Ecology, 86(7), 2005, pp. 1704±1714 ᭧ 2005 by the Ecological Society of America

EVOLUTIONARY RESPONSES TO CHANGING CLIMATE

MARGARET B. DAVIS,1,3 RUTH G. SHAW,1 AND JULIE R. ETTERSON2 1Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, Minnesota 55108 USA 2Department of Biology, University of Minnesota, Duluth, Minnesota 55812 USA

Abstract. Until now, Quaternary paleoecologists have regarded evolution as a slow process relative to climate change, predicting that the primary biotic response to changing climate is not adaptation, but instead (1) persistence in situ if changing climate remains within the species' tolerance limits, (2) range shifts (migration) to regions where climate is currently within the species' tolerance limits, or (3) extinction. We argue here that all three of these outcomes involve evolutionary processes. Genetic differentiation within species is ubiquitous, commonly via adaptation of populations to differing environmental conditions. Detectable adaptive divergence evolves on a time scale comparable to change in climate, within decades for herbaceous plant species, and within centuries or millennia for longer-lived trees, implying that biologically signi®cant evolutionary response can ac- company temporal change in climate. Models and empirical studies suggest that the speed with which a population adapts to a changing environment affects invasion rate of new habitat and thus migration rate, population growth rate and thus probability of extinction, and growth and mortality of individual plants and thus productivity of regional vegetation. Recent models and experiments investigate the stability of species tolerance limits, the in¯uence of environmental gradients on marginal populations, and the interplay of de- mography, gene ¯ow, mutation rate, and other genetic processes on the rate of adaptation to changed environments. New techniques enable ecologists to document adaptation to changing conditions directly by resurrecting ancient populations from propagules buried in decades-old sediment. Improved taxonomic resolution from morphological studies of macrofossils and DNA recovered from pollen grains and macroremains provides additional information on range shifts, changes in population sizes, and extinctions. Collaboration between paleoecologists and evolutionary biologists can re®ne interpretations of paleo- records, and improve predictions of biotic response to anticipated climate change. Key words: adaptation; climate change; evolutionary constraints; Quaternary paleoecology; range shifts; tolerance limits. Special Feature

INTRODUCTION sult in major differences in biological form. Accord- Adaptation to changes in the environment is an im- ingly, a fundamental assumption of paleoecology has been that the rate of evolution is far slower than the portant and nearly universal aspect of biotic response rate of climate change (Bennett 1997, Webb 1997, Jack- to climate change. We argue here that adaptive re- son 2000), with meaningful evolutionary adaptations, sponses affect species persistence, migration rate, and such as the origination of taxa, occurring on the time- forest productivity. Thus more complete understanding scale of millions of years. Climate changes much more of adaptive responses to climate must be incorporated rapidly, because superimposed on glacial cycles into interpretations of Quaternary paleorecords. Fur- 100 000 years in length are variations on millennial, thermore, fossil records can provide tests of evolu- centennial, and even decadal time scales. For example, tionary hypotheses, enhancing understanding of the during the most recent glacial-interglacial transition, a evolutionary consequences of climate change. time of rapid warming, there was a brief reversal lasting It is remarkable that paleoecologists reconstructing several centuries. At this time paleorecords from the late-Quaternary environments so seldom discuss the north Atlantic region record a temperature drop of sev- possibility of adaptation to changing climate. They eral degrees C within decades (Huntley et al. 1997). have tended to adopt the perspective of Darwin, who Paleoecologists have argued that such rapid environ- emphasized that vast periods of geologic time allow mental changes overwhelm evolutionary processes, great opportunity for the accumulation of many slight causing extinction except where climate remains within differences among organisms that, collectively, can re- preexisting tolerance limits for a species (Bennett 1997). Contributing to this view has been the sparse- Manuscript received 24 November 2003; accepted 16 June ness of the record of new plant species during the Qua- 2004; ®nal version received 4 October 2004. Corresponding Ed- itor (ad hoc): L. J. Graumlich. For reprints of this Special Feature, ternary and the apparent limitations of fossils, espe- see footnote 1, p. 1667. cially pollen, to record traits involved in adaptation to 3 E-mail: [email protected] climate, such as phenology and physiology. Further- 1704 July 2005 PALEOPERSPECTIVES IN ECOLOGY 1705 more, latitudinal range shifts of tree taxa, well docu- et al. 1989, Burger and Lynch 1995). Thus, adaptive mented in Quaternary sediments, are compatible with evolution affects all of the primary responses to chang- the view that species persist only within the environ- ing climate predicted by paleoecologistsÐ``tolerance, ments to which they are already adapted, even as those migration, or extinction'' (Jackson 2000:294). We re- environments shift in space (Prentice et al. 1991, Jack- interpret examples from the Quaternary record that son 2000). demonstrate how evolutionary models can expand un- Moreover, paleoclimate reconstructions rely on the derstanding. Last, we review recent contributions by premise that each species has a unique set of limits in Quaternary paleoecologists that utilize paleorecords to its tolerance to various aspects of the environment, de- demonstrate adaptations to environmental change. ®ning a multidimensional ecological niche (Jackson 2000). Paleoecologists have focused on physical niche GENETIC CHANGE IN PLANTS dimensions, determining for particular species the re- DURING THE QUATERNARY alized limits of physiological tolerances to factors such For animal phyla, particularly mammals, both spe- as minimum temperature or growing degree days. ciation events and extinctions are well documented dur- When species-speci®c tolerances are plotted on a map ing the past two million years. In contrast, the Qua- of modern climate, they quite accurately delimit the ternary fossil record documents few examples of new present geographical distribution of the species in ques- species of vascular plants (Comes and Kadereit 1998), tion (Peterson et al. 1999). Paleoclimate reconstruction reinforcing the impression that, particularly in these employs these environmental attributes of species to organisms, evolution is a slow process. Speciation is, infer the distribution of climate at an ancient time from however, only one aspect of evolutionary change. With- the distribution and abundance of fossils. Thus, paleo- in species, genetic differentiation among populations climate reconstruction depends on the assumption that attests to the ubiquity and rapidity of evolutionary species tolerance limits remain stable in time, that is, change. evolutionarily inert. In practice, a certain amount of Spatial substructuring of populations is evidenced by change might not be noticed because reconstructions variation at putatively neutral genetic marker loci, re- Feature Special are often at a coarse geographical scale (Prentice et al. ¯ecting current mating patterns and/or previous iso- 1991), with broad con®dence intervals surrounding lation of populations. Phylogeographers use such mark- temperature and precipitation estimates. Fossil records ers as a basis for inferring locations of refuges during used for validation are often sparse, especially for older the last glaciation, and pathways of migration since time horizons. Nevertheless, recent reviews regard rap- then (e.g., Cruzan and Templeton 2000, Hewitt 2000). id evolution as the exception, affecting only ``some Fossil evidence has valuably informed such studies. local populations of a species . . . while others undergo For example, allozyme and mitochondrial DNA extinction or disperse to newly suitable sites'' (Jackson (mtDNA) divergence has been calibrated against the 2000:294). Given this context, discussions of biotic actual time since isolation of tree populations in the response to future climate emphasize predicted range American Southwest. Time of isolation was determined shifts, focusing on seed dispersal and establishment as from migration histories documented by macroremains potentially limiting processes (e.g., Clark et al. 1998). preserved in packrat middens (Hamrick et al. 1994). Here we consider evolution in relation to climate and Allozymes in a series of populations of lodgepole pine discuss its relevance to processes paleoecologists con- (Pinus contorta), the ages of which were determined sider important, including population persistence in from radiocarbon-dated fossil-pollen records, suggest situ, range shifts, and extinction. We review the evi- a progressive loss of alleles in the course of northward dence for adaptation of plant populations to spatial var- migration in western Canada during the Holocene iation in environment and discuss the potential for evo- (Cwynar and MacDonald 1987). Reduced allelic di- lutionary response to temporal variation. We emphasize versity away from putative glacial refugia has been that climate change on various time scales imposes documented for several plant species, while Pinus pum- selection regimes that may lead to adaptive changes in ila shows reductions in diversity at some loci and in- plants and animals, whether or not their ranges shift creased diversity at others (Tani et al. 1996). (Davis and Shaw 2001). The degree of adaptation de- Adaptative differentiation among populations within pends on the interplay of natural selection with other a species is documented by clinal variation in physi- evolutionary processes, such as gene ¯ow, genetic drift, ological, phenological, and ®tness traits in relation to and mutation, and also with demography. A lag in ad- latitudinal or elevational gradients in climate. Such var- aptation implies reduction in growth and survival of iation has been shown for many species, beginning with individual plants as well as in the overall productivity the classic studies of Turesson (1922) and Clausen et of regional vegetation (Rehfeldt et al. 1999, 2002). The al. (1940) and continuing with recent papers too nu- rate of adaptation in¯uences the rate at which popu- merous to list here. The distribution of climate-sensi- lations invade newly available habitat (GarcõÂa-Ramos tive traits within species is studied in common-garden and Rodriguez 2002), and also the probability that pop- (provenance) experiments, in which plants from dif- ulations will die out within their present ranges (Pease ferent geographical locations are grown together at a Special Feature ;seeg,Riat 94 ae 98 eflte al. et Rehfeldt 1988, 2004 Etterson Lacey 2002, 1984, 1999, Reinartz (Fig. e.g., environment see local its 1; to adapted which well of relatively each is populations, of series plant a herbaceous comprise and species tree most that show sampled. studies are These populations which from sites into different reciprocally the transplanted are approach, special this a of as or case climate, differing with locations of series 1706 eprtr fnaetlnce tp,adtefeunyo curneo h aeppltos(elzdnce costhe of across niche) studies (realized common-garden populations from same generalized the are of Diagrams occurrence of (bottom). frequency gradient the temperature and same (top), niche) (fundamental temperature n lnlvraini epnet lmt a accrued has climate to North response in differentiation variation in genetic clinal that and species show Europe herbaceous and America introduced Similarly, mid-Holocene. of the studies until ice covered continental was region by the because several most, past at the years within thousand happened Hurme have 1989, must 1997) (Muona al. Finland et in occupies currently it ifrnito.Freape dpaino ct pine Scots of ( adaptation example, For differentiation. iu sylvestris Pinus pce Etro 2004 1999) herbaceous (Etterson some al. species in 30% et by production (Rehfeldt seed reduce pine and Canadian lodgepole in of 20% by populations production biomass gases reduce greenhouse could of pre- concentrations differences doubled climate for example dicted for reduc- large: The be ®tness. can i.e., tion fecundity, as and growth, 2). survival individuals' (Fig. as reduces well 1996) climate both novel (Carter at location; a greater locations Thus, mortality source colder and and the less warmer be to to tends sites similar growth test at temperatures highest are with rates growth populations, tree F ueoseape ouettesedo adaptive of speed the document examples Numerous IG n n ftegain n era rmusial aia tteohredo h rdet PnlBi oie rmDavis from modi®ed is B (Panel gradient. at the habitat of suitable end a newly other under into the spread and at populations (top), habitat as unsuitable climate space closer from stable in populations and retreat [2001].) a local shifting and means Shaw of under is gradient means phenotypic and range gradient phenotypic the the hypothetical the climate of Meanwhile, bring depicting end a will optima. one Diagram along regime ®tness selection species (B) changed changed the plant [1999].) the to time, a al. In of et (bottom). populations climate Rehfeldt changing of from means reproduced ®tness is optimal A (Panel Canada. .()Darmaia ersnaino h rwhadmraiyrsos ftest rdet ntema annual mean the in gradients to trees of response mortality and growth the of representation Diagrammatical (A) 1. . otedvreeeain n latitudes and elevations diverse the to ) a ). a losePae1.Frmany For 1). Plate see also ; AGRTB AI TAL. ET DAVIS B. MARGARET ic h ieo salsmn ntecniet i.e., ( continent, century the a or on decades establishment within of time the since at 1984; nartz aito noaccount. genetic taking into collec- than variation as rather species individuals identical treat consid- of they tions not because have issues these climate ered changing to response examining forest stand-simulators date, To response change. their climate in to differ for that changing species potential by among the in¯uenced competition be The and also may populations. seeds, evolution adaptive of and pollen ¯ux both demographic of populations among dispersal ¯ow gene through rel- of for extent variation the traits, genetic genotypes, evant of nature individual and of distribution depend breadth the also ecological will and answers the change But upon critical. climate are Of of duration change? rate its climate and magnitude to the prior how pro- course those and And match ®tness likely? to for require ductivity equally it gradient would generations climate many new a populations all to of adaptation the Is change. re- before climate exhibited response, of they onset selection biomass and via ®tness could, the cover range species through- a populations generations out adaptively. of number a evolve after initially, selection reduced but may be new may ®tness traits changes, a climate When which impose also under will regime, climate in temporal a change ®tness, in variation genetic of expression the 1998). Schmid and Weber oteetn htsaildfeecsi lmt elicit climate in differences spatial that extent the To acscarota Daucus ae 1988; Lacey , ebsu thapsus Verbascum iu contorta Pinus clg,Vl 6 o 7 No. 86, Vol. Ecology, Solidago nwestern in Rei- , sp., July 2005 PALEOPERSPECTIVES IN ECOLOGY 1707

PLATE 1. Illustration of genetic differentiation in the rate of phenological development of populations of Chamaecrista faciculata sampled from an environmental gradient across the Great Plains. These plants were grown in a common garden in Minnesota and sampled in early October just prior to the ®rst hard frost. (Right) Minnesota genotype with fully ripening pods. (Middle) Kansas genotype in the process of pod maturation. (Left) Oklahoma genotype at the peak of ¯owering. Photo credit: J. R. Etterson. pca Feature Special Genetic variation means that climate changes will many populations grow best in climates similar to their affect populations differently throughout a species place of origin, northern populations of each of these range, and populations will vary in the rate of adap- conifers grow more rapidly in warmer climates than in tation. This point is illustrated by lodgepole pine, jack the climates they actually occupy (e.g., population A pine, Scots pine, and Siberian larch, which have been in Fig. 1) (Rehfeldt et al. 1999, 2002, 2004). Rehfeldt extensively studied in provenance trials. Although et al. (2004) attribute the phenomenon to a negative genetic relationship between tree growth rate and cold hardiness, speculating that cold-tolerant genotypes are outcompeted during stand thinning by faster-growing cold-intolerant genotypes. The discrepancy between optimal and realized growth environments means that climate warming could represent a change to which the northern populations readily adapt. Even for these new- ly established populations, however, differences in photoperiod or other aspects of the environment can impose selection. At the southern edge of a species' range, in contrast, populations may grow poorly in warmer conditions. Here, populations could be extir- pated rapidly as climate warms to levels outside the tolerance limits of individual trees. In the center of the range, novel climate will reduce individual growth rates and increase mortality of existing genotypes; thus productivity of forests dominated by any of these co- nifers will be reduced, at least in the short term, even in the center of the range (Rehfeldt et al. 1999, 2002, FIG. 2. The 20-yr height (percentage of plantation mean) 2004). of 118 populations of Pinus contorta ssp. latifolia (black dots) and ssp. contorta (open circles) grown at 60 test sites in western Canada. Growth is plotted against the difference of GENETIC CONSTRAINTS ON FUTURE ADAPTATION mean annual temperature between the planting site and the site of origin. Positive values denote transfers into a warmer The rate at which adaptation can proceed is critical climate; negative values denote transfers into a colder climate. for predicting plant response to climate change. Trees For these populations, growth is maximal at test sites with climate closely similar to the climate at the site of origin. produce seeds copiously, and, despite the failure of (The ®gure is reproduced from Rehfeldt et al. [1999].) many seeds to germinate, thousands of seedlings es- Special Feature lmt.Arcn td ftepareannual, prairie the of study changing recent to A adaptation climate. impede could that constraints response. support to selection available variability could genetic selection reduce or directional severely 10 strong but of generations variation, es- more genetic These suf®cient conditions. assume warmer timates under poorly populations grow southern and that central popula- well for but northern millennium conditions, a the warmer over under for well century grow that a could tions as trees little long-lived as these require of Scots adaptation and Thus, pine lodgepole pine. of generations populations 13 particular to for one require would decades warming coming anticipated in following that adaptation estimate of to experiments recovery changes selection generational in rate from growth data in use 2002) ge- (1999, of al. Rehfeldt et frequency conditions. climate novel the tolerate that increase notypes could the forest a selection Over from thinned 1). stand, are (Table juveniles reach that reproduce to decades and several survives of canopy seedlings forest fraction and the seeds miniscule of A cohort selection. each ge- to available variation the netic of exposure facilitates sexual from reproduction proli®cacy This 1). (Table year each tablish 1708 .. eftikes nacs®ns,weesiseffect its trait, whereas one ®tness, on enhances allele thickness, an leaf of e.g., to effect either the due which in are pleiotropy, correlations genetic of and The Etterson direction 2001). 3, the (Fig. Shaw climate to changed a antagonistic under are selection that traits correlations genetic among may of evolution because antici- slowed Adaptive substantially the change. be than climate slower of these rate be in pated to evolution predicted adaptive is of populations rate the variance, netic mutwslwra h eihr fteseisrange species the of 2004 the periphery (Etterson the although at selection, lower was under amount traits most for variation evdadaepeitdt oenrhadi h fu- the 2004 in northward (Etterson move to ture ob- thickness. predicted were are latitude leaf and to served and corresponding selection number, in Clines leaf phenolog- in¯uence development, of that rate Traits ical the including Plains. measured, Great were the ®tness in arid- gradient an along were ity gardens seedlings common in Pedigreed climate planted 2001). reciprocally drier Shaw and and warmer (Etterson a under evolution impede may adaptive ®tness for important traits among relations acit fasciculata maecrista elto fvraiiyi nyoeo h genetic the of one only is variability of Depletion aoytes15trees/ha 145 seedlings/ha 000 725 individuals/ha 500 seeds´ha 000 000 3000±10 tree´ha 1 1991±1995) (average, canopy reaching Trees trees Canopy trees understory and Saplings values) Seedlings annual of (range Seeds b ABLE .Dsiesgicn eeto n ge- and selection signi®cant Despite ). T idresAe,GgbcCut,Mcia,USA. Michigan, County, Gogebic Area, Wilderness a .Dmgah fsgrmpe( maple sugar of Demography 1. .Ppltoshroe genetic harbored Populations ). eosrtsta eei cor- genetic that demonstrates , aaee Value Parameter AGRTB AI TAL. ET DAVIS B. MARGARET Cha- crsaccharum Acer iis elct ie ftebacterium tolerance the species of changed lines of Replicate lability to limits. and adaptation regime both Experiments temperature species. demonstrate been different bacteria has of in conditions number a physical in in shown change to response least at magnitude. in by of changes change order past of one exceed rate to future predicted is the particu- climate as are today, adaptation important to larly impediments but known, poor- generally ly is impedi- change genetic climate to of adaptation to extent ments The cor- determined. is the readily which of not disequilibrium), genetic nature linkage of genetic (pleiotropy, extent the relation the on thus depends hotter, cor- and constraint, in genetic traits of ®tness among lability highest The relations evolve. in will result climates that drier combina- traits that of genetic likelihood tions Adverse the loci. reduce as- different may the correlations at disequilibrium, alleles linkage of to sociation or ®tness, development, phenological reduces of rate e.g., trait, another on efrac Mnode l 99.Cneunl,in Consequently, 1999). these al. competitive et (Mongold reduce performance consistently temperatures higher oeo eei osrit neouinudrchanging under evolution the in constraints demonstrate genetic studies of role These did frequency. temperatures in higher increase of muta- tolerance new density, conferring low tions critical once a However, reached populations. populations declining population in ancestral only the evolves by tolerated that than extreme h vltoayptnilt xedterneabove range the extend to 42 potential evolutionary of investigation the Further Period, adaptation. Quaternary impedes the generally during experienced variable as that climate, view the the against argues of 1992, This al. 2001). any et Lenski (Bennett for temperatures constant increased at ®tness held lines which over range the ept hs oeta meiet,evolutionary impediments, potential these Despite ovral eprtr vle nrae ®tness increased evolved 20 temperature a throughout subjected variable Lines 1992). al. to et (Bennett limit lethal the of ttehgettmeaueue,42 greatest used, ancestor, temperature the highest to the relative at ®tness, rate in the increase with experienced, of it temperature the population to each adapted generations, 2000 Over 2001). Lenski etdt aibetmeaue (10 temperatures sub- was variable lines to of set jected the one and throughout tolerated, typically temperatures directional range to distinct subjected under were cell, selection single a from rived Њ eeldta uain ofrigtlrneto tolerance conferring mutations that revealed C .coli E. ,19±98 npo ,Sylvania A, plot in 1991±1998, ), Ϫ 1 ´yr utrs dpaint eprtr more temperature to adaptation cultures, Ϫ Њ 1 ag ftmeaue,bodrthan broader temperatures, of range C Ϫ 1 ´yr Ϫ 1 clg,Vl 6 o 7 No. 86, Vol. Ecology, Њ ,wti degree a within C, Њ ira range; diurnal C .coli E. l de- all , July 2005 PALEOPERSPECTIVES IN ECOLOGY 1709

FIG. 3. Illustration of the in¯uence of genetic correlations among traits on selection response, reproduced from Etterson and Shaw (2001). (A) Hypothetical positive genetic correlation between two traits (each point represents the breeding value, similar to a family mean, for each of two traits). There are two selection scenarios: for R (reinforcing selection), the depicted rA (correlation between traits) is in accord with the direction of selection, enhancing evolutionary response; for A (antagonistic selection), the depicted rA (correlation between traits) is in the opposite direction from selection, inhibiting evolutionary response. (B) Scatter plot of reproductive stage and leaf number breeding values for a Minnesota population of Chamaecrista fasciculata when grown in the hotter, drier climate of Oklahoma, showing signi®cant negative genetic correlation that is antagonistic to the positive vector of joint selection on these traits. (C) Scatter plot of the Minnesota population leaf thickness and leaf number breeding values, showing a signi®cant positive genetic correlation that is also antagonistic to the negative vector of joint selection. Both (B) and (C) are examples of adverse correlations between traits that are predicted to limit adaptive evolutionary response of Minnesota populations of this species under conditions of higher temperature and soil moisture stress. pca Feature Special climate. Most importantly, they demonstrate the evo- within the Holocene appear to correspond well with lutionary lability of limits of environmental tolerance, the distributions of fossils (Fig. 4a), suggesting that the even when genetic variation is restricted to variation relationship between climate and pollen abundance has generated by spontaneous mutation. Clearly, when in- remained stable over the past 24 000 years for the more ¯ux of variation due to mutation is added to the stand- than two dozen eastern North American oak species ing genetic variation already present in populations of considered collectively. However, spruce pollen distri- diploid organisms, tolerance limits for a species or pop- bution is underpredicted by the model 24 000, 21 000, ulation should not be regarded as ®xed. and 16 000 calendar years ago (Fig. 4b). In this case a probable explanation is greater breadth of tolerance EVOLUTIONARY MODELS INFORM INTERPRETATION limits in the past for the genus Picea because the extinct OF THE PALEORECORD spruce species, Picea Critch®eldii, was distributed Interpretations of fossils often assume stability of widely in southeastern United States. This species, species tolerance limits. This issue is examined in re- known only from fossil remains, was apparently adapt- cently developed evolutionary theory, which considers ed to warmer climate than other eastern American the interplay of evolutionary and demographic pro- spruce species, given its co-occurrence with temperate cesses in the evolution of tolerance limits. The differ- deciduous trees in the southern Mississippi valley. It ential population growth rates of central and peripheral died out around 15 000 years ago (Jackson and Weng populations appear to produce a bias toward stability 1999). Ackerly (2003) suggests that diminished com- of tolerance limits. Gene ¯ow from more central pop- petition from congeners might promote adaptation of ulations through pollen or seed dispersal overwhelms trailing-edge species to changing climate, but in this genetic adaptation in the much smaller peripheral pop- case extinction occurred instead, even as other spruce ulations, reducing ®tness (Antonovics 1976, GarcõÂa- species migrated northward. Climate changes were ex- Ramos and Kirkpatrick 1997). ceptionally rapid at the time Picea Critch®eldii became Although paleoecologists generally assume constan- extinct, in some regions rivaling in speed future chang- cy of environmental tolerance limits, paleoecological es predicted to result from greenhouse warming (Hunt- data can sometimes be used to test the hypothesis that ley et al. 1997). limits have changed over time. An example is a study A third illustration is provided by eastern hemlock that predicts fossil pollen distributions at various time (Tsuga canadensis). The distribution of pollen from horizons from global climate model output, using trans- this tree species in the three oldest time horizons is fer functions derived from patterns of modern pollen overpredicted by the climate model (Fig. 4c). Over- and modern climate (Prentice et al. 1991). Predictions prediction using parameters derived from modern pop- of oak pollen distributions in North America during the ulations suggests that tolerance limits for this species last glacial maximum and at various time horizons might have been narrower in the past than they are at Special Feature 1710 g)adsxyugrtm nevl,cmae ople bnac rdce rmciaemdlotu,uigtransfer using output, model predicted and climate Observed from 1950. ( before predicted years spruce calibrated for abundance in comparisons pollen expressed Similar is (B) to Time well. climate. compared correspond and abundance pollen intervals, modern time from derived younger functions six and ago) F o h he lettm oios ugsigbodrevrnetltlrne tta ieta tpeet ehp because perhaps present, at than time that at tolerances environmental broader species suggesting extinct horizons, time the oldest three the for IG oa.Oeepaaini arwn ftetlrnelmt fteseisa httm.Peitoscrepn etrto better correspond [1991].) Predictions al. time. et Prentice that from at modi®ed than species is steeper the ®gure were but of (The gradients predicted, yr. limits temperature correctly 6000 tolerance is latitudinal last the appears) the when of ®rst during horizons, narrowing deposited pollen time a records hemlock earlier fossil is where the explanation locations at One from overpredicted today. (judged is refuge density hemlock population the of location The .()Fsi a ( oak Fossil (A) 4. . ie Critch®eldii Picea Quercus p. olnaudnei atr ot mrc uigtefl-lca 2 0 years 000 (24 full-glacial the during America North eastern in abundance pollen spp.) a tl rsn.()Smlrcmaiosfresenhmok( hemlock eastern for comparisons Similar (C) present. still was AGRTB AI TAL. ET DAVIS B. MARGARET Picea p..I hscs,ple bnac sunderpredicted is abundance pollen case, this In spp.). clg,Vl 6 o 7 No. 86, Vol. Ecology, sg canadensis Tsuga ). July 2005 PALEOPERSPECTIVES IN ECOLOGY 1711

is not possible at present to assess how applicable these different cases are to particular species. Latitudinal temperature gradients are anticipated to become less steep in future as high latitudes warm more rapidly than low latitudes under the in¯uence of green- house gases. This scenario was examined by GarcõÂa- Ramos and Kirkpatrick (1997). They modi®ed the Kirkpatrick-Barton model to examine population dy- namics and genetic changes within a population along a climate gradient that varied in steepness. Lessening of the gradient in the model increased the speed of FIG. 5. Theoretical depiction of population density along adaptation and thus the expansion rate for marginal an environmental gradient. X indicates location along the gra- populations invading new habitat. ϭ dient, only half of which is shown in the ®gure. X 0 where Case and Taper (2000) extended the Kirkpatrick-Bar- the environment is optimal for the species. B is an index of the steepness of the gradient. When B is small, population ton model to explore the interaction between environ- density is at carrying capacity K* wherever environmental mental gradients and interspeci®c competition. Along conditions are close to optimal, and the environmental am- environmental gradients, competition from neighbor- plitude for the species is large. When B is large, indicating ing species plays a critical role by reducing densities a steep gradient, population density falls to low levels, gene migration overwhelms marginal populations, and range limits of marginal populations, augmenting the effect of gene contract. (The ®gure is reproduced from Kirkpatrick and Bar- ¯ow from populations nearer the center in swamping ton [1997].) out adaptations to local environments. Case and Taper examined different scenarios in which interspeci®c competition interacts with environmental gradients of present. Of course, errors may explain the overpred- varying steepness to limit the sizes of species ranges. iction, for example, problems in the climate predictions Gomulkiewicz and Holt (1995) have modeled the prob- Feature Special or errors in evaluating the climate-pollen transfer func- lem of adaptation in populations that are suf®ciently tion. Background vegetation with higher pollen pro- maladapted that they persist only as a result of im- ductivity suppressing hemlock pollen percentages is a migration, ``black-hole sinks.'' They investigated con- third possibility. ditions under which the population evolves such that Kirkpatrick and Barton (1997) develop a model that its growth becomes positive before its numbers decline offers a possible evolutionary explanation for this dis- to zero. Their model shows that, the smaller the sink crepancy, considering that latitudinal temperature gra- population and the more maladapted it is, the more dients were steeper than today during the last glacial likely it is that it will become extinct before it achieves maximum. Their model investigates adaptation in a se- a positive growth rate. The consequence, in this in- ries of populations along an environmental gradient stance, is that the range contracts. (Fig. 5). Parameters describe gene ¯ow and steepness The effect on evolutionary response of temporal con- of the environmental gradient (B in Fig. 5). When the tinuity in the trajectory of environmental change is gradient is gradual, pollen and seed dispersal bring to addressed by Pease et al. (1989). These authors used each adjacent population genes selected in similar en- a model to examine the relative importance of evolu- vironments. Under this circumstance, marginal popu- tion, migration and habitat selection to population ®t- lations in the model may adapt to extreme conditions, ness in the course of a range shift induced by contin- and the species tolerance limits and geographic range uously changing climate. They modeled a population expand. When the environmental gradient is steep, with maximum ®tness at a point along a climate gra- however, populations subject to drastically different en- dient. Environmental parameters affecting ®tness vironmental conditions are growing in close juxtapo- changed steadily through time at all points along the sition, and gene ¯ow from more central populations gradient. If climate changed suf®ciently slowly, the may overwhelm adaptation in marginal populations, species persisted, shifting its range along the climate such that they become demographic sinks or go extinct. gradient. Persistence of the species also depended on In this way, both the species boundary and physiolog- genetic variability and the pace of evolutionary ad- ical tolerance range can shrink. We note, however, that aptation to the changing climate. more recent work of Barton (2001) demonstrates that Evolution in an environment undergoing constant the outcome, in which limits to a species range evolve, temporal change has also been modeled by BuÈrger and is highly sensitive to Kirkpatrick and Barton's (1997) Lynch (1995). With effects of mutations on phenotypes assumption of constant genetic variance. The plausible symmetrically distributed around zero, they found that alternative, in which genetic variance evolves along the mean phenotype evolves in a lag behind the phe- with trait means, can lead to inde®nite range expansion. notypic optimum as the optimum changes with chang- Because genetic details that would in¯uence the evo- ing environment. The chance of extinction depends on lution of variance of quantitative traits are elusive, it the magnitude of this lag, which, in turn, depends both Special Feature tes nti td,tepyilgclrsossof responses physiological with direct the associated permitted study, traits Daphnia age this of in In series time years ®tness. a 35 of to observation 0 horizons from time successive ranging from dating subpopulations dis- the Like 2005). al. et of Hairston 1996, covery al. (Suy- et species of ama provided distributions under- historical our has the re®ning of old level, standing species years the 000 at 150 identi®cations grains from pollen and age, in fossil decades several sediments lake in eggs of predictions models. the climate incorporate global and papers reconstructions recent climate more paleoclimate step- by these followed a whereas and stasis, preceded imposed climate, models in change Older sophisticated. ingly super- trajectories. ®nd climate long-term paleoecologists many on the that imposed this on scales complicate variability time will climate different It consider mutation. to in¯ux to the scenario on due and variation change environmental of of rate the on 1712 ouain.Rcnl,DArcvrdfrom recovered contemporary DNA in Recently, markers populations. neutral infor- from coincident the derived mation supplementing changes change, evolutionary environmental with of providing now evidence are fossils direct Well-preserved 1994). Hamrick al. genetic (e.g., et hypotheses contemporary evolutionary used of test to be studies patterns infor- can with that This conjunction context species. in historical animal a provides and mation plant of abundance eaa iesae lnsof clones scale: time decadal tne l 05.Freape oprsnof comparison example, Hair- For in 2005). cited al. references et (see ston sediments lake in eggs resting buried from hatched populations in observed been 1992). Fetcher and (McGraw these 6A) (Fig. for plants found perennial were temperature to much phys- and response in from iological differences germinated seeds Signi®cant horizons. with were soil conditions younger earlier, common century in grown a over soli¯uction by soils lobes arctic in two buried of species, graminoid Seeds populations. ``resurrected'' resulting of responses the environmental the comparing directly horizons, time and different at deposited pre- sediment animals in and served plants of propagules reviving further, past. the of climates tolerance changed ecosystem species' under of in limits lability the species on individual bear and of processes, role the luminate ynbcei eaeaudn Hiso ta.1999) al. et (Hairston abundant before became deposited cyanobacteria eggs resting 35-year-old from orig- inating clones than cyanobacteria toxin-containing resis- to more tant signi®cantly are Constance Lake eutrophic eitoso lmt ngntcmdl r increas- are models genetic in climate of Depictions aercrsrva hne nps itiuinand distribution past in changes reveal Paleorecords iial,eouinr hne nzolntnhave zooplankton in changes evolutionary Similarly, step a goes Ecology'' ``Resurrection of ®eld new The U eosrtdeouinr dpaino the on adaptation evolutionary demonstrated IGTHE SING ie Critch®eldii Picea E VOLUTIONARY F OSSIL R H uhiet®ain il- identi®cations such , CR TO ECORD YPOTHESES Daphnia rmmodern, from AGRTB AI TAL. ET DAVIS B. MARGARET T EST Daphnia Daphnia Fg B.I aeSuperior, Lake In 6B). (Fig. rwhcabrcniin of conditions growth-chamber eesb 90 n aermie bnatsubsequently. abundant high time, remained reached same have 1960s, the and late At the 1970, during by Cyanobac- increase levels 1992±1997. to from began youngest from teria the date populations and oldest 1962±1971, The sediment. Constance Lake rmHiso ta.[99,wt emsinfrom permission reproduced with [1999], is al. B et (Panel Hairston toxins. from cyanobacteria to resistance etlcag vrhlseouinr processes, environ- evolutionary rapid overwhelms that idea change provide the mental They against times. organisms evidence generation in strong even long traits, relatively adaptive with evolu- in demonstrate change they tionary Nevertheless, far). (so years half-century. species past of the dur- ing ecosystem contamination industrial lake by a (2005) induced replacements on al. effects et al. the Hairston et enrichment document methods, similar (Kerfoot and Using environment 1999). near-shore dredging the as changed replacement, and to change up species morphological century rapid 20th document the present in the early from dating sediments etsesae02 rod PnlAi erdcdfrom reproduced subpop- is of toxin of A ulations cyanobacteria to (Panel Elsevier.) sensitivity from Differential old. permission (B) with yr [1992], Fetcher 0±20 and McGraw are seeds gest in eurce rmseso ifrn gsbre under buried ages are seeds different oldest of The lobes. seeds soli¯uction from resurrected tions riso h eaa iescale. time adaptive decadal in changes the demonstrate on (B) traits and (A) examples Both F IG eurce ouain nld nytels 150 last the only include populations Resurrected .()Dfeeta epnet eprtr under temperature to response Differential (A) 6. . Daphnia Daphnia ace rmrsigeg eoee from recovered eggs resting from hatched ouain eeoe increased developed populations Daphnia ae bigelowii Carex clg,Vl 6 o 7 No. 86, Vol. Ecology, ϳ 7 rod h youn- the old; yr 175 eurce from resurrected subpopula- Nature .) July 2005 PALEOPERSPECTIVES IN ECOLOGY 1713 preventing adaptation to local environments as they (grants DMS 0083468 and DEB9221371), the Guggenheim vary in time and space (Webb 1997, Jackson 2000). Foundation, and by the Mellon Foundation. LITERATURE CITED CONCLUSIONS Ackerly, D. D. 2003. Community assembly, niche conser- vatism, and adaptive evolution in changing environments. Adaptive responses to climate, while clearly impor- International Journal of Plant Science 164:S165±S184. tant, are not yet well understood. Future research Antonovics, J. 1976. The nature of limits to natural selection. should have the goal of determining the pace of adap- Annals of the Missouri Botanical Garden 63:224±247. tive changes in different species and groups of organ- Barton, N. H. 2001. Adaptation at the edge of a species' isms. How closely can adaptation be expected to track range. Pages 365±392 in J. Silvertown and J. Antonovics, editors. Integrating ecology and evolution in a spatial con- climate change, particularly changes as rapid as en- text. Special Symposia of the British Ecological Society, visioned for the future? How will adaptation be affected Blackwell Science, Oxford, UK. by changed environmental gradients? We have re- Bennett, A. F., R. E. Lenski, and J. E. Mittler. 1992. Evo- viewed several processes that might limit rates of ad- lutionary adaptation to temperature. I. Fitness responses to Escherichia coli to changes in its thermal environment. aptation to changing climate. But how prevalent and Evolution 46:16±30. how strong are evolutionary constraints due to adverse Bennett, K. D. 1997. Evolution and ecology: the pace of life. genetic correlations among traits, as encountered in Cambridge University Press, Cambridge, UK. Chamaecrista fasciculata (Etterson and Shaw 2001) BuÈrger, R., and M. Lynch. 1995. Evolution and extinction in and E. coli (Mongold et al. 1999), and how persistent a changing environment: a quantitative genetic analysis. Evolution 49:151±163. will they be? Do differences in rates of adaptation Carter, K. K. 1996. Provenance tests as indicators of growth among organisms differing in breeding systems, spatial response to climate change in 10 north temperate tree spe- genetic structure, or demographic properties account cies. Canadian Journal of Forestry Research 26:1089± for phenomena observed in the fossil record, such as 1095. Case, T. J., and M. L. Taper. 2000. Interspeci®c competition, different migration rates? Does adaptation explain why environmental gradients, gene ¯ow and coevolution of spe-

some species survived as tiny populations in multiple cies' borders. American Naturalist 155:583±605. Feature Special refuges, while others maintained continuous popula- Clark, J. S., et al. 1998. Reid's paradox of rapid plant mi- tions, shifting to different latitudes? Can differences gration: dispersal theory and interpretation of paleoeco- among taxa in rates or degrees of adaptation explain logical records. BioScience 48:13±24. Clausen, J., D. D. Keck, and W. M. Hiesey. 1940. Experi- why some ancient forest communities have no analogue mental studies on the nature of species. I. The effect of at present? Do differences in rates of adaptation to varied environment on western North American Plants. changing environments determine which taxa persist Publication 520. Carnegie Institution of Washington, Wash- and which become extinct? ington, D.C., USA. Comes, H. P., and J. W. Kadereit. 1998. The effect of Qua- Answers to these questions will help in predicting ternary climatic changes on plant distribution and evolu- how populations and ecosystems are likely to respond tion. Trends in Plant Science 3:432±438. to the changes in climate occurring as greenhouse gases Cruzan, M. B., and A. R. Templeton. 2000. Paleoecology and accumulate in the atmosphere. But they will also help coalescence: phylogeographic analysis of hypotheses from to provide more complete explanations of the past. Un- the fossil record. Trends in Ecology and Evolution 15:491± 496. til now evolutionary responses to changing environ- Cwynar, L. C., and G. M. MacDonald. 1987. Geographic ments have hardly been considered in the vast literature variation of lodgepole pine in relation to population history. about the late Quaternary. In contrast, genetic theory, American Naturalist 129:463±469. models and experiments that deal with adaptation to a Davis, M. B., and R. G. Shaw. 2001. Range shifts and adap- tive responses to Quaternary climate change. Science 292: continuously changing environment are progressing 673±679. rapidly. By using knowledge from the past we may be Etterson, J. R. 2004a. Evolutionary potential of Chamae- able to accelerate research into the mechanisms of ad- crista fasciculata in relation to climate change: I. Clinal aptation to changing environments, obtaining a more patterns of selection along an environmental gradient in the complete understanding of the past as well as more Great Plains. Evolution 58:1446±1458. Etterson, J. R. 2004b. Evolutionary potential of Chamae- realistic predictions of the future. crista fasciculata in relation to climate change: II. Genetic architecture of three populations reciprocally planted along ACKNOWLEDGMENTS an environmental gradient in the Great Plains. Evolution Our particular thanks go to the editors of this Special Fea- 58:1459±1471. ture, Linda Brubaker, Lisa Graumlich, and Shinya Sugita. We Etterson, J. R., and R. G. Shaw. 2001. Constraint to adaptive received stimulating comments and criticism from reviewers evolution in response to global warming. Science 294:151± David Ackerly and Brian Huntley, and from Gerald Rehfeldt, 154. Linda Brubaker, Eric Lonsdorf, Stacy Halpern, and Bryan GarcõÂa-Ramos, G., and M. Kirkpatrick. 1997. Genetic models Holtz. We also express our gratitude to Christine Douglas, of adaptation and gene ¯ow in peripheral populations. Evo- James Ferrari and numerous undergraduate assistants for lution 51:21±18. compiling the data presented in Table 1. We apologize to the GarcõÂa-Ramos, G., and D. Rodriguez. 2002. Evolutionary many authors whose work on this subject could not be cited speed of species invasions. Evolution 56:661±668. because of space limitations. Readers who wish a more com- Gomulkiewicz, R., and R. D. Holt. 1995. When does evo- plete list of references should consult the Appendix. This lution by natural selection prevent extinction. Evolution work was supported by the National Science Foundation 49:201±207. Special Feature 1714 um,P,R eo .Svlie,adT akoe.1997. Paakkonen. T. and Savolainen, O. Repo, R. P., Hurme, ae,E .18.Lttdnlvraini erdcietim- a reproductive in of variation Evolution Latitudinal 1988. 1997. P. E. Barton. Lacey, H. N. and M., Kirkpatrick, new A 1999. Weider. J. L. and Robbins, A. J. C., W. Kerfoot, extinc- Quaternary Late 1999. Weng. C. and T., S. Jackson, ako,S .20.Oto h adnadit h cooler? the into and garden the of Out 2000. T. S. Jackson, arc,J . .F cnbl n .V el.19.Dis- 1994. Wells. V. P. and Schnabel, F. A. L., J. Hamrick, artn .G,J. .Lmet .E aee,C .Holt- L. C. Caceres, E. C. Lampert, W. Jr., G., N. Hairston, crw .B,adN ece.19.Rsos ftundra of Response 1992. Fetcher. N. and B., J. McGraw, ute,B,W rmr .V ogn .C rnie and Prentice, C. H. Morgan, V. ice A. Cramer, Quaternary W. the B., of Huntley, legacy genetic The 2000. G. Hewitt, esi .E 01 etn noois v eeso eco- of tenets ®ve Antonovics' Testing 2001. E. R. Lenski, lmtcaatto fbdstadfothriesi Scots in hardiness frost ( and set pine bud of adaptation Climatic Springer-Ver- 47. I Germany. Volume Berlin, terres- Series. lag, of ASI NATO responses biota. evolutionary trial and environmental rapid spatial future the and and Past Prentice, changes: editors. C. Allen, H. M. Morgan, R. V. J. A. Cramer, W. Huntley, B. n fasotlvdmonocarp, short-lived a of ing Naturalist American range. species and Limnology paleolimnology. experimental Oceanography descrip- and combining reconstruction: tive historical to approach (USA) Science of Academy 13852. National Proceedings America. the North eastern of in species tree a of Con- tion Haven, New 6. Volume USA. necticut, Paleon- Papers. ecosystems. Society terrestrial tological phanerozoic of Evolution s287±308 Pag- paleoecology. es time deep- on perspective Quaternary A search fGetBsncnfr.Pgs147±161 Pages conifers. Basin populations Great among of and within diversity genetic of tribution ee,L .Wie,U ade n .M ot 1999. Post. M. D. and Nature eggs. Gaedke, dormant by U. revealed evolution Weider, Rapid J. L. meier, Ecol- response. ecosystem ogy pelagic and pollution industrial artn .G,C .Kan,L .Dma n .W Ef¯er. W. S. and Demma, P. L. Kearns, M. C. G., N. Hairston, ln ouain ociai hne ae 359±376 Pages change. climatic to populations plant UK. Oxford, and achievement Science, Ecology: Blackwell editors. challenge. Levin, S. and Huntly, J. it oftr niomna hne.Pgs487±504 Pages terrestrial changes. of environmental response future the Predicting to 1997. biota Allen. M. R. J. Nature ages. editors. USA. Basin. Witters, Colorado, Great W. Niwot, and W. Press, Plateau Colorado and Colorado of Thome, the University of H. history K. Natural Clair, St. L. feooyadgntc.Pgs25±45 Pages genetics. interface and the ecology at bacteria of with experiments genetics: logical Ecology Archives cdmcPes e ok e ok USA. climate. York, New changing York, a New in Press, ecosystems Academic Arctic editor. Chapin, 05 Species-speci®c 2005. opeebbigah frfrne sdi rprn h eiwi vial nEAsEetoi aaArchive: Data ESA's Electronic in available is review the preparing in used references of bibliography complete A 86 iu sylvestris Pinus E086-092-A1. 27 :1669±1678. :716±723. 69 in :220±232. 405 .Gsad n .A iihl,editors. DiMichele, A. W. and Gastaldo A. 44 :1232±1247. :907±913. .Cnda ora fFrs Re- Forest of Journal Canadian ). Daphnia acscarota Daucus hntps itr of history a phenotypes: 150 :1±23. in in .C rs,N. Press, C. M. AGRTB AI TAL. ET DAVIS B. MARGARET .T ae,L. Hager, T. K. 96 (Apiaceae). 401 :13847± :466. in APPENDIX in F. ogl,J . .F ent,adR .Lnk.19.Evo- 1999. Lenski. E. R. and Bennett, F. A. A., J. Mongold, enrz .A 94 iehsoyvraino omnmul- common of variation history Life 1984. A. J. Reinartz, uaa . .Kwmr,I ioht,K ohmr,Y. Yoshimura, K. Kinoshita, I. Kawamuro, K. Y., Suyama, ai . .Tmr,M rk,adK ha 96 Genetic 1996. Ohba. K. and Araki, M. Tomaru, N. N., Tani, eflt .E,N .Thbkv,adE .Preoa 2004. Parfenova. I. E. and Tchebakova, M. N. E., G. Rehfeldt, Vegetation 1991. III. Webb, T. and Bartlein, J. P. C., Prentice, 1999. Sanchez-Cordero. V. and of Soberon, model J. A T., A. 1989. Peterson, Bull. J. J. and Lande, R. M., C. Pease, eflt .E,J .Thbkv,Y .Preoa .R. W. Parfenova, I. Y. Tchebakova, M. J. E., G. Rehfeldt, ursn .12.Tegntpcrsos ftepatspe- plant the of response genotypic The 1922. G. Turreson, eb . I.19.Sailrsos fpattx oclimate to taxa plant of response Spatial 1997. III. T., Webb, un,O 90 ouaingntc nfrs reimprove- tree forest in genetics Population 1990. O. Muona, eflt .E,C .Yn,D .Siteos,adD A. D. and Spittlehouse, L. D. Ying, C. C. E., G. Rehfeldt, uinr dpaint eprtr.VI xeso fthe of of limit Extension thermal VII. upper temperature. to adaptation lutionary ee,E,adB cmd 98 aiuia ouaindif- population Latitudinal 1998. Schmid. B. and E., Weber, en( lein Monographs Ecological lto yaisadtmn frpouto.Junlof Journal reproduction. of timing Ecology and dynamics ulation smr,adH aaaa 96 N eunefo fos- of from pollen sequence DNA sil 1996. Takahara. H. and Tsumura, eei Systems Genetic iest n ifrnito nppltoso Japanese of populations ( pine in stone differentiation and diversity ftetmeaeadbra oet.Rcn eerhand Research Breeding Recent and forests. Genetics in boreal Developments and temperate the conifers of in climate-change and climate to responses Genetic last the since Ecology America maximum. North glacial eastern in change climate and time. evolutionary in niches Science ecological of Conservatism changing a in Ecology evolution environment. and dispersal, growth, population USA. Mas- genetics, sachusetts, Sunderland, Sinauer, population resources. Plant genetic editors. and Weir, breeding, S. B. and Kahler, pc® epnet lmt in Intra- climate 2002. Milyiutin. to I. response L. and speci®c Kuzmina, A. N. Wykoff, oetResearch Forest ist h aia.Hereditas habitat. the to cies hne aaoclgclprpcie ae 57±72 Pages perspective. palaeoecological a change: et ae 282±298 Pages ment. 394. ue noErp.Aeia ora fBotany of Journal 1121. American Europe. into duced hneBiology Change aitn r 99 eei epne ociaein climate to responses Genetic 1999. Jr. Hamilton, contorta eetaini w pce of species two in ferentiation bi- terrestrial Germany. of Berlin, responses Springer-Verlag, evolutionary ota. and chang- environmental spatial J. rapid the and future es: Prentice, and C. Past H. editors. Morgan, Allen, V. A. Cramer, W. Huntley, ebsu thapsus Verbascum ih rat,ciaecag,adreforestation. and change, climate breadth, niche : 285 72 :897±912. iu pumila Pinus :1265±1267. be spp. Abies 26 71 8 :1±18. :1454±1462. :145±149. in shrci coli Escherichia 70 69 .I aiuia ifrne npop- in differences Latitudinal I. ). rmPesoeepa.Gnsand Genes peat. Pleistocene from .H rw,M .Ceg .L. A. Clegg, T. M. Brown, H. A. :1657±1664. nJpn aainJunlof Journal Canadian Japan. in ) :375±407. 72 3 :2038±2056. Solidago :211±350. iu sylvestris Pinus clg,Vl 6 o 7 No. 86, Vol. Ecology, Evolution . Atrca)intro- (Asteraceae) 1 :113±130. Ecological 85 Global . 53 :1110± :386± Pinus in B.