Seminar in Plant Systematics and Evolution
Seminar in Plant Systematics and Evolution BOTANY 940
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19 R S Defries M C Hanson J R G Townshend R Sholberg rm 1 Remote Sens 19 3141 1998 s o Prince 5 N Coward Biogeogr 22 815 1995 M A White P Thornton S W unning R R Nemani arm Interaction 4 1 2000 L Zhou etalj Geo Rer AmIOS 106 20069 2001 3 M E James S N V Kalluri Int 1 Remote Sens 15 3347 19 C D Keeling er al 50 Reference Series No 0021 Scripps Institution of Oceanography University of California San Diego 2001 D J Barrett Global Biogeochem Cycle 16 101029 20026130011860 2002 NNNNN a N xo N m 26 L Gu er al Science 299 2035 2003 27 P S Curtis X Wang OecoIogia 113 299 1998 y P S Bakwin D J Jacob D R Fiuiarraldj GeopIgr Res 95 16851 1990 E A Graham s s Mulkey K Kimjima N 0 Phillips s J Wright Proc Natl Acad Sci USA 100 572 2003 M H Costa J A Foley 1 Geophys Res 104 14189 1999 N to w o K Wolter M S Timlin Weather 53 315 1998 We thank the reviewers and A Ke ser for helpful comments This work was supported by grants from m ASA Earth Science Enterprise and Intelligent Data Understanding program to RRN SWR RBM 1010 10 Glacial Refugia Hotspots But Not Melting Pots of Genetic Diversity R my J Petit1 Itziar Aguinagalde2 JacquesLouis de Beaulieu3 Christiane Bittkau4T Simon Brewer3i Rachid Cheddadi3 Richard Ennos5 Silvia Fineschi6 Delphine Grivet1 Martin Lascoux7 Aparajita Mohanty2 Gerhard MijllerStarck4 Brigitte DemesureMusch8 Anna Palm 7 Juan Pedro Martin2 Sarah Rendell l Giovanni G Vendramin9 Glacial refuge areas are expected to harbor a large fraction of the intraspecific biodiversity of the temperate biota To test this hypothesis we studied chloroplast NA variation in 22 widespread European trees and shrubs sampled in the same gions especially those with low seed dispersal abilities However the genetically l mos iverse populations were not locate d in the south but at intermediate a itudes a likely consequence of the admixture of divergent lineages colonizing the continent from separate refugia During the long glacial episodes of the Qua temar European forests were considerably more restricted than in the present intergla 1Institut National de la Redlerdle Agronomique UMR Biodiversit G nes et Ecosyst mes F33612 Cestas France 2Departamento Biolog la Vegetal Escuela T c nica Superior de Ingenieros Agronomos Universidad Po lit cnica de Ma ri E28040 Madrid Spain 3Institut M diterran en d Ecologie et de Pal o cologie Facult de St Jerome F13397 Marseille France 4Technisd1e Uni versitat Miinchen Fachgebiet Forstgenetik D85354 Freising Germany 5Institute of Ecolog and Resource Management University of Edinburgh Edinburgh EH9 3JU Scotland UK 5CNR Istituto di Biologia groambi entale e Forestale 05010 PoranoTR Italy 7Depart m Conservatoire G n tique des Arbres Forestiers F45160 Ardon France 9CNR Istituto di Genetica Vegetale Sezione di Firenze 50134 Firenze Italy whom correspondence should be addressed E mail petit pierrotoninra TPresent address Institut fijr Spezielle Botanik und Botanischer Garten Johannes GutenbergUniversitat Mainz D55099 Mainz German Present address CEREGE Europ le M diterran en de l Arbois F13545 AixenProvence France Present address University of California Los Angeles Organismic Biology Ecology and Evolution Los An geles CA 90024 USA Present address International Centre for Genetic Engineering and Biotechnology Aruna Asaf Ali Marg New Delhi110067 India Present address Department of Plant Sciences Uni versity of Oxford Oxford OX1 3R5 UK www5ciencemagorg SCIENCE VOL 300 6JUNE 2003 cial because the Mediterranean Sea in the and unsuitable environment in the north restricted temperate tree and shrub taxa to the Iberian Italian and Balkan penirrsulas For instance at the time of the last glacial max imum 25000 to 17000 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 ste etundra area in eastern central and 175 A er climate warming some of these surviving popula tions expanded whereas others remained trapped and either became extinct or persisted by shi ing altitude 2 6 As a consequence of prolonged isolation extant tree popula tions situated close to refugia should be high ly divergent especially if they were not the source 0 the ex ansion Another related pre diction is that intraspecifrc diversity should decline away from refugia as a c m 3quot lt7 8 u u these predictions 9 Furthermore vidualistic migration behavior of tree species during interglacial periods 6 9 and the pres rthem refu urope ran ewrde genetic surveys of a few wellinvestigated R E P O R T S and CJT CDK and SCP received financial support S pa from NSF ATM701720527 the U tment of Energy DEVEGO3V95ER62075 and NASA NAcsr 11217 Supporting Online Material wwwsciencemagorgcgicontentfull30056251560 Materials and Methods Figs S1 to S9 Tables S1 and S2 References 24 January 2003 accepted 29 April 2003 s Europe using standardized sampling and lecular screening techniques Such lmowl edge on the genetic consequences of the re cent 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 ds only Because colonization of new hab itats occurs through s c DN P g unaffected by subsequent pollen movements 13 We have investigated patterns of cp ests selected on the basis of their high species richness and limited human in uence table 81 About 10 individuals per species were sampled from each forest following a stan d procedure I 4 Polymorphisms were The degree of sub sity GST was estimated for each species 15 16 This measure partly reflects the dispersal ability of the species considere although longterm range fragmentation should play a role Low GST va ues irrdrcatrve of high levels of gene flow through seeds were found in Salix and in Populus 009 to 011 characterized both by light winddispersed cottony seeds 39 animalingest belowaverage va ues n contr with anima cached seeds ie nuts e ibit ed higher than average values Table 1 To compare forests with each other we calculated the mean number of haplotypes and withinpopulation gene diversity by averaging across species in each forest mble 82 We also ca ated measure that expresses the average genetic divergence of the forest from all re mairring populations 1 7 mble 2 The high 0 Q e whereas average or belowaverage values were 1563 REPORTS found in tlne rest of Europe Fig l Pattems of diversity across forests were very different botln mean number of haplo s Fig 2 and gene diversity table S2 were higher in Central ranoe u em Germany and Slovakia whereas tlne southemr and northemmost popur lations generally had low or average diversity witln tlne exception of southwestem Sweden To assess tlne consistency of tlnese patterns gence as shown by tlne signi cant and positive ST and rD r G thuLz Cullumz Rubus or SuEx did not cone form well to this pattern Eor haplotype diversir fv nn rrlax nlM quot 39 case excluding Cmpimls bdulus for which Warm within population diversity was not detected each of me tive nearest foresLs was represented by connecn39ng lines wiun conn39nuous black lines 39 39 case Tab 39 39 39 39 39 39 dnnwd Iinp 39 39 39 hi h r man Fig1 39 39 39 39 Hiahnrmanaverage 39 39 39 39 39 39 prupururrarru e mean gray to er gray lines 39 The alu39urde is indioeted by gray shadings l39 n m ha 13mm ed 1 Dmbe increases from 500 m1000and gt1000 m Pastsea levels at21ka BP 18 Mc ka BP15 ka BP 13 VD 8quot V3 96 W m 5 5 Mc ka BP and 12 ka BP 10 Mc ka BP are indioated by black dotted lines 12 the woody flora from northern Europe exhibit ent pattern of divergence loc in soutlnem and central Italy Corsica and the Balkan peninsula but extending into northern Italy Cr 39 omania ie at relatively high latitudes This is in agreement with recent frndirrgs of tree remains slightly and diffuse populations of these species during ice ages 13720 H 2 39 39 Ie end as divergent as those from the other peninsulas asgfor Fig 1 Diversity is highest at relan39vely high lan39mdes norm of are unree European peninsulas may be due to any oftlne following causes First 39 parts of Europe and would be locamd further barrier to colonization atter the last iceage Europe resulting in lower divergence of the south Third for several species especially 39 Iberian populations Second the Iberian pean those that conform best to the overall patten of Spain western Erance Britain and Ireland were sula seems to have been ex sed to 39cularly divergence ie Amer s phtmms Cbin unimd by a land bridge during the postglacial severe climatic episodes ie arid and cold durr ms present distribution fossil pollen period due to lower sea levels Fig 1 As a ingtlne Quaternary 22 thereforethetemperate chNA 23 or other genetic data 24 suggest con uenceinsever species suchasQuzrcuS tree populations that survived throughout sucr that 39 39 39 in from or the 12 szzm 21 Fruxl39mls and Ikx Iberian cessive ice ages world be smaller than in other Balkans entered Iberia from the ncnh Ihis it 1554 6JUNE 2003 VOL 300 SCIENCE www3ciencemagnrg REPORTS Table 1 List and parameter values for the 22 species investigated The seed correlation between the pattern of divergence of a given species and the dispersal mode was defined as follows Ac animalcached Ail animalingest pattern of divergence for all species combined excluding that particular ed Wc cottony winddispersed Ww win ed winddispersed Way wind spe ies whereas rH corresponds to the same correlation for allelic richness dispersed and animalingested Ed explosive dehiscence rD measures the asterisk indicates P lt 005 Nc not computed Total no of Species Family Seed dispersal mode No of populations haplotypes CrST rD rH Acer campestre Aceraceae Ww 16 14 071 065 007 Acer pseudoplatanus Aceraceae Ww 19 22 0 66 0 62 0 60 Alnus glu in sa Betulaceae Ww 25 12 081 0 62 0 26 Betula pendula Betulaceae Ww 23 9 0 42 0 02 0 48 Calluna vulgaris Ericaceae a 17 12 0 59 0 22 0 39 Carpmus betulus Betulaceae Ww 18 4 1 00 081 Corylus avellana Betulaceae Ac 24 5 0 89 073 0 66 Crataegus monogyna Rosaceae i 21 4 024 014 0 76 Cytisus scoparius Fabaceae Ed 18 24 057 054 0 61 Fagus sylvatica Fagaceae Ac 23 6 0 74 070 0 07 Fraxinus sp Oleaceae Ww 24 7 086 008 041 Hedera sp Arali Ai 22 11 057 021 058 Ilex aquifolium Aquifoliaceae Ai 16 8 0 60 018 0 47 Populus tremula Salicaceae Wc 23 30 011 047 054 Prunus avium Rosaceae Ai 23 16 029 078 042 Prunus spinosa Rosaceae Ai 25 50 032 044 0 57 Que Fagaceae Ac 25 10 084 040 0 31 Rubus sp Rosaceae Ai 23 15 0 31 004 0 34 Salix caprea Salicaceae Wc 25 29 009 01 6 001 Sorbus torminalis Rosaceae Ai 17 26 033 011 0 69 Tilia cordata Tiliaceae Ww 16 16 0 57 045 0 66 Ulmaceae Ww 25 41 047 034 010 Mean 213 169 054 036 042 would also reduce the genetic divergence of sic withinpopulation diversity 27 the genetic iquot 9 CaSeSr demonstrating the EXiStence 0f 3 Phylor northern Iberian populations uniqueness of southeastern European popula geographic mumquot for 3 5PM 7939 17 A strong overall pattern of isolationrbyrdistance was The strikingly different pattern of intiapopu tions should largely outweigh their low diversity detected through regression analysis of Pairwise lation diversity which peaks north of the main for longterm conservation purposes measures of N3 a ainst distances in kilometers To mountain ranges ratherthan south of them may s 39 the importance of gla ma Teas Showmg intrinsmllx high PW Wequot gence independently of the particular distribution of be due to one of the followmg causes First the c1al relict forest tree populations but warns the Populations sampled we used a distancerfree mixing of colonization routes and the subse agairis simple genetic criteria to identify estimate of divergence The residuals of the regresr quent admixture of divergent chNA haplo them Such results apply to intraspecific di 5i d Ptahif Wise dwarf again Stance were types could create such a pattern especially if versity only It would now be of interest to m Pzim lyglrfaja Ch 1239 201 2003 the glacial re igia that were the source of colo contrast them With patterns of species rich 19 A Palme er al Herediiy in press nization were present not far to the south of ness as these should also have been affected I GendeuvRRJAF Emquot 40 EIC01l1111v35 r39vt ft 0 c0 5 these regions 4 5 This be strengthened but perhaps notto the same extent by the R M F39Snmez Gs 39i er a mm Wquot 1939 95 2002 b the evolution of higher dispersal ability in legacy of past climate changes 287 9 23 D Griver R J perir Come Caner 4 47 2003 newly colonized as opposed to remgial pow 24 B Comps er al Genen39cx 157 389 2001 lations 25 resulting in increased levels of seed References and Notes 83 Ge39rlg39lMgggfclg39 i 1261923333 1 ow away from refugm anauy retreating K D Bennett Evoiun39on and Ecology The Pace 0 Life 2739 39 quot 39 28 C b d U P C b d 1997 R J Petit er al Conserv Biol 12 844 1998 southern edges of the ranges may Ve ecome am 39 quot39V39 5539 am 3939 l K J Willis R J Whittaker Science 295 12452002 gt gt 2 K D Bennett er aij Bio 90 r 18 103 1991 39 dissected to the point that local populations loSt 3 Cytofor wwwpierrotoninrafrCytoforMapst 2939 M39 Ignes39rzsbgbjansson39 PmC39 Naquot Acad39 5039 U39S39A39 dlversny Regardless 0f the underlymg 439 K39 J39 W39ll39s er 3quot Quaquot Rex39 5339 203 wool 30 We thank S Diamandis D Cromory F Popescu and mechanisms this pattern of diversity does con agarlquL39g L39girxtkggi g szg gggfll D Slade for providing material for analysis from trast with that predicted under simple models 0f 7 c M Hewitt 39Bioi j Linn Soc 58 247 1996 I E32355 J M L39oauveL Vimsa 39g39erk 3 colonization Le a gradual decrease indiversrty 8 c M Hewitt Narure 405 907 2000 temnidans of ONF fame the f r my of ce of away fromthe source populations 7 8 Recent 12 glib 3 El ma a5148 817 399 Bovenden and Kelheim G rmany and t e forestry WI 0 quot 0C theoremm modeis have Shown how genetlc d1 e offices of t e Imlian Nationa Park of Casentino of gt gt gt 11 R J Petit R Bialozyt S Brewer R Cheddadi B C l b d fAlt G d B It i f Vers y may be better Preserved dmmg colom Com s in Imamarmy Ecology and Homequot in a sririn39 i39riquot r curtain r3 3331 31L Ya onthallpfeViO lSW assumed but they do not 553 Jglfvezmggd Aquott2 9quot quot3if E 5 thank M Anzidei L Bertel s Carnevale A c M a we cience or 57 I Predict Increased leeISItY 11 26 In fact 12 R J Petit er ai For Ecol Manageplse 492002 S E e SKELEEJ39IE39S39 managed dlver 1ty Wsmld be a9meved mOS y 13 R J P tit 9 alv HerediW 71v 53 1 93l Supported by the Commission of the Euro ean Corny through the redistribution melting pot of the 14 Materiais and met odsrate aVallable as SUPPDthg munities Agriculture and Fisheries FAIR specific genetic information a ea Y present amng Pop 15 f i ge a 144 1237 1 99M RTD Program Cyt0f0tquot ulatlons 111 re lgla 9 30m 0t SP0 5 lea 16 For each species we also computed Ng a parameter supp gc39itg cgem lnlg quotEgr zl muWM ZSuBDm areas where diversity has been created Be similar to GST but which takes into account similarr Materials and geth s cause the contribution of a population to teal ities between haplotypes75 Values are reported in References le S ean value across Spe es was 0 or g spec1es diversity depends more on its diver compared With 5 SP washlgherthan CST Tables 51 to 5 gence from other populations than on its intrin in 17 out of 22 cases and signifirandy so P lt 005 10 February 2003 accepted 29 April 2003 www5ciencemagorg SCIENCE VOL 300 GJUNE 2003 1565