrett Global Biogeochem Cycles 16 10 1029 2002GB0011860 2002 26 L Gu et al Science 299 2035 2003 27 P S Curtis X Wang Oecologia 113 299 1998 28 S M Fan S C Wofsy P S Bakwin D J Jacob D R Fitziarrald J Geophys Res 95 16851 1990 29 E A Graham S S Mulkey K Kitajima N G Phillips S J Wright Proc Natl Acad Sci U S A 100 572 2003 30 M H Costa J A Foley J Geophys Res 104 14189 1999 31 K Wolter M S Timlin Weather 53 315 1998 32 We thank the reviewers and A Keyser for helpful comments This work was supported by grants from the NASA Earth Science Enterprise and Intelligent Data Understanding program to R R N S W R R B M Glacial Refugia Hotspots But Not Melting Pots of Genetic Diversity Re my J Petit 1 Itziar Aguinagalde 2 Jacques Louis de Beaulieu 3 Christiane Bittkau 4 Simon Brewer 3 Rachid Cheddadi 3 Richard Ennos 5 Silvia Fineschi 6 Delphine Grivet 1 Martin Lascoux 7 Aparajita Mohanty 2 Gerhard Mu ller Starck 4 Brigitte Demesure Musch 8 Anna Palme 7 Juan Pedro Mart n 2 Sarah Rendell 5 Giovanni G Vendramin9 Glacial refuge areas are expected to harbor a large fraction of the intraspeci c biodiversity of the temperate biota To test this hypothesis we studied chloroplast DNA variation in 22 widespread European trees and shrubs sampled in the same forests Most species had genetically divergent populations in Mediterranean regions especially those with low seed dispersal abilities However the genetically most diverse populations were not located in the south but at intermediate latitudes a likely consequence of the admixture of divergent lineages colonizing the continent from separate refugia During the long glacial episodes of the Quaternary European forests were considerably more restricted than in the present intergla1 Institut National de la Recherche Agronomique UMR Biodiversite Ge nes et Ecosyste mes F 33612 Cestas France 2Departamento Biolog a Vegetal Escuela Te cnica Superior de Ingenieros Agro nomos Universidad Polite cnica de Madrid E 28040 Madrid Spain 3Institut Me diterrane en d Ecologie et de Pale oe cologie Faculte de St Je ro me F 13397 Marseille France 4Technische Universita t Mu nchen Fachgebiet Forstgenetik D 85354 Freising Germany 5Institute of Ecology and Resource Management University of Edinburgh Edinburgh EH9 3JU Scotland UK 6CNR Istituto di Biologia Agroambientale e Forestale I 05010 Porano TR Italy 7Department of Conservation Biology and Genetics Evolutionary Biology Centre Uppsala University 75236 Uppsala Sweden 8Of ce National des Fore ts De partement des Recherches Techniques Conservatoire Ge ne tique des Arbres Forestiers F 45160 Ardon France 9CNR Istituto di Genetica Vegetale Sezione di Firenze I 50134 Firenze Italy To whom correspondence should be addressed Email petit pierroton inra fr Present address Institut fu r Spezielle Botanik und Botanischer Garten Johannes Gutenberg Universita t Mainz D 55099 Mainz Germany Present address CEREGE Europo le Me diterrane en de l Arbois F 13545 Aix en Provence France Present address University of California Los Angeles Organismic Biology Ecology and Evolution Los Angeles CA 90024 USA Present address International Centre for Genetic Engineering and Biotechnology Aruna Asaf Ali Marg New Delhi 110067 India Present address Department of Plant Sciences University of Oxford Oxford OX1 3RB UK cial because the Mediterranean Sea in the south and unsuitable environment in the north restricted temperate tree and shrub taxa to the Iberian Italian and Balkan peninsulas For instance at the time of the last glacial maximum 25 000 to 17 000 years ago networks of fossil pollen data and macrofossil remains such as charcoals indicate that several tree species were localized in small favorable spots within the Mediterranean region but also at the southern edge of the cold and dry steppe tundra area in eastern central and southwestern Europe 1 5 After climate warming some of these surviving populations expanded whereas others remained trapped and either became extinct or persisted by shifting altitude 2 6 As a consequence of prolonged isolation extant tree populations situated close to refugia should be highly divergent especially if they were not the source of the expansion Another related prediction is that intraspecific diversity should decline away from refugia as a consequence of successive founder events during postglacial colonization 7 8 However species attributes such as colonizing ability may alter these predictions 9 Furthermore the individualistic migration behavior of tree species during interglacial periods 6 9 and the presence of more northern refugia 4 5 may have blurred this pattern In Europe range wide genetic surveys of a few well investigated and C J T C D K and S C P received nancial support from NSF ATM 01 20527 the U S Department of Energy DE FG03 95ER62075 and NASA NAG511217 Supporting Online Material www sciencemag org cgi content full 300 5625 1560 DC1 Materials and Methods Figs S1 to S9 Tables S1 and S2 References 24 January 2003 accepted 29 April 2003 tree species have been performed 10 12 but it is difficult to generalize from these studies To get a broader picture and to test the previous predictions we gathered data from several woody angiosperm taxa across Europe using standardized sampling and molecular screening techniques Such knowledge on the genetic consequences of the recent history of woody plant species may be critical for the conservation and sustainable management of their genetic resources Plastids are generally maternally inherited in angiosperms and therefore moved by seeds only Because colonization of new habitats occurs through seeds chloroplast DNA cpDNA markers provide information on past changes in species distribution that is unaffected by subsequent pollen movements 13 We have investigated patterns of cpDNA diversity in 22 woody species These were sampled in the same 25 European forests selected on the basis of their high species richness and limited human influence table S1 About 10 individuals per species were sampled from each forest
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